Abstract

There is a hypothesis that augmentation of the drainage and clearing function of the meningeal lymphatic vessels (MLVs) might be a promising therapeutic target for preventing neurological diseases. Here we investigate mechanisms of photobiomodulation (PBM, 1267 nm) of lymphatic drainage and clearance. Our results obtained at optical coherence tomography (OCT) give strong evidence that low PBM doses (5 and 10 J/cm2) stimulate drainage function of the lymphatic vessels via vasodilation (OCT data on the mesenteric lymphatics) and stimulation of lymphatic clearance (OCT data on clearance of gold nanorods from the brain) that was supported by confocal imaging of clearance of FITC-dextran from the cortex via MLVs. We assume that PBM-mediated relaxation of the lymphatic vessels can be possible mechanisms underlying increasing the permeability of the lymphatic endothelium that allows molecules transported by the lymphatic vessels and explain PBM stimulation of lymphatic drainage and clearance. These findings open new strategies for the stimulation of MLVs functions and non-pharmacological therapy of brain diseases.

© 2020 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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Corrections

29 January 2020: A typographical correction was made to the author listing.


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2019 (1)

2018 (3)

S. Da Mesquita, A. Louveau, A. Vaccari, I. Smirnov, R. C. Cornelison, K. M. Kingsmore, C. Contarino, S. Onengut-Gumuscu, E. Farber, D. Raper, K. E. Viar, R. D. Powell, W. Baker, N. Dabhi, R. Bai, R. Cao, S. Hu, S. S. Rich, J. M. Munson, M. B. Lopes, C. C. Overall, S. T. Acton, and J. Kipnis, “Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease,” Nature 560(7717), 185–191 (2018).
[Crossref]

O. Semyachkina-Glushkovskaya, D. Postnov, and J. Kurths, “Blood−Brain Barrier, Lymphatic Clearance, and Recovery: Ariadne’s Thread in Labyrinths of Hypotheses,” Int. J. Mol. Sci. 19(12), 3818 (2018).
[Crossref]

O. Semyachkina-Glushkovskaya, V. Chehonin, E. Borisova, I. Fedosov, A. Namykin, A. Abdurashitov, A. Shirokov, B. Khlebtsov, Y. Lyubun, N. Navolokin, M. Ulanova, N. Shushunova, A. Khorovodov, I. Agranovich, A. Bodrova, M. Sagatova, A. E. Shareef, E. Saranceva, T. Iskra, M. Dvoryatkina, E. Zhinchenko, O. Sindeeva, V. Tuchin, and J. Kurths, “Photodynamic opening of the blood-brain barrier and pathways of brain clearing,” J. Biophotonics 11(8), e201700287 (2018).
[Crossref]

2017 (3)

M. Absinta, S.-K. Ha, G. Nair, P. Satil, N. J. Luciano, M. Palisoc, A. Louveau, K. A. Zaghloul, S. Pittaluga, J. Kipnis, and D. S. Reich, “Human and nonhuman primate meninges harbor lymphatic vessels that can be visualized noninvasively by MRI,” eLife 6, e29738 (2017).
[Crossref]

O. Semyachkina-Glushkovskaya, A. Abdurashitov, A. Dubrovsky, D. Bragin, O. Bragina, N. Shushunova, G. Maslyakova, N. Navolokin, A. Bucharskaya, V. Tuchin, J. Kurths, and A. Shirokov, “Application of optical coherence tomography for in vivo monitoring of the meningeal lymphatic vessels during opening of blood-brain barrier: mechanisms of brain clearing,” J. Biomed. Opt. 22(12), 1–9 (2017).
[Crossref]

S. Antila, S. Karaman, H. Nurmi, M. Airavaara, M. Voutilainen, T. Mathivet, D. Chilov, Z. Li, T. Koppinen, J. Park, S. Fang, A. Aspelung, M. Saarma, A. Eichmann, J. Thomas, and K. Alitalo, “Development and plasticity of meningeal lymphatic vessels,” J. Exp. Med. 214(12), 3645–3667 (2017).
[Crossref]

2016 (2)

M. Lohrberg and J. Wilting, “The lymphatic vascular system of the mouse head,” Cell Tissue Res. 366(3), 667–677 (2016).
[Crossref]

J. Scallan, S. Zawieja, J. Castorena-Gonzalez, and M. Davis, “Lymphatic pumping: mechanics, mechanisms and malfunction,” J. Physiol. 594(20), 5749–5768 (2016).
[Crossref]

2015 (3)

E. Kuan, S. Ivanov, E. Bridenbaugh, G. Victora, W. Wang, E. Childs, A. Platt, C. Jakubzick, R. Mason, A. Gashev, M. Nussenzweig, M. Swartz, M. Dustin, D. Zawieja, and G. Randolph, “Collecting lymphatic vessel permeability facilitates adipose tissue inflammation and distribution of antigen to lymph node – homing adipose tissue dendritic cells,” J. Immunol. 194(11), 5200–5210 (2015).
[Crossref]

I. Louveau, T. Smirnov, J. Keyes, S. Eccles, J. Rouhani, N. Peske, D. Derecki, J. Castle, K. Mandell, T. Lee, J. Harris, and Kipnis, “Structural and functional features of central nervous system lymphatic vessels,” Nature 523(7560), 337–341 (2015).
[Crossref]

S. Aspelund, S. Antila, T. Proulx, S. Karlsen, M. Karaman, H. Detmar, K. A. Wiig, and Alitalo, “A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules,” J. Exp. Med. 212(7), 991–999 (2015).
[Crossref]

2014 (2)

W. Kilarski, A. Muchowicz, M. Wachowska, R. Mezyk-Kopec, J. Golab, and M. Swartz, “Nowak-Sliwinska. Optimization and regeneration kinetics of lymphatic-specific photodynamic therapy in the mouse dermis,” Angiogenesis 17(2), 347–357 (2014).
[Crossref]

I. Nizamutdinova, D. Maejima, T. Nagai, E. Bridenbaugh, S. Thangaswamy, V. Chatterjee, C. Meininger, and A. Gashev, “Involvement of histamine in endothelium-dependent relaxation of mesenteric lymphatic vessels,” Microcirculation 21(7), 640–648 (2014).
[Crossref]

2013 (2)

O. Gasheva, A. Gashev, and D. Zawieja, “Cyclic guanosine monophosphate and the dependent protein kinase regulate lymphatic contractility in rat thoracic duct,” J. Physiol. 591(18), 4549–4565 (2013).
[Crossref]

S. G. Sokolovski, S. A. Zolotovskaya, A. Goltsov, C. Pourreyron, A. P. South, and E. U. Rafailov, “Infrared laser pulse triggers increased singlet oxygen production in tumour cells,” Sci. Rep. 3(1), 3484 (2013)..
[Crossref]

2012 (1)

P. Dunkel, C. L. Chai, B. Sperlágh, P. B. Huleatt, and P. Mátyus, “Clinical utility of neuroprotective agents in neurodegenerative diseases: current status of drug development for Alzheimer’s, Parkinson’s and Huntington’s diseases, and amyotrophic lateral sclerosis,” Expert Opin. Invest. Drugs 21(9), 1267–1308 (2012).
[Crossref]

2011 (1)

M. Davis, E. Rahbar, A. Gashev, D. Zawieja, and J. Moore, “Determinants of valve gating in collecting lymphatic vessels from rat mesentery,” Am J. Physiol. Heart Circ. Physiol. 301(1), H48–H60 (2011).
[Crossref]

2008 (1)

N. L. Harvey, “The link between lymphatic function and adipose biology,” Ann. N. Y. Acad. Sci. 1131(1), 82–88 (2008).
[Crossref]

2005 (1)

T. I. Karu, L. V. Pyatibrat, and N. I. Afanasyeva, “Cellular effects of low power laser therapy can be mediated by nitric oxide,” Lasers Surg. Med. 36(4), 307–314 (2005).
[Crossref]

2004 (1)

F. Murad, “Discovery of some of the biological effects of nitric oxide and its role in cell signaling,” Biosci. Rep. 24(4-5), 453–474 (2004).
[Crossref]

2002 (1)

A. Gashev, M. Davis, and D. Zawieja, “Inhibition of the active lymph pump by flow in rat mesenteric lymphatics and thoracic duct,” J. Physiol. 540(3), 1023–1037 (2002).
[Crossref]

1996 (1)

J. C. Drapierand and J. B. Hibbs, “Aconitases: a class of metalloproteins highly sensitive to nitric oxide synthesis,” Methods Enzymol. 269, 26–36 (1996).
[Crossref]

1993 (1)

J. C. Drapier, H. Hirling, J. Wietzerbin, P. Kaldy, and L. C. Kühn, “Biosynthesis of nitric oxide activates iron regulatory factor in macrophages,” EMBO J. 12(9), 3643–3649 (1993).
[Crossref]

1992 (2)

S. Dimmeler, F. Lottspeich, and B. Brune, “Nitric oxide causes ADPribosylation and inhibition of glyceraldehyde-3- phosphate dehydrogenase,” J. Biol. Chem. 267(24), 16771–16774 (1992).

J. S. Stamler, D. I. Simon, J. A. Osborne, M. E. Mullins, O. Jaraki, T. Michel, D. Singel, and J. Loscalzo, “S-nitrosylation of proteins with nitric oxide: synthesis and characterization of biologically active compounds,” Proc. Natl. Acad. Sci. U. S. A. 89(1), 444–448 (1992).
[Crossref]

1991 (1)

M. Lepoivre, F. Fieschi, J. Coves, L. Thelander, and M. Fontecave, “Inactivation of ribonucleotide reductase by nitric oxide,” Biochem. Biophys. Res. Commun. 179(1), 442–448 (1991).
[Crossref]

1988 (1)

C. Joachim, L. Duffy, J. Morris, and D. Selkoe, “Protein chemical and immunocytochemical studies of meningovascular β-amyloid protein in Alzheimer’s disease and normal aging,” Brain Res. 474(1), 100–111 (1988).
[Crossref]

1979 (1)

J. W. Prineas, “Multiple sclerosis: Presence of lymphatic capillaries and lymphoid tissues in the brain and spinal cord,” Science 203(4385), 1123–1125 (1979).
[Crossref]

1975 (1)

B. Zweifach and J. Prather, “Micromanipulation of pressure in terminal lymphatics in the rat mesentery,” Am. J. Physiol. 228(5), 1326–1335 (1975).
[Crossref]

Abdurashitov, A.

E. Zinchenko, N. Navolokin, A. Shirokov, B. Khlebtsov, A. Dunbrovsky, E. Saranceva, A. Abdurashitov, A. Khorovodov, A. Terskov, A. Mamedova, M. Klimova, I. Agranovich, D. Martinov, V. Tuchin, O. Semyachkina-Glushkovskaya, and J. Kurths, “Pilot study of transcranial photobiomodulation of lymphatic clearance of beta-amyloid from the mouse brain: breakthrough strategies for nonpharmacologic therapy of Alzheimer’s disease,” Biomed. Opt. Express 10(8), 4003–4017 (2019).
[Crossref]

O. Semyachkina-Glushkovskaya, V. Chehonin, E. Borisova, I. Fedosov, A. Namykin, A. Abdurashitov, A. Shirokov, B. Khlebtsov, Y. Lyubun, N. Navolokin, M. Ulanova, N. Shushunova, A. Khorovodov, I. Agranovich, A. Bodrova, M. Sagatova, A. E. Shareef, E. Saranceva, T. Iskra, M. Dvoryatkina, E. Zhinchenko, O. Sindeeva, V. Tuchin, and J. Kurths, “Photodynamic opening of the blood-brain barrier and pathways of brain clearing,” J. Biophotonics 11(8), e201700287 (2018).
[Crossref]

O. Semyachkina-Glushkovskaya, A. Abdurashitov, A. Dubrovsky, D. Bragin, O. Bragina, N. Shushunova, G. Maslyakova, N. Navolokin, A. Bucharskaya, V. Tuchin, J. Kurths, and A. Shirokov, “Application of optical coherence tomography for in vivo monitoring of the meningeal lymphatic vessels during opening of blood-brain barrier: mechanisms of brain clearing,” J. Biomed. Opt. 22(12), 1–9 (2017).
[Crossref]

Absinta, M.

M. Absinta, S.-K. Ha, G. Nair, P. Satil, N. J. Luciano, M. Palisoc, A. Louveau, K. A. Zaghloul, S. Pittaluga, J. Kipnis, and D. S. Reich, “Human and nonhuman primate meninges harbor lymphatic vessels that can be visualized noninvasively by MRI,” eLife 6, e29738 (2017).
[Crossref]

Acton, S. T.

S. Da Mesquita, A. Louveau, A. Vaccari, I. Smirnov, R. C. Cornelison, K. M. Kingsmore, C. Contarino, S. Onengut-Gumuscu, E. Farber, D. Raper, K. E. Viar, R. D. Powell, W. Baker, N. Dabhi, R. Bai, R. Cao, S. Hu, S. S. Rich, J. M. Munson, M. B. Lopes, C. C. Overall, S. T. Acton, and J. Kipnis, “Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease,” Nature 560(7717), 185–191 (2018).
[Crossref]

Afanasyeva, N. I.

T. I. Karu, L. V. Pyatibrat, and N. I. Afanasyeva, “Cellular effects of low power laser therapy can be mediated by nitric oxide,” Lasers Surg. Med. 36(4), 307–314 (2005).
[Crossref]

Agranovich, I.

E. Zinchenko, N. Navolokin, A. Shirokov, B. Khlebtsov, A. Dunbrovsky, E. Saranceva, A. Abdurashitov, A. Khorovodov, A. Terskov, A. Mamedova, M. Klimova, I. Agranovich, D. Martinov, V. Tuchin, O. Semyachkina-Glushkovskaya, and J. Kurths, “Pilot study of transcranial photobiomodulation of lymphatic clearance of beta-amyloid from the mouse brain: breakthrough strategies for nonpharmacologic therapy of Alzheimer’s disease,” Biomed. Opt. Express 10(8), 4003–4017 (2019).
[Crossref]

O. Semyachkina-Glushkovskaya, V. Chehonin, E. Borisova, I. Fedosov, A. Namykin, A. Abdurashitov, A. Shirokov, B. Khlebtsov, Y. Lyubun, N. Navolokin, M. Ulanova, N. Shushunova, A. Khorovodov, I. Agranovich, A. Bodrova, M. Sagatova, A. E. Shareef, E. Saranceva, T. Iskra, M. Dvoryatkina, E. Zhinchenko, O. Sindeeva, V. Tuchin, and J. Kurths, “Photodynamic opening of the blood-brain barrier and pathways of brain clearing,” J. Biophotonics 11(8), e201700287 (2018).
[Crossref]

Airavaara, M.

S. Antila, S. Karaman, H. Nurmi, M. Airavaara, M. Voutilainen, T. Mathivet, D. Chilov, Z. Li, T. Koppinen, J. Park, S. Fang, A. Aspelung, M. Saarma, A. Eichmann, J. Thomas, and K. Alitalo, “Development and plasticity of meningeal lymphatic vessels,” J. Exp. Med. 214(12), 3645–3667 (2017).
[Crossref]

Alitalo,

S. Aspelund, S. Antila, T. Proulx, S. Karlsen, M. Karaman, H. Detmar, K. A. Wiig, and Alitalo, “A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules,” J. Exp. Med. 212(7), 991–999 (2015).
[Crossref]

Alitalo, K.

S. Antila, S. Karaman, H. Nurmi, M. Airavaara, M. Voutilainen, T. Mathivet, D. Chilov, Z. Li, T. Koppinen, J. Park, S. Fang, A. Aspelung, M. Saarma, A. Eichmann, J. Thomas, and K. Alitalo, “Development and plasticity of meningeal lymphatic vessels,” J. Exp. Med. 214(12), 3645–3667 (2017).
[Crossref]

Antila, S.

S. Antila, S. Karaman, H. Nurmi, M. Airavaara, M. Voutilainen, T. Mathivet, D. Chilov, Z. Li, T. Koppinen, J. Park, S. Fang, A. Aspelung, M. Saarma, A. Eichmann, J. Thomas, and K. Alitalo, “Development and plasticity of meningeal lymphatic vessels,” J. Exp. Med. 214(12), 3645–3667 (2017).
[Crossref]

S. Aspelund, S. Antila, T. Proulx, S. Karlsen, M. Karaman, H. Detmar, K. A. Wiig, and Alitalo, “A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules,” J. Exp. Med. 212(7), 991–999 (2015).
[Crossref]

Aspelund, S.

S. Aspelund, S. Antila, T. Proulx, S. Karlsen, M. Karaman, H. Detmar, K. A. Wiig, and Alitalo, “A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules,” J. Exp. Med. 212(7), 991–999 (2015).
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Aspelung, A.

S. Antila, S. Karaman, H. Nurmi, M. Airavaara, M. Voutilainen, T. Mathivet, D. Chilov, Z. Li, T. Koppinen, J. Park, S. Fang, A. Aspelung, M. Saarma, A. Eichmann, J. Thomas, and K. Alitalo, “Development and plasticity of meningeal lymphatic vessels,” J. Exp. Med. 214(12), 3645–3667 (2017).
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Bai, R.

S. Da Mesquita, A. Louveau, A. Vaccari, I. Smirnov, R. C. Cornelison, K. M. Kingsmore, C. Contarino, S. Onengut-Gumuscu, E. Farber, D. Raper, K. E. Viar, R. D. Powell, W. Baker, N. Dabhi, R. Bai, R. Cao, S. Hu, S. S. Rich, J. M. Munson, M. B. Lopes, C. C. Overall, S. T. Acton, and J. Kipnis, “Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease,” Nature 560(7717), 185–191 (2018).
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Baker, W.

S. Da Mesquita, A. Louveau, A. Vaccari, I. Smirnov, R. C. Cornelison, K. M. Kingsmore, C. Contarino, S. Onengut-Gumuscu, E. Farber, D. Raper, K. E. Viar, R. D. Powell, W. Baker, N. Dabhi, R. Bai, R. Cao, S. Hu, S. S. Rich, J. M. Munson, M. B. Lopes, C. C. Overall, S. T. Acton, and J. Kipnis, “Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease,” Nature 560(7717), 185–191 (2018).
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Bodrova, A.

O. Semyachkina-Glushkovskaya, V. Chehonin, E. Borisova, I. Fedosov, A. Namykin, A. Abdurashitov, A. Shirokov, B. Khlebtsov, Y. Lyubun, N. Navolokin, M. Ulanova, N. Shushunova, A. Khorovodov, I. Agranovich, A. Bodrova, M. Sagatova, A. E. Shareef, E. Saranceva, T. Iskra, M. Dvoryatkina, E. Zhinchenko, O. Sindeeva, V. Tuchin, and J. Kurths, “Photodynamic opening of the blood-brain barrier and pathways of brain clearing,” J. Biophotonics 11(8), e201700287 (2018).
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Borisova, E.

O. Semyachkina-Glushkovskaya, V. Chehonin, E. Borisova, I. Fedosov, A. Namykin, A. Abdurashitov, A. Shirokov, B. Khlebtsov, Y. Lyubun, N. Navolokin, M. Ulanova, N. Shushunova, A. Khorovodov, I. Agranovich, A. Bodrova, M. Sagatova, A. E. Shareef, E. Saranceva, T. Iskra, M. Dvoryatkina, E. Zhinchenko, O. Sindeeva, V. Tuchin, and J. Kurths, “Photodynamic opening of the blood-brain barrier and pathways of brain clearing,” J. Biophotonics 11(8), e201700287 (2018).
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O. Semyachkina-Glushkovskaya, A. Abdurashitov, A. Dubrovsky, D. Bragin, O. Bragina, N. Shushunova, G. Maslyakova, N. Navolokin, A. Bucharskaya, V. Tuchin, J. Kurths, and A. Shirokov, “Application of optical coherence tomography for in vivo monitoring of the meningeal lymphatic vessels during opening of blood-brain barrier: mechanisms of brain clearing,” J. Biomed. Opt. 22(12), 1–9 (2017).
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O. Semyachkina-Glushkovskaya, A. Abdurashitov, A. Dubrovsky, D. Bragin, O. Bragina, N. Shushunova, G. Maslyakova, N. Navolokin, A. Bucharskaya, V. Tuchin, J. Kurths, and A. Shirokov, “Application of optical coherence tomography for in vivo monitoring of the meningeal lymphatic vessels during opening of blood-brain barrier: mechanisms of brain clearing,” J. Biomed. Opt. 22(12), 1–9 (2017).
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E. Kuan, S. Ivanov, E. Bridenbaugh, G. Victora, W. Wang, E. Childs, A. Platt, C. Jakubzick, R. Mason, A. Gashev, M. Nussenzweig, M. Swartz, M. Dustin, D. Zawieja, and G. Randolph, “Collecting lymphatic vessel permeability facilitates adipose tissue inflammation and distribution of antigen to lymph node – homing adipose tissue dendritic cells,” J. Immunol. 194(11), 5200–5210 (2015).
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I. Nizamutdinova, D. Maejima, T. Nagai, E. Bridenbaugh, S. Thangaswamy, V. Chatterjee, C. Meininger, and A. Gashev, “Involvement of histamine in endothelium-dependent relaxation of mesenteric lymphatic vessels,” Microcirculation 21(7), 640–648 (2014).
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S. Dimmeler, F. Lottspeich, and B. Brune, “Nitric oxide causes ADPribosylation and inhibition of glyceraldehyde-3- phosphate dehydrogenase,” J. Biol. Chem. 267(24), 16771–16774 (1992).

Bucharskaya, A.

O. Semyachkina-Glushkovskaya, A. Abdurashitov, A. Dubrovsky, D. Bragin, O. Bragina, N. Shushunova, G. Maslyakova, N. Navolokin, A. Bucharskaya, V. Tuchin, J. Kurths, and A. Shirokov, “Application of optical coherence tomography for in vivo monitoring of the meningeal lymphatic vessels during opening of blood-brain barrier: mechanisms of brain clearing,” J. Biomed. Opt. 22(12), 1–9 (2017).
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Cao, R.

S. Da Mesquita, A. Louveau, A. Vaccari, I. Smirnov, R. C. Cornelison, K. M. Kingsmore, C. Contarino, S. Onengut-Gumuscu, E. Farber, D. Raper, K. E. Viar, R. D. Powell, W. Baker, N. Dabhi, R. Bai, R. Cao, S. Hu, S. S. Rich, J. M. Munson, M. B. Lopes, C. C. Overall, S. T. Acton, and J. Kipnis, “Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease,” Nature 560(7717), 185–191 (2018).
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Castle, J.

I. Louveau, T. Smirnov, J. Keyes, S. Eccles, J. Rouhani, N. Peske, D. Derecki, J. Castle, K. Mandell, T. Lee, J. Harris, and Kipnis, “Structural and functional features of central nervous system lymphatic vessels,” Nature 523(7560), 337–341 (2015).
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Castorena-Gonzalez, J.

J. Scallan, S. Zawieja, J. Castorena-Gonzalez, and M. Davis, “Lymphatic pumping: mechanics, mechanisms and malfunction,” J. Physiol. 594(20), 5749–5768 (2016).
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P. Dunkel, C. L. Chai, B. Sperlágh, P. B. Huleatt, and P. Mátyus, “Clinical utility of neuroprotective agents in neurodegenerative diseases: current status of drug development for Alzheimer’s, Parkinson’s and Huntington’s diseases, and amyotrophic lateral sclerosis,” Expert Opin. Invest. Drugs 21(9), 1267–1308 (2012).
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Chatterjee, V.

I. Nizamutdinova, D. Maejima, T. Nagai, E. Bridenbaugh, S. Thangaswamy, V. Chatterjee, C. Meininger, and A. Gashev, “Involvement of histamine in endothelium-dependent relaxation of mesenteric lymphatic vessels,” Microcirculation 21(7), 640–648 (2014).
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Chehonin, V.

O. Semyachkina-Glushkovskaya, V. Chehonin, E. Borisova, I. Fedosov, A. Namykin, A. Abdurashitov, A. Shirokov, B. Khlebtsov, Y. Lyubun, N. Navolokin, M. Ulanova, N. Shushunova, A. Khorovodov, I. Agranovich, A. Bodrova, M. Sagatova, A. E. Shareef, E. Saranceva, T. Iskra, M. Dvoryatkina, E. Zhinchenko, O. Sindeeva, V. Tuchin, and J. Kurths, “Photodynamic opening of the blood-brain barrier and pathways of brain clearing,” J. Biophotonics 11(8), e201700287 (2018).
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Childs, E.

E. Kuan, S. Ivanov, E. Bridenbaugh, G. Victora, W. Wang, E. Childs, A. Platt, C. Jakubzick, R. Mason, A. Gashev, M. Nussenzweig, M. Swartz, M. Dustin, D. Zawieja, and G. Randolph, “Collecting lymphatic vessel permeability facilitates adipose tissue inflammation and distribution of antigen to lymph node – homing adipose tissue dendritic cells,” J. Immunol. 194(11), 5200–5210 (2015).
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S. Antila, S. Karaman, H. Nurmi, M. Airavaara, M. Voutilainen, T. Mathivet, D. Chilov, Z. Li, T. Koppinen, J. Park, S. Fang, A. Aspelung, M. Saarma, A. Eichmann, J. Thomas, and K. Alitalo, “Development and plasticity of meningeal lymphatic vessels,” J. Exp. Med. 214(12), 3645–3667 (2017).
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S. Da Mesquita, A. Louveau, A. Vaccari, I. Smirnov, R. C. Cornelison, K. M. Kingsmore, C. Contarino, S. Onengut-Gumuscu, E. Farber, D. Raper, K. E. Viar, R. D. Powell, W. Baker, N. Dabhi, R. Bai, R. Cao, S. Hu, S. S. Rich, J. M. Munson, M. B. Lopes, C. C. Overall, S. T. Acton, and J. Kipnis, “Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease,” Nature 560(7717), 185–191 (2018).
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S. Da Mesquita, A. Louveau, A. Vaccari, I. Smirnov, R. C. Cornelison, K. M. Kingsmore, C. Contarino, S. Onengut-Gumuscu, E. Farber, D. Raper, K. E. Viar, R. D. Powell, W. Baker, N. Dabhi, R. Bai, R. Cao, S. Hu, S. S. Rich, J. M. Munson, M. B. Lopes, C. C. Overall, S. T. Acton, and J. Kipnis, “Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease,” Nature 560(7717), 185–191 (2018).
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Coves, J.

M. Lepoivre, F. Fieschi, J. Coves, L. Thelander, and M. Fontecave, “Inactivation of ribonucleotide reductase by nitric oxide,” Biochem. Biophys. Res. Commun. 179(1), 442–448 (1991).
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H. F. Cserr and C. S. Patlak, “Secretion and bulk flow of interstitial fluid. In Physiology and Pharmacology of the Blood-Brain Barrier,” M. W. B. Bradbury, P. Cuatrecasas, and H. Herken, eds.; Handbook of Experimental Pharmacology, 103 (Springer, 1992), pp. 245–261 .

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S. Da Mesquita, A. Louveau, A. Vaccari, I. Smirnov, R. C. Cornelison, K. M. Kingsmore, C. Contarino, S. Onengut-Gumuscu, E. Farber, D. Raper, K. E. Viar, R. D. Powell, W. Baker, N. Dabhi, R. Bai, R. Cao, S. Hu, S. S. Rich, J. M. Munson, M. B. Lopes, C. C. Overall, S. T. Acton, and J. Kipnis, “Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease,” Nature 560(7717), 185–191 (2018).
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S. Da Mesquita, A. Louveau, A. Vaccari, I. Smirnov, R. C. Cornelison, K. M. Kingsmore, C. Contarino, S. Onengut-Gumuscu, E. Farber, D. Raper, K. E. Viar, R. D. Powell, W. Baker, N. Dabhi, R. Bai, R. Cao, S. Hu, S. S. Rich, J. M. Munson, M. B. Lopes, C. C. Overall, S. T. Acton, and J. Kipnis, “Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease,” Nature 560(7717), 185–191 (2018).
[Crossref]

Davis, M.

J. Scallan, S. Zawieja, J. Castorena-Gonzalez, and M. Davis, “Lymphatic pumping: mechanics, mechanisms and malfunction,” J. Physiol. 594(20), 5749–5768 (2016).
[Crossref]

M. Davis, E. Rahbar, A. Gashev, D. Zawieja, and J. Moore, “Determinants of valve gating in collecting lymphatic vessels from rat mesentery,” Am J. Physiol. Heart Circ. Physiol. 301(1), H48–H60 (2011).
[Crossref]

A. Gashev, M. Davis, and D. Zawieja, “Inhibition of the active lymph pump by flow in rat mesenteric lymphatics and thoracic duct,” J. Physiol. 540(3), 1023–1037 (2002).
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I. Louveau, T. Smirnov, J. Keyes, S. Eccles, J. Rouhani, N. Peske, D. Derecki, J. Castle, K. Mandell, T. Lee, J. Harris, and Kipnis, “Structural and functional features of central nervous system lymphatic vessels,” Nature 523(7560), 337–341 (2015).
[Crossref]

Detmar, H.

S. Aspelund, S. Antila, T. Proulx, S. Karlsen, M. Karaman, H. Detmar, K. A. Wiig, and Alitalo, “A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules,” J. Exp. Med. 212(7), 991–999 (2015).
[Crossref]

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S. Dimmeler, F. Lottspeich, and B. Brune, “Nitric oxide causes ADPribosylation and inhibition of glyceraldehyde-3- phosphate dehydrogenase,” J. Biol. Chem. 267(24), 16771–16774 (1992).

Drapier, J. C.

J. C. Drapier, H. Hirling, J. Wietzerbin, P. Kaldy, and L. C. Kühn, “Biosynthesis of nitric oxide activates iron regulatory factor in macrophages,” EMBO J. 12(9), 3643–3649 (1993).
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J. C. Drapierand and J. B. Hibbs, “Aconitases: a class of metalloproteins highly sensitive to nitric oxide synthesis,” Methods Enzymol. 269, 26–36 (1996).
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Dubrovsky, A.

O. Semyachkina-Glushkovskaya, A. Abdurashitov, A. Dubrovsky, D. Bragin, O. Bragina, N. Shushunova, G. Maslyakova, N. Navolokin, A. Bucharskaya, V. Tuchin, J. Kurths, and A. Shirokov, “Application of optical coherence tomography for in vivo monitoring of the meningeal lymphatic vessels during opening of blood-brain barrier: mechanisms of brain clearing,” J. Biomed. Opt. 22(12), 1–9 (2017).
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C. Joachim, L. Duffy, J. Morris, and D. Selkoe, “Protein chemical and immunocytochemical studies of meningovascular β-amyloid protein in Alzheimer’s disease and normal aging,” Brain Res. 474(1), 100–111 (1988).
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Dunkel, P.

P. Dunkel, C. L. Chai, B. Sperlágh, P. B. Huleatt, and P. Mátyus, “Clinical utility of neuroprotective agents in neurodegenerative diseases: current status of drug development for Alzheimer’s, Parkinson’s and Huntington’s diseases, and amyotrophic lateral sclerosis,” Expert Opin. Invest. Drugs 21(9), 1267–1308 (2012).
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E. Kuan, S. Ivanov, E. Bridenbaugh, G. Victora, W. Wang, E. Childs, A. Platt, C. Jakubzick, R. Mason, A. Gashev, M. Nussenzweig, M. Swartz, M. Dustin, D. Zawieja, and G. Randolph, “Collecting lymphatic vessel permeability facilitates adipose tissue inflammation and distribution of antigen to lymph node – homing adipose tissue dendritic cells,” J. Immunol. 194(11), 5200–5210 (2015).
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O. Semyachkina-Glushkovskaya, V. Chehonin, E. Borisova, I. Fedosov, A. Namykin, A. Abdurashitov, A. Shirokov, B. Khlebtsov, Y. Lyubun, N. Navolokin, M. Ulanova, N. Shushunova, A. Khorovodov, I. Agranovich, A. Bodrova, M. Sagatova, A. E. Shareef, E. Saranceva, T. Iskra, M. Dvoryatkina, E. Zhinchenko, O. Sindeeva, V. Tuchin, and J. Kurths, “Photodynamic opening of the blood-brain barrier and pathways of brain clearing,” J. Biophotonics 11(8), e201700287 (2018).
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I. Louveau, T. Smirnov, J. Keyes, S. Eccles, J. Rouhani, N. Peske, D. Derecki, J. Castle, K. Mandell, T. Lee, J. Harris, and Kipnis, “Structural and functional features of central nervous system lymphatic vessels,” Nature 523(7560), 337–341 (2015).
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S. Antila, S. Karaman, H. Nurmi, M. Airavaara, M. Voutilainen, T. Mathivet, D. Chilov, Z. Li, T. Koppinen, J. Park, S. Fang, A. Aspelung, M. Saarma, A. Eichmann, J. Thomas, and K. Alitalo, “Development and plasticity of meningeal lymphatic vessels,” J. Exp. Med. 214(12), 3645–3667 (2017).
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S. Antila, S. Karaman, H. Nurmi, M. Airavaara, M. Voutilainen, T. Mathivet, D. Chilov, Z. Li, T. Koppinen, J. Park, S. Fang, A. Aspelung, M. Saarma, A. Eichmann, J. Thomas, and K. Alitalo, “Development and plasticity of meningeal lymphatic vessels,” J. Exp. Med. 214(12), 3645–3667 (2017).
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S. Da Mesquita, A. Louveau, A. Vaccari, I. Smirnov, R. C. Cornelison, K. M. Kingsmore, C. Contarino, S. Onengut-Gumuscu, E. Farber, D. Raper, K. E. Viar, R. D. Powell, W. Baker, N. Dabhi, R. Bai, R. Cao, S. Hu, S. S. Rich, J. M. Munson, M. B. Lopes, C. C. Overall, S. T. Acton, and J. Kipnis, “Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease,” Nature 560(7717), 185–191 (2018).
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O. Semyachkina-Glushkovskaya, V. Chehonin, E. Borisova, I. Fedosov, A. Namykin, A. Abdurashitov, A. Shirokov, B. Khlebtsov, Y. Lyubun, N. Navolokin, M. Ulanova, N. Shushunova, A. Khorovodov, I. Agranovich, A. Bodrova, M. Sagatova, A. E. Shareef, E. Saranceva, T. Iskra, M. Dvoryatkina, E. Zhinchenko, O. Sindeeva, V. Tuchin, and J. Kurths, “Photodynamic opening of the blood-brain barrier and pathways of brain clearing,” J. Biophotonics 11(8), e201700287 (2018).
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M. Lepoivre, F. Fieschi, J. Coves, L. Thelander, and M. Fontecave, “Inactivation of ribonucleotide reductase by nitric oxide,” Biochem. Biophys. Res. Commun. 179(1), 442–448 (1991).
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M. Lepoivre, F. Fieschi, J. Coves, L. Thelander, and M. Fontecave, “Inactivation of ribonucleotide reductase by nitric oxide,” Biochem. Biophys. Res. Commun. 179(1), 442–448 (1991).
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E. Kuan, S. Ivanov, E. Bridenbaugh, G. Victora, W. Wang, E. Childs, A. Platt, C. Jakubzick, R. Mason, A. Gashev, M. Nussenzweig, M. Swartz, M. Dustin, D. Zawieja, and G. Randolph, “Collecting lymphatic vessel permeability facilitates adipose tissue inflammation and distribution of antigen to lymph node – homing adipose tissue dendritic cells,” J. Immunol. 194(11), 5200–5210 (2015).
[Crossref]

I. Nizamutdinova, D. Maejima, T. Nagai, E. Bridenbaugh, S. Thangaswamy, V. Chatterjee, C. Meininger, and A. Gashev, “Involvement of histamine in endothelium-dependent relaxation of mesenteric lymphatic vessels,” Microcirculation 21(7), 640–648 (2014).
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O. Gasheva, A. Gashev, and D. Zawieja, “Cyclic guanosine monophosphate and the dependent protein kinase regulate lymphatic contractility in rat thoracic duct,” J. Physiol. 591(18), 4549–4565 (2013).
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M. Davis, E. Rahbar, A. Gashev, D. Zawieja, and J. Moore, “Determinants of valve gating in collecting lymphatic vessels from rat mesentery,” Am J. Physiol. Heart Circ. Physiol. 301(1), H48–H60 (2011).
[Crossref]

A. Gashev, M. Davis, and D. Zawieja, “Inhibition of the active lymph pump by flow in rat mesenteric lymphatics and thoracic duct,” J. Physiol. 540(3), 1023–1037 (2002).
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Gasheva, O.

O. Gasheva, A. Gashev, and D. Zawieja, “Cyclic guanosine monophosphate and the dependent protein kinase regulate lymphatic contractility in rat thoracic duct,” J. Physiol. 591(18), 4549–4565 (2013).
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W. Kilarski, A. Muchowicz, M. Wachowska, R. Mezyk-Kopec, J. Golab, and M. Swartz, “Nowak-Sliwinska. Optimization and regeneration kinetics of lymphatic-specific photodynamic therapy in the mouse dermis,” Angiogenesis 17(2), 347–357 (2014).
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I. Louveau, T. Smirnov, J. Keyes, S. Eccles, J. Rouhani, N. Peske, D. Derecki, J. Castle, K. Mandell, T. Lee, J. Harris, and Kipnis, “Structural and functional features of central nervous system lymphatic vessels,” Nature 523(7560), 337–341 (2015).
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J. C. Drapierand and J. B. Hibbs, “Aconitases: a class of metalloproteins highly sensitive to nitric oxide synthesis,” Methods Enzymol. 269, 26–36 (1996).
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J. C. Drapier, H. Hirling, J. Wietzerbin, P. Kaldy, and L. C. Kühn, “Biosynthesis of nitric oxide activates iron regulatory factor in macrophages,” EMBO J. 12(9), 3643–3649 (1993).
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S. Da Mesquita, A. Louveau, A. Vaccari, I. Smirnov, R. C. Cornelison, K. M. Kingsmore, C. Contarino, S. Onengut-Gumuscu, E. Farber, D. Raper, K. E. Viar, R. D. Powell, W. Baker, N. Dabhi, R. Bai, R. Cao, S. Hu, S. S. Rich, J. M. Munson, M. B. Lopes, C. C. Overall, S. T. Acton, and J. Kipnis, “Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease,” Nature 560(7717), 185–191 (2018).
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P. Dunkel, C. L. Chai, B. Sperlágh, P. B. Huleatt, and P. Mátyus, “Clinical utility of neuroprotective agents in neurodegenerative diseases: current status of drug development for Alzheimer’s, Parkinson’s and Huntington’s diseases, and amyotrophic lateral sclerosis,” Expert Opin. Invest. Drugs 21(9), 1267–1308 (2012).
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Iskra, T.

O. Semyachkina-Glushkovskaya, V. Chehonin, E. Borisova, I. Fedosov, A. Namykin, A. Abdurashitov, A. Shirokov, B. Khlebtsov, Y. Lyubun, N. Navolokin, M. Ulanova, N. Shushunova, A. Khorovodov, I. Agranovich, A. Bodrova, M. Sagatova, A. E. Shareef, E. Saranceva, T. Iskra, M. Dvoryatkina, E. Zhinchenko, O. Sindeeva, V. Tuchin, and J. Kurths, “Photodynamic opening of the blood-brain barrier and pathways of brain clearing,” J. Biophotonics 11(8), e201700287 (2018).
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E. Kuan, S. Ivanov, E. Bridenbaugh, G. Victora, W. Wang, E. Childs, A. Platt, C. Jakubzick, R. Mason, A. Gashev, M. Nussenzweig, M. Swartz, M. Dustin, D. Zawieja, and G. Randolph, “Collecting lymphatic vessel permeability facilitates adipose tissue inflammation and distribution of antigen to lymph node – homing adipose tissue dendritic cells,” J. Immunol. 194(11), 5200–5210 (2015).
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E. Kuan, S. Ivanov, E. Bridenbaugh, G. Victora, W. Wang, E. Childs, A. Platt, C. Jakubzick, R. Mason, A. Gashev, M. Nussenzweig, M. Swartz, M. Dustin, D. Zawieja, and G. Randolph, “Collecting lymphatic vessel permeability facilitates adipose tissue inflammation and distribution of antigen to lymph node – homing adipose tissue dendritic cells,” J. Immunol. 194(11), 5200–5210 (2015).
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Kaldy, P.

J. C. Drapier, H. Hirling, J. Wietzerbin, P. Kaldy, and L. C. Kühn, “Biosynthesis of nitric oxide activates iron regulatory factor in macrophages,” EMBO J. 12(9), 3643–3649 (1993).
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Figures (2)

Fig. 1.
Fig. 1. Schematic illustration of PBM of function of mesenteric lymphatics.
Fig. 2.
Fig. 2. The PBM of lymphatic tone and contraction: I – PBM-dose related changes in tone of the mesenteric lymphatic vessels; II – The changes in diameter (um) of the mesenteric lymphatic vessels and lymph flow (um/sec) in them before and after tPBM (10 J/cm2); III - The illustration of changes in diameter of the mesenteric lymphatic vessel in systole (A) and diastole (C) before (A and C) after (B and D) PBM (10 J/cm2), scale bars are 100 µm (see also Visualization 1); IV – The time-related changes of diameter of the mesenteric lymphatic vessels before (A) and after (B) PBM (10 J/cm2), scale bars are 5 µm; V – Schematic illustration of PBM-mediated relaxation of the mesenteric lymphatic vessel; VI - The OCT monitoring of the rate of accumulation of GNRs in dcLN in untreated mice and in mice received tPBM (64 J/cm2 via the intact skull and 10 J/cm2 on the brain surface) after GNRs injection into the cisterna magna, the right lateral ventricle, the cortex, the hippocampus; *** - p < 0.001 vs. basal level. n = 10 in each group; VII – The illustration of clearance of FITC-dextran (green color) from the brain via MLVs (blue color), which are located close to the cerebral veins (red color, labeled by NG2).

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