Abstract

Direct intravital imaging of an endothelial surface layer (ESL) in pulmonary microcirculation could be a valuable approach to investigate the role of a vascular endothelial barrier in various pathological conditions. Despite its importance as a marker of endothelial cell damage and impairment of the vascular system, in vivo visualization of ESL has remained a challenging technical issue. In this work, we implemented a pulmonary microcirculation imaging system integrated to a custom-design video-rate laser scanning confocal microscopy platform. Using the system, a real-time cellular-level microscopic imaging of the lung was successfully performed, which facilitated a clear identification of individual flowing erythrocytes in pulmonary capillaries. Subcellular level pulmonary ESL was identified in vivo by fluorescence angiography using a dextran conjugated fluorophore to label blood plasma and the red blood cell (RBC) exclusion imaging analysis. Degradation of ESL width was directly evaluated in a murine sepsis model in vivo, suggesting an impairment of pulmonary vascular endothelium and endothelial barrier dysfunction.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2017 (1)

A. N. Rizzo and S. M. Dudek, “Endothelial Glycocalyx Repair: Building a Wall to Protect the Lung during Sepsis,” Am. J. Respir. Cell Mol. Biol. 56(6), 687–688 (2017).
[Crossref] [PubMed]

2016 (3)

S. M. Haeger, Y. Yang, and E. P. Schmidt, “Heparan Sulfate in the Developing, Healthy, and Injured Lung,” Am. J. Respir. Cell Mol. Biol. 55(1), 5–11 (2016).
[Crossref] [PubMed]

E. P. Schmidt, K. H. Overdier, X. Sun, L. Lin, X. Liu, Y. Yang, L. A. Ammons, T. D. Hiller, M. A. Suflita, Y. Yu, Y. Chen, F. Zhang, C. Cothren Burlew, C. L. Edelstein, I. S. Douglas, and R. J. Linhardt, “Urinary Glycosaminoglycans Predict Outcomes in Septic Shock and Acute Respiratory Distress Syndrome,” Am. J. Respir. Crit. Care Med. 194(4), 439–449 (2016).
[Crossref] [PubMed]

K. Kim, K. Choe, I. Park, P. Kim, and Y. Park, “Holographic intravital microscopy for 2-D and 3-D imaging intact circulating blood cells in microcapillaries of live mice,” Sci. Rep. 6(1), 33084 (2016).
[Crossref] [PubMed]

2015 (3)

2014 (5)

Y. Hwang, J. Ahn, J. Mun, S. Bae, Y. U. Jeong, N. A. Vinokurov, and P. Kim, “In vivo analysis of THz wave irradiation induced acute inflammatory response in skin by laser-scanning confocal microscopy,” Opt. Express 22(10), 11465–11475 (2014).
[Crossref] [PubMed]

E. P. Schmidt, G. Li, L. Li, L. Fu, Y. Yang, K. H. Overdier, I. S. Douglas, and R. J. Linhardt, “The circulating glycosaminoglycan signature of respiratory failure in critically ill adults,” J. Biol. Chem. 289(12), 8194–8202 (2014).
[Crossref] [PubMed]

D. H. Lee, M. J. Dane, B. M. van den Berg, M. G. Boels, J. W. van Teeffelen, R. de Mutsert, M. den Heijer, F. R. Rosendaal, J. van der Vlag, A. J. van Zonneveld, H. Vink, T. J. Rabelink, and NEO study group, “Deeper penetration of erythrocytes into the endothelial glycocalyx is associated with impaired microvascular perfusion,” PLoS One 9(5), e96477 (2014).
[Crossref] [PubMed]

A. D. Aguirre, C. Vinegoni, M. Sebas, and R. Weissleder, “Intravital imaging of cardiac function at the single-cell level,” Proc. Natl. Acad. Sci. U.S.A. 111(31), 11257–11262 (2014).
[Crossref] [PubMed]

M. R. Looney and J. Bhattacharya, “Live imaging of the lung,” Annu. Rev. Physiol. 76(1), 431–445 (2014).
[Crossref] [PubMed]

2013 (2)

K. Jung, P. Kim, F. Leuschner, R. Gorbatov, J. K. Kim, T. Ueno, M. Nahrendorf, and S. H. Yun, “Endoscopic time-lapse imaging of immune cells in infarcted mouse hearts,” Circ. Res. 112(6), 891–899 (2013).
[Crossref] [PubMed]

K. Choe, Y. Hwang, H. Seo, and P. Kim, “In vivo high spatiotemporal resolution visualization of circulating T lymphocytes in high endothelial venules of lymph nodes,” J. Biomed. Opt. 18(3), 036005 (2013).
[Crossref] [PubMed]

2012 (6)

M. Sallisalmi, J. Tenhunen, R. Yang, N. Oksala, and V. Pettilä, “Vascular adhesion protein-1 and syndecan-1 in septic shock,” Acta Anaesthesiol. Scand. 56(3), 316–322 (2012).
[Crossref] [PubMed]

E. P. Schmidt, Y. Yang, W. J. Janssen, A. Gandjeva, M. J. Perez, L. Barthel, R. L. Zemans, J. C. Bowman, D. E. Koyanagi, Z. X. Yunt, L. P. Smith, S. S. Cheng, K. H. Overdier, K. R. Thompson, M. W. Geraci, I. S. Douglas, D. B. Pearse, and R. M. Tuder, “The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis,” Nat. Med. 18(8), 1217–1223 (2012).
[Crossref] [PubMed]

A. Burke-Gaffney and T. W. Evans, “Lest we forget the endothelial glycocalyx in sepsis,” Crit. Care 16(2), 121 (2012).
[Crossref] [PubMed]

P. I. Johansson, J. Stensballe, L. S. Rasmussen, and S. R. Ostrowski, “High circulating adrenaline levels at admission predict increased mortality after trauma,” J. Trauma Acute Care Surg. 72(2), 428–436 (2012).
[Crossref] [PubMed]

C. Vinegoni, S. Lee, R. Gorbatov, and R. Weissleder, “Motion compensation using a suctioning stabilizer for intravital microscopy,” Intravital 1(2), 115–121 (2012).
[Crossref] [PubMed]

S. Grundmann, K. Fink, L. Rabadzhieva, N. Bourgeois, T. Schwab, M. Moser, C. Bode, and H. J. Busch, “Perturbation of the endothelial glycocalyx in post cardiac arrest syndrome,” Resuscitation 83(6), 715–720 (2012).
[Crossref] [PubMed]

2011 (3)

G. Matute-Bello, G. Downey, B. B. Moore, S. D. Groshong, M. A. Matthay, A. S. Slutsky, W. M. Kuebler, and G. Acute Lung Injury in Animals Study Group, “An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals,” Am. J. Respir. Cell Mol. Biol. 44(5), 725–738 (2011).
[Crossref] [PubMed]

J. Steppan, S. Hofer, B. Funke, T. Brenner, M. Henrich, E. Martin, J. Weitz, U. Hofmann, and M. A. Weigand, “Sepsis and major abdominal surgery lead to flaking of the endothelial glycocalix,” J. Surg. Res. 165(1), 136–141 (2011).
[Crossref] [PubMed]

M. R. Looney, E. E. Thornton, D. Sen, W. J. Lamm, R. W. Glenny, and M. F. Krummel, “Stabilized imaging of immune surveillance in the mouse lung,” Nat. Methods 8(1), 91–96 (2011).
[Crossref] [PubMed]

2010 (3)

P. Kim, E. Chung, H. Yamashita, K. E. Hung, A. Mizoguchi, R. Kucherlapati, D. Fukumura, R. K. Jain, and S. H. Yun, “In vivo wide-area cellular imaging by side-view endomicroscopy,” Nat. Methods 7(4), 303–305 (2010).
[Crossref] [PubMed]

J. W. VanTeeffelen, J. Brands, and H. Vink, “Agonist-induced impairment of glycocalyx exclusion properties: contribution to coronary effects of adenosine,” Cardiovasc. Res. 87(2), 311–319 (2010).
[Crossref] [PubMed]

B. F. Becker, D. Chappell, D. Bruegger, T. Annecke, and M. Jacob, “Therapeutic strategies targeting the endothelial glycocalyx: acute deficits, but great potential,” Cardiovasc. Res. 87(2), 300–310 (2010).
[Crossref] [PubMed]

2009 (1)

D. Rittirsch, M. S. Huber-Lang, M. A. Flierl, and P. A. Ward, “Immunodesign of experimental sepsis by cecal ligation and puncture,” Nat. Protoc. 4(1), 31–36 (2009).
[Crossref] [PubMed]

2008 (5)

P. Kim, M. Puoris’haag, D. Côté, C. P. Lin, and S. H. Yun, “In vivo confocal and multiphoton microendoscopy,” J. Biomed. Opt. 13(1), 010501 (2008).
[Crossref] [PubMed]

M. Guizar-Sicairos, S. T. Thurman, and J. R. Fienup, “Efficient subpixel image registration algorithms,” Opt. Lett. 33(2), 156–158 (2008).
[Crossref] [PubMed]

D. R. Potter and E. R. Damiano, “The hydrodynamically relevant endothelial cell glycocalyx observed in vivo is absent in vitro,” Circ. Res. 102(7), 770–776 (2008).
[Crossref] [PubMed]

A. Nelson, I. Berkestedt, A. Schmidtchen, L. Ljunggren, and M. Bodelsson, “Increased levels of glycosaminoglycans during septic shock: relation to mortality and the antibacterial actions of plasma,” Shock 30(6), 623–627 (2008).
[Crossref] [PubMed]

X. Marechal, R. Favory, O. Joulin, D. Montaigne, S. Hassoun, B. Decoster, F. Zerimech, and R. Neviere, “Endothelial glycocalyx damage during endotoxemia coincides with microcirculatory dysfunction and vascular oxidative stress,” Shock 29(5), 572–576 (2008).
[PubMed]

2007 (4)

S. Weinbaum, J. M. Tarbell, and E. R. Damiano, “The structure and function of the endothelial glycocalyx layer,” Annu. Rev. Biomed. Eng. 9(1), 121–167 (2007).
[Crossref] [PubMed]

A. P. Stevens, V. Hlady, and R. O. Dull, “Fluorescence correlation spectroscopy can probe albumin dynamics inside lung endothelial glycocalyx,” Am. J. Physiol. Lung Cell. Mol. Physiol. 293(2), L328–L335 (2007).
[Crossref] [PubMed]

M. Rehm, D. Bruegger, F. Christ, P. Conzen, M. Thiel, M. Jacob, D. Chappell, M. Stoeckelhuber, U. Welsch, B. Reichart, K. Peter, and B. F. Becker, “Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia,” Circulation 116(17), 1896–1906 (2007).
[Crossref] [PubMed]

S. Reitsma, D. W. Slaaf, H. Vink, M. A. van Zandvoort, and M. G. oude Egbrink, “The endothelial glycocalyx: composition, functions, and visualization,” Pflugers Arch. 454(3), 345–359 (2007).
[Crossref] [PubMed]

2006 (1)

Y. Han, S. Weinbaum, J. A. E. Spaan, and H. Vink, “Large-deformation analysis of the elastic recoil of fibre layers in a Brinkman medium with application to the endothelial glycocalyx,” J. Fluid Mech. 554(-1), 217 (2006).
[Crossref]

2005 (3)

H. Noguchi and G. Gompper, “Shape transitions of fluid vesicles and red blood cells in capillary flows,” Proc. Natl. Acad. Sci. U.S.A. 102(40), 14159–14164 (2005).
[Crossref] [PubMed]

C. J. Zuurbier, C. Demirci, A. Koeman, H. Vink, and C. Ince, “Short-term hyperglycemia increases endothelial glycocalyx permeability and acutely decreases lineal density of capillaries with flowing red blood cells,” J. Appl. Physiol. 99(4), 1471–1476 (2005).
[Crossref] [PubMed]

W. J. Lamm, S. L. Bernard, W. W. Wagner, and R. W. Glenny, “Intravital microscopic observations of 15-microm microspheres lodging in the pulmonary microcirculation,” J. Appl. Physiol. 98(6), 2242–2248 (2005).
[Crossref] [PubMed]

2004 (1)

J. King, T. Hamil, J. Creighton, S. Wu, P. Bhat, F. McDonald, and T. Stevens, “Structural and functional characteristics of lung macro- and microvascular endothelial cell phenotypes,” Microvasc. Res. 67(2), 139–151 (2004).
[Crossref] [PubMed]

2003 (2)

B. M. van den Berg, H. Vink, and J. A. Spaan, “The endothelial glycocalyx protects against myocardial edema,” Circ. Res. 92(6), 592–594 (2003).
[Crossref] [PubMed]

S. Weinbaum, X. Zhang, Y. Han, H. Vink, and S. C. Cowin, “Mechanotransduction and flow across the endothelial glycocalyx,” Proc. Natl. Acad. Sci. U.S.A. 100(13), 7988–7995 (2003).
[Crossref] [PubMed]

2001 (2)

T. W. Secomb, R. Hsu, and A. R. Pries, “Motion of red blood cells in a capillary with an endothelial surface layer: effect of flow velocity,” Am. J. Physiol. Heart Circ. Physiol. 281(2), H629–H636 (2001).
[Crossref] [PubMed]

B. Afessa, B. Green, I. Delke, and K. Koch, “Systemic inflammatory response syndrome, organ failure, and outcome in critically ill obstetric patients treated in an ICU,” Chest 120(4), 1271–1277 (2001).
[Crossref] [PubMed]

2000 (1)

H. Vink and B. R. Duling, “Capillary endothelial surface layer selectively reduces plasma solute distribution volume,” Am. J. Physiol. Heart Circ. Physiol. 278(1), H285–H289 (2000).
[Crossref] [PubMed]

1996 (1)

H. Vink and B. R. Duling, “Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries,” Circ. Res. 79(3), 581–589 (1996).
[Crossref] [PubMed]

1995 (1)

L. D. Hudson, J. A. Milberg, D. Anardi, and R. J. Maunder, “Clinical risks for development of the acute respiratory distress syndrome,” Am. J. Respir. Crit. Care Med. 151(2), 293–301 (1995).
[Crossref] [PubMed]

1969 (1)

R. Skalak and P. I. Branemark, “Deformation of red blood cells in capillaries,” Science 164(3880), 717–719 (1969).
[Crossref] [PubMed]

Afessa, B.

B. Afessa, B. Green, I. Delke, and K. Koch, “Systemic inflammatory response syndrome, organ failure, and outcome in critically ill obstetric patients treated in an ICU,” Chest 120(4), 1271–1277 (2001).
[Crossref] [PubMed]

Aguirre, A. D.

A. D. Aguirre, C. Vinegoni, M. Sebas, and R. Weissleder, “Intravital imaging of cardiac function at the single-cell level,” Proc. Natl. Acad. Sci. U.S.A. 111(31), 11257–11262 (2014).
[Crossref] [PubMed]

Ahn, J.

Ahn, S.

K. Choe, J. Y. Jang, I. Park, Y. Kim, S. Ahn, D. Y. Park, Y. K. Hong, K. Alitalo, G. Y. Koh, and P. Kim, “Intravital imaging of intestinal lacteals unveils lipid drainage through contractility,” J. Clin. Invest. 125(11), 4042–4052 (2015).
[Crossref] [PubMed]

Alitalo, K.

K. Choe, J. Y. Jang, I. Park, Y. Kim, S. Ahn, D. Y. Park, Y. K. Hong, K. Alitalo, G. Y. Koh, and P. Kim, “Intravital imaging of intestinal lacteals unveils lipid drainage through contractility,” J. Clin. Invest. 125(11), 4042–4052 (2015).
[Crossref] [PubMed]

Ammons, L. A.

E. P. Schmidt, K. H. Overdier, X. Sun, L. Lin, X. Liu, Y. Yang, L. A. Ammons, T. D. Hiller, M. A. Suflita, Y. Yu, Y. Chen, F. Zhang, C. Cothren Burlew, C. L. Edelstein, I. S. Douglas, and R. J. Linhardt, “Urinary Glycosaminoglycans Predict Outcomes in Septic Shock and Acute Respiratory Distress Syndrome,” Am. J. Respir. Crit. Care Med. 194(4), 439–449 (2016).
[Crossref] [PubMed]

Anardi, D.

L. D. Hudson, J. A. Milberg, D. Anardi, and R. J. Maunder, “Clinical risks for development of the acute respiratory distress syndrome,” Am. J. Respir. Crit. Care Med. 151(2), 293–301 (1995).
[Crossref] [PubMed]

Annecke, T.

B. F. Becker, D. Chappell, D. Bruegger, T. Annecke, and M. Jacob, “Therapeutic strategies targeting the endothelial glycocalyx: acute deficits, but great potential,” Cardiovasc. Res. 87(2), 300–310 (2010).
[Crossref] [PubMed]

Bae, S.

Barthel, L.

E. P. Schmidt, Y. Yang, W. J. Janssen, A. Gandjeva, M. J. Perez, L. Barthel, R. L. Zemans, J. C. Bowman, D. E. Koyanagi, Z. X. Yunt, L. P. Smith, S. S. Cheng, K. H. Overdier, K. R. Thompson, M. W. Geraci, I. S. Douglas, D. B. Pearse, and R. M. Tuder, “The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis,” Nat. Med. 18(8), 1217–1223 (2012).
[Crossref] [PubMed]

Becker, B. F.

B. F. Becker, D. Chappell, D. Bruegger, T. Annecke, and M. Jacob, “Therapeutic strategies targeting the endothelial glycocalyx: acute deficits, but great potential,” Cardiovasc. Res. 87(2), 300–310 (2010).
[Crossref] [PubMed]

M. Rehm, D. Bruegger, F. Christ, P. Conzen, M. Thiel, M. Jacob, D. Chappell, M. Stoeckelhuber, U. Welsch, B. Reichart, K. Peter, and B. F. Becker, “Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia,” Circulation 116(17), 1896–1906 (2007).
[Crossref] [PubMed]

Berkestedt, I.

A. Nelson, I. Berkestedt, A. Schmidtchen, L. Ljunggren, and M. Bodelsson, “Increased levels of glycosaminoglycans during septic shock: relation to mortality and the antibacterial actions of plasma,” Shock 30(6), 623–627 (2008).
[Crossref] [PubMed]

Bernard, S. L.

W. J. Lamm, S. L. Bernard, W. W. Wagner, and R. W. Glenny, “Intravital microscopic observations of 15-microm microspheres lodging in the pulmonary microcirculation,” J. Appl. Physiol. 98(6), 2242–2248 (2005).
[Crossref] [PubMed]

Bhat, P.

J. King, T. Hamil, J. Creighton, S. Wu, P. Bhat, F. McDonald, and T. Stevens, “Structural and functional characteristics of lung macro- and microvascular endothelial cell phenotypes,” Microvasc. Res. 67(2), 139–151 (2004).
[Crossref] [PubMed]

Bhattacharya, J.

M. R. Looney and J. Bhattacharya, “Live imaging of the lung,” Annu. Rev. Physiol. 76(1), 431–445 (2014).
[Crossref] [PubMed]

Bode, C.

S. Grundmann, K. Fink, L. Rabadzhieva, N. Bourgeois, T. Schwab, M. Moser, C. Bode, and H. J. Busch, “Perturbation of the endothelial glycocalyx in post cardiac arrest syndrome,” Resuscitation 83(6), 715–720 (2012).
[Crossref] [PubMed]

Bodelsson, M.

A. Nelson, I. Berkestedt, A. Schmidtchen, L. Ljunggren, and M. Bodelsson, “Increased levels of glycosaminoglycans during septic shock: relation to mortality and the antibacterial actions of plasma,” Shock 30(6), 623–627 (2008).
[Crossref] [PubMed]

Boels, M. G.

D. H. Lee, M. J. Dane, B. M. van den Berg, M. G. Boels, J. W. van Teeffelen, R. de Mutsert, M. den Heijer, F. R. Rosendaal, J. van der Vlag, A. J. van Zonneveld, H. Vink, T. J. Rabelink, and NEO study group, “Deeper penetration of erythrocytes into the endothelial glycocalyx is associated with impaired microvascular perfusion,” PLoS One 9(5), e96477 (2014).
[Crossref] [PubMed]

Bourgeois, N.

S. Grundmann, K. Fink, L. Rabadzhieva, N. Bourgeois, T. Schwab, M. Moser, C. Bode, and H. J. Busch, “Perturbation of the endothelial glycocalyx in post cardiac arrest syndrome,” Resuscitation 83(6), 715–720 (2012).
[Crossref] [PubMed]

Bowman, J. C.

E. P. Schmidt, Y. Yang, W. J. Janssen, A. Gandjeva, M. J. Perez, L. Barthel, R. L. Zemans, J. C. Bowman, D. E. Koyanagi, Z. X. Yunt, L. P. Smith, S. S. Cheng, K. H. Overdier, K. R. Thompson, M. W. Geraci, I. S. Douglas, D. B. Pearse, and R. M. Tuder, “The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis,” Nat. Med. 18(8), 1217–1223 (2012).
[Crossref] [PubMed]

Brands, J.

J. W. VanTeeffelen, J. Brands, and H. Vink, “Agonist-induced impairment of glycocalyx exclusion properties: contribution to coronary effects of adenosine,” Cardiovasc. Res. 87(2), 311–319 (2010).
[Crossref] [PubMed]

Branemark, P. I.

R. Skalak and P. I. Branemark, “Deformation of red blood cells in capillaries,” Science 164(3880), 717–719 (1969).
[Crossref] [PubMed]

Brenner, T.

J. Steppan, S. Hofer, B. Funke, T. Brenner, M. Henrich, E. Martin, J. Weitz, U. Hofmann, and M. A. Weigand, “Sepsis and major abdominal surgery lead to flaking of the endothelial glycocalix,” J. Surg. Res. 165(1), 136–141 (2011).
[Crossref] [PubMed]

Bruegger, D.

B. F. Becker, D. Chappell, D. Bruegger, T. Annecke, and M. Jacob, “Therapeutic strategies targeting the endothelial glycocalyx: acute deficits, but great potential,” Cardiovasc. Res. 87(2), 300–310 (2010).
[Crossref] [PubMed]

M. Rehm, D. Bruegger, F. Christ, P. Conzen, M. Thiel, M. Jacob, D. Chappell, M. Stoeckelhuber, U. Welsch, B. Reichart, K. Peter, and B. F. Becker, “Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia,” Circulation 116(17), 1896–1906 (2007).
[Crossref] [PubMed]

Burke-Gaffney, A.

A. Burke-Gaffney and T. W. Evans, “Lest we forget the endothelial glycocalyx in sepsis,” Crit. Care 16(2), 121 (2012).
[Crossref] [PubMed]

Busch, H. J.

S. Grundmann, K. Fink, L. Rabadzhieva, N. Bourgeois, T. Schwab, M. Moser, C. Bode, and H. J. Busch, “Perturbation of the endothelial glycocalyx in post cardiac arrest syndrome,” Resuscitation 83(6), 715–720 (2012).
[Crossref] [PubMed]

Chappell, D.

B. F. Becker, D. Chappell, D. Bruegger, T. Annecke, and M. Jacob, “Therapeutic strategies targeting the endothelial glycocalyx: acute deficits, but great potential,” Cardiovasc. Res. 87(2), 300–310 (2010).
[Crossref] [PubMed]

M. Rehm, D. Bruegger, F. Christ, P. Conzen, M. Thiel, M. Jacob, D. Chappell, M. Stoeckelhuber, U. Welsch, B. Reichart, K. Peter, and B. F. Becker, “Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia,” Circulation 116(17), 1896–1906 (2007).
[Crossref] [PubMed]

Chen, Y.

E. P. Schmidt, K. H. Overdier, X. Sun, L. Lin, X. Liu, Y. Yang, L. A. Ammons, T. D. Hiller, M. A. Suflita, Y. Yu, Y. Chen, F. Zhang, C. Cothren Burlew, C. L. Edelstein, I. S. Douglas, and R. J. Linhardt, “Urinary Glycosaminoglycans Predict Outcomes in Septic Shock and Acute Respiratory Distress Syndrome,” Am. J. Respir. Crit. Care Med. 194(4), 439–449 (2016).
[Crossref] [PubMed]

Cheng, S. S.

E. P. Schmidt, Y. Yang, W. J. Janssen, A. Gandjeva, M. J. Perez, L. Barthel, R. L. Zemans, J. C. Bowman, D. E. Koyanagi, Z. X. Yunt, L. P. Smith, S. S. Cheng, K. H. Overdier, K. R. Thompson, M. W. Geraci, I. S. Douglas, D. B. Pearse, and R. M. Tuder, “The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis,” Nat. Med. 18(8), 1217–1223 (2012).
[Crossref] [PubMed]

Choe, K.

K. Kim, K. Choe, I. Park, P. Kim, and Y. Park, “Holographic intravital microscopy for 2-D and 3-D imaging intact circulating blood cells in microcapillaries of live mice,” Sci. Rep. 6(1), 33084 (2016).
[Crossref] [PubMed]

H. Seo, Y. Hwang, K. Choe, and P. Kim, “In vivo quantitation of injected circulating tumor cells from great saphenous vein based on video-rate confocal microscopy,” Biomed. Opt. Express 6(6), 2158–2167 (2015).
[Crossref] [PubMed]

J. Ahn, K. Choe, T. Wang, Y. Hwang, E. Song, K. H. Kim, and P. Kim, “In vivo longitudinal cellular imaging of small intestine by side-view endomicroscopy,” Biomed. Opt. Express 6(10), 3963–3972 (2015).
[Crossref] [PubMed]

K. Choe, J. Y. Jang, I. Park, Y. Kim, S. Ahn, D. Y. Park, Y. K. Hong, K. Alitalo, G. Y. Koh, and P. Kim, “Intravital imaging of intestinal lacteals unveils lipid drainage through contractility,” J. Clin. Invest. 125(11), 4042–4052 (2015).
[Crossref] [PubMed]

K. Choe, Y. Hwang, H. Seo, and P. Kim, “In vivo high spatiotemporal resolution visualization of circulating T lymphocytes in high endothelial venules of lymph nodes,” J. Biomed. Opt. 18(3), 036005 (2013).
[Crossref] [PubMed]

Christ, F.

M. Rehm, D. Bruegger, F. Christ, P. Conzen, M. Thiel, M. Jacob, D. Chappell, M. Stoeckelhuber, U. Welsch, B. Reichart, K. Peter, and B. F. Becker, “Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia,” Circulation 116(17), 1896–1906 (2007).
[Crossref] [PubMed]

Chung, E.

P. Kim, E. Chung, H. Yamashita, K. E. Hung, A. Mizoguchi, R. Kucherlapati, D. Fukumura, R. K. Jain, and S. H. Yun, “In vivo wide-area cellular imaging by side-view endomicroscopy,” Nat. Methods 7(4), 303–305 (2010).
[Crossref] [PubMed]

Conzen, P.

M. Rehm, D. Bruegger, F. Christ, P. Conzen, M. Thiel, M. Jacob, D. Chappell, M. Stoeckelhuber, U. Welsch, B. Reichart, K. Peter, and B. F. Becker, “Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia,” Circulation 116(17), 1896–1906 (2007).
[Crossref] [PubMed]

Côté, D.

P. Kim, M. Puoris’haag, D. Côté, C. P. Lin, and S. H. Yun, “In vivo confocal and multiphoton microendoscopy,” J. Biomed. Opt. 13(1), 010501 (2008).
[Crossref] [PubMed]

Cothren Burlew, C.

E. P. Schmidt, K. H. Overdier, X. Sun, L. Lin, X. Liu, Y. Yang, L. A. Ammons, T. D. Hiller, M. A. Suflita, Y. Yu, Y. Chen, F. Zhang, C. Cothren Burlew, C. L. Edelstein, I. S. Douglas, and R. J. Linhardt, “Urinary Glycosaminoglycans Predict Outcomes in Septic Shock and Acute Respiratory Distress Syndrome,” Am. J. Respir. Crit. Care Med. 194(4), 439–449 (2016).
[Crossref] [PubMed]

Cowin, S. C.

S. Weinbaum, X. Zhang, Y. Han, H. Vink, and S. C. Cowin, “Mechanotransduction and flow across the endothelial glycocalyx,” Proc. Natl. Acad. Sci. U.S.A. 100(13), 7988–7995 (2003).
[Crossref] [PubMed]

Creighton, J.

J. King, T. Hamil, J. Creighton, S. Wu, P. Bhat, F. McDonald, and T. Stevens, “Structural and functional characteristics of lung macro- and microvascular endothelial cell phenotypes,” Microvasc. Res. 67(2), 139–151 (2004).
[Crossref] [PubMed]

Damiano, E. R.

D. R. Potter and E. R. Damiano, “The hydrodynamically relevant endothelial cell glycocalyx observed in vivo is absent in vitro,” Circ. Res. 102(7), 770–776 (2008).
[Crossref] [PubMed]

S. Weinbaum, J. M. Tarbell, and E. R. Damiano, “The structure and function of the endothelial glycocalyx layer,” Annu. Rev. Biomed. Eng. 9(1), 121–167 (2007).
[Crossref] [PubMed]

Dane, M. J.

D. H. Lee, M. J. Dane, B. M. van den Berg, M. G. Boels, J. W. van Teeffelen, R. de Mutsert, M. den Heijer, F. R. Rosendaal, J. van der Vlag, A. J. van Zonneveld, H. Vink, T. J. Rabelink, and NEO study group, “Deeper penetration of erythrocytes into the endothelial glycocalyx is associated with impaired microvascular perfusion,” PLoS One 9(5), e96477 (2014).
[Crossref] [PubMed]

de Mutsert, R.

D. H. Lee, M. J. Dane, B. M. van den Berg, M. G. Boels, J. W. van Teeffelen, R. de Mutsert, M. den Heijer, F. R. Rosendaal, J. van der Vlag, A. J. van Zonneveld, H. Vink, T. J. Rabelink, and NEO study group, “Deeper penetration of erythrocytes into the endothelial glycocalyx is associated with impaired microvascular perfusion,” PLoS One 9(5), e96477 (2014).
[Crossref] [PubMed]

Decoster, B.

X. Marechal, R. Favory, O. Joulin, D. Montaigne, S. Hassoun, B. Decoster, F. Zerimech, and R. Neviere, “Endothelial glycocalyx damage during endotoxemia coincides with microcirculatory dysfunction and vascular oxidative stress,” Shock 29(5), 572–576 (2008).
[PubMed]

Delke, I.

B. Afessa, B. Green, I. Delke, and K. Koch, “Systemic inflammatory response syndrome, organ failure, and outcome in critically ill obstetric patients treated in an ICU,” Chest 120(4), 1271–1277 (2001).
[Crossref] [PubMed]

Demirci, C.

C. J. Zuurbier, C. Demirci, A. Koeman, H. Vink, and C. Ince, “Short-term hyperglycemia increases endothelial glycocalyx permeability and acutely decreases lineal density of capillaries with flowing red blood cells,” J. Appl. Physiol. 99(4), 1471–1476 (2005).
[Crossref] [PubMed]

den Heijer, M.

D. H. Lee, M. J. Dane, B. M. van den Berg, M. G. Boels, J. W. van Teeffelen, R. de Mutsert, M. den Heijer, F. R. Rosendaal, J. van der Vlag, A. J. van Zonneveld, H. Vink, T. J. Rabelink, and NEO study group, “Deeper penetration of erythrocytes into the endothelial glycocalyx is associated with impaired microvascular perfusion,” PLoS One 9(5), e96477 (2014).
[Crossref] [PubMed]

Douglas, I. S.

E. P. Schmidt, K. H. Overdier, X. Sun, L. Lin, X. Liu, Y. Yang, L. A. Ammons, T. D. Hiller, M. A. Suflita, Y. Yu, Y. Chen, F. Zhang, C. Cothren Burlew, C. L. Edelstein, I. S. Douglas, and R. J. Linhardt, “Urinary Glycosaminoglycans Predict Outcomes in Septic Shock and Acute Respiratory Distress Syndrome,” Am. J. Respir. Crit. Care Med. 194(4), 439–449 (2016).
[Crossref] [PubMed]

E. P. Schmidt, G. Li, L. Li, L. Fu, Y. Yang, K. H. Overdier, I. S. Douglas, and R. J. Linhardt, “The circulating glycosaminoglycan signature of respiratory failure in critically ill adults,” J. Biol. Chem. 289(12), 8194–8202 (2014).
[Crossref] [PubMed]

E. P. Schmidt, Y. Yang, W. J. Janssen, A. Gandjeva, M. J. Perez, L. Barthel, R. L. Zemans, J. C. Bowman, D. E. Koyanagi, Z. X. Yunt, L. P. Smith, S. S. Cheng, K. H. Overdier, K. R. Thompson, M. W. Geraci, I. S. Douglas, D. B. Pearse, and R. M. Tuder, “The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis,” Nat. Med. 18(8), 1217–1223 (2012).
[Crossref] [PubMed]

Downey, G.

G. Matute-Bello, G. Downey, B. B. Moore, S. D. Groshong, M. A. Matthay, A. S. Slutsky, W. M. Kuebler, and G. Acute Lung Injury in Animals Study Group, “An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals,” Am. J. Respir. Cell Mol. Biol. 44(5), 725–738 (2011).
[Crossref] [PubMed]

Dudek, S. M.

A. N. Rizzo and S. M. Dudek, “Endothelial Glycocalyx Repair: Building a Wall to Protect the Lung during Sepsis,” Am. J. Respir. Cell Mol. Biol. 56(6), 687–688 (2017).
[Crossref] [PubMed]

Duling, B. R.

H. Vink and B. R. Duling, “Capillary endothelial surface layer selectively reduces plasma solute distribution volume,” Am. J. Physiol. Heart Circ. Physiol. 278(1), H285–H289 (2000).
[Crossref] [PubMed]

H. Vink and B. R. Duling, “Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries,” Circ. Res. 79(3), 581–589 (1996).
[Crossref] [PubMed]

Dull, R. O.

A. P. Stevens, V. Hlady, and R. O. Dull, “Fluorescence correlation spectroscopy can probe albumin dynamics inside lung endothelial glycocalyx,” Am. J. Physiol. Lung Cell. Mol. Physiol. 293(2), L328–L335 (2007).
[Crossref] [PubMed]

Edelstein, C. L.

E. P. Schmidt, K. H. Overdier, X. Sun, L. Lin, X. Liu, Y. Yang, L. A. Ammons, T. D. Hiller, M. A. Suflita, Y. Yu, Y. Chen, F. Zhang, C. Cothren Burlew, C. L. Edelstein, I. S. Douglas, and R. J. Linhardt, “Urinary Glycosaminoglycans Predict Outcomes in Septic Shock and Acute Respiratory Distress Syndrome,” Am. J. Respir. Crit. Care Med. 194(4), 439–449 (2016).
[Crossref] [PubMed]

Evans, T. W.

A. Burke-Gaffney and T. W. Evans, “Lest we forget the endothelial glycocalyx in sepsis,” Crit. Care 16(2), 121 (2012).
[Crossref] [PubMed]

Favory, R.

X. Marechal, R. Favory, O. Joulin, D. Montaigne, S. Hassoun, B. Decoster, F. Zerimech, and R. Neviere, “Endothelial glycocalyx damage during endotoxemia coincides with microcirculatory dysfunction and vascular oxidative stress,” Shock 29(5), 572–576 (2008).
[PubMed]

Fienup, J. R.

Fink, K.

S. Grundmann, K. Fink, L. Rabadzhieva, N. Bourgeois, T. Schwab, M. Moser, C. Bode, and H. J. Busch, “Perturbation of the endothelial glycocalyx in post cardiac arrest syndrome,” Resuscitation 83(6), 715–720 (2012).
[Crossref] [PubMed]

Flierl, M. A.

D. Rittirsch, M. S. Huber-Lang, M. A. Flierl, and P. A. Ward, “Immunodesign of experimental sepsis by cecal ligation and puncture,” Nat. Protoc. 4(1), 31–36 (2009).
[Crossref] [PubMed]

Fu, L.

E. P. Schmidt, G. Li, L. Li, L. Fu, Y. Yang, K. H. Overdier, I. S. Douglas, and R. J. Linhardt, “The circulating glycosaminoglycan signature of respiratory failure in critically ill adults,” J. Biol. Chem. 289(12), 8194–8202 (2014).
[Crossref] [PubMed]

Fukumura, D.

P. Kim, E. Chung, H. Yamashita, K. E. Hung, A. Mizoguchi, R. Kucherlapati, D. Fukumura, R. K. Jain, and S. H. Yun, “In vivo wide-area cellular imaging by side-view endomicroscopy,” Nat. Methods 7(4), 303–305 (2010).
[Crossref] [PubMed]

Funke, B.

J. Steppan, S. Hofer, B. Funke, T. Brenner, M. Henrich, E. Martin, J. Weitz, U. Hofmann, and M. A. Weigand, “Sepsis and major abdominal surgery lead to flaking of the endothelial glycocalix,” J. Surg. Res. 165(1), 136–141 (2011).
[Crossref] [PubMed]

Gandjeva, A.

E. P. Schmidt, Y. Yang, W. J. Janssen, A. Gandjeva, M. J. Perez, L. Barthel, R. L. Zemans, J. C. Bowman, D. E. Koyanagi, Z. X. Yunt, L. P. Smith, S. S. Cheng, K. H. Overdier, K. R. Thompson, M. W. Geraci, I. S. Douglas, D. B. Pearse, and R. M. Tuder, “The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis,” Nat. Med. 18(8), 1217–1223 (2012).
[Crossref] [PubMed]

Geraci, M. W.

E. P. Schmidt, Y. Yang, W. J. Janssen, A. Gandjeva, M. J. Perez, L. Barthel, R. L. Zemans, J. C. Bowman, D. E. Koyanagi, Z. X. Yunt, L. P. Smith, S. S. Cheng, K. H. Overdier, K. R. Thompson, M. W. Geraci, I. S. Douglas, D. B. Pearse, and R. M. Tuder, “The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis,” Nat. Med. 18(8), 1217–1223 (2012).
[Crossref] [PubMed]

Glenny, R. W.

M. R. Looney, E. E. Thornton, D. Sen, W. J. Lamm, R. W. Glenny, and M. F. Krummel, “Stabilized imaging of immune surveillance in the mouse lung,” Nat. Methods 8(1), 91–96 (2011).
[Crossref] [PubMed]

W. J. Lamm, S. L. Bernard, W. W. Wagner, and R. W. Glenny, “Intravital microscopic observations of 15-microm microspheres lodging in the pulmonary microcirculation,” J. Appl. Physiol. 98(6), 2242–2248 (2005).
[Crossref] [PubMed]

Gompper, G.

H. Noguchi and G. Gompper, “Shape transitions of fluid vesicles and red blood cells in capillary flows,” Proc. Natl. Acad. Sci. U.S.A. 102(40), 14159–14164 (2005).
[Crossref] [PubMed]

Gorbatov, R.

K. Jung, P. Kim, F. Leuschner, R. Gorbatov, J. K. Kim, T. Ueno, M. Nahrendorf, and S. H. Yun, “Endoscopic time-lapse imaging of immune cells in infarcted mouse hearts,” Circ. Res. 112(6), 891–899 (2013).
[Crossref] [PubMed]

C. Vinegoni, S. Lee, R. Gorbatov, and R. Weissleder, “Motion compensation using a suctioning stabilizer for intravital microscopy,” Intravital 1(2), 115–121 (2012).
[Crossref] [PubMed]

Green, B.

B. Afessa, B. Green, I. Delke, and K. Koch, “Systemic inflammatory response syndrome, organ failure, and outcome in critically ill obstetric patients treated in an ICU,” Chest 120(4), 1271–1277 (2001).
[Crossref] [PubMed]

Groshong, S. D.

G. Matute-Bello, G. Downey, B. B. Moore, S. D. Groshong, M. A. Matthay, A. S. Slutsky, W. M. Kuebler, and G. Acute Lung Injury in Animals Study Group, “An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals,” Am. J. Respir. Cell Mol. Biol. 44(5), 725–738 (2011).
[Crossref] [PubMed]

Grundmann, S.

S. Grundmann, K. Fink, L. Rabadzhieva, N. Bourgeois, T. Schwab, M. Moser, C. Bode, and H. J. Busch, “Perturbation of the endothelial glycocalyx in post cardiac arrest syndrome,” Resuscitation 83(6), 715–720 (2012).
[Crossref] [PubMed]

Guizar-Sicairos, M.

Haeger, S. M.

S. M. Haeger, Y. Yang, and E. P. Schmidt, “Heparan Sulfate in the Developing, Healthy, and Injured Lung,” Am. J. Respir. Cell Mol. Biol. 55(1), 5–11 (2016).
[Crossref] [PubMed]

Hamil, T.

J. King, T. Hamil, J. Creighton, S. Wu, P. Bhat, F. McDonald, and T. Stevens, “Structural and functional characteristics of lung macro- and microvascular endothelial cell phenotypes,” Microvasc. Res. 67(2), 139–151 (2004).
[Crossref] [PubMed]

Han, Y.

Y. Han, S. Weinbaum, J. A. E. Spaan, and H. Vink, “Large-deformation analysis of the elastic recoil of fibre layers in a Brinkman medium with application to the endothelial glycocalyx,” J. Fluid Mech. 554(-1), 217 (2006).
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S. Weinbaum, X. Zhang, Y. Han, H. Vink, and S. C. Cowin, “Mechanotransduction and flow across the endothelial glycocalyx,” Proc. Natl. Acad. Sci. U.S.A. 100(13), 7988–7995 (2003).
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Hassoun, S.

X. Marechal, R. Favory, O. Joulin, D. Montaigne, S. Hassoun, B. Decoster, F. Zerimech, and R. Neviere, “Endothelial glycocalyx damage during endotoxemia coincides with microcirculatory dysfunction and vascular oxidative stress,” Shock 29(5), 572–576 (2008).
[PubMed]

Henrich, M.

J. Steppan, S. Hofer, B. Funke, T. Brenner, M. Henrich, E. Martin, J. Weitz, U. Hofmann, and M. A. Weigand, “Sepsis and major abdominal surgery lead to flaking of the endothelial glycocalix,” J. Surg. Res. 165(1), 136–141 (2011).
[Crossref] [PubMed]

Hiller, T. D.

E. P. Schmidt, K. H. Overdier, X. Sun, L. Lin, X. Liu, Y. Yang, L. A. Ammons, T. D. Hiller, M. A. Suflita, Y. Yu, Y. Chen, F. Zhang, C. Cothren Burlew, C. L. Edelstein, I. S. Douglas, and R. J. Linhardt, “Urinary Glycosaminoglycans Predict Outcomes in Septic Shock and Acute Respiratory Distress Syndrome,” Am. J. Respir. Crit. Care Med. 194(4), 439–449 (2016).
[Crossref] [PubMed]

Hlady, V.

A. P. Stevens, V. Hlady, and R. O. Dull, “Fluorescence correlation spectroscopy can probe albumin dynamics inside lung endothelial glycocalyx,” Am. J. Physiol. Lung Cell. Mol. Physiol. 293(2), L328–L335 (2007).
[Crossref] [PubMed]

Hofer, S.

J. Steppan, S. Hofer, B. Funke, T. Brenner, M. Henrich, E. Martin, J. Weitz, U. Hofmann, and M. A. Weigand, “Sepsis and major abdominal surgery lead to flaking of the endothelial glycocalix,” J. Surg. Res. 165(1), 136–141 (2011).
[Crossref] [PubMed]

Hofmann, U.

J. Steppan, S. Hofer, B. Funke, T. Brenner, M. Henrich, E. Martin, J. Weitz, U. Hofmann, and M. A. Weigand, “Sepsis and major abdominal surgery lead to flaking of the endothelial glycocalix,” J. Surg. Res. 165(1), 136–141 (2011).
[Crossref] [PubMed]

Hong, Y. K.

K. Choe, J. Y. Jang, I. Park, Y. Kim, S. Ahn, D. Y. Park, Y. K. Hong, K. Alitalo, G. Y. Koh, and P. Kim, “Intravital imaging of intestinal lacteals unveils lipid drainage through contractility,” J. Clin. Invest. 125(11), 4042–4052 (2015).
[Crossref] [PubMed]

Hsu, R.

T. W. Secomb, R. Hsu, and A. R. Pries, “Motion of red blood cells in a capillary with an endothelial surface layer: effect of flow velocity,” Am. J. Physiol. Heart Circ. Physiol. 281(2), H629–H636 (2001).
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Huber-Lang, M. S.

D. Rittirsch, M. S. Huber-Lang, M. A. Flierl, and P. A. Ward, “Immunodesign of experimental sepsis by cecal ligation and puncture,” Nat. Protoc. 4(1), 31–36 (2009).
[Crossref] [PubMed]

Hudson, L. D.

L. D. Hudson, J. A. Milberg, D. Anardi, and R. J. Maunder, “Clinical risks for development of the acute respiratory distress syndrome,” Am. J. Respir. Crit. Care Med. 151(2), 293–301 (1995).
[Crossref] [PubMed]

Hung, K. E.

P. Kim, E. Chung, H. Yamashita, K. E. Hung, A. Mizoguchi, R. Kucherlapati, D. Fukumura, R. K. Jain, and S. H. Yun, “In vivo wide-area cellular imaging by side-view endomicroscopy,” Nat. Methods 7(4), 303–305 (2010).
[Crossref] [PubMed]

Hwang, Y.

Ince, C.

C. J. Zuurbier, C. Demirci, A. Koeman, H. Vink, and C. Ince, “Short-term hyperglycemia increases endothelial glycocalyx permeability and acutely decreases lineal density of capillaries with flowing red blood cells,” J. Appl. Physiol. 99(4), 1471–1476 (2005).
[Crossref] [PubMed]

Jacob, M.

B. F. Becker, D. Chappell, D. Bruegger, T. Annecke, and M. Jacob, “Therapeutic strategies targeting the endothelial glycocalyx: acute deficits, but great potential,” Cardiovasc. Res. 87(2), 300–310 (2010).
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M. Rehm, D. Bruegger, F. Christ, P. Conzen, M. Thiel, M. Jacob, D. Chappell, M. Stoeckelhuber, U. Welsch, B. Reichart, K. Peter, and B. F. Becker, “Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia,” Circulation 116(17), 1896–1906 (2007).
[Crossref] [PubMed]

Jain, R. K.

P. Kim, E. Chung, H. Yamashita, K. E. Hung, A. Mizoguchi, R. Kucherlapati, D. Fukumura, R. K. Jain, and S. H. Yun, “In vivo wide-area cellular imaging by side-view endomicroscopy,” Nat. Methods 7(4), 303–305 (2010).
[Crossref] [PubMed]

Jang, J. Y.

K. Choe, J. Y. Jang, I. Park, Y. Kim, S. Ahn, D. Y. Park, Y. K. Hong, K. Alitalo, G. Y. Koh, and P. Kim, “Intravital imaging of intestinal lacteals unveils lipid drainage through contractility,” J. Clin. Invest. 125(11), 4042–4052 (2015).
[Crossref] [PubMed]

Janssen, W. J.

E. P. Schmidt, Y. Yang, W. J. Janssen, A. Gandjeva, M. J. Perez, L. Barthel, R. L. Zemans, J. C. Bowman, D. E. Koyanagi, Z. X. Yunt, L. P. Smith, S. S. Cheng, K. H. Overdier, K. R. Thompson, M. W. Geraci, I. S. Douglas, D. B. Pearse, and R. M. Tuder, “The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis,” Nat. Med. 18(8), 1217–1223 (2012).
[Crossref] [PubMed]

Jeong, Y. U.

Johansson, P. I.

P. I. Johansson, J. Stensballe, L. S. Rasmussen, and S. R. Ostrowski, “High circulating adrenaline levels at admission predict increased mortality after trauma,” J. Trauma Acute Care Surg. 72(2), 428–436 (2012).
[Crossref] [PubMed]

Joulin, O.

X. Marechal, R. Favory, O. Joulin, D. Montaigne, S. Hassoun, B. Decoster, F. Zerimech, and R. Neviere, “Endothelial glycocalyx damage during endotoxemia coincides with microcirculatory dysfunction and vascular oxidative stress,” Shock 29(5), 572–576 (2008).
[PubMed]

Jung, K.

K. Jung, P. Kim, F. Leuschner, R. Gorbatov, J. K. Kim, T. Ueno, M. Nahrendorf, and S. H. Yun, “Endoscopic time-lapse imaging of immune cells in infarcted mouse hearts,” Circ. Res. 112(6), 891–899 (2013).
[Crossref] [PubMed]

Kim, J. K.

K. Jung, P. Kim, F. Leuschner, R. Gorbatov, J. K. Kim, T. Ueno, M. Nahrendorf, and S. H. Yun, “Endoscopic time-lapse imaging of immune cells in infarcted mouse hearts,” Circ. Res. 112(6), 891–899 (2013).
[Crossref] [PubMed]

Kim, K.

K. Kim, K. Choe, I. Park, P. Kim, and Y. Park, “Holographic intravital microscopy for 2-D and 3-D imaging intact circulating blood cells in microcapillaries of live mice,” Sci. Rep. 6(1), 33084 (2016).
[Crossref] [PubMed]

Kim, K. H.

Kim, P.

K. Kim, K. Choe, I. Park, P. Kim, and Y. Park, “Holographic intravital microscopy for 2-D and 3-D imaging intact circulating blood cells in microcapillaries of live mice,” Sci. Rep. 6(1), 33084 (2016).
[Crossref] [PubMed]

J. Ahn, K. Choe, T. Wang, Y. Hwang, E. Song, K. H. Kim, and P. Kim, “In vivo longitudinal cellular imaging of small intestine by side-view endomicroscopy,” Biomed. Opt. Express 6(10), 3963–3972 (2015).
[Crossref] [PubMed]

H. Seo, Y. Hwang, K. Choe, and P. Kim, “In vivo quantitation of injected circulating tumor cells from great saphenous vein based on video-rate confocal microscopy,” Biomed. Opt. Express 6(6), 2158–2167 (2015).
[Crossref] [PubMed]

K. Choe, J. Y. Jang, I. Park, Y. Kim, S. Ahn, D. Y. Park, Y. K. Hong, K. Alitalo, G. Y. Koh, and P. Kim, “Intravital imaging of intestinal lacteals unveils lipid drainage through contractility,” J. Clin. Invest. 125(11), 4042–4052 (2015).
[Crossref] [PubMed]

Y. Hwang, J. Ahn, J. Mun, S. Bae, Y. U. Jeong, N. A. Vinokurov, and P. Kim, “In vivo analysis of THz wave irradiation induced acute inflammatory response in skin by laser-scanning confocal microscopy,” Opt. Express 22(10), 11465–11475 (2014).
[Crossref] [PubMed]

K. Jung, P. Kim, F. Leuschner, R. Gorbatov, J. K. Kim, T. Ueno, M. Nahrendorf, and S. H. Yun, “Endoscopic time-lapse imaging of immune cells in infarcted mouse hearts,” Circ. Res. 112(6), 891–899 (2013).
[Crossref] [PubMed]

K. Choe, Y. Hwang, H. Seo, and P. Kim, “In vivo high spatiotemporal resolution visualization of circulating T lymphocytes in high endothelial venules of lymph nodes,” J. Biomed. Opt. 18(3), 036005 (2013).
[Crossref] [PubMed]

P. Kim, E. Chung, H. Yamashita, K. E. Hung, A. Mizoguchi, R. Kucherlapati, D. Fukumura, R. K. Jain, and S. H. Yun, “In vivo wide-area cellular imaging by side-view endomicroscopy,” Nat. Methods 7(4), 303–305 (2010).
[Crossref] [PubMed]

P. Kim, M. Puoris’haag, D. Côté, C. P. Lin, and S. H. Yun, “In vivo confocal and multiphoton microendoscopy,” J. Biomed. Opt. 13(1), 010501 (2008).
[Crossref] [PubMed]

Kim, Y.

K. Choe, J. Y. Jang, I. Park, Y. Kim, S. Ahn, D. Y. Park, Y. K. Hong, K. Alitalo, G. Y. Koh, and P. Kim, “Intravital imaging of intestinal lacteals unveils lipid drainage through contractility,” J. Clin. Invest. 125(11), 4042–4052 (2015).
[Crossref] [PubMed]

King, J.

J. King, T. Hamil, J. Creighton, S. Wu, P. Bhat, F. McDonald, and T. Stevens, “Structural and functional characteristics of lung macro- and microvascular endothelial cell phenotypes,” Microvasc. Res. 67(2), 139–151 (2004).
[Crossref] [PubMed]

Koch, K.

B. Afessa, B. Green, I. Delke, and K. Koch, “Systemic inflammatory response syndrome, organ failure, and outcome in critically ill obstetric patients treated in an ICU,” Chest 120(4), 1271–1277 (2001).
[Crossref] [PubMed]

Koeman, A.

C. J. Zuurbier, C. Demirci, A. Koeman, H. Vink, and C. Ince, “Short-term hyperglycemia increases endothelial glycocalyx permeability and acutely decreases lineal density of capillaries with flowing red blood cells,” J. Appl. Physiol. 99(4), 1471–1476 (2005).
[Crossref] [PubMed]

Koh, G. Y.

K. Choe, J. Y. Jang, I. Park, Y. Kim, S. Ahn, D. Y. Park, Y. K. Hong, K. Alitalo, G. Y. Koh, and P. Kim, “Intravital imaging of intestinal lacteals unveils lipid drainage through contractility,” J. Clin. Invest. 125(11), 4042–4052 (2015).
[Crossref] [PubMed]

Koyanagi, D. E.

E. P. Schmidt, Y. Yang, W. J. Janssen, A. Gandjeva, M. J. Perez, L. Barthel, R. L. Zemans, J. C. Bowman, D. E. Koyanagi, Z. X. Yunt, L. P. Smith, S. S. Cheng, K. H. Overdier, K. R. Thompson, M. W. Geraci, I. S. Douglas, D. B. Pearse, and R. M. Tuder, “The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis,” Nat. Med. 18(8), 1217–1223 (2012).
[Crossref] [PubMed]

Krummel, M. F.

M. R. Looney, E. E. Thornton, D. Sen, W. J. Lamm, R. W. Glenny, and M. F. Krummel, “Stabilized imaging of immune surveillance in the mouse lung,” Nat. Methods 8(1), 91–96 (2011).
[Crossref] [PubMed]

Kucherlapati, R.

P. Kim, E. Chung, H. Yamashita, K. E. Hung, A. Mizoguchi, R. Kucherlapati, D. Fukumura, R. K. Jain, and S. H. Yun, “In vivo wide-area cellular imaging by side-view endomicroscopy,” Nat. Methods 7(4), 303–305 (2010).
[Crossref] [PubMed]

Kuebler, W. M.

G. Matute-Bello, G. Downey, B. B. Moore, S. D. Groshong, M. A. Matthay, A. S. Slutsky, W. M. Kuebler, and G. Acute Lung Injury in Animals Study Group, “An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals,” Am. J. Respir. Cell Mol. Biol. 44(5), 725–738 (2011).
[Crossref] [PubMed]

Lamm, W. J.

M. R. Looney, E. E. Thornton, D. Sen, W. J. Lamm, R. W. Glenny, and M. F. Krummel, “Stabilized imaging of immune surveillance in the mouse lung,” Nat. Methods 8(1), 91–96 (2011).
[Crossref] [PubMed]

W. J. Lamm, S. L. Bernard, W. W. Wagner, and R. W. Glenny, “Intravital microscopic observations of 15-microm microspheres lodging in the pulmonary microcirculation,” J. Appl. Physiol. 98(6), 2242–2248 (2005).
[Crossref] [PubMed]

Lee, D. H.

D. H. Lee, M. J. Dane, B. M. van den Berg, M. G. Boels, J. W. van Teeffelen, R. de Mutsert, M. den Heijer, F. R. Rosendaal, J. van der Vlag, A. J. van Zonneveld, H. Vink, T. J. Rabelink, and NEO study group, “Deeper penetration of erythrocytes into the endothelial glycocalyx is associated with impaired microvascular perfusion,” PLoS One 9(5), e96477 (2014).
[Crossref] [PubMed]

Lee, S.

C. Vinegoni, S. Lee, R. Gorbatov, and R. Weissleder, “Motion compensation using a suctioning stabilizer for intravital microscopy,” Intravital 1(2), 115–121 (2012).
[Crossref] [PubMed]

Leuschner, F.

K. Jung, P. Kim, F. Leuschner, R. Gorbatov, J. K. Kim, T. Ueno, M. Nahrendorf, and S. H. Yun, “Endoscopic time-lapse imaging of immune cells in infarcted mouse hearts,” Circ. Res. 112(6), 891–899 (2013).
[Crossref] [PubMed]

Li, G.

E. P. Schmidt, G. Li, L. Li, L. Fu, Y. Yang, K. H. Overdier, I. S. Douglas, and R. J. Linhardt, “The circulating glycosaminoglycan signature of respiratory failure in critically ill adults,” J. Biol. Chem. 289(12), 8194–8202 (2014).
[Crossref] [PubMed]

Li, L.

E. P. Schmidt, G. Li, L. Li, L. Fu, Y. Yang, K. H. Overdier, I. S. Douglas, and R. J. Linhardt, “The circulating glycosaminoglycan signature of respiratory failure in critically ill adults,” J. Biol. Chem. 289(12), 8194–8202 (2014).
[Crossref] [PubMed]

Lin, C. P.

P. Kim, M. Puoris’haag, D. Côté, C. P. Lin, and S. H. Yun, “In vivo confocal and multiphoton microendoscopy,” J. Biomed. Opt. 13(1), 010501 (2008).
[Crossref] [PubMed]

Lin, L.

E. P. Schmidt, K. H. Overdier, X. Sun, L. Lin, X. Liu, Y. Yang, L. A. Ammons, T. D. Hiller, M. A. Suflita, Y. Yu, Y. Chen, F. Zhang, C. Cothren Burlew, C. L. Edelstein, I. S. Douglas, and R. J. Linhardt, “Urinary Glycosaminoglycans Predict Outcomes in Septic Shock and Acute Respiratory Distress Syndrome,” Am. J. Respir. Crit. Care Med. 194(4), 439–449 (2016).
[Crossref] [PubMed]

Linhardt, R. J.

E. P. Schmidt, K. H. Overdier, X. Sun, L. Lin, X. Liu, Y. Yang, L. A. Ammons, T. D. Hiller, M. A. Suflita, Y. Yu, Y. Chen, F. Zhang, C. Cothren Burlew, C. L. Edelstein, I. S. Douglas, and R. J. Linhardt, “Urinary Glycosaminoglycans Predict Outcomes in Septic Shock and Acute Respiratory Distress Syndrome,” Am. J. Respir. Crit. Care Med. 194(4), 439–449 (2016).
[Crossref] [PubMed]

E. P. Schmidt, G. Li, L. Li, L. Fu, Y. Yang, K. H. Overdier, I. S. Douglas, and R. J. Linhardt, “The circulating glycosaminoglycan signature of respiratory failure in critically ill adults,” J. Biol. Chem. 289(12), 8194–8202 (2014).
[Crossref] [PubMed]

Liu, X.

E. P. Schmidt, K. H. Overdier, X. Sun, L. Lin, X. Liu, Y. Yang, L. A. Ammons, T. D. Hiller, M. A. Suflita, Y. Yu, Y. Chen, F. Zhang, C. Cothren Burlew, C. L. Edelstein, I. S. Douglas, and R. J. Linhardt, “Urinary Glycosaminoglycans Predict Outcomes in Septic Shock and Acute Respiratory Distress Syndrome,” Am. J. Respir. Crit. Care Med. 194(4), 439–449 (2016).
[Crossref] [PubMed]

Ljunggren, L.

A. Nelson, I. Berkestedt, A. Schmidtchen, L. Ljunggren, and M. Bodelsson, “Increased levels of glycosaminoglycans during septic shock: relation to mortality and the antibacterial actions of plasma,” Shock 30(6), 623–627 (2008).
[Crossref] [PubMed]

Looney, M. R.

M. R. Looney and J. Bhattacharya, “Live imaging of the lung,” Annu. Rev. Physiol. 76(1), 431–445 (2014).
[Crossref] [PubMed]

M. R. Looney, E. E. Thornton, D. Sen, W. J. Lamm, R. W. Glenny, and M. F. Krummel, “Stabilized imaging of immune surveillance in the mouse lung,” Nat. Methods 8(1), 91–96 (2011).
[Crossref] [PubMed]

Marechal, X.

X. Marechal, R. Favory, O. Joulin, D. Montaigne, S. Hassoun, B. Decoster, F. Zerimech, and R. Neviere, “Endothelial glycocalyx damage during endotoxemia coincides with microcirculatory dysfunction and vascular oxidative stress,” Shock 29(5), 572–576 (2008).
[PubMed]

Martin, E.

J. Steppan, S. Hofer, B. Funke, T. Brenner, M. Henrich, E. Martin, J. Weitz, U. Hofmann, and M. A. Weigand, “Sepsis and major abdominal surgery lead to flaking of the endothelial glycocalix,” J. Surg. Res. 165(1), 136–141 (2011).
[Crossref] [PubMed]

Matthay, M. A.

G. Matute-Bello, G. Downey, B. B. Moore, S. D. Groshong, M. A. Matthay, A. S. Slutsky, W. M. Kuebler, and G. Acute Lung Injury in Animals Study Group, “An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals,” Am. J. Respir. Cell Mol. Biol. 44(5), 725–738 (2011).
[Crossref] [PubMed]

Matute-Bello, G.

G. Matute-Bello, G. Downey, B. B. Moore, S. D. Groshong, M. A. Matthay, A. S. Slutsky, W. M. Kuebler, and G. Acute Lung Injury in Animals Study Group, “An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals,” Am. J. Respir. Cell Mol. Biol. 44(5), 725–738 (2011).
[Crossref] [PubMed]

Maunder, R. J.

L. D. Hudson, J. A. Milberg, D. Anardi, and R. J. Maunder, “Clinical risks for development of the acute respiratory distress syndrome,” Am. J. Respir. Crit. Care Med. 151(2), 293–301 (1995).
[Crossref] [PubMed]

McDonald, F.

J. King, T. Hamil, J. Creighton, S. Wu, P. Bhat, F. McDonald, and T. Stevens, “Structural and functional characteristics of lung macro- and microvascular endothelial cell phenotypes,” Microvasc. Res. 67(2), 139–151 (2004).
[Crossref] [PubMed]

Milberg, J. A.

L. D. Hudson, J. A. Milberg, D. Anardi, and R. J. Maunder, “Clinical risks for development of the acute respiratory distress syndrome,” Am. J. Respir. Crit. Care Med. 151(2), 293–301 (1995).
[Crossref] [PubMed]

Mizoguchi, A.

P. Kim, E. Chung, H. Yamashita, K. E. Hung, A. Mizoguchi, R. Kucherlapati, D. Fukumura, R. K. Jain, and S. H. Yun, “In vivo wide-area cellular imaging by side-view endomicroscopy,” Nat. Methods 7(4), 303–305 (2010).
[Crossref] [PubMed]

Montaigne, D.

X. Marechal, R. Favory, O. Joulin, D. Montaigne, S. Hassoun, B. Decoster, F. Zerimech, and R. Neviere, “Endothelial glycocalyx damage during endotoxemia coincides with microcirculatory dysfunction and vascular oxidative stress,” Shock 29(5), 572–576 (2008).
[PubMed]

Moore, B. B.

G. Matute-Bello, G. Downey, B. B. Moore, S. D. Groshong, M. A. Matthay, A. S. Slutsky, W. M. Kuebler, and G. Acute Lung Injury in Animals Study Group, “An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals,” Am. J. Respir. Cell Mol. Biol. 44(5), 725–738 (2011).
[Crossref] [PubMed]

Moser, M.

S. Grundmann, K. Fink, L. Rabadzhieva, N. Bourgeois, T. Schwab, M. Moser, C. Bode, and H. J. Busch, “Perturbation of the endothelial glycocalyx in post cardiac arrest syndrome,” Resuscitation 83(6), 715–720 (2012).
[Crossref] [PubMed]

Mun, J.

Nahrendorf, M.

K. Jung, P. Kim, F. Leuschner, R. Gorbatov, J. K. Kim, T. Ueno, M. Nahrendorf, and S. H. Yun, “Endoscopic time-lapse imaging of immune cells in infarcted mouse hearts,” Circ. Res. 112(6), 891–899 (2013).
[Crossref] [PubMed]

Nelson, A.

A. Nelson, I. Berkestedt, A. Schmidtchen, L. Ljunggren, and M. Bodelsson, “Increased levels of glycosaminoglycans during septic shock: relation to mortality and the antibacterial actions of plasma,” Shock 30(6), 623–627 (2008).
[Crossref] [PubMed]

Neviere, R.

X. Marechal, R. Favory, O. Joulin, D. Montaigne, S. Hassoun, B. Decoster, F. Zerimech, and R. Neviere, “Endothelial glycocalyx damage during endotoxemia coincides with microcirculatory dysfunction and vascular oxidative stress,” Shock 29(5), 572–576 (2008).
[PubMed]

Noguchi, H.

H. Noguchi and G. Gompper, “Shape transitions of fluid vesicles and red blood cells in capillary flows,” Proc. Natl. Acad. Sci. U.S.A. 102(40), 14159–14164 (2005).
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Oksala, N.

M. Sallisalmi, J. Tenhunen, R. Yang, N. Oksala, and V. Pettilä, “Vascular adhesion protein-1 and syndecan-1 in septic shock,” Acta Anaesthesiol. Scand. 56(3), 316–322 (2012).
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Ostrowski, S. R.

P. I. Johansson, J. Stensballe, L. S. Rasmussen, and S. R. Ostrowski, “High circulating adrenaline levels at admission predict increased mortality after trauma,” J. Trauma Acute Care Surg. 72(2), 428–436 (2012).
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oude Egbrink, M. G.

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E. P. Schmidt, K. H. Overdier, X. Sun, L. Lin, X. Liu, Y. Yang, L. A. Ammons, T. D. Hiller, M. A. Suflita, Y. Yu, Y. Chen, F. Zhang, C. Cothren Burlew, C. L. Edelstein, I. S. Douglas, and R. J. Linhardt, “Urinary Glycosaminoglycans Predict Outcomes in Septic Shock and Acute Respiratory Distress Syndrome,” Am. J. Respir. Crit. Care Med. 194(4), 439–449 (2016).
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E. P. Schmidt, G. Li, L. Li, L. Fu, Y. Yang, K. H. Overdier, I. S. Douglas, and R. J. Linhardt, “The circulating glycosaminoglycan signature of respiratory failure in critically ill adults,” J. Biol. Chem. 289(12), 8194–8202 (2014).
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K. Kim, K. Choe, I. Park, P. Kim, and Y. Park, “Holographic intravital microscopy for 2-D and 3-D imaging intact circulating blood cells in microcapillaries of live mice,” Sci. Rep. 6(1), 33084 (2016).
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E. P. Schmidt, Y. Yang, W. J. Janssen, A. Gandjeva, M. J. Perez, L. Barthel, R. L. Zemans, J. C. Bowman, D. E. Koyanagi, Z. X. Yunt, L. P. Smith, S. S. Cheng, K. H. Overdier, K. R. Thompson, M. W. Geraci, I. S. Douglas, D. B. Pearse, and R. M. Tuder, “The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis,” Nat. Med. 18(8), 1217–1223 (2012).
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M. Sallisalmi, J. Tenhunen, R. Yang, N. Oksala, and V. Pettilä, “Vascular adhesion protein-1 and syndecan-1 in septic shock,” Acta Anaesthesiol. Scand. 56(3), 316–322 (2012).
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T. W. Secomb, R. Hsu, and A. R. Pries, “Motion of red blood cells in a capillary with an endothelial surface layer: effect of flow velocity,” Am. J. Physiol. Heart Circ. Physiol. 281(2), H629–H636 (2001).
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D. H. Lee, M. J. Dane, B. M. van den Berg, M. G. Boels, J. W. van Teeffelen, R. de Mutsert, M. den Heijer, F. R. Rosendaal, J. van der Vlag, A. J. van Zonneveld, H. Vink, T. J. Rabelink, and NEO study group, “Deeper penetration of erythrocytes into the endothelial glycocalyx is associated with impaired microvascular perfusion,” PLoS One 9(5), e96477 (2014).
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S. Reitsma, D. W. Slaaf, H. Vink, M. A. van Zandvoort, and M. G. oude Egbrink, “The endothelial glycocalyx: composition, functions, and visualization,” Pflugers Arch. 454(3), 345–359 (2007).
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D. Rittirsch, M. S. Huber-Lang, M. A. Flierl, and P. A. Ward, “Immunodesign of experimental sepsis by cecal ligation and puncture,” Nat. Protoc. 4(1), 31–36 (2009).
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D. H. Lee, M. J. Dane, B. M. van den Berg, M. G. Boels, J. W. van Teeffelen, R. de Mutsert, M. den Heijer, F. R. Rosendaal, J. van der Vlag, A. J. van Zonneveld, H. Vink, T. J. Rabelink, and NEO study group, “Deeper penetration of erythrocytes into the endothelial glycocalyx is associated with impaired microvascular perfusion,” PLoS One 9(5), e96477 (2014).
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M. Sallisalmi, J. Tenhunen, R. Yang, N. Oksala, and V. Pettilä, “Vascular adhesion protein-1 and syndecan-1 in septic shock,” Acta Anaesthesiol. Scand. 56(3), 316–322 (2012).
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E. P. Schmidt, K. H. Overdier, X. Sun, L. Lin, X. Liu, Y. Yang, L. A. Ammons, T. D. Hiller, M. A. Suflita, Y. Yu, Y. Chen, F. Zhang, C. Cothren Burlew, C. L. Edelstein, I. S. Douglas, and R. J. Linhardt, “Urinary Glycosaminoglycans Predict Outcomes in Septic Shock and Acute Respiratory Distress Syndrome,” Am. J. Respir. Crit. Care Med. 194(4), 439–449 (2016).
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A. D. Aguirre, C. Vinegoni, M. Sebas, and R. Weissleder, “Intravital imaging of cardiac function at the single-cell level,” Proc. Natl. Acad. Sci. U.S.A. 111(31), 11257–11262 (2014).
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B. M. van den Berg, H. Vink, and J. A. Spaan, “The endothelial glycocalyx protects against myocardial edema,” Circ. Res. 92(6), 592–594 (2003).
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Y. Han, S. Weinbaum, J. A. E. Spaan, and H. Vink, “Large-deformation analysis of the elastic recoil of fibre layers in a Brinkman medium with application to the endothelial glycocalyx,” J. Fluid Mech. 554(-1), 217 (2006).
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P. I. Johansson, J. Stensballe, L. S. Rasmussen, and S. R. Ostrowski, “High circulating adrenaline levels at admission predict increased mortality after trauma,” J. Trauma Acute Care Surg. 72(2), 428–436 (2012).
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J. Steppan, S. Hofer, B. Funke, T. Brenner, M. Henrich, E. Martin, J. Weitz, U. Hofmann, and M. A. Weigand, “Sepsis and major abdominal surgery lead to flaking of the endothelial glycocalix,” J. Surg. Res. 165(1), 136–141 (2011).
[Crossref] [PubMed]

Weinbaum, S.

S. Weinbaum, J. M. Tarbell, and E. R. Damiano, “The structure and function of the endothelial glycocalyx layer,” Annu. Rev. Biomed. Eng. 9(1), 121–167 (2007).
[Crossref] [PubMed]

Y. Han, S. Weinbaum, J. A. E. Spaan, and H. Vink, “Large-deformation analysis of the elastic recoil of fibre layers in a Brinkman medium with application to the endothelial glycocalyx,” J. Fluid Mech. 554(-1), 217 (2006).
[Crossref]

S. Weinbaum, X. Zhang, Y. Han, H. Vink, and S. C. Cowin, “Mechanotransduction and flow across the endothelial glycocalyx,” Proc. Natl. Acad. Sci. U.S.A. 100(13), 7988–7995 (2003).
[Crossref] [PubMed]

Weissleder, R.

A. D. Aguirre, C. Vinegoni, M. Sebas, and R. Weissleder, “Intravital imaging of cardiac function at the single-cell level,” Proc. Natl. Acad. Sci. U.S.A. 111(31), 11257–11262 (2014).
[Crossref] [PubMed]

C. Vinegoni, S. Lee, R. Gorbatov, and R. Weissleder, “Motion compensation using a suctioning stabilizer for intravital microscopy,” Intravital 1(2), 115–121 (2012).
[Crossref] [PubMed]

Weitz, J.

J. Steppan, S. Hofer, B. Funke, T. Brenner, M. Henrich, E. Martin, J. Weitz, U. Hofmann, and M. A. Weigand, “Sepsis and major abdominal surgery lead to flaking of the endothelial glycocalix,” J. Surg. Res. 165(1), 136–141 (2011).
[Crossref] [PubMed]

Welsch, U.

M. Rehm, D. Bruegger, F. Christ, P. Conzen, M. Thiel, M. Jacob, D. Chappell, M. Stoeckelhuber, U. Welsch, B. Reichart, K. Peter, and B. F. Becker, “Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia,” Circulation 116(17), 1896–1906 (2007).
[Crossref] [PubMed]

Wu, S.

J. King, T. Hamil, J. Creighton, S. Wu, P. Bhat, F. McDonald, and T. Stevens, “Structural and functional characteristics of lung macro- and microvascular endothelial cell phenotypes,” Microvasc. Res. 67(2), 139–151 (2004).
[Crossref] [PubMed]

Yamashita, H.

P. Kim, E. Chung, H. Yamashita, K. E. Hung, A. Mizoguchi, R. Kucherlapati, D. Fukumura, R. K. Jain, and S. H. Yun, “In vivo wide-area cellular imaging by side-view endomicroscopy,” Nat. Methods 7(4), 303–305 (2010).
[Crossref] [PubMed]

Yang, R.

M. Sallisalmi, J. Tenhunen, R. Yang, N. Oksala, and V. Pettilä, “Vascular adhesion protein-1 and syndecan-1 in septic shock,” Acta Anaesthesiol. Scand. 56(3), 316–322 (2012).
[Crossref] [PubMed]

Yang, Y.

E. P. Schmidt, K. H. Overdier, X. Sun, L. Lin, X. Liu, Y. Yang, L. A. Ammons, T. D. Hiller, M. A. Suflita, Y. Yu, Y. Chen, F. Zhang, C. Cothren Burlew, C. L. Edelstein, I. S. Douglas, and R. J. Linhardt, “Urinary Glycosaminoglycans Predict Outcomes in Septic Shock and Acute Respiratory Distress Syndrome,” Am. J. Respir. Crit. Care Med. 194(4), 439–449 (2016).
[Crossref] [PubMed]

S. M. Haeger, Y. Yang, and E. P. Schmidt, “Heparan Sulfate in the Developing, Healthy, and Injured Lung,” Am. J. Respir. Cell Mol. Biol. 55(1), 5–11 (2016).
[Crossref] [PubMed]

E. P. Schmidt, G. Li, L. Li, L. Fu, Y. Yang, K. H. Overdier, I. S. Douglas, and R. J. Linhardt, “The circulating glycosaminoglycan signature of respiratory failure in critically ill adults,” J. Biol. Chem. 289(12), 8194–8202 (2014).
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E. P. Schmidt, Y. Yang, W. J. Janssen, A. Gandjeva, M. J. Perez, L. Barthel, R. L. Zemans, J. C. Bowman, D. E. Koyanagi, Z. X. Yunt, L. P. Smith, S. S. Cheng, K. H. Overdier, K. R. Thompson, M. W. Geraci, I. S. Douglas, D. B. Pearse, and R. M. Tuder, “The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis,” Nat. Med. 18(8), 1217–1223 (2012).
[Crossref] [PubMed]

Yu, Y.

E. P. Schmidt, K. H. Overdier, X. Sun, L. Lin, X. Liu, Y. Yang, L. A. Ammons, T. D. Hiller, M. A. Suflita, Y. Yu, Y. Chen, F. Zhang, C. Cothren Burlew, C. L. Edelstein, I. S. Douglas, and R. J. Linhardt, “Urinary Glycosaminoglycans Predict Outcomes in Septic Shock and Acute Respiratory Distress Syndrome,” Am. J. Respir. Crit. Care Med. 194(4), 439–449 (2016).
[Crossref] [PubMed]

Yun, S. H.

K. Jung, P. Kim, F. Leuschner, R. Gorbatov, J. K. Kim, T. Ueno, M. Nahrendorf, and S. H. Yun, “Endoscopic time-lapse imaging of immune cells in infarcted mouse hearts,” Circ. Res. 112(6), 891–899 (2013).
[Crossref] [PubMed]

P. Kim, E. Chung, H. Yamashita, K. E. Hung, A. Mizoguchi, R. Kucherlapati, D. Fukumura, R. K. Jain, and S. H. Yun, “In vivo wide-area cellular imaging by side-view endomicroscopy,” Nat. Methods 7(4), 303–305 (2010).
[Crossref] [PubMed]

P. Kim, M. Puoris’haag, D. Côté, C. P. Lin, and S. H. Yun, “In vivo confocal and multiphoton microendoscopy,” J. Biomed. Opt. 13(1), 010501 (2008).
[Crossref] [PubMed]

Yunt, Z. X.

E. P. Schmidt, Y. Yang, W. J. Janssen, A. Gandjeva, M. J. Perez, L. Barthel, R. L. Zemans, J. C. Bowman, D. E. Koyanagi, Z. X. Yunt, L. P. Smith, S. S. Cheng, K. H. Overdier, K. R. Thompson, M. W. Geraci, I. S. Douglas, D. B. Pearse, and R. M. Tuder, “The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis,” Nat. Med. 18(8), 1217–1223 (2012).
[Crossref] [PubMed]

Zemans, R. L.

E. P. Schmidt, Y. Yang, W. J. Janssen, A. Gandjeva, M. J. Perez, L. Barthel, R. L. Zemans, J. C. Bowman, D. E. Koyanagi, Z. X. Yunt, L. P. Smith, S. S. Cheng, K. H. Overdier, K. R. Thompson, M. W. Geraci, I. S. Douglas, D. B. Pearse, and R. M. Tuder, “The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis,” Nat. Med. 18(8), 1217–1223 (2012).
[Crossref] [PubMed]

Zerimech, F.

X. Marechal, R. Favory, O. Joulin, D. Montaigne, S. Hassoun, B. Decoster, F. Zerimech, and R. Neviere, “Endothelial glycocalyx damage during endotoxemia coincides with microcirculatory dysfunction and vascular oxidative stress,” Shock 29(5), 572–576 (2008).
[PubMed]

Zhang, F.

E. P. Schmidt, K. H. Overdier, X. Sun, L. Lin, X. Liu, Y. Yang, L. A. Ammons, T. D. Hiller, M. A. Suflita, Y. Yu, Y. Chen, F. Zhang, C. Cothren Burlew, C. L. Edelstein, I. S. Douglas, and R. J. Linhardt, “Urinary Glycosaminoglycans Predict Outcomes in Septic Shock and Acute Respiratory Distress Syndrome,” Am. J. Respir. Crit. Care Med. 194(4), 439–449 (2016).
[Crossref] [PubMed]

Zhang, X.

S. Weinbaum, X. Zhang, Y. Han, H. Vink, and S. C. Cowin, “Mechanotransduction and flow across the endothelial glycocalyx,” Proc. Natl. Acad. Sci. U.S.A. 100(13), 7988–7995 (2003).
[Crossref] [PubMed]

Zuurbier, C. J.

C. J. Zuurbier, C. Demirci, A. Koeman, H. Vink, and C. Ince, “Short-term hyperglycemia increases endothelial glycocalyx permeability and acutely decreases lineal density of capillaries with flowing red blood cells,” J. Appl. Physiol. 99(4), 1471–1476 (2005).
[Crossref] [PubMed]

Acta Anaesthesiol. Scand. (1)

M. Sallisalmi, J. Tenhunen, R. Yang, N. Oksala, and V. Pettilä, “Vascular adhesion protein-1 and syndecan-1 in septic shock,” Acta Anaesthesiol. Scand. 56(3), 316–322 (2012).
[Crossref] [PubMed]

Am. J. Physiol. Heart Circ. Physiol. (2)

T. W. Secomb, R. Hsu, and A. R. Pries, “Motion of red blood cells in a capillary with an endothelial surface layer: effect of flow velocity,” Am. J. Physiol. Heart Circ. Physiol. 281(2), H629–H636 (2001).
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H. Vink and B. R. Duling, “Capillary endothelial surface layer selectively reduces plasma solute distribution volume,” Am. J. Physiol. Heart Circ. Physiol. 278(1), H285–H289 (2000).
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Am. J. Physiol. Lung Cell. Mol. Physiol. (1)

A. P. Stevens, V. Hlady, and R. O. Dull, “Fluorescence correlation spectroscopy can probe albumin dynamics inside lung endothelial glycocalyx,” Am. J. Physiol. Lung Cell. Mol. Physiol. 293(2), L328–L335 (2007).
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Am. J. Respir. Cell Mol. Biol. (3)

A. N. Rizzo and S. M. Dudek, “Endothelial Glycocalyx Repair: Building a Wall to Protect the Lung during Sepsis,” Am. J. Respir. Cell Mol. Biol. 56(6), 687–688 (2017).
[Crossref] [PubMed]

S. M. Haeger, Y. Yang, and E. P. Schmidt, “Heparan Sulfate in the Developing, Healthy, and Injured Lung,” Am. J. Respir. Cell Mol. Biol. 55(1), 5–11 (2016).
[Crossref] [PubMed]

G. Matute-Bello, G. Downey, B. B. Moore, S. D. Groshong, M. A. Matthay, A. S. Slutsky, W. M. Kuebler, and G. Acute Lung Injury in Animals Study Group, “An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals,” Am. J. Respir. Cell Mol. Biol. 44(5), 725–738 (2011).
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Am. J. Respir. Crit. Care Med. (2)

E. P. Schmidt, K. H. Overdier, X. Sun, L. Lin, X. Liu, Y. Yang, L. A. Ammons, T. D. Hiller, M. A. Suflita, Y. Yu, Y. Chen, F. Zhang, C. Cothren Burlew, C. L. Edelstein, I. S. Douglas, and R. J. Linhardt, “Urinary Glycosaminoglycans Predict Outcomes in Septic Shock and Acute Respiratory Distress Syndrome,” Am. J. Respir. Crit. Care Med. 194(4), 439–449 (2016).
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Annu. Rev. Biomed. Eng. (1)

S. Weinbaum, J. M. Tarbell, and E. R. Damiano, “The structure and function of the endothelial glycocalyx layer,” Annu. Rev. Biomed. Eng. 9(1), 121–167 (2007).
[Crossref] [PubMed]

Annu. Rev. Physiol. (1)

M. R. Looney and J. Bhattacharya, “Live imaging of the lung,” Annu. Rev. Physiol. 76(1), 431–445 (2014).
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Biomed. Opt. Express (2)

Cardiovasc. Res. (2)

B. F. Becker, D. Chappell, D. Bruegger, T. Annecke, and M. Jacob, “Therapeutic strategies targeting the endothelial glycocalyx: acute deficits, but great potential,” Cardiovasc. Res. 87(2), 300–310 (2010).
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J. W. VanTeeffelen, J. Brands, and H. Vink, “Agonist-induced impairment of glycocalyx exclusion properties: contribution to coronary effects of adenosine,” Cardiovasc. Res. 87(2), 311–319 (2010).
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Chest (1)

B. Afessa, B. Green, I. Delke, and K. Koch, “Systemic inflammatory response syndrome, organ failure, and outcome in critically ill obstetric patients treated in an ICU,” Chest 120(4), 1271–1277 (2001).
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Circ. Res. (4)

D. R. Potter and E. R. Damiano, “The hydrodynamically relevant endothelial cell glycocalyx observed in vivo is absent in vitro,” Circ. Res. 102(7), 770–776 (2008).
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H. Vink and B. R. Duling, “Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries,” Circ. Res. 79(3), 581–589 (1996).
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B. M. van den Berg, H. Vink, and J. A. Spaan, “The endothelial glycocalyx protects against myocardial edema,” Circ. Res. 92(6), 592–594 (2003).
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K. Jung, P. Kim, F. Leuschner, R. Gorbatov, J. K. Kim, T. Ueno, M. Nahrendorf, and S. H. Yun, “Endoscopic time-lapse imaging of immune cells in infarcted mouse hearts,” Circ. Res. 112(6), 891–899 (2013).
[Crossref] [PubMed]

Circulation (1)

M. Rehm, D. Bruegger, F. Christ, P. Conzen, M. Thiel, M. Jacob, D. Chappell, M. Stoeckelhuber, U. Welsch, B. Reichart, K. Peter, and B. F. Becker, “Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia,” Circulation 116(17), 1896–1906 (2007).
[Crossref] [PubMed]

Crit. Care (1)

A. Burke-Gaffney and T. W. Evans, “Lest we forget the endothelial glycocalyx in sepsis,” Crit. Care 16(2), 121 (2012).
[Crossref] [PubMed]

Intravital (1)

C. Vinegoni, S. Lee, R. Gorbatov, and R. Weissleder, “Motion compensation using a suctioning stabilizer for intravital microscopy,” Intravital 1(2), 115–121 (2012).
[Crossref] [PubMed]

J. Appl. Physiol. (2)

C. J. Zuurbier, C. Demirci, A. Koeman, H. Vink, and C. Ince, “Short-term hyperglycemia increases endothelial glycocalyx permeability and acutely decreases lineal density of capillaries with flowing red blood cells,” J. Appl. Physiol. 99(4), 1471–1476 (2005).
[Crossref] [PubMed]

W. J. Lamm, S. L. Bernard, W. W. Wagner, and R. W. Glenny, “Intravital microscopic observations of 15-microm microspheres lodging in the pulmonary microcirculation,” J. Appl. Physiol. 98(6), 2242–2248 (2005).
[Crossref] [PubMed]

J. Biol. Chem. (1)

E. P. Schmidt, G. Li, L. Li, L. Fu, Y. Yang, K. H. Overdier, I. S. Douglas, and R. J. Linhardt, “The circulating glycosaminoglycan signature of respiratory failure in critically ill adults,” J. Biol. Chem. 289(12), 8194–8202 (2014).
[Crossref] [PubMed]

J. Biomed. Opt. (2)

P. Kim, M. Puoris’haag, D. Côté, C. P. Lin, and S. H. Yun, “In vivo confocal and multiphoton microendoscopy,” J. Biomed. Opt. 13(1), 010501 (2008).
[Crossref] [PubMed]

K. Choe, Y. Hwang, H. Seo, and P. Kim, “In vivo high spatiotemporal resolution visualization of circulating T lymphocytes in high endothelial venules of lymph nodes,” J. Biomed. Opt. 18(3), 036005 (2013).
[Crossref] [PubMed]

J. Clin. Invest. (1)

K. Choe, J. Y. Jang, I. Park, Y. Kim, S. Ahn, D. Y. Park, Y. K. Hong, K. Alitalo, G. Y. Koh, and P. Kim, “Intravital imaging of intestinal lacteals unveils lipid drainage through contractility,” J. Clin. Invest. 125(11), 4042–4052 (2015).
[Crossref] [PubMed]

J. Fluid Mech. (1)

Y. Han, S. Weinbaum, J. A. E. Spaan, and H. Vink, “Large-deformation analysis of the elastic recoil of fibre layers in a Brinkman medium with application to the endothelial glycocalyx,” J. Fluid Mech. 554(-1), 217 (2006).
[Crossref]

J. Surg. Res. (1)

J. Steppan, S. Hofer, B. Funke, T. Brenner, M. Henrich, E. Martin, J. Weitz, U. Hofmann, and M. A. Weigand, “Sepsis and major abdominal surgery lead to flaking of the endothelial glycocalix,” J. Surg. Res. 165(1), 136–141 (2011).
[Crossref] [PubMed]

J. Trauma Acute Care Surg. (1)

P. I. Johansson, J. Stensballe, L. S. Rasmussen, and S. R. Ostrowski, “High circulating adrenaline levels at admission predict increased mortality after trauma,” J. Trauma Acute Care Surg. 72(2), 428–436 (2012).
[Crossref] [PubMed]

Microvasc. Res. (1)

J. King, T. Hamil, J. Creighton, S. Wu, P. Bhat, F. McDonald, and T. Stevens, “Structural and functional characteristics of lung macro- and microvascular endothelial cell phenotypes,” Microvasc. Res. 67(2), 139–151 (2004).
[Crossref] [PubMed]

Nat. Med. (1)

E. P. Schmidt, Y. Yang, W. J. Janssen, A. Gandjeva, M. J. Perez, L. Barthel, R. L. Zemans, J. C. Bowman, D. E. Koyanagi, Z. X. Yunt, L. P. Smith, S. S. Cheng, K. H. Overdier, K. R. Thompson, M. W. Geraci, I. S. Douglas, D. B. Pearse, and R. M. Tuder, “The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis,” Nat. Med. 18(8), 1217–1223 (2012).
[Crossref] [PubMed]

Nat. Methods (2)

M. R. Looney, E. E. Thornton, D. Sen, W. J. Lamm, R. W. Glenny, and M. F. Krummel, “Stabilized imaging of immune surveillance in the mouse lung,” Nat. Methods 8(1), 91–96 (2011).
[Crossref] [PubMed]

P. Kim, E. Chung, H. Yamashita, K. E. Hung, A. Mizoguchi, R. Kucherlapati, D. Fukumura, R. K. Jain, and S. H. Yun, “In vivo wide-area cellular imaging by side-view endomicroscopy,” Nat. Methods 7(4), 303–305 (2010).
[Crossref] [PubMed]

Nat. Protoc. (1)

D. Rittirsch, M. S. Huber-Lang, M. A. Flierl, and P. A. Ward, “Immunodesign of experimental sepsis by cecal ligation and puncture,” Nat. Protoc. 4(1), 31–36 (2009).
[Crossref] [PubMed]

Opt. Express (1)

Opt. Lett. (1)

Pflugers Arch. (1)

S. Reitsma, D. W. Slaaf, H. Vink, M. A. van Zandvoort, and M. G. oude Egbrink, “The endothelial glycocalyx: composition, functions, and visualization,” Pflugers Arch. 454(3), 345–359 (2007).
[Crossref] [PubMed]

PLoS One (1)

D. H. Lee, M. J. Dane, B. M. van den Berg, M. G. Boels, J. W. van Teeffelen, R. de Mutsert, M. den Heijer, F. R. Rosendaal, J. van der Vlag, A. J. van Zonneveld, H. Vink, T. J. Rabelink, and NEO study group, “Deeper penetration of erythrocytes into the endothelial glycocalyx is associated with impaired microvascular perfusion,” PLoS One 9(5), e96477 (2014).
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Proc. Natl. Acad. Sci. U.S.A. (3)

H. Noguchi and G. Gompper, “Shape transitions of fluid vesicles and red blood cells in capillary flows,” Proc. Natl. Acad. Sci. U.S.A. 102(40), 14159–14164 (2005).
[Crossref] [PubMed]

A. D. Aguirre, C. Vinegoni, M. Sebas, and R. Weissleder, “Intravital imaging of cardiac function at the single-cell level,” Proc. Natl. Acad. Sci. U.S.A. 111(31), 11257–11262 (2014).
[Crossref] [PubMed]

S. Weinbaum, X. Zhang, Y. Han, H. Vink, and S. C. Cowin, “Mechanotransduction and flow across the endothelial glycocalyx,” Proc. Natl. Acad. Sci. U.S.A. 100(13), 7988–7995 (2003).
[Crossref] [PubMed]

Resuscitation (1)

S. Grundmann, K. Fink, L. Rabadzhieva, N. Bourgeois, T. Schwab, M. Moser, C. Bode, and H. J. Busch, “Perturbation of the endothelial glycocalyx in post cardiac arrest syndrome,” Resuscitation 83(6), 715–720 (2012).
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Sci. Rep. (1)

K. Kim, K. Choe, I. Park, P. Kim, and Y. Park, “Holographic intravital microscopy for 2-D and 3-D imaging intact circulating blood cells in microcapillaries of live mice,” Sci. Rep. 6(1), 33084 (2016).
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Science (1)

R. Skalak and P. I. Branemark, “Deformation of red blood cells in capillaries,” Science 164(3880), 717–719 (1969).
[Crossref] [PubMed]

Shock (2)

X. Marechal, R. Favory, O. Joulin, D. Montaigne, S. Hassoun, B. Decoster, F. Zerimech, and R. Neviere, “Endothelial glycocalyx damage during endotoxemia coincides with microcirculatory dysfunction and vascular oxidative stress,” Shock 29(5), 572–576 (2008).
[PubMed]

A. Nelson, I. Berkestedt, A. Schmidtchen, L. Ljunggren, and M. Bodelsson, “Increased levels of glycosaminoglycans during septic shock: relation to mortality and the antibacterial actions of plasma,” Shock 30(6), 623–627 (2008).
[Crossref] [PubMed]

Supplementary Material (7)

NameDescription
» Visualization 1       In vivo real-time imaging of individual flowing erythrocytes inside the pulmonary capillary
» Visualization 2       In vivo three-dimensional subcellular-level pulmonary imaging of H2B-eGFP/ß-actin-DsRed mouse
» Visualization 3       In vivo three-dimensional pulmonary imaging of H2B-eGFP/ß-actin-DsRed mouse
» Visualization 4       In vivo three-dimensional pulmonary imaging of H2B-eGFP/ß-actin-DsRed mouse with surface-rendering (ß-actin) and spot-detection (histone H2B)
» Visualization 5       In vivo three-dimensional subcellular-level pulmonary imaging of H2B-eGFP/ß-actin-DsRed mouse with surface-rendering (ß-actin) and spot-detection (histone H2B) - Magnified view
» Visualization 6       In vivo real-time imaging of circulating erythrocyte and exclusion zone in the pulmonary capillary
» Visualization 7       Comparison of the endothelial surface layer in sham and CLP model

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Figures (3)

Fig. 1
Fig. 1 In vivo cellular-level three-dimensional pulmonary imaging. (a) Schematic of the intravital pulmonary imaging including the micro-suction-based window. (b) Photograph of intravital pulmonary imaging setup consisted of a mechanical ventilator, pulse oximetry, animal stage, heating pad for body temperature regulation, and imaging window. (c) Wide-area mosaic and magnified image of the lung vasculature visualized by intravenously injected FITC dextran. Individual alveoli and capillary were clearly distinguished. Scale bars, 500 μm (mosaic), 100 μm (magnified). (d) Wide-area mosaic and subcellular level 3D intravital lung imaging of nucleus and cytoplasm of individual pulmonary cells in Histone H2B-eGFP/β-actin-DsRed double transgenic mouse (see also Visualization 2). Scale bars, 100 μm (mosaic), 10 μm (magnified). (e-f) Intravital pulmonary imaging of CSF1R-GFP cells representing alveolar macrophages and CX3CR1GFP/+ cells representing mononuclear phagocytic cells. Blood vessels were visualized by intravenously injected TMR dextran. Scale bars, 100 μm.
Fig. 2
Fig. 2 Real-time imaging of circulating erythrocyte for visualization of exclusion zone inside the pulmonary capillary. (a-b) Representative real-time pulmonary capillary imaging with fluorescence angiography using intravenously injected FITC dextran. Individual circulating erythrocyte inside pulmonary capillary was identified in the single frame. (c-d) Averaged image highlight the track of flowing erythrocytes and its exclusion zone inside pulmonary capillary (see also Visualization 6). Scale bar, 10 μm.
Fig. 3
Fig. 3 In vivo imaging of endothelial surface layer degradation in a sepsis-induced lung injury model. (a-b) Representative image and magnified view of exclusion zone representing ESL in sham and CLP model (see also Visualization 7). (c-d) Identification of capillary lumen, erythrocyte, and ESL from fluorescence intensity profile along the yellow dashed line in (a) and (b), sham and CLP model, respectively. (e-g) Comparison of capillary diameter (n = 30 per group), ESL (n = 30 per group), and RBC velocity (n = 17 and 14, respectively) in sham and CLP model (Mean ± S.D., two-tailed t-test, *: P < 0.001). Scale bar, 10 μm.

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