Abstract

In vivo, longitudinal observation of tumorigenesis in a live mouse model over an extended time period has been actively pursued to obtain a better understanding of the cellular and molecular mechanism in a highly complex tumor microenvironment. However, common intravital imaging approaches based on a conventional laser scanning confocal or a two-photon microscope have been mostly limited to the observation of superficial parts of the solid tumor tissue. In this work, we implemented a small diameter needle-shaped side-view confocal endomicroscope that can be directly inserted into a solid tumor in a minimally-invasive manner in vivo. By inserting the side-view endomicroscope into the breast tumor from the surface, we achieved in vivo depth-wise cellular-level visualization of microvasculature and fluorescently labeled tumor cells located deeply inside the tumor. In addition, we successfully performed longitudinal depth-wise visualization of a growing breast tumor over three weeks in a live mouse model, which revealed dynamic changes in microvasculature such as a decreasing amount of intratumoral blood vessels over time.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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  24. J. K. Kim, J. W. Choi, and S. H. Yun, “350-mu m side-view optical probe for imaging the murine brain in vivo from the cortex to the hypothalamus,” J. Biomed. Opt. 18(5), 050502 (2013).
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  25. J. K. Kim, J. W. Choi, and S. H. Yun, “Optical fine-needle imaging biopsy of the brain,” Biomed. Opt. Express 4(12), 2846–2854 (2013).
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  26. Q. Fang, A. Curatolo, P. Wijesinghe, Y. L. Yeow, J. Hamzah, P. B. Noble, K. Karnowski, D. D. Sampson, R. Ganss, J. K. Kim, W. M. Lee, and B. F. Kennedy, “Ultrahigh-resolution optical coherence elastography through a micro-endoscope: towards in vivo imaging of cellular-scale mechanics,” Biomed. Opt. Express 8(11), 5127–5138 (2017).
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    [Crossref] [PubMed]
  28. 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).
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  29. 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]
  30. I. Park, K. Choe, H. Seo, Y. Hwang, E. Song, J. Ahn, Y. Hwan Jo, and P. Kim, “Intravital imaging of a pulmonary endothelial surface layer in a murine sepsis model,” Biomed. Opt. Express 9(5), 2383–2393 (2018).
    [Crossref] [PubMed]
  31. 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]
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    [Crossref] [PubMed]

2018 (3)

S. Lee, H. Jeong, E. Anguluan, and J. G. Kim, “Biphasic tumor oxygenation during respiratory challenge may predict tumor response duringchemotherapy,” Curr. Opt. Photon. 2, 1–6 (2018).

E. Dondossola, S. Alexander, B. M. Holzapfel, S. Filippini, M. W. Starbuck, R. M. Hoffman, N. Navone, E. M. De-Juan-Pardo, C. J. Logothetis, D. W. Hutmacher, and P. Friedl, “Intravital microscopy of osteolytic progression and therapy response of cancer lesions in the bone,” Sci. Transl. Med. 10(452), eaao5726 (2018).
[Crossref] [PubMed]

I. Park, K. Choe, H. Seo, Y. Hwang, E. Song, J. Ahn, Y. Hwan Jo, and P. Kim, “Intravital imaging of a pulmonary endothelial surface layer in a murine sepsis model,” Biomed. Opt. Express 9(5), 2383–2393 (2018).
[Crossref] [PubMed]

2017 (2)

2016 (1)

S. Qi, H. Li, L. Lu, Z. Qi, L. Liu, L. Chen, G. Shen, L. Fu, Q. Luo, and Z. Zhang, “Long-term intravital imaging of the multicolor-coded tumor microenvironment during combination immunotherapy,” eLife 5, e14756 (2016).
[Crossref] [PubMed]

2015 (2)

S. Junankar, G. Shay, J. Jurczyluk, N. Ali, J. Down, N. Pocock, A. Parker, A. Nguyen, S. Sun, B. Kashemirov, C. E. McKenna, P. I. Croucher, A. Swarbrick, K. Weilbaecher, T. G. Phan, and M. J. Rogers, “Real-time intravital imaging establishes tumor-associated macrophages as the extraskeletal target of bisphosphonate action in cancer,” Cancer Discov. 5(1), 35–42 (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]

2014 (2)

2013 (6)

J. K. Kim, J. W. Choi, and S. H. Yun, “350-mu m side-view optical probe for imaging the murine brain in vivo from the cortex to the hypothalamus,” J. Biomed. Opt. 18(5), 050502 (2013).
[Crossref]

J. K. Kim, J. W. Choi, and S. H. Yun, “Optical fine-needle imaging biopsy of the brain,” Biomed. Opt. Express 4(12), 2846–2854 (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]

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]

L. Ritsma, E. J. A. Steller, S. I. J. Ellenbroek, O. Kranenburg, I. H. Borel Rinkes, and J. van Rheenen, “Surgical implantation of an abdominal imaging window for intravital microscopy,” Nat. Protoc. 8(3), 583–594 (2013).
[Crossref] [PubMed]

Y. Mao, E. T. Keller, D. H. Garfield, K. Shen, and J. Wang, “Stromal cells in tumor microenvironment and breast cancer,” Cancer Metastasis Rev. 32(1-2), 303–315 (2013).
[Crossref] [PubMed]

2012 (2)

B. J. Vakoc, D. Fukumura, R. K. Jain, and B. E. Bouma, “Cancer imaging by optical coherence tomography: preclinical progress and clinical potential,” Nat. Rev. Cancer 12(5), 363–368 (2012).
[Crossref] [PubMed]

L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schäfer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, I. H. B. Rinkes, O. Kranenburg, and J. van Rheenen, “Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
[Crossref] [PubMed]

2011 (3)

R. S. Pillai, D. Lorenser, and D. D. Sampson, “Deep-tissue access with confocal fluorescence microendoscopy through hypodermic needles,” Opt. Express 19(8), 7213–7221 (2011).
[Crossref] [PubMed]

G. M. Palmer, A. N. Fontanella, S. Shan, G. Hanna, G. Zhang, C. L. Fraser, and M. W. Dewhirst, “In vivo optical molecular imaging and analysis in mice using dorsal window chamber models applied to hypoxia, vasculature and fluorescent reporters,” Nat. Protoc. 6(9), 1355–1366 (2011).
[Crossref] [PubMed]

E. Beerling, L. Ritsma, N. Vrisekoop, P. W. B. Derksen, and J. van Rheenen, “Intravital microscopy: new insights into metastasis of tumors,” J. Cell Sci. 124(3), 299–310 (2011).
[Crossref] [PubMed]

2010 (1)

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]

2009 (2)

J. A. Joyce and J. W. Pollard, “Microenvironmental regulation of metastasis,” Nat. Rev. Cancer 9(4), 239–252 (2009).
[Crossref] [PubMed]

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
[Crossref] [PubMed]

2008 (2)

D. Kedrin, B. Gligorijevic, J. Wyckoff, V. V. Verkhusha, J. Condeelis, J. E. Segall, and J. van Rheenen, “Intravital imaging of metastatic behavior through a mammary imaging window,” Nat. Methods 5(12), 1019–1021 (2008).
[Crossref] [PubMed]

T. L. Whiteside, “The tumor microenvironment and its role in promoting tumor growth,” Oncogene 27(45), 5904–5912 (2008).
[Crossref] [PubMed]

2006 (1)

A. Mantovani, T. Schioppa, C. Porta, P. Allavena, and A. Sica, “Role of tumor-associated macrophages in tumor progression and invasion,” Cancer Metastasis Rev. 25(3), 315–322 (2006).
[Crossref] [PubMed]

2004 (2)

A. M. Bode and Z. Dong, “Post-translational modification of p53 in tumorigenesis,” Nat. Rev. Cancer 4(10), 793–805 (2004).
[Crossref] [PubMed]

A.-K. Hadjantonakis and V. E. Papaioannou, “Dynamic in vivo imaging and cell tracking using a histone fluorescent protein fusion in mice,” BMC Biotechnol. 4(1), 33 (2004).
[Crossref] [PubMed]

2003 (1)

G. Bergers and L. E. Benjamin, “Tumorigenesis and the angiogenic switch,” Nat. Rev. Cancer 3(6), 401–410 (2003).
[Crossref] [PubMed]

2002 (1)

R. K. Jain, L. L. Munn, and D. Fukumura, “Dissecting tumour pathophysiology using intravital microscopy,” Nat. Rev. Cancer 2(4), 266–276 (2002).
[Crossref] [PubMed]

2001 (1)

R. K. Jain, “Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy,” Nat. Med. 7(9), 987–989 (2001).
[Crossref] [PubMed]

1993 (1)

H. A. Lehr, M. Leunig, M. D. Menger, D. Nolte, and K. Messmer, “Dorsal skinfold chamber technique for intravital microscopy in nude mice,” Am. J. Pathol. 143(4), 1055–1062 (1993).
[PubMed]

1990 (1)

S. Aznavoorian, M. L. Stracke, H. Krutzsch, E. Schiffmann, and L. A. Liotta, “Signal transduction for chemotaxis and haptotaxis by matrix molecules in tumor cells,” J. Cell Biol. 110(4), 1427–1438 (1990).
[Crossref] [PubMed]

Ahn, J.

Alexander, S.

E. Dondossola, S. Alexander, B. M. Holzapfel, S. Filippini, M. W. Starbuck, R. M. Hoffman, N. Navone, E. M. De-Juan-Pardo, C. J. Logothetis, D. W. Hutmacher, and P. Friedl, “Intravital microscopy of osteolytic progression and therapy response of cancer lesions in the bone,” Sci. Transl. Med. 10(452), eaao5726 (2018).
[Crossref] [PubMed]

Ali, N.

S. Junankar, G. Shay, J. Jurczyluk, N. Ali, J. Down, N. Pocock, A. Parker, A. Nguyen, S. Sun, B. Kashemirov, C. E. McKenna, P. I. Croucher, A. Swarbrick, K. Weilbaecher, T. G. Phan, and M. J. Rogers, “Real-time intravital imaging establishes tumor-associated macrophages as the extraskeletal target of bisphosphonate action in cancer,” Cancer Discov. 5(1), 35–42 (2015).
[Crossref] [PubMed]

Allavena, P.

A. Mantovani, T. Schioppa, C. Porta, P. Allavena, and A. Sica, “Role of tumor-associated macrophages in tumor progression and invasion,” Cancer Metastasis Rev. 25(3), 315–322 (2006).
[Crossref] [PubMed]

Anguluan, E.

Aznavoorian, S.

S. Aznavoorian, M. L. Stracke, H. Krutzsch, E. Schiffmann, and L. A. Liotta, “Signal transduction for chemotaxis and haptotaxis by matrix molecules in tumor cells,” J. Cell Biol. 110(4), 1427–1438 (1990).
[Crossref] [PubMed]

Bae, S.

Beerling, E.

L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schäfer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, I. H. B. Rinkes, O. Kranenburg, and J. van Rheenen, “Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
[Crossref] [PubMed]

E. Beerling, L. Ritsma, N. Vrisekoop, P. W. B. Derksen, and J. van Rheenen, “Intravital microscopy: new insights into metastasis of tumors,” J. Cell Sci. 124(3), 299–310 (2011).
[Crossref] [PubMed]

Benjamin, L. E.

G. Bergers and L. E. Benjamin, “Tumorigenesis and the angiogenic switch,” Nat. Rev. Cancer 3(6), 401–410 (2003).
[Crossref] [PubMed]

Bergers, G.

G. Bergers and L. E. Benjamin, “Tumorigenesis and the angiogenic switch,” Nat. Rev. Cancer 3(6), 401–410 (2003).
[Crossref] [PubMed]

Bode, A. M.

A. M. Bode and Z. Dong, “Post-translational modification of p53 in tumorigenesis,” Nat. Rev. Cancer 4(10), 793–805 (2004).
[Crossref] [PubMed]

Bonhoeffer, T.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
[Crossref] [PubMed]

Borel Rinkes, I. H.

L. Ritsma, E. J. A. Steller, S. I. J. Ellenbroek, O. Kranenburg, I. H. Borel Rinkes, and J. van Rheenen, “Surgical implantation of an abdominal imaging window for intravital microscopy,” Nat. Protoc. 8(3), 583–594 (2013).
[Crossref] [PubMed]

Bouma, B. E.

B. J. Vakoc, D. Fukumura, R. K. Jain, and B. E. Bouma, “Cancer imaging by optical coherence tomography: preclinical progress and clinical potential,” Nat. Rev. Cancer 12(5), 363–368 (2012).
[Crossref] [PubMed]

Chen, L.

S. Qi, H. Li, L. Lu, Z. Qi, L. Liu, L. Chen, G. Shen, L. Fu, Q. Luo, and Z. Zhang, “Long-term intravital imaging of the multicolor-coded tumor microenvironment during combination immunotherapy,” eLife 5, e14756 (2016).
[Crossref] [PubMed]

Choe, K.

Choi, J. W.

J. K. Kim, J. W. Choi, and S. H. Yun, “Optical fine-needle imaging biopsy of the brain,” Biomed. Opt. Express 4(12), 2846–2854 (2013).
[Crossref] [PubMed]

J. K. Kim, J. W. Choi, and S. H. Yun, “350-mu m side-view optical probe for imaging the murine brain in vivo from the cortex to the hypothalamus,” J. Biomed. Opt. 18(5), 050502 (2013).
[Crossref]

Chow, D. K.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
[Crossref] [PubMed]

Chuckowree, J.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
[Crossref] [PubMed]

Chung, E.

S. W. Yoo, H.-J. Park, G. Oh, S. Hwang, M. Yun, T. Wang, Y.-S. Seo, J.-J. Min, K. H. Kim, E.-S. Kim, Y. L. Kim, and E. Chung, “Non-ablative fractional thulium laser irradiation suppresses early tumor growth,” Curr. Opt. Photon. 1(1), 51–59 (2017).
[Crossref]

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).
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Condeelis, J.

D. Kedrin, B. Gligorijevic, J. Wyckoff, V. V. Verkhusha, J. Condeelis, J. E. Segall, and J. van Rheenen, “Intravital imaging of metastatic behavior through a mammary imaging window,” Nat. Methods 5(12), 1019–1021 (2008).
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S. Junankar, G. Shay, J. Jurczyluk, N. Ali, J. Down, N. Pocock, A. Parker, A. Nguyen, S. Sun, B. Kashemirov, C. E. McKenna, P. I. Croucher, A. Swarbrick, K. Weilbaecher, T. G. Phan, and M. J. Rogers, “Real-time intravital imaging establishes tumor-associated macrophages as the extraskeletal target of bisphosphonate action in cancer,” Cancer Discov. 5(1), 35–42 (2015).
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de Graaff, A.

L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schäfer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, I. H. B. Rinkes, O. Kranenburg, and J. van Rheenen, “Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
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L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schäfer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, I. H. B. Rinkes, O. Kranenburg, and J. van Rheenen, “Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
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A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
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E. Dondossola, S. Alexander, B. M. Holzapfel, S. Filippini, M. W. Starbuck, R. M. Hoffman, N. Navone, E. M. De-Juan-Pardo, C. J. Logothetis, D. W. Hutmacher, and P. Friedl, “Intravital microscopy of osteolytic progression and therapy response of cancer lesions in the bone,” Sci. Transl. Med. 10(452), eaao5726 (2018).
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S. Junankar, G. Shay, J. Jurczyluk, N. Ali, J. Down, N. Pocock, A. Parker, A. Nguyen, S. Sun, B. Kashemirov, C. E. McKenna, P. I. Croucher, A. Swarbrick, K. Weilbaecher, T. G. Phan, and M. J. Rogers, “Real-time intravital imaging establishes tumor-associated macrophages as the extraskeletal target of bisphosphonate action in cancer,” Cancer Discov. 5(1), 35–42 (2015).
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Edmond, M.

Ellenbroek, S. I. J.

L. Ritsma, E. J. A. Steller, S. I. J. Ellenbroek, O. Kranenburg, I. H. Borel Rinkes, and J. van Rheenen, “Surgical implantation of an abdominal imaging window for intravital microscopy,” Nat. Protoc. 8(3), 583–594 (2013).
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Fang, Q.

Filippini, S.

E. Dondossola, S. Alexander, B. M. Holzapfel, S. Filippini, M. W. Starbuck, R. M. Hoffman, N. Navone, E. M. De-Juan-Pardo, C. J. Logothetis, D. W. Hutmacher, and P. Friedl, “Intravital microscopy of osteolytic progression and therapy response of cancer lesions in the bone,” Sci. Transl. Med. 10(452), eaao5726 (2018).
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G. M. Palmer, A. N. Fontanella, S. Shan, G. Hanna, G. Zhang, C. L. Fraser, and M. W. Dewhirst, “In vivo optical molecular imaging and analysis in mice using dorsal window chamber models applied to hypoxia, vasculature and fluorescent reporters,” Nat. Protoc. 6(9), 1355–1366 (2011).
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G. M. Palmer, A. N. Fontanella, S. Shan, G. Hanna, G. Zhang, C. L. Fraser, and M. W. Dewhirst, “In vivo optical molecular imaging and analysis in mice using dorsal window chamber models applied to hypoxia, vasculature and fluorescent reporters,” Nat. Protoc. 6(9), 1355–1366 (2011).
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E. Dondossola, S. Alexander, B. M. Holzapfel, S. Filippini, M. W. Starbuck, R. M. Hoffman, N. Navone, E. M. De-Juan-Pardo, C. J. Logothetis, D. W. Hutmacher, and P. Friedl, “Intravital microscopy of osteolytic progression and therapy response of cancer lesions in the bone,” Sci. Transl. Med. 10(452), eaao5726 (2018).
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Fu, L.

S. Qi, H. Li, L. Lu, Z. Qi, L. Liu, L. Chen, G. Shen, L. Fu, Q. Luo, and Z. Zhang, “Long-term intravital imaging of the multicolor-coded tumor microenvironment during combination immunotherapy,” eLife 5, e14756 (2016).
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B. J. Vakoc, D. Fukumura, R. K. Jain, and B. E. Bouma, “Cancer imaging by optical coherence tomography: preclinical progress and clinical potential,” Nat. Rev. Cancer 12(5), 363–368 (2012).
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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).
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R. K. Jain, L. L. Munn, and D. Fukumura, “Dissecting tumour pathophysiology using intravital microscopy,” Nat. Rev. Cancer 2(4), 266–276 (2002).
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Ganss, R.

Garfield, D. H.

Y. Mao, E. T. Keller, D. H. Garfield, K. Shen, and J. Wang, “Stromal cells in tumor microenvironment and breast cancer,” Cancer Metastasis Rev. 32(1-2), 303–315 (2013).
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L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schäfer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, I. H. B. Rinkes, O. Kranenburg, and J. van Rheenen, “Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
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D. Kedrin, B. Gligorijevic, J. Wyckoff, V. V. Verkhusha, J. Condeelis, J. E. Segall, and J. van Rheenen, “Intravital imaging of metastatic behavior through a mammary imaging window,” Nat. Methods 5(12), 1019–1021 (2008).
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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).
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Hadjantonakis, A.-K.

A.-K. Hadjantonakis and V. E. Papaioannou, “Dynamic in vivo imaging and cell tracking using a histone fluorescent protein fusion in mice,” BMC Biotechnol. 4(1), 33 (2004).
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Hamzah, J.

Hanna, G.

G. M. Palmer, A. N. Fontanella, S. Shan, G. Hanna, G. Zhang, C. L. Fraser, and M. W. Dewhirst, “In vivo optical molecular imaging and analysis in mice using dorsal window chamber models applied to hypoxia, vasculature and fluorescent reporters,” Nat. Protoc. 6(9), 1355–1366 (2011).
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A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
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Hoffman, R. M.

E. Dondossola, S. Alexander, B. M. Holzapfel, S. Filippini, M. W. Starbuck, R. M. Hoffman, N. Navone, E. M. De-Juan-Pardo, C. J. Logothetis, D. W. Hutmacher, and P. Friedl, “Intravital microscopy of osteolytic progression and therapy response of cancer lesions in the bone,” Sci. Transl. Med. 10(452), eaao5726 (2018).
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Holtmaat, A.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
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E. Dondossola, S. Alexander, B. M. Holzapfel, S. Filippini, M. W. Starbuck, R. M. Hoffman, N. Navone, E. M. De-Juan-Pardo, C. J. Logothetis, D. W. Hutmacher, and P. Friedl, “Intravital microscopy of osteolytic progression and therapy response of cancer lesions in the bone,” Sci. Transl. Med. 10(452), eaao5726 (2018).
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A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
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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).
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E. Dondossola, S. Alexander, B. M. Holzapfel, S. Filippini, M. W. Starbuck, R. M. Hoffman, N. Navone, E. M. De-Juan-Pardo, C. J. Logothetis, D. W. Hutmacher, and P. Friedl, “Intravital microscopy of osteolytic progression and therapy response of cancer lesions in the bone,” Sci. Transl. Med. 10(452), eaao5726 (2018).
[Crossref] [PubMed]

Hwan Jo, Y.

Hwang, S.

Hwang, Y.

Jain, R. K.

B. J. Vakoc, D. Fukumura, R. K. Jain, and B. E. Bouma, “Cancer imaging by optical coherence tomography: preclinical progress and clinical potential,” Nat. Rev. Cancer 12(5), 363–368 (2012).
[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]

R. K. Jain, L. L. Munn, and D. Fukumura, “Dissecting tumour pathophysiology using intravital microscopy,” Nat. Rev. Cancer 2(4), 266–276 (2002).
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R. K. Jain, “Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy,” Nat. Med. 7(9), 987–989 (2001).
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Jeong, Y. U.

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J. A. Joyce and J. W. Pollard, “Microenvironmental regulation of metastasis,” Nat. Rev. Cancer 9(4), 239–252 (2009).
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S. Junankar, G. Shay, J. Jurczyluk, N. Ali, J. Down, N. Pocock, A. Parker, A. Nguyen, S. Sun, B. Kashemirov, C. E. McKenna, P. I. Croucher, A. Swarbrick, K. Weilbaecher, T. G. Phan, and M. J. Rogers, “Real-time intravital imaging establishes tumor-associated macrophages as the extraskeletal target of bisphosphonate action in cancer,” Cancer Discov. 5(1), 35–42 (2015).
[Crossref] [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).
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S. Junankar, G. Shay, J. Jurczyluk, N. Ali, J. Down, N. Pocock, A. Parker, A. Nguyen, S. Sun, B. Kashemirov, C. E. McKenna, P. I. Croucher, A. Swarbrick, K. Weilbaecher, T. G. Phan, and M. J. Rogers, “Real-time intravital imaging establishes tumor-associated macrophages as the extraskeletal target of bisphosphonate action in cancer,” Cancer Discov. 5(1), 35–42 (2015).
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Karnowski, K.

Kashemirov, B.

S. Junankar, G. Shay, J. Jurczyluk, N. Ali, J. Down, N. Pocock, A. Parker, A. Nguyen, S. Sun, B. Kashemirov, C. E. McKenna, P. I. Croucher, A. Swarbrick, K. Weilbaecher, T. G. Phan, and M. J. Rogers, “Real-time intravital imaging establishes tumor-associated macrophages as the extraskeletal target of bisphosphonate action in cancer,” Cancer Discov. 5(1), 35–42 (2015).
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Keck, T.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
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Kedrin, D.

D. Kedrin, B. Gligorijevic, J. Wyckoff, V. V. Verkhusha, J. Condeelis, J. E. Segall, and J. van Rheenen, “Intravital imaging of metastatic behavior through a mammary imaging window,” Nat. Methods 5(12), 1019–1021 (2008).
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Y. Mao, E. T. Keller, D. H. Garfield, K. Shen, and J. Wang, “Stromal cells in tumor microenvironment and breast cancer,” Cancer Metastasis Rev. 32(1-2), 303–315 (2013).
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Kennedy, B. F.

Kim, E.-S.

Kim, J. G.

Kim, J. K.

Q. Fang, A. Curatolo, P. Wijesinghe, Y. L. Yeow, J. Hamzah, P. B. Noble, K. Karnowski, D. D. Sampson, R. Ganss, J. K. Kim, W. M. Lee, and B. F. Kennedy, “Ultrahigh-resolution optical coherence elastography through a micro-endoscope: towards in vivo imaging of cellular-scale mechanics,” Biomed. Opt. Express 8(11), 5127–5138 (2017).
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J. K. Kim, J. W. Choi, and S. H. Yun, “Optical fine-needle imaging biopsy of the brain,” Biomed. Opt. Express 4(12), 2846–2854 (2013).
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J. K. Kim, J. W. Choi, and S. H. Yun, “350-mu m side-view optical probe for imaging the murine brain in vivo from the cortex to the hypothalamus,” J. Biomed. Opt. 18(5), 050502 (2013).
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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).
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Kim, K. H.

Kim, P.

I. Park, K. Choe, H. Seo, Y. Hwang, E. Song, J. Ahn, Y. Hwan Jo, and P. Kim, “Intravital imaging of a pulmonary endothelial surface layer in a murine sepsis model,” Biomed. Opt. Express 9(5), 2383–2393 (2018).
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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).
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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).
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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).
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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]

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).
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Kim, Y. L.

Kirk, R. W.

Knott, G.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
[Crossref] [PubMed]

Kranenburg, O.

L. Ritsma, E. J. A. Steller, S. I. J. Ellenbroek, O. Kranenburg, I. H. Borel Rinkes, and J. van Rheenen, “Surgical implantation of an abdominal imaging window for intravital microscopy,” Nat. Protoc. 8(3), 583–594 (2013).
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L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schäfer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, I. H. B. Rinkes, O. Kranenburg, and J. van Rheenen, “Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
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S. Aznavoorian, M. L. Stracke, H. Krutzsch, E. Schiffmann, and L. A. Liotta, “Signal transduction for chemotaxis and haptotaxis by matrix molecules in tumor cells,” J. Cell Biol. 110(4), 1427–1438 (1990).
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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).
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Lee, S.

Lee, W. C. A.

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
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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, H.

S. Qi, H. Li, L. Lu, Z. Qi, L. Liu, L. Chen, G. Shen, L. Fu, Q. Luo, and Z. Zhang, “Long-term intravital imaging of the multicolor-coded tumor microenvironment during combination immunotherapy,” eLife 5, e14756 (2016).
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Liotta, L. A.

S. Aznavoorian, M. L. Stracke, H. Krutzsch, E. Schiffmann, and L. A. Liotta, “Signal transduction for chemotaxis and haptotaxis by matrix molecules in tumor cells,” J. Cell Biol. 110(4), 1427–1438 (1990).
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Liu, L.

S. Qi, H. Li, L. Lu, Z. Qi, L. Liu, L. Chen, G. Shen, L. Fu, Q. Luo, and Z. Zhang, “Long-term intravital imaging of the multicolor-coded tumor microenvironment during combination immunotherapy,” eLife 5, e14756 (2016).
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Logothetis, C. J.

E. Dondossola, S. Alexander, B. M. Holzapfel, S. Filippini, M. W. Starbuck, R. M. Hoffman, N. Navone, E. M. De-Juan-Pardo, C. J. Logothetis, D. W. Hutmacher, and P. Friedl, “Intravital microscopy of osteolytic progression and therapy response of cancer lesions in the bone,” Sci. Transl. Med. 10(452), eaao5726 (2018).
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L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schäfer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, I. H. B. Rinkes, O. Kranenburg, and J. van Rheenen, “Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
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S. Junankar, G. Shay, J. Jurczyluk, N. Ali, J. Down, N. Pocock, A. Parker, A. Nguyen, S. Sun, B. Kashemirov, C. E. McKenna, P. I. Croucher, A. Swarbrick, K. Weilbaecher, T. G. Phan, and M. J. Rogers, “Real-time intravital imaging establishes tumor-associated macrophages as the extraskeletal target of bisphosphonate action in cancer,” Cancer Discov. 5(1), 35–42 (2015).
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Nolte, D.

H. A. Lehr, M. Leunig, M. D. Menger, D. Nolte, and K. Messmer, “Dorsal skinfold chamber technique for intravital microscopy in nude mice,” Am. J. Pathol. 143(4), 1055–1062 (1993).
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S. Junankar, G. Shay, J. Jurczyluk, N. Ali, J. Down, N. Pocock, A. Parker, A. Nguyen, S. Sun, B. Kashemirov, C. E. McKenna, P. I. Croucher, A. Swarbrick, K. Weilbaecher, T. G. Phan, and M. J. Rogers, “Real-time intravital imaging establishes tumor-associated macrophages as the extraskeletal target of bisphosphonate action in cancer,” Cancer Discov. 5(1), 35–42 (2015).
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Pocock, N.

S. Junankar, G. Shay, J. Jurczyluk, N. Ali, J. Down, N. Pocock, A. Parker, A. Nguyen, S. Sun, B. Kashemirov, C. E. McKenna, P. I. Croucher, A. Swarbrick, K. Weilbaecher, T. G. Phan, and M. J. Rogers, “Real-time intravital imaging establishes tumor-associated macrophages as the extraskeletal target of bisphosphonate action in cancer,” Cancer Discov. 5(1), 35–42 (2015).
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L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schäfer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, I. H. B. Rinkes, O. Kranenburg, and J. van Rheenen, “Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
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L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schäfer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, I. H. B. Rinkes, O. Kranenburg, and J. van Rheenen, “Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
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L. Ritsma, E. J. A. Steller, S. I. J. Ellenbroek, O. Kranenburg, I. H. Borel Rinkes, and J. van Rheenen, “Surgical implantation of an abdominal imaging window for intravital microscopy,” Nat. Protoc. 8(3), 583–594 (2013).
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L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schäfer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, I. H. B. Rinkes, O. Kranenburg, and J. van Rheenen, “Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
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E. Beerling, L. Ritsma, N. Vrisekoop, P. W. B. Derksen, and J. van Rheenen, “Intravital microscopy: new insights into metastasis of tumors,” J. Cell Sci. 124(3), 299–310 (2011).
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Rogers, M. J.

S. Junankar, G. Shay, J. Jurczyluk, N. Ali, J. Down, N. Pocock, A. Parker, A. Nguyen, S. Sun, B. Kashemirov, C. E. McKenna, P. I. Croucher, A. Swarbrick, K. Weilbaecher, T. G. Phan, and M. J. Rogers, “Real-time intravital imaging establishes tumor-associated macrophages as the extraskeletal target of bisphosphonate action in cancer,” Cancer Discov. 5(1), 35–42 (2015).
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Schäfer, R.

L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schäfer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, I. H. B. Rinkes, O. Kranenburg, and J. van Rheenen, “Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
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A. Mantovani, T. Schioppa, C. Porta, P. Allavena, and A. Sica, “Role of tumor-associated macrophages in tumor progression and invasion,” Cancer Metastasis Rev. 25(3), 315–322 (2006).
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L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schäfer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, I. H. B. Rinkes, O. Kranenburg, and J. van Rheenen, “Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
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D. Kedrin, B. Gligorijevic, J. Wyckoff, V. V. Verkhusha, J. Condeelis, J. E. Segall, and J. van Rheenen, “Intravital imaging of metastatic behavior through a mammary imaging window,” Nat. Methods 5(12), 1019–1021 (2008).
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L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schäfer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, I. H. B. Rinkes, O. Kranenburg, and J. van Rheenen, “Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
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G. M. Palmer, A. N. Fontanella, S. Shan, G. Hanna, G. Zhang, C. L. Fraser, and M. W. Dewhirst, “In vivo optical molecular imaging and analysis in mice using dorsal window chamber models applied to hypoxia, vasculature and fluorescent reporters,” Nat. Protoc. 6(9), 1355–1366 (2011).
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S. Junankar, G. Shay, J. Jurczyluk, N. Ali, J. Down, N. Pocock, A. Parker, A. Nguyen, S. Sun, B. Kashemirov, C. E. McKenna, P. I. Croucher, A. Swarbrick, K. Weilbaecher, T. G. Phan, and M. J. Rogers, “Real-time intravital imaging establishes tumor-associated macrophages as the extraskeletal target of bisphosphonate action in cancer,” Cancer Discov. 5(1), 35–42 (2015).
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Shen, G.

S. Qi, H. Li, L. Lu, Z. Qi, L. Liu, L. Chen, G. Shen, L. Fu, Q. Luo, and Z. Zhang, “Long-term intravital imaging of the multicolor-coded tumor microenvironment during combination immunotherapy,” eLife 5, e14756 (2016).
[Crossref] [PubMed]

Shen, K.

Y. Mao, E. T. Keller, D. H. Garfield, K. Shen, and J. Wang, “Stromal cells in tumor microenvironment and breast cancer,” Cancer Metastasis Rev. 32(1-2), 303–315 (2013).
[Crossref] [PubMed]

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A. Mantovani, T. Schioppa, C. Porta, P. Allavena, and A. Sica, “Role of tumor-associated macrophages in tumor progression and invasion,” Cancer Metastasis Rev. 25(3), 315–322 (2006).
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Song, E.

Starbuck, M. W.

E. Dondossola, S. Alexander, B. M. Holzapfel, S. Filippini, M. W. Starbuck, R. M. Hoffman, N. Navone, E. M. De-Juan-Pardo, C. J. Logothetis, D. W. Hutmacher, and P. Friedl, “Intravital microscopy of osteolytic progression and therapy response of cancer lesions in the bone,” Sci. Transl. Med. 10(452), eaao5726 (2018).
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Steller, E. J. A.

L. Ritsma, E. J. A. Steller, S. I. J. Ellenbroek, O. Kranenburg, I. H. Borel Rinkes, and J. van Rheenen, “Surgical implantation of an abdominal imaging window for intravital microscopy,” Nat. Protoc. 8(3), 583–594 (2013).
[Crossref] [PubMed]

L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schäfer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, I. H. B. Rinkes, O. Kranenburg, and J. van Rheenen, “Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
[Crossref] [PubMed]

Stracke, M. L.

S. Aznavoorian, M. L. Stracke, H. Krutzsch, E. Schiffmann, and L. A. Liotta, “Signal transduction for chemotaxis and haptotaxis by matrix molecules in tumor cells,” J. Cell Biol. 110(4), 1427–1438 (1990).
[Crossref] [PubMed]

Sun, S.

S. Junankar, G. Shay, J. Jurczyluk, N. Ali, J. Down, N. Pocock, A. Parker, A. Nguyen, S. Sun, B. Kashemirov, C. E. McKenna, P. I. Croucher, A. Swarbrick, K. Weilbaecher, T. G. Phan, and M. J. Rogers, “Real-time intravital imaging establishes tumor-associated macrophages as the extraskeletal target of bisphosphonate action in cancer,” Cancer Discov. 5(1), 35–42 (2015).
[Crossref] [PubMed]

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A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
[Crossref] [PubMed]

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S. Junankar, G. Shay, J. Jurczyluk, N. Ali, J. Down, N. Pocock, A. Parker, A. Nguyen, S. Sun, B. Kashemirov, C. E. McKenna, P. I. Croucher, A. Swarbrick, K. Weilbaecher, T. G. Phan, and M. J. Rogers, “Real-time intravital imaging establishes tumor-associated macrophages as the extraskeletal target of bisphosphonate action in cancer,” Cancer Discov. 5(1), 35–42 (2015).
[Crossref] [PubMed]

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A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
[Crossref] [PubMed]

Ueno, T.

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).
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L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schäfer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, I. H. B. Rinkes, O. Kranenburg, and J. van Rheenen, “Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
[Crossref] [PubMed]

van Rheenen, J.

L. Ritsma, E. J. A. Steller, S. I. J. Ellenbroek, O. Kranenburg, I. H. Borel Rinkes, and J. van Rheenen, “Surgical implantation of an abdominal imaging window for intravital microscopy,” Nat. Protoc. 8(3), 583–594 (2013).
[Crossref] [PubMed]

L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schäfer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, I. H. B. Rinkes, O. Kranenburg, and J. van Rheenen, “Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
[Crossref] [PubMed]

E. Beerling, L. Ritsma, N. Vrisekoop, P. W. B. Derksen, and J. van Rheenen, “Intravital microscopy: new insights into metastasis of tumors,” J. Cell Sci. 124(3), 299–310 (2011).
[Crossref] [PubMed]

D. Kedrin, B. Gligorijevic, J. Wyckoff, V. V. Verkhusha, J. Condeelis, J. E. Segall, and J. van Rheenen, “Intravital imaging of metastatic behavior through a mammary imaging window,” Nat. Methods 5(12), 1019–1021 (2008).
[Crossref] [PubMed]

Verkhusha, V. V.

D. Kedrin, B. Gligorijevic, J. Wyckoff, V. V. Verkhusha, J. Condeelis, J. E. Segall, and J. van Rheenen, “Intravital imaging of metastatic behavior through a mammary imaging window,” Nat. Methods 5(12), 1019–1021 (2008).
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Vinokurov, N. A.

Vrisekoop, N.

L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schäfer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, I. H. B. Rinkes, O. Kranenburg, and J. van Rheenen, “Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
[Crossref] [PubMed]

E. Beerling, L. Ritsma, N. Vrisekoop, P. W. B. Derksen, and J. van Rheenen, “Intravital microscopy: new insights into metastasis of tumors,” J. Cell Sci. 124(3), 299–310 (2011).
[Crossref] [PubMed]

Wang, J.

Y. Mao, E. T. Keller, D. H. Garfield, K. Shen, and J. Wang, “Stromal cells in tumor microenvironment and breast cancer,” Cancer Metastasis Rev. 32(1-2), 303–315 (2013).
[Crossref] [PubMed]

Wang, T.

Weilbaecher, K.

S. Junankar, G. Shay, J. Jurczyluk, N. Ali, J. Down, N. Pocock, A. Parker, A. Nguyen, S. Sun, B. Kashemirov, C. E. McKenna, P. I. Croucher, A. Swarbrick, K. Weilbaecher, T. G. Phan, and M. J. Rogers, “Real-time intravital imaging establishes tumor-associated macrophages as the extraskeletal target of bisphosphonate action in cancer,” Cancer Discov. 5(1), 35–42 (2015).
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T. L. Whiteside, “The tumor microenvironment and its role in promoting tumor growth,” Oncogene 27(45), 5904–5912 (2008).
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A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
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Wyckoff, J.

D. Kedrin, B. Gligorijevic, J. Wyckoff, V. V. Verkhusha, J. Condeelis, J. E. Segall, and J. van Rheenen, “Intravital imaging of metastatic behavior through a mammary imaging window,” Nat. Methods 5(12), 1019–1021 (2008).
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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, X.

Yeow, Y. L.

Yoo, S. W.

Yun, M.

Yun, S. H.

J. K. Kim, J. W. Choi, and S. H. Yun, “Optical fine-needle imaging biopsy of the brain,” Biomed. Opt. Express 4(12), 2846–2854 (2013).
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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).
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J. K. Kim, J. W. Choi, and S. H. Yun, “350-mu m side-view optical probe for imaging the murine brain in vivo from the cortex to the hypothalamus,” J. Biomed. Opt. 18(5), 050502 (2013).
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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).
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Zhang, G.

G. M. Palmer, A. N. Fontanella, S. Shan, G. Hanna, G. Zhang, C. L. Fraser, and M. W. Dewhirst, “In vivo optical molecular imaging and analysis in mice using dorsal window chamber models applied to hypoxia, vasculature and fluorescent reporters,” Nat. Protoc. 6(9), 1355–1366 (2011).
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Zhang, Z.

S. Qi, H. Li, L. Lu, Z. Qi, L. Liu, L. Chen, G. Shen, L. Fu, Q. Luo, and Z. Zhang, “Long-term intravital imaging of the multicolor-coded tumor microenvironment during combination immunotherapy,” eLife 5, e14756 (2016).
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Zomer, A.

L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schäfer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, I. H. B. Rinkes, O. Kranenburg, and J. van Rheenen, “Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
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Biomed. Opt. Express (5)

BMC Biotechnol. (1)

A.-K. Hadjantonakis and V. E. Papaioannou, “Dynamic in vivo imaging and cell tracking using a histone fluorescent protein fusion in mice,” BMC Biotechnol. 4(1), 33 (2004).
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Cancer Discov. (1)

S. Junankar, G. Shay, J. Jurczyluk, N. Ali, J. Down, N. Pocock, A. Parker, A. Nguyen, S. Sun, B. Kashemirov, C. E. McKenna, P. I. Croucher, A. Swarbrick, K. Weilbaecher, T. G. Phan, and M. J. Rogers, “Real-time intravital imaging establishes tumor-associated macrophages as the extraskeletal target of bisphosphonate action in cancer,” Cancer Discov. 5(1), 35–42 (2015).
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Cancer Metastasis Rev. (2)

Y. Mao, E. T. Keller, D. H. Garfield, K. Shen, and J. Wang, “Stromal cells in tumor microenvironment and breast cancer,” Cancer Metastasis Rev. 32(1-2), 303–315 (2013).
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A. Mantovani, T. Schioppa, C. Porta, P. Allavena, and A. Sica, “Role of tumor-associated macrophages in tumor progression and invasion,” Cancer Metastasis Rev. 25(3), 315–322 (2006).
[Crossref] [PubMed]

Circ. Res. (1)

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]

Curr. Opt. Photon. (2)

eLife (1)

S. Qi, H. Li, L. Lu, Z. Qi, L. Liu, L. Chen, G. Shen, L. Fu, Q. Luo, and Z. Zhang, “Long-term intravital imaging of the multicolor-coded tumor microenvironment during combination immunotherapy,” eLife 5, e14756 (2016).
[Crossref] [PubMed]

J. Biomed. Opt. (2)

J. K. Kim, J. W. Choi, and S. H. Yun, “350-mu m side-view optical probe for imaging the murine brain in vivo from the cortex to the hypothalamus,” J. Biomed. Opt. 18(5), 050502 (2013).
[Crossref]

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).
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J. Cell Biol. (1)

S. Aznavoorian, M. L. Stracke, H. Krutzsch, E. Schiffmann, and L. A. Liotta, “Signal transduction for chemotaxis and haptotaxis by matrix molecules in tumor cells,” J. Cell Biol. 110(4), 1427–1438 (1990).
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J. Cell Sci. (1)

E. Beerling, L. Ritsma, N. Vrisekoop, P. W. B. Derksen, and J. van Rheenen, “Intravital microscopy: new insights into metastasis of tumors,” J. Cell Sci. 124(3), 299–310 (2011).
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Nat. Med. (1)

R. K. Jain, “Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy,” Nat. Med. 7(9), 987–989 (2001).
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Nat. Methods (2)

D. Kedrin, B. Gligorijevic, J. Wyckoff, V. V. Verkhusha, J. Condeelis, J. E. Segall, and J. van Rheenen, “Intravital imaging of metastatic behavior through a mammary imaging window,” Nat. Methods 5(12), 1019–1021 (2008).
[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. (3)

L. Ritsma, E. J. A. Steller, S. I. J. Ellenbroek, O. Kranenburg, I. H. Borel Rinkes, and J. van Rheenen, “Surgical implantation of an abdominal imaging window for intravital microscopy,” Nat. Protoc. 8(3), 583–594 (2013).
[Crossref] [PubMed]

G. M. Palmer, A. N. Fontanella, S. Shan, G. Hanna, G. Zhang, C. L. Fraser, and M. W. Dewhirst, “In vivo optical molecular imaging and analysis in mice using dorsal window chamber models applied to hypoxia, vasculature and fluorescent reporters,” Nat. Protoc. 6(9), 1355–1366 (2011).
[Crossref] [PubMed]

A. Holtmaat, T. Bonhoeffer, D. K. Chow, J. Chuckowree, V. De Paola, S. B. Hofer, M. Hübener, T. Keck, G. Knott, W. C. A. Lee, R. Mostany, T. D. Mrsic-Flogel, E. Nedivi, C. Portera-Cailliau, K. Svoboda, J. T. Trachtenberg, and L. Wilbrecht, “Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window,” Nat. Protoc. 4(8), 1128–1144 (2009).
[Crossref] [PubMed]

Nat. Rev. Cancer (5)

B. J. Vakoc, D. Fukumura, R. K. Jain, and B. E. Bouma, “Cancer imaging by optical coherence tomography: preclinical progress and clinical potential,” Nat. Rev. Cancer 12(5), 363–368 (2012).
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A. M. Bode and Z. Dong, “Post-translational modification of p53 in tumorigenesis,” Nat. Rev. Cancer 4(10), 793–805 (2004).
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G. Bergers and L. E. Benjamin, “Tumorigenesis and the angiogenic switch,” Nat. Rev. Cancer 3(6), 401–410 (2003).
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J. A. Joyce and J. W. Pollard, “Microenvironmental regulation of metastasis,” Nat. Rev. Cancer 9(4), 239–252 (2009).
[Crossref] [PubMed]

Oncogene (1)

T. L. Whiteside, “The tumor microenvironment and its role in promoting tumor growth,” Oncogene 27(45), 5904–5912 (2008).
[Crossref] [PubMed]

Opt. Express (2)

Sci. Transl. Med. (2)

L. Ritsma, E. J. A. Steller, E. Beerling, C. J. M. Loomans, A. Zomer, C. Gerlach, N. Vrisekoop, D. Seinstra, L. van Gurp, R. Schäfer, D. A. Raats, A. de Graaff, T. N. Schumacher, E. J. P. de Koning, I. H. B. Rinkes, O. Kranenburg, and J. van Rheenen, “Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis,” Sci. Transl. Med. 4(158), 158ra145 (2012).
[Crossref] [PubMed]

E. Dondossola, S. Alexander, B. M. Holzapfel, S. Filippini, M. W. Starbuck, R. M. Hoffman, N. Navone, E. M. De-Juan-Pardo, C. J. Logothetis, D. W. Hutmacher, and P. Friedl, “Intravital microscopy of osteolytic progression and therapy response of cancer lesions in the bone,” Sci. Transl. Med. 10(452), eaao5726 (2018).
[Crossref] [PubMed]

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Figures (4)

Fig. 1
Fig. 1 (a) Schematic of the fabricated needle-shaped side-view endomicroscope packaged into a 22G hypodermal needle tip. (b) Schematic and photo of the custom-built video-rate laser-scanning confocal microscope system and the needle-shaped side-view endomicroscope positioned under the objective lens (M: Mirror, ND: Neutral density filter, DBS: Dichroic beam splitter, BPF: Band pass filter, PMT: Photomultiplier tube). (c) Schematic of the insertion of needle-shaped side-view endomicroscope into the skin to visualize deeper region in vivo. The dotted circle presents a representative single FOV image showing nuclei (green) and blood vessels (red) acquired in the dermis. Scale bar: 50 μm. (d) Depth-wise mosaic image constructed by continuously acquired single FOV images during the insertion of the side-view endomicroscope in the mouse dorsal skin. Scale bar: 100 μm.
Fig. 2
Fig. 2 (a) Schematic of the in vivo depth-wise visualization of solid breast tumor tissue with needle-shaped side-view endomicroscope. (b) Representative single FOV endomicroscopic images obtained at various depth in the solid breast tumor at day 9 and 21. Scale bars: 50 μm.
Fig. 3
Fig. 3 Depth-wise mosaic images of the growing tumor obtained from a single mouse from day 9 to 21 with 3 day intervals after the inoculation of the cancer cells with continuous insertion of the needle-shaped side-view endomicroscope from the top to the bottom of the breast tumor.
Fig. 4
Fig. 4 (a) Representative depth-wise in vivo side-view endomicroscopic imaging result of orthotropic breast tumor moue model and conventional ex vivo confocal microscopic imaging result of cryosectioned tumor tissue slices dissected from similar mouse model at day 9 after 4T1 cancer cells inoculation. Scale bars: 1 mm. (b, c) Comparative quantitative analysis of whole tumor height and the intra-tumoral vessel area using the side-view needle-type side-view endomicroscopic tumor images and the cryosectioned confocal microscopic tumor images at day 9, 12, 15, 18, and 21.