Abstract

In cancer research there is a fundamental need for animal models that allow the in vivo longitudinal visualization and quantification of tumor development, nanotherapeutic delivery, the tumor microenvironment including blood vessels, macrophages, fibroblasts, immune cells, and extracellular matrix, and the tissue response to treatment. To address this need, we developed a novel mouse ocular xenograft model. Green fluorescent protein (GFP) expressing human glioblastoma cells (between 500 and 10,000) were implanted into the subretinal space of immunodeficient mice (56 eyes). The resultant xenografts were imaged in vivo non-invasively with combined fluorescence scanning laser ophthalmoscopy (SLO) and volumetric optical coherence tomography (OCT) for a period up to several months. Most xenografts exhibited a latent phase followed by a stable or rapidly increasing volume, but about 1/3 underwent spontaneous remission. After prescribed growth, a population of tumors was treated with intravenously delivered doxorubicin-containing porphyrin and cholic acid-based nanoparticles (“nanodox”). Fluorescence resonance energy transfer (FRET) emission (doxorubicin → porphyrin) was used to localize nanodox in the xenografts, and 690 nm light exposure to activate it. Such photo-nanotherapy was highly effective in reducing tumor volume. Histopathology and flow cytometry revealed CD4 + and CD8 + immune cell infiltration of xenografts. Overall, the ocular model shows potential for examining the relationships between neoplastic growth, neovascularization and other features of the immune microenvironment, and for evaluating treatment response longitudinally in vivo.

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

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References

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2017 (5)

M. B. Gutowski, L. Wilson, R. N. Van Gelder, and K. L. Pepple, “In Vivo Bioluminescence Imaging for Longitudinal Monitoring of Inflammation in Animal Models of Uveitis,” Invest. Ophthalmol. Vis. Sci. 58(3), 1521–1528 (2017).
[Crossref] [PubMed]

A. M. Meleis, A. Mahtabfar, S. Danish, and R. A. Foty, “Dexamethasone-mediated inhibition of Glioblastoma neurosphere dispersal in an ex vivo organotypic neural assay,” PLoS One 12(10), e0186483 (2017).
[Crossref] [PubMed]

M. J. Ochocinska, B. V. Zlokovic, P. C. Searson, A. T. Crowder, R. P. Kraig, J. Y. Ljubimova, T. G. Mainprize, W. A. Banks, R. Q. Warren, A. Kindzelski, W. Timmer, and C. H. Liu, “NIH workshop report on the trans-agency blood-brain interface workshop 2016: exploring key challenges and opportunities associated with the blood, brain and their interface,” Fluids Barriers CNS 14(1), 12 (2017).
[Crossref] [PubMed]

N. Shonka, V. A. Venur, and M. S. Ahluwalia, “Targeted Treatment of Brain Metastases,” Curr. Neurol. Neurosci. Rep. 17(4), 37 (2017).
[Crossref] [PubMed]

T. Ashizawa, A. Iizuka, C. Nonomura, R. Kondou, C. Maeda, H. Miyata, T. Sugino, K. Mitsuya, N. Hayashi, Y. Nakasu, K. Maruyama, K. Yamaguchi, I. Katano, M. Ito, and Y. Akiyama, “Antitumor Effect of Programmed Death-1 (PD-1) Blockade in Humanized the NOG-MHC Double Knockout Mouse,” Clin. Cancer Res. 23(1), 149–158 (2017).
[Crossref] [PubMed]

2016 (3)

J. J. Morton, G. Bird, Y. Refaeli, and A. Jimeno, “Humanized Mouse Xenograft Models: Narrowing the Tumor-Microenvironment Gap,” Cancer Res. 76(21), 6153–6158 (2016).
[Crossref] [PubMed]

S. Mo, B. Krawitz, E. Efstathiadis, L. Geyman, R. Weitz, T. Y. Chui, J. Carroll, A. Dubra, and R. B. Rosen, “Imaging Foveal Microvasculature: Optical Coherence Tomography Angiography Versus Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Vis. Sci. 57(9), OCT130 (2016).
[Crossref] [PubMed]

J. Lee and R. Rosen, “Optical Coherence Tomography Angiography in Diabetes,” Curr. Diab. Rep. 16(12), 123 (2016).
[Crossref] [PubMed]

2015 (8)

F. W. van Leeuwen, J. C. Hardwick, and A. R. van Erkel, “Luminescence-based Imaging Approaches in the Field of Interventional Molecular Imaging,” Radiology 276(1), 12–29 (2015).
[Crossref] [PubMed]

E. Salmon, C. Bernard Ir, and R. Hustinx, “Pitfalls and Limitations of PET/CT in Brain Imaging,” Semin. Nucl. Med. 45(6), 541–551 (2015).
[Crossref] [PubMed]

C.-P. Day, G. Merlino, and T. Van Dyke, “Preclinical mouse cancer models: a maze of opportunities and challenges,” Cell 163(1), 39–53 (2015).
[Crossref] [PubMed]

P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, and et al.., “In vivo wide-field multispectral SLO-OCT mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Muller glia, and mapping of the mouse choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref] [PubMed]

P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy-optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Müller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref] [PubMed]

R. J. Zawadzki, P. Zhang, A. Zam, E. B. Miller, M. Goswami, X. Wang, R. S. Jonnal, S. H. Lee, D. Y. Kim, J. G. Flannery, J. S. Werner, M. E. Burns, and E. N. Pugh, “Adaptive-optics SLO imaging combined with widefield OCT and SLO enables precise 3D localization of fluorescent cells in the mouse retina,” Biomed. Opt. Express 6(6), 2191–2210 (2015).
[Crossref] [PubMed]

B. Sparta, M. Pargett, M. Minguet, K. Distor, G. Bell, and J. G. Albeck, “Receptor Level Mechanisms Are Required for Epidermal Growth Factor (EGF)-stimulated Extracellular Signal-regulated Kinase (ERK) Activity Pulses,” J. Biol. Chem. 290(41), 24784–24792 (2015).
[Crossref] [PubMed]

L. Legroux, C. L. Pittet, D. Beauseigle, G. Deblois, A. Prat, and N. Arbour, “An optimized method to process mouse CNS to simultaneously analyze neural cells and leukocytes by flow cytometry,” J. Neurosci. Methods 247, 23–31 (2015).
[Crossref] [PubMed]

2014 (9)

A. J. Iqbal, E. McNeill, T. S. Kapellos, D. Regan-Komito, S. Norman, S. Burd, N. Smart, D. E. Machemer, E. Stylianou, H. McShane, K. M. Channon, A. Chawla, and D. R. Greaves, “Human CD68 promoter GFP transgenic mice allow analysis of monocyte to macrophage differentiation in vivo,” Blood 124(15), e33–e44 (2014).
[Crossref] [PubMed]

S. U. Shah, A. Mashayekhi, C. L. Shields, H. S. Walia, G. B. Hubbard, J. Zhang, and J. A. Shields, “Uveal metastasis from lung cancer: clinical features, treatment, and outcome in 194 patients,” Ophthalmology 121(1), 352–357 (2014).
[Crossref] [PubMed]

E. S. Levine, A. Zam, P. Zhang, A. Pechko, X. Wang, P. FitzGerald, E. N. Pugh, R. J. Zawadzki, and M. E. Burns, “Rapid light-induced activation of retinal microglia in mice lacking Arrestin-1,” Vision Res. 102, 71–79 (2014).
[Crossref] [PubMed]

Y. Jian, J. Xu, M. A. Gradowski, S. Bonora, R. J. Zawadzki, and M. V. Sarunic, “Wavefront sensorless adaptive optics optical coherence tomography for in vivo retinal imaging in mice,” Biomed. Opt. Express 5(2), 547–559 (2014).
[Crossref] [PubMed]

D. M. Schwartz, J. Fingler, D. Y. Kim, R. J. Zawadzki, L. S. Morse, S. S. Park, S. E. Fraser, and J. S. Werner, “Phase-variance optical coherence tomography: a technique for noninvasive angiography,” Ophthalmology 121(1), 180–187 (2014).
[Crossref] [PubMed]

A. Z. Zam and E. N. Pugh Jr, andR. J. Zawadzki, “Evaluation of OCT for quantitative in vivo measurements of changes in neural tissue scattering in longitudinal studies of retinal degeneration in mice,” Proc. SPIE 8934, 893422 (2014).
[Crossref]

A. Z. Zam and E. N. Pugh Jr, andR. J. Zawadzki, “Evaluation of OCT for quantitative in vivo measurements of changes in neural tissue scattering in longitudinal studies of retinal degeneration in mice,” Proc. SPIE 8934, 893422 (2014).
[Crossref]

P. Z. Zhang and E. N. Pugh, Jr, andR. J. Zawadzki, “Evaluation of state-of-the-art imaging systems for in vivo monitoring of retinal structure in mice: current capabilities and limitations,” Proc. SPIE 8930, 893005 (2014).
[Crossref]

P. Z. Zhang and E. N. Pugh, Jr, andR. J. Zawadzki, “Evaluation of state-of-the-art imaging systems for in vivo monitoring of retinal structure in mice: current capabilities and limitations,” Proc. SPIE 8930, 893005 (2014).
[Crossref]

Y. Li, T. Y. Lin, Y. Luo, Q. Liu, W. Xiao, W. Guo, D. Lac, H. Zhang, C. Feng, S. Wachsmann-Hogiu, J. H. Walton, S. R. Cherry, D. J. Rowland, D. Kukis, C. Pan, and K. S. Lam, “A smart and versatile theranostic nanomedicine platform based on nanoporphyrin,” Nat. Commun. 5(1), 4712 (2014).
[Crossref] [PubMed]

C. Ricard, F. Stanchi, G. Rougon, and F. Debarbieux, “An orthotopic glioblastoma mouse model maintaining brain parenchymal physical constraints and suitable for intravital two-photon microscopy,” J. Vis. Exp. 86, 86 (2014).
[Crossref] [PubMed]

2013 (8)

L. García-Rojas, G. Adame-Ocampo, G. Mendoza-Vázquez, E. Alexánderson, and J. L. Tovilla-Canales, “Orbital positron emission tomography/computed tomography (PET/CT) imaging findings in Graves ophthalmopathy,” BMC Res. Notes 6(1), 353 (2013).
[Crossref] [PubMed]

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

M. Saxena and G. Christofori, “Rebuilding cancer metastasis in the mouse,” Mol. Oncol. 7(2), 283–296 (2013).
[Crossref] [PubMed]

R. Muzaffar, M. A. Shousha, L. Sarajlic, and M. M. Osman, “Ophthalmologic abnormalities on FDG-PET/CT: a pictorial essay,” Cancer Imaging 13(1), 100–112 (2013).
[Crossref] [PubMed]

H. Matsumoto, J. W. Miller, and D. G. Vavvas, “Retinal detachment model in rodents by subretinal injection of sodium hyaluronate,” J. Vis. Exp. 79, 50660 (2013).
[Crossref] [PubMed]

D. Y. Kim, J. Fingler, R. J. Zawadzki, S. S. Park, L. S. Morse, D. M. Schwartz, S. E. Fraser, and J. S. Werner, “Optical imaging of the chorioretinal vasculature in the living human eye,” Proc. Natl. Acad. Sci. U.S.A. 110(35), 14354–14359 (2013).
[Crossref] [PubMed]

R. C. Eagle, “The pathology of ocular cancer,” Eye (Lond.) 27(2), 128–136 (2013).
[Crossref] [PubMed]

V. M. L. Cohen, “Ocular metastases,” Eye (Lond.) 27(2), 137–141 (2013).
[Crossref] [PubMed]

2012 (1)

T. L. Chiu, M. J. Wang, and C. C. Su, “The treatment of glioblastoma multiforme through activation of microglia and TRAIL induced by rAAV2-mediated IL-12 in a syngeneic rat model,” J. Biomed. Sci. 19(1), 45 (2012).
[Crossref] [PubMed]

2011 (3)

D. Y. Kim, J. Fingler, J. S. Werner, D. M. Schwartz, S. E. Fraser, and R. J. Zawadzki, “In vivo volumetric imaging of human retinal circulation with phase-variance optical coherence tomography,” Biomed. Opt. Express 2(6), 1504–1513 (2011).
[Crossref] [PubMed]

D. R. Williams, “Imaging single cells in the living retina,” Vision Res. 51(13), 1379–1396 (2011).
[Crossref] [PubMed]

R. P. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. Med. 17(2), 223–228 (2011).
[Crossref] [PubMed]

2010 (1)

N. Saederup, A. E. Cardona, K. Croft, M. Mizutani, A. C. Cotleur, C. L. Tsou, R. M. Ransohoff, and I. F. Charo, “Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice,” PLoS One 5(10), e13693 (2010).
[Crossref] [PubMed]

2009 (1)

G. E. Koehl, A. Gaumann, and E. K. Geissler, “Intravital microscopy of tumor angiogenesis and regression in the dorsal skin fold chamber: mechanistic insights and preclinical testing of therapeutic strategies,” Clin. Exp. Metastasis 26(4), 329–344 (2009).
[Crossref] [PubMed]

2008 (3)

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]

J. Miyamoto, K. Tatsuzawa, K. Owada, T. Kawabe, H. Sasajima, and K. Mineura, “Usefulness and Limitations of Fluorine-18-Fluorodeoxyglucose Positron Emission Tomography for the Detection of Malignancy of Orbital Tumors,” Neurol. Med. Chir. (Tokyo) 48(11), 495–499 (2008).
[Crossref] [PubMed]

W. Drexler and J. G. Fujimoto, “State-of-the-art retinal optical coherence tomography,” Prog. Retin. Eye Res. 27(1), 45–88 (2008).
[Crossref] [PubMed]

2007 (2)

R. J. Zawadzki, A. R. Fuller, D. F. Wiley, B. Hamann, S. S. Choi, and J. S. Werner, “Adaptation of a support vector machine algorithm for segmentation and visualization of retinal structures in volumetric optical coherence tomography data sets,” J. Biomed. Opt. 12(4), 041206 (2007).
[Crossref] [PubMed]

A. Fuller, R. Zawadzki, S. Choi, D. Wiley, J. Werner, and B. Hamann, “Segmentation of three-dimensional retinal image data,” IEEE Trans. Vis. Comput. Graph. 13(6), 1719–1726 (2007).
[Crossref] [PubMed]

2004 (1)

P. F. Sharp, A. Manivannan, H. Xu, and J. V. Forrester, “The scanning laser ophthalmoscope--a review of its role in bioscience and medicine,” Phys. Med. Biol. 49(7), 1085–1096 (2004).
[Crossref] [PubMed]

2003 (1)

H. Demirci, C. L. Shields, A. N. Chao, and J. A. Shields, “Uveal metastasis from breast cancer in 264 patients,” Am. J. Ophthalmol. 136(2), 264–271 (2003).
[Crossref] [PubMed]

1991 (1)

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[Crossref] [PubMed]

Adame-Ocampo, G.

L. García-Rojas, G. Adame-Ocampo, G. Mendoza-Vázquez, E. Alexánderson, and J. L. Tovilla-Canales, “Orbital positron emission tomography/computed tomography (PET/CT) imaging findings in Graves ophthalmopathy,” BMC Res. Notes 6(1), 353 (2013).
[Crossref] [PubMed]

Ahluwalia, M. S.

N. Shonka, V. A. Venur, and M. S. Ahluwalia, “Targeted Treatment of Brain Metastases,” Curr. Neurol. Neurosci. Rep. 17(4), 37 (2017).
[Crossref] [PubMed]

Akiyama, Y.

T. Ashizawa, A. Iizuka, C. Nonomura, R. Kondou, C. Maeda, H. Miyata, T. Sugino, K. Mitsuya, N. Hayashi, Y. Nakasu, K. Maruyama, K. Yamaguchi, I. Katano, M. Ito, and Y. Akiyama, “Antitumor Effect of Programmed Death-1 (PD-1) Blockade in Humanized the NOG-MHC Double Knockout Mouse,” Clin. Cancer Res. 23(1), 149–158 (2017).
[Crossref] [PubMed]

Albeck, J. G.

B. Sparta, M. Pargett, M. Minguet, K. Distor, G. Bell, and J. G. Albeck, “Receptor Level Mechanisms Are Required for Epidermal Growth Factor (EGF)-stimulated Extracellular Signal-regulated Kinase (ERK) Activity Pulses,” J. Biol. Chem. 290(41), 24784–24792 (2015).
[Crossref] [PubMed]

Alexánderson, E.

L. García-Rojas, G. Adame-Ocampo, G. Mendoza-Vázquez, E. Alexánderson, and J. L. Tovilla-Canales, “Orbital positron emission tomography/computed tomography (PET/CT) imaging findings in Graves ophthalmopathy,” BMC Res. Notes 6(1), 353 (2013).
[Crossref] [PubMed]

Arbour, N.

L. Legroux, C. L. Pittet, D. Beauseigle, G. Deblois, A. Prat, and N. Arbour, “An optimized method to process mouse CNS to simultaneously analyze neural cells and leukocytes by flow cytometry,” J. Neurosci. Methods 247, 23–31 (2015).
[Crossref] [PubMed]

Ashizawa, T.

T. Ashizawa, A. Iizuka, C. Nonomura, R. Kondou, C. Maeda, H. Miyata, T. Sugino, K. Mitsuya, N. Hayashi, Y. Nakasu, K. Maruyama, K. Yamaguchi, I. Katano, M. Ito, and Y. Akiyama, “Antitumor Effect of Programmed Death-1 (PD-1) Blockade in Humanized the NOG-MHC Double Knockout Mouse,” Clin. Cancer Res. 23(1), 149–158 (2017).
[Crossref] [PubMed]

Attardo, A.

R. P. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. Med. 17(2), 223–228 (2011).
[Crossref] [PubMed]

Banks, W. A.

M. J. Ochocinska, B. V. Zlokovic, P. C. Searson, A. T. Crowder, R. P. Kraig, J. Y. Ljubimova, T. G. Mainprize, W. A. Banks, R. Q. Warren, A. Kindzelski, W. Timmer, and C. H. Liu, “NIH workshop report on the trans-agency blood-brain interface workshop 2016: exploring key challenges and opportunities associated with the blood, brain and their interface,” Fluids Barriers CNS 14(1), 12 (2017).
[Crossref] [PubMed]

Barretto, R. P.

R. P. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. Med. 17(2), 223–228 (2011).
[Crossref] [PubMed]

Beauseigle, D.

L. Legroux, C. L. Pittet, D. Beauseigle, G. Deblois, A. Prat, and N. Arbour, “An optimized method to process mouse CNS to simultaneously analyze neural cells and leukocytes by flow cytometry,” J. Neurosci. Methods 247, 23–31 (2015).
[Crossref] [PubMed]

Bell, G.

B. Sparta, M. Pargett, M. Minguet, K. Distor, G. Bell, and J. G. Albeck, “Receptor Level Mechanisms Are Required for Epidermal Growth Factor (EGF)-stimulated Extracellular Signal-regulated Kinase (ERK) Activity Pulses,” J. Biol. Chem. 290(41), 24784–24792 (2015).
[Crossref] [PubMed]

Bernard Ir, C.

E. Salmon, C. Bernard Ir, and R. Hustinx, “Pitfalls and Limitations of PET/CT in Brain Imaging,” Semin. Nucl. Med. 45(6), 541–551 (2015).
[Crossref] [PubMed]

Bird, G.

J. J. Morton, G. Bird, Y. Refaeli, and A. Jimeno, “Humanized Mouse Xenograft Models: Narrowing the Tumor-Microenvironment Gap,” Cancer Res. 76(21), 6153–6158 (2016).
[Crossref] [PubMed]

Bonora, S.

Borel Rinkes, I. H. M.

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

Burd, S.

A. J. Iqbal, E. McNeill, T. S. Kapellos, D. Regan-Komito, S. Norman, S. Burd, N. Smart, D. E. Machemer, E. Stylianou, H. McShane, K. M. Channon, A. Chawla, and D. R. Greaves, “Human CD68 promoter GFP transgenic mice allow analysis of monocyte to macrophage differentiation in vivo,” Blood 124(15), e33–e44 (2014).
[Crossref] [PubMed]

Burns, M. E.

R. J. Zawadzki, P. Zhang, A. Zam, E. B. Miller, M. Goswami, X. Wang, R. S. Jonnal, S. H. Lee, D. Y. Kim, J. G. Flannery, J. S. Werner, M. E. Burns, and E. N. Pugh, “Adaptive-optics SLO imaging combined with widefield OCT and SLO enables precise 3D localization of fluorescent cells in the mouse retina,” Biomed. Opt. Express 6(6), 2191–2210 (2015).
[Crossref] [PubMed]

P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy-optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Müller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref] [PubMed]

E. S. Levine, A. Zam, P. Zhang, A. Pechko, X. Wang, P. FitzGerald, E. N. Pugh, R. J. Zawadzki, and M. E. Burns, “Rapid light-induced activation of retinal microglia in mice lacking Arrestin-1,” Vision Res. 102, 71–79 (2014).
[Crossref] [PubMed]

Capps, G.

R. P. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. Med. 17(2), 223–228 (2011).
[Crossref] [PubMed]

Cardona, A. E.

N. Saederup, A. E. Cardona, K. Croft, M. Mizutani, A. C. Cotleur, C. L. Tsou, R. M. Ransohoff, and I. F. Charo, “Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice,” PLoS One 5(10), e13693 (2010).
[Crossref] [PubMed]

Carroll, J.

S. Mo, B. Krawitz, E. Efstathiadis, L. Geyman, R. Weitz, T. Y. Chui, J. Carroll, A. Dubra, and R. B. Rosen, “Imaging Foveal Microvasculature: Optical Coherence Tomography Angiography Versus Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Vis. Sci. 57(9), OCT130 (2016).
[Crossref] [PubMed]

Chang, W.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[Crossref] [PubMed]

Channon, K. M.

A. J. Iqbal, E. McNeill, T. S. Kapellos, D. Regan-Komito, S. Norman, S. Burd, N. Smart, D. E. Machemer, E. Stylianou, H. McShane, K. M. Channon, A. Chawla, and D. R. Greaves, “Human CD68 promoter GFP transgenic mice allow analysis of monocyte to macrophage differentiation in vivo,” Blood 124(15), e33–e44 (2014).
[Crossref] [PubMed]

Chao, A. N.

H. Demirci, C. L. Shields, A. N. Chao, and J. A. Shields, “Uveal metastasis from breast cancer in 264 patients,” Am. J. Ophthalmol. 136(2), 264–271 (2003).
[Crossref] [PubMed]

Charo, I. F.

N. Saederup, A. E. Cardona, K. Croft, M. Mizutani, A. C. Cotleur, C. L. Tsou, R. M. Ransohoff, and I. F. Charo, “Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice,” PLoS One 5(10), e13693 (2010).
[Crossref] [PubMed]

Chawla, A.

A. J. Iqbal, E. McNeill, T. S. Kapellos, D. Regan-Komito, S. Norman, S. Burd, N. Smart, D. E. Machemer, E. Stylianou, H. McShane, K. M. Channon, A. Chawla, and D. R. Greaves, “Human CD68 promoter GFP transgenic mice allow analysis of monocyte to macrophage differentiation in vivo,” Blood 124(15), e33–e44 (2014).
[Crossref] [PubMed]

Cherry, S. R.

Y. Li, T. Y. Lin, Y. Luo, Q. Liu, W. Xiao, W. Guo, D. Lac, H. Zhang, C. Feng, S. Wachsmann-Hogiu, J. H. Walton, S. R. Cherry, D. J. Rowland, D. Kukis, C. Pan, and K. S. Lam, “A smart and versatile theranostic nanomedicine platform based on nanoporphyrin,” Nat. Commun. 5(1), 4712 (2014).
[Crossref] [PubMed]

Chiu, T. L.

T. L. Chiu, M. J. Wang, and C. C. Su, “The treatment of glioblastoma multiforme through activation of microglia and TRAIL induced by rAAV2-mediated IL-12 in a syngeneic rat model,” J. Biomed. Sci. 19(1), 45 (2012).
[Crossref] [PubMed]

Choi, S.

A. Fuller, R. Zawadzki, S. Choi, D. Wiley, J. Werner, and B. Hamann, “Segmentation of three-dimensional retinal image data,” IEEE Trans. Vis. Comput. Graph. 13(6), 1719–1726 (2007).
[Crossref] [PubMed]

Choi, S. S.

R. J. Zawadzki, A. R. Fuller, D. F. Wiley, B. Hamann, S. S. Choi, and J. S. Werner, “Adaptation of a support vector machine algorithm for segmentation and visualization of retinal structures in volumetric optical coherence tomography data sets,” J. Biomed. Opt. 12(4), 041206 (2007).
[Crossref] [PubMed]

Christofori, G.

M. Saxena and G. Christofori, “Rebuilding cancer metastasis in the mouse,” Mol. Oncol. 7(2), 283–296 (2013).
[Crossref] [PubMed]

Chui, T. Y.

S. Mo, B. Krawitz, E. Efstathiadis, L. Geyman, R. Weitz, T. Y. Chui, J. Carroll, A. Dubra, and R. B. Rosen, “Imaging Foveal Microvasculature: Optical Coherence Tomography Angiography Versus Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Vis. Sci. 57(9), OCT130 (2016).
[Crossref] [PubMed]

Cohen, V. M. L.

V. M. L. Cohen, “Ocular metastases,” Eye (Lond.) 27(2), 137–141 (2013).
[Crossref] [PubMed]

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).
[Crossref] [PubMed]

Cotleur, A. C.

N. Saederup, A. E. Cardona, K. Croft, M. Mizutani, A. C. Cotleur, C. L. Tsou, R. M. Ransohoff, and I. F. Charo, “Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice,” PLoS One 5(10), e13693 (2010).
[Crossref] [PubMed]

Croft, K.

N. Saederup, A. E. Cardona, K. Croft, M. Mizutani, A. C. Cotleur, C. L. Tsou, R. M. Ransohoff, and I. F. Charo, “Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice,” PLoS One 5(10), e13693 (2010).
[Crossref] [PubMed]

Crowder, A. T.

M. J. Ochocinska, B. V. Zlokovic, P. C. Searson, A. T. Crowder, R. P. Kraig, J. Y. Ljubimova, T. G. Mainprize, W. A. Banks, R. Q. Warren, A. Kindzelski, W. Timmer, and C. H. Liu, “NIH workshop report on the trans-agency blood-brain interface workshop 2016: exploring key challenges and opportunities associated with the blood, brain and their interface,” Fluids Barriers CNS 14(1), 12 (2017).
[Crossref] [PubMed]

Danish, S.

A. M. Meleis, A. Mahtabfar, S. Danish, and R. A. Foty, “Dexamethasone-mediated inhibition of Glioblastoma neurosphere dispersal in an ex vivo organotypic neural assay,” PLoS One 12(10), e0186483 (2017).
[Crossref] [PubMed]

Day, C.-P.

C.-P. Day, G. Merlino, and T. Van Dyke, “Preclinical mouse cancer models: a maze of opportunities and challenges,” Cell 163(1), 39–53 (2015).
[Crossref] [PubMed]

Debarbieux, F.

C. Ricard, F. Stanchi, G. Rougon, and F. Debarbieux, “An orthotopic glioblastoma mouse model maintaining brain parenchymal physical constraints and suitable for intravital two-photon microscopy,” J. Vis. Exp. 86, 86 (2014).
[Crossref] [PubMed]

Deblois, G.

L. Legroux, C. L. Pittet, D. Beauseigle, G. Deblois, A. Prat, and N. Arbour, “An optimized method to process mouse CNS to simultaneously analyze neural cells and leukocytes by flow cytometry,” J. Neurosci. Methods 247, 23–31 (2015).
[Crossref] [PubMed]

Demirci, H.

H. Demirci, C. L. Shields, A. N. Chao, and J. A. Shields, “Uveal metastasis from breast cancer in 264 patients,” Am. J. Ophthalmol. 136(2), 264–271 (2003).
[Crossref] [PubMed]

Distor, K.

B. Sparta, M. Pargett, M. Minguet, K. Distor, G. Bell, and J. G. Albeck, “Receptor Level Mechanisms Are Required for Epidermal Growth Factor (EGF)-stimulated Extracellular Signal-regulated Kinase (ERK) Activity Pulses,” J. Biol. Chem. 290(41), 24784–24792 (2015).
[Crossref] [PubMed]

Drexler, W.

W. Drexler and J. G. Fujimoto, “State-of-the-art retinal optical coherence tomography,” Prog. Retin. Eye Res. 27(1), 45–88 (2008).
[Crossref] [PubMed]

Dubra, A.

S. Mo, B. Krawitz, E. Efstathiadis, L. Geyman, R. Weitz, T. Y. Chui, J. Carroll, A. Dubra, and R. B. Rosen, “Imaging Foveal Microvasculature: Optical Coherence Tomography Angiography Versus Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Vis. Sci. 57(9), OCT130 (2016).
[Crossref] [PubMed]

Eagle, R. C.

R. C. Eagle, “The pathology of ocular cancer,” Eye (Lond.) 27(2), 128–136 (2013).
[Crossref] [PubMed]

Efstathiadis, E.

S. Mo, B. Krawitz, E. Efstathiadis, L. Geyman, R. Weitz, T. Y. Chui, J. Carroll, A. Dubra, and R. B. Rosen, “Imaging Foveal Microvasculature: Optical Coherence Tomography Angiography Versus Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Vis. Sci. 57(9), OCT130 (2016).
[Crossref] [PubMed]

Ellenbroek, S. I. J.

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

et,

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[Crossref] [PubMed]

Feng, C.

Y. Li, T. Y. Lin, Y. Luo, Q. Liu, W. Xiao, W. Guo, D. Lac, H. Zhang, C. Feng, S. Wachsmann-Hogiu, J. H. Walton, S. R. Cherry, D. J. Rowland, D. Kukis, C. Pan, and K. S. Lam, “A smart and versatile theranostic nanomedicine platform based on nanoporphyrin,” Nat. Commun. 5(1), 4712 (2014).
[Crossref] [PubMed]

Fingler, J.

D. M. Schwartz, J. Fingler, D. Y. Kim, R. J. Zawadzki, L. S. Morse, S. S. Park, S. E. Fraser, and J. S. Werner, “Phase-variance optical coherence tomography: a technique for noninvasive angiography,” Ophthalmology 121(1), 180–187 (2014).
[Crossref] [PubMed]

D. Y. Kim, J. Fingler, R. J. Zawadzki, S. S. Park, L. S. Morse, D. M. Schwartz, S. E. Fraser, and J. S. Werner, “Optical imaging of the chorioretinal vasculature in the living human eye,” Proc. Natl. Acad. Sci. U.S.A. 110(35), 14354–14359 (2013).
[Crossref] [PubMed]

D. Y. Kim, J. Fingler, J. S. Werner, D. M. Schwartz, S. E. Fraser, and R. J. Zawadzki, “In vivo volumetric imaging of human retinal circulation with phase-variance optical coherence tomography,” Biomed. Opt. Express 2(6), 1504–1513 (2011).
[Crossref] [PubMed]

FitzGerald, P.

E. S. Levine, A. Zam, P. Zhang, A. Pechko, X. Wang, P. FitzGerald, E. N. Pugh, R. J. Zawadzki, and M. E. Burns, “Rapid light-induced activation of retinal microglia in mice lacking Arrestin-1,” Vision Res. 102, 71–79 (2014).
[Crossref] [PubMed]

Flannery, J. G.

Flotte, T.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[Crossref] [PubMed]

Forrester, J. V.

P. F. Sharp, A. Manivannan, H. Xu, and J. V. Forrester, “The scanning laser ophthalmoscope--a review of its role in bioscience and medicine,” Phys. Med. Biol. 49(7), 1085–1096 (2004).
[Crossref] [PubMed]

Foty, R. A.

A. M. Meleis, A. Mahtabfar, S. Danish, and R. A. Foty, “Dexamethasone-mediated inhibition of Glioblastoma neurosphere dispersal in an ex vivo organotypic neural assay,” PLoS One 12(10), e0186483 (2017).
[Crossref] [PubMed]

Fraser, S. E.

D. M. Schwartz, J. Fingler, D. Y. Kim, R. J. Zawadzki, L. S. Morse, S. S. Park, S. E. Fraser, and J. S. Werner, “Phase-variance optical coherence tomography: a technique for noninvasive angiography,” Ophthalmology 121(1), 180–187 (2014).
[Crossref] [PubMed]

D. Y. Kim, J. Fingler, R. J. Zawadzki, S. S. Park, L. S. Morse, D. M. Schwartz, S. E. Fraser, and J. S. Werner, “Optical imaging of the chorioretinal vasculature in the living human eye,” Proc. Natl. Acad. Sci. U.S.A. 110(35), 14354–14359 (2013).
[Crossref] [PubMed]

D. Y. Kim, J. Fingler, J. S. Werner, D. M. Schwartz, S. E. Fraser, and R. J. Zawadzki, “In vivo volumetric imaging of human retinal circulation with phase-variance optical coherence tomography,” Biomed. Opt. Express 2(6), 1504–1513 (2011).
[Crossref] [PubMed]

Fujimoto, J. G.

W. Drexler and J. G. Fujimoto, “State-of-the-art retinal optical coherence tomography,” Prog. Retin. Eye Res. 27(1), 45–88 (2008).
[Crossref] [PubMed]

Fuller, A.

A. Fuller, R. Zawadzki, S. Choi, D. Wiley, J. Werner, and B. Hamann, “Segmentation of three-dimensional retinal image data,” IEEE Trans. Vis. Comput. Graph. 13(6), 1719–1726 (2007).
[Crossref] [PubMed]

Fuller, A. R.

R. J. Zawadzki, A. R. Fuller, D. F. Wiley, B. Hamann, S. S. Choi, and J. S. Werner, “Adaptation of a support vector machine algorithm for segmentation and visualization of retinal structures in volumetric optical coherence tomography data sets,” J. Biomed. Opt. 12(4), 041206 (2007).
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B. Sparta, M. Pargett, M. Minguet, K. Distor, G. Bell, and J. G. Albeck, “Receptor Level Mechanisms Are Required for Epidermal Growth Factor (EGF)-stimulated Extracellular Signal-regulated Kinase (ERK) Activity Pulses,” J. Biol. Chem. 290(41), 24784–24792 (2015).
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D. M. Schwartz, J. Fingler, D. Y. Kim, R. J. Zawadzki, L. S. Morse, S. S. Park, S. E. Fraser, and J. S. Werner, “Phase-variance optical coherence tomography: a technique for noninvasive angiography,” Ophthalmology 121(1), 180–187 (2014).
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J. J. Morton, G. Bird, Y. Refaeli, and A. Jimeno, “Humanized Mouse Xenograft Models: Narrowing the Tumor-Microenvironment Gap,” Cancer Res. 76(21), 6153–6158 (2016).
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R. Muzaffar, M. A. Shousha, L. Sarajlic, and M. M. Osman, “Ophthalmologic abnormalities on FDG-PET/CT: a pictorial essay,” Cancer Imaging 13(1), 100–112 (2013).
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D. M. Schwartz, J. Fingler, D. Y. Kim, R. J. Zawadzki, L. S. Morse, S. S. Park, S. E. Fraser, and J. S. Werner, “Phase-variance optical coherence tomography: a technique for noninvasive angiography,” Ophthalmology 121(1), 180–187 (2014).
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A. Z. Zam and E. N. Pugh Jr, andR. J. Zawadzki, “Evaluation of OCT for quantitative in vivo measurements of changes in neural tissue scattering in longitudinal studies of retinal degeneration in mice,” Proc. SPIE 8934, 893422 (2014).
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P. Z. Zhang and E. N. Pugh, Jr, andR. J. Zawadzki, “Evaluation of state-of-the-art imaging systems for in vivo monitoring of retinal structure in mice: current capabilities and limitations,” Proc. SPIE 8930, 893005 (2014).
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E. S. Levine, A. Zam, P. Zhang, A. Pechko, X. Wang, P. FitzGerald, E. N. Pugh, R. J. Zawadzki, and M. E. Burns, “Rapid light-induced activation of retinal microglia in mice lacking Arrestin-1,” Vision Res. 102, 71–79 (2014).
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D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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N. Saederup, A. E. Cardona, K. Croft, M. Mizutani, A. C. Cotleur, C. L. Tsou, R. M. Ransohoff, and I. F. Charo, “Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice,” PLoS One 5(10), e13693 (2010).
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J. J. Morton, G. Bird, Y. Refaeli, and A. Jimeno, “Humanized Mouse Xenograft Models: Narrowing the Tumor-Microenvironment Gap,” Cancer Res. 76(21), 6153–6158 (2016).
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J. Lee and R. Rosen, “Optical Coherence Tomography Angiography in Diabetes,” Curr. Diab. Rep. 16(12), 123 (2016).
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S. Mo, B. Krawitz, E. Efstathiadis, L. Geyman, R. Weitz, T. Y. Chui, J. Carroll, A. Dubra, and R. B. Rosen, “Imaging Foveal Microvasculature: Optical Coherence Tomography Angiography Versus Adaptive Optics Scanning Light Ophthalmoscope Fluorescein Angiography,” Invest. Ophthalmol. Vis. Sci. 57(9), OCT130 (2016).
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Y. Li, T. Y. Lin, Y. Luo, Q. Liu, W. Xiao, W. Guo, D. Lac, H. Zhang, C. Feng, S. Wachsmann-Hogiu, J. H. Walton, S. R. Cherry, D. J. Rowland, D. Kukis, C. Pan, and K. S. Lam, “A smart and versatile theranostic nanomedicine platform based on nanoporphyrin,” Nat. Commun. 5(1), 4712 (2014).
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N. Saederup, A. E. Cardona, K. Croft, M. Mizutani, A. C. Cotleur, C. L. Tsou, R. M. Ransohoff, and I. F. Charo, “Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice,” PLoS One 5(10), e13693 (2010).
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R. Muzaffar, M. A. Shousha, L. Sarajlic, and M. M. Osman, “Ophthalmologic abnormalities on FDG-PET/CT: a pictorial essay,” Cancer Imaging 13(1), 100–112 (2013).
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P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy-optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Müller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
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Y. Jian, J. Xu, M. A. Gradowski, S. Bonora, R. J. Zawadzki, and M. V. Sarunic, “Wavefront sensorless adaptive optics optical coherence tomography for in vivo retinal imaging in mice,” Biomed. Opt. Express 5(2), 547–559 (2014).
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J. Miyamoto, K. Tatsuzawa, K. Owada, T. Kawabe, H. Sasajima, and K. Mineura, “Usefulness and Limitations of Fluorine-18-Fluorodeoxyglucose Positron Emission Tomography for the Detection of Malignancy of Orbital Tumors,” Neurol. Med. Chir. (Tokyo) 48(11), 495–499 (2008).
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D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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D. M. Schwartz, J. Fingler, D. Y. Kim, R. J. Zawadzki, L. S. Morse, S. S. Park, S. E. Fraser, and J. S. Werner, “Phase-variance optical coherence tomography: a technique for noninvasive angiography,” Ophthalmology 121(1), 180–187 (2014).
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D. Y. Kim, J. Fingler, J. S. Werner, D. M. Schwartz, S. E. Fraser, and R. J. Zawadzki, “In vivo volumetric imaging of human retinal circulation with phase-variance optical coherence tomography,” Biomed. Opt. Express 2(6), 1504–1513 (2011).
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S. U. Shah, A. Mashayekhi, C. L. Shields, H. S. Walia, G. B. Hubbard, J. Zhang, and J. A. Shields, “Uveal metastasis from lung cancer: clinical features, treatment, and outcome in 194 patients,” Ophthalmology 121(1), 352–357 (2014).
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N. Shonka, V. A. Venur, and M. S. Ahluwalia, “Targeted Treatment of Brain Metastases,” Curr. Neurol. Neurosci. Rep. 17(4), 37 (2017).
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R. Muzaffar, M. A. Shousha, L. Sarajlic, and M. M. Osman, “Ophthalmologic abnormalities on FDG-PET/CT: a pictorial essay,” Cancer Imaging 13(1), 100–112 (2013).
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A. J. Iqbal, E. McNeill, T. S. Kapellos, D. Regan-Komito, S. Norman, S. Burd, N. Smart, D. E. Machemer, E. Stylianou, H. McShane, K. M. Channon, A. Chawla, and D. R. Greaves, “Human CD68 promoter GFP transgenic mice allow analysis of monocyte to macrophage differentiation in vivo,” Blood 124(15), e33–e44 (2014).
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B. Sparta, M. Pargett, M. Minguet, K. Distor, G. Bell, and J. G. Albeck, “Receptor Level Mechanisms Are Required for Epidermal Growth Factor (EGF)-stimulated Extracellular Signal-regulated Kinase (ERK) Activity Pulses,” J. Biol. Chem. 290(41), 24784–24792 (2015).
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C. Ricard, F. Stanchi, G. Rougon, and F. Debarbieux, “An orthotopic glioblastoma mouse model maintaining brain parenchymal physical constraints and suitable for intravital two-photon microscopy,” J. Vis. Exp. 86, 86 (2014).
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L. Ritsma, E. J. A. Steller, S. I. J. Ellenbroek, O. Kranenburg, I. H. M. 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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D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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A. J. Iqbal, E. McNeill, T. S. Kapellos, D. Regan-Komito, S. Norman, S. Burd, N. Smart, D. E. Machemer, E. Stylianou, H. McShane, K. M. Channon, A. Chawla, and D. R. Greaves, “Human CD68 promoter GFP transgenic mice allow analysis of monocyte to macrophage differentiation in vivo,” Blood 124(15), e33–e44 (2014).
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D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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R. J. Zawadzki, A. R. Fuller, D. F. Wiley, B. Hamann, S. S. Choi, and J. S. Werner, “Adaptation of a support vector machine algorithm for segmentation and visualization of retinal structures in volumetric optical coherence tomography data sets,” J. Biomed. Opt. 12(4), 041206 (2007).
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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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P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, and et al.., “In vivo wide-field multispectral SLO-OCT mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Muller glia, and mapping of the mouse choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
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E. S. Levine, A. Zam, P. Zhang, A. Pechko, X. Wang, P. FitzGerald, E. N. Pugh, R. J. Zawadzki, and M. E. Burns, “Rapid light-induced activation of retinal microglia in mice lacking Arrestin-1,” Vision Res. 102, 71–79 (2014).
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A. Z. Zam and E. N. Pugh Jr, andR. J. Zawadzki, “Evaluation of OCT for quantitative in vivo measurements of changes in neural tissue scattering in longitudinal studies of retinal degeneration in mice,” Proc. SPIE 8934, 893422 (2014).
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Zawadzki, R.

A. Fuller, R. Zawadzki, S. Choi, D. Wiley, J. Werner, and B. Hamann, “Segmentation of three-dimensional retinal image data,” IEEE Trans. Vis. Comput. Graph. 13(6), 1719–1726 (2007).
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Zawadzki, R. J.

R. J. Zawadzki, P. Zhang, A. Zam, E. B. Miller, M. Goswami, X. Wang, R. S. Jonnal, S. H. Lee, D. Y. Kim, J. G. Flannery, J. S. Werner, M. E. Burns, and E. N. Pugh, “Adaptive-optics SLO imaging combined with widefield OCT and SLO enables precise 3D localization of fluorescent cells in the mouse retina,” Biomed. Opt. Express 6(6), 2191–2210 (2015).
[Crossref] [PubMed]

P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy-optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Müller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref] [PubMed]

D. M. Schwartz, J. Fingler, D. Y. Kim, R. J. Zawadzki, L. S. Morse, S. S. Park, S. E. Fraser, and J. S. Werner, “Phase-variance optical coherence tomography: a technique for noninvasive angiography,” Ophthalmology 121(1), 180–187 (2014).
[Crossref] [PubMed]

P. Z. Zhang and E. N. Pugh, Jr, andR. J. Zawadzki, “Evaluation of state-of-the-art imaging systems for in vivo monitoring of retinal structure in mice: current capabilities and limitations,” Proc. SPIE 8930, 893005 (2014).
[Crossref]

A. Z. Zam and E. N. Pugh Jr, andR. J. Zawadzki, “Evaluation of OCT for quantitative in vivo measurements of changes in neural tissue scattering in longitudinal studies of retinal degeneration in mice,” Proc. SPIE 8934, 893422 (2014).
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E. S. Levine, A. Zam, P. Zhang, A. Pechko, X. Wang, P. FitzGerald, E. N. Pugh, R. J. Zawadzki, and M. E. Burns, “Rapid light-induced activation of retinal microglia in mice lacking Arrestin-1,” Vision Res. 102, 71–79 (2014).
[Crossref] [PubMed]

D. Y. Kim, J. Fingler, R. J. Zawadzki, S. S. Park, L. S. Morse, D. M. Schwartz, S. E. Fraser, and J. S. Werner, “Optical imaging of the chorioretinal vasculature in the living human eye,” Proc. Natl. Acad. Sci. U.S.A. 110(35), 14354–14359 (2013).
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D. Y. Kim, J. Fingler, J. S. Werner, D. M. Schwartz, S. E. Fraser, and R. J. Zawadzki, “In vivo volumetric imaging of human retinal circulation with phase-variance optical coherence tomography,” Biomed. Opt. Express 2(6), 1504–1513 (2011).
[Crossref] [PubMed]

R. J. Zawadzki, A. R. Fuller, D. F. Wiley, B. Hamann, S. S. Choi, and J. S. Werner, “Adaptation of a support vector machine algorithm for segmentation and visualization of retinal structures in volumetric optical coherence tomography data sets,” J. Biomed. Opt. 12(4), 041206 (2007).
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Zhang, H.

Y. Li, T. Y. Lin, Y. Luo, Q. Liu, W. Xiao, W. Guo, D. Lac, H. Zhang, C. Feng, S. Wachsmann-Hogiu, J. H. Walton, S. R. Cherry, D. J. Rowland, D. Kukis, C. Pan, and K. S. Lam, “A smart and versatile theranostic nanomedicine platform based on nanoporphyrin,” Nat. Commun. 5(1), 4712 (2014).
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Zhang, J.

S. U. Shah, A. Mashayekhi, C. L. Shields, H. S. Walia, G. B. Hubbard, J. Zhang, and J. A. Shields, “Uveal metastasis from lung cancer: clinical features, treatment, and outcome in 194 patients,” Ophthalmology 121(1), 352–357 (2014).
[Crossref] [PubMed]

Zhang, P.

R. J. Zawadzki, P. Zhang, A. Zam, E. B. Miller, M. Goswami, X. Wang, R. S. Jonnal, S. H. Lee, D. Y. Kim, J. G. Flannery, J. S. Werner, M. E. Burns, and E. N. Pugh, “Adaptive-optics SLO imaging combined with widefield OCT and SLO enables precise 3D localization of fluorescent cells in the mouse retina,” Biomed. Opt. Express 6(6), 2191–2210 (2015).
[Crossref] [PubMed]

P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, and et al.., “In vivo wide-field multispectral SLO-OCT mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Muller glia, and mapping of the mouse choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref] [PubMed]

P. Zhang, A. Zam, Y. Jian, X. Wang, Y. Li, K. S. Lam, M. E. Burns, M. V. Sarunic, E. N. Pugh, and R. J. Zawadzki, “In vivo wide-field multispectral scanning laser ophthalmoscopy-optical coherence tomography mouse retinal imager: longitudinal imaging of ganglion cells, microglia, and Müller glia, and mapping of the mouse retinal and choroidal vasculature,” J. Biomed. Opt. 20(12), 126005 (2015).
[Crossref] [PubMed]

E. S. Levine, A. Zam, P. Zhang, A. Pechko, X. Wang, P. FitzGerald, E. N. Pugh, R. J. Zawadzki, and M. E. Burns, “Rapid light-induced activation of retinal microglia in mice lacking Arrestin-1,” Vision Res. 102, 71–79 (2014).
[Crossref] [PubMed]

Zhang, P. Z.

P. Z. Zhang and E. N. Pugh, Jr, andR. J. Zawadzki, “Evaluation of state-of-the-art imaging systems for in vivo monitoring of retinal structure in mice: current capabilities and limitations,” Proc. SPIE 8930, 893005 (2014).
[Crossref]

Ziv, Y.

R. P. Barretto, T. H. Ko, J. C. Jung, T. J. Wang, G. Capps, A. C. Waters, Y. Ziv, A. Attardo, L. Recht, and M. J. Schnitzer, “Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy,” Nat. Med. 17(2), 223–228 (2011).
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M. J. Ochocinska, B. V. Zlokovic, P. C. Searson, A. T. Crowder, R. P. Kraig, J. Y. Ljubimova, T. G. Mainprize, W. A. Banks, R. Q. Warren, A. Kindzelski, W. Timmer, and C. H. Liu, “NIH workshop report on the trans-agency blood-brain interface workshop 2016: exploring key challenges and opportunities associated with the blood, brain and their interface,” Fluids Barriers CNS 14(1), 12 (2017).
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Am. J. Ophthalmol. (1)

H. Demirci, C. L. Shields, A. N. Chao, and J. A. Shields, “Uveal metastasis from breast cancer in 264 patients,” Am. J. Ophthalmol. 136(2), 264–271 (2003).
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Biomed. Opt. Express (3)

Blood (1)

A. J. Iqbal, E. McNeill, T. S. Kapellos, D. Regan-Komito, S. Norman, S. Burd, N. Smart, D. E. Machemer, E. Stylianou, H. McShane, K. M. Channon, A. Chawla, and D. R. Greaves, “Human CD68 promoter GFP transgenic mice allow analysis of monocyte to macrophage differentiation in vivo,” Blood 124(15), e33–e44 (2014).
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BMC Res. Notes (1)

L. García-Rojas, G. Adame-Ocampo, G. Mendoza-Vázquez, E. Alexánderson, and J. L. Tovilla-Canales, “Orbital positron emission tomography/computed tomography (PET/CT) imaging findings in Graves ophthalmopathy,” BMC Res. Notes 6(1), 353 (2013).
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Cancer Imaging (1)

R. Muzaffar, M. A. Shousha, L. Sarajlic, and M. M. Osman, “Ophthalmologic abnormalities on FDG-PET/CT: a pictorial essay,” Cancer Imaging 13(1), 100–112 (2013).
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J. J. Morton, G. Bird, Y. Refaeli, and A. Jimeno, “Humanized Mouse Xenograft Models: Narrowing the Tumor-Microenvironment Gap,” Cancer Res. 76(21), 6153–6158 (2016).
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Cell (1)

C.-P. Day, G. Merlino, and T. Van Dyke, “Preclinical mouse cancer models: a maze of opportunities and challenges,” Cell 163(1), 39–53 (2015).
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Clin. Cancer Res. (1)

T. Ashizawa, A. Iizuka, C. Nonomura, R. Kondou, C. Maeda, H. Miyata, T. Sugino, K. Mitsuya, N. Hayashi, Y. Nakasu, K. Maruyama, K. Yamaguchi, I. Katano, M. Ito, and Y. Akiyama, “Antitumor Effect of Programmed Death-1 (PD-1) Blockade in Humanized the NOG-MHC Double Knockout Mouse,” Clin. Cancer Res. 23(1), 149–158 (2017).
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Clin. Exp. Metastasis (1)

G. E. Koehl, A. Gaumann, and E. K. Geissler, “Intravital microscopy of tumor angiogenesis and regression in the dorsal skin fold chamber: mechanistic insights and preclinical testing of therapeutic strategies,” Clin. Exp. Metastasis 26(4), 329–344 (2009).
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Curr. Diab. Rep. (1)

J. Lee and R. Rosen, “Optical Coherence Tomography Angiography in Diabetes,” Curr. Diab. Rep. 16(12), 123 (2016).
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Curr. Neurol. Neurosci. Rep. (1)

N. Shonka, V. A. Venur, and M. S. Ahluwalia, “Targeted Treatment of Brain Metastases,” Curr. Neurol. Neurosci. Rep. 17(4), 37 (2017).
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Eye (Lond.) (2)

R. C. Eagle, “The pathology of ocular cancer,” Eye (Lond.) 27(2), 128–136 (2013).
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V. M. L. Cohen, “Ocular metastases,” Eye (Lond.) 27(2), 137–141 (2013).
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Fluids Barriers CNS (1)

M. J. Ochocinska, B. V. Zlokovic, P. C. Searson, A. T. Crowder, R. P. Kraig, J. Y. Ljubimova, T. G. Mainprize, W. A. Banks, R. Q. Warren, A. Kindzelski, W. Timmer, and C. H. Liu, “NIH workshop report on the trans-agency blood-brain interface workshop 2016: exploring key challenges and opportunities associated with the blood, brain and their interface,” Fluids Barriers CNS 14(1), 12 (2017).
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IEEE Trans. Vis. Comput. Graph. (1)

A. Fuller, R. Zawadzki, S. Choi, D. Wiley, J. Werner, and B. Hamann, “Segmentation of three-dimensional retinal image data,” IEEE Trans. Vis. Comput. Graph. 13(6), 1719–1726 (2007).
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Supplementary Material (2)

NameDescription
» Visualization 1       OCT volumetric morphology. A 3D representation of the data is provided.
» Visualization 2       OCTA volumetric angiography: A 3D representation of the data is provided.

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Figures (6)

Fig. 1
Fig. 1 Creation and characterization of ocular xenograft with simultaneous SLO (ex 488 nm) and OCT (860 nm) over wide retinal field (51 deg visual angle). A. Schematic illustrating subretinal transplantation of GFP+ glioblastoma cells. B-E. All panels are from the right eye of a nude mouse injected 104 days earlier with 5000 glioblastoma cells. B, C. SLO reflectance and fluorescence images. The optic nerve head is in the lower right corner of the images. Inset in C: GFP emission spectrum recorded from the two regions defined by the boxes superimposed on the fluorescence image. Da-f. OCT volumetric results. A 3D representation is shown (see also Visualization 1), along with en face presentations at left of the tumor (b, yellow), the retina anterior to the tumor (a, red) and posterior (c, blue; choroid, sclera). (In the central 3D representations z-axis grid lines are spaced 80 μm apart, while x-,y- grid lines are spaced by160 μm.) (d) En face view of the anterior retinal surface with the segmented tumor superimposed as a color-coded depth map. (e) and (f) B-scans (depth slices) taken at the position of red dashed arrow in (d); in (e) the strength of the OCT signal is presented in gray-scale, while in (f) the structures are color coded as in (a-c). Ea-f. OCT volumetric angiography: the same OCT data were analyzed for temporal phase-variance, which identifies voxels with red blood cell movement. The color coding of the panels corresponds to that used in E (see also Visualization 2). Note the tumor neovascularization in Eb, d, f.
Fig. 2
Fig. 2 Growth pattern of an ocular glioblastoma measured in vivo over a two-month period. The upper two rows of images present SLO reflectance and fluorescence images, while the bottom three rows present simultaneously acquired OCT results (see Fig. 1 for details of acquisition and analysis). The series of green SLO fluorescence images reveal the location of GFP+ cells (the baseline fluorescence image was contrast-enhanced to reveal the major blood vessels). The first row of OCT images presents a color-coded tumor thickness map overlaid on an en face image of the superficial retinal surface (gray). The second row presents a depth color-coded angiogram, with red corresponding to the normal superficial retinal vasculature, yellow the tumor vasculature, and blue the posterior (choroidal) vasculature (as in Fig. 1(E)). The lowermost row of images presents slices (B-scans) through the OCT volume data taken at the position of the white dashed lines overlaid on the thickness maps, with depth color coding corresponding to that used for the vasculature and serve to illustrate the disposition of the tumor in 3D, and its increasing volume. All images have the same length scale (center of figure).
Fig. 3
Fig. 3 Growth patterns of glioblastoma xenografts. A. Type 1: tumors whose volume exceeded 150 nL and that underwent highly accelerated growth (n = 8). The yellow filled symbols are from the tumor imaged in Fig. 1, while the dark blue filled symbols are from the tumor imaged in Fig. 2. A dashed line has been drawn at a volume of 150 nL; for comparison, the total volume of the retina from its vitreal surface to the posterior choroid in the 51 deg image field is between 5- and 10-fold greater. B. Type 2a: tumors that exhibited a plateau phase of growth (n = 10); arrows identify 4 growth patterns that appeared (post hoc) to be accelerating at the time the mouse was sacrificed. C. Type 2b: tumors that grew to a maximum volume and then underwent spontaneous decline (n = 9). Different colored symbols and lines are used for different tumors: each symbol represents the tumor volume derived (cf. Figs. 1, 2) from OCT measurements on the post-transplantation day indicated by the abscissa, while the smooth lines connecting the points are splines (the dashed black line in panel C represents a 20 day gap, which was omitted so that the lattermost time points of this xenograft would fit on a 110 day scale).
Fig. 4
Fig. 4 Treatment of ocular glioblastomas with nanodoxorubicin. A. Schematic diagram of the 20 nm PEG-porphyrin nanoparticle loaded in its core with doxorubicin (see Li et al., 2010 for details). 488 nm light excites doxorubicin: in solution its emission peak is at 590 nm; confined in the nanodox particle, excited doxorubicin non-radiatively transfers energy to the porphyrin, which has a FRET emission peak at ~680 nm. B. Fluorescence emission (ex 488 nm) from a GFP+ glioblastoma on different days after the transplant (yellow squares on fluorescence images indicate regions from which the emission spectra were taken). The spectrum and image of day 25 were taken without nanodox, while those of days 35 and 45 were taken after tail-vein injection of nanodox. The strong GFP emission of the glioblastoma cells dominates the mid-spectral range, but a distinctive emission band peaking at 680 nm is present: lower plot (“FRET”) shows the data in the dashed box of the upper plot on expanded scales. C. Limited (3X) treatment of Type 1 tumors with nanodox. Each symbol represents the tumor volume on the day of a treatment. D. Aggressive nanodox treatment of xenografts beginning around day 20 to 30 after transplantation. Treatment continued in each case until the tumor declined to ~50% of its maximal volume or less. The black filled symbols correspond to a Type 1 tumor (Fig. 3(A)) that reached a maximum volume of 420 nL. (In C, D tumor measurements are only plotted as symbols for the days of treatment; volume measurements from other days are not illustrated by discrete points, but rather presented by the continuous lines (splines), as in Fig. 3.). E. Treatment protocol illustrated in form of flow chart.
Fig. 5
Fig. 5 Histology and histopathology of ocular xenografts. A, B. Montage of images of cryosections of eyes with glioblastoma xenografts, immuno-labeled to highlight features of the tumors, including GFP (expressed in the glioblastoma cells), vasculature (collagen IV), and MHC differentiation marker CD8. The panels at right are confocal slices from the center of the cryosection, immunolabeled as indicated on the figure; the same images are presented overlaid with 50% transparency on the montage. Aa, triply labeled portion of the tumor (DAPI, GFP, collagen IV); Ab, same confocal slice as Aa, but without the GFP immunolabel; Ac confocal slice from a control region where no tumor cells were present, labeled as Ab. Aa-Ac serve to illustrate the tumor neovascularization and its interconnection with the choroidal vasculature, and also the pattern of collagen IV labeling of normal retinal (superior) and choroidal (posterior) vasculature. Ba, triply labeled portion of the tumor (DAPI, GFP, CD8); Bb, same confocal slice as Ba, but with the GFP labeling removed; Bc, control region illustrating normal pattern of CD8 labeling. The Type 1 tumor of panel A was created with the injection of 10,000 cells in 1 μL, and the animal sacrificed 13 weeks after injection; growth data from this tumor are also shown in Fig. 3(A), filled dark blue symbols. The Type 1 tumor of panel B was created by the injection of 5000 cells in 0.5 μL, and the mouse sacrificed 10 weeks after injection. Its initial growth trajectory is shown in Fig. 3(A) (filled black circles); the tumor was treated with light-activated nanodox, and the treatment series illustrated in Fig. 4(D) (filled black symbols).
Fig. 6
Fig. 6 Flow cytometry of cells from an eye with a xenograft glioblastoma reveals a tumor-associated increase in cells expressing CD8 epitope. In all four panels the ordinate gives the fluorescence intensity of cells labeled with an anti-GFP antibody tagged with Alexa 488 dye, while the abscissa is the fluorescence intensity of cells labeled with antibodies to CD4 (upper row of panels) or CD8 (lower row) conjugated to Pacific Blue dye. The left column of panels was obtained with cells from the eye that had a glioblastoma xenograft, while the right column of panels was obtained with exactly the same gating parameters from the cells identically harvested from the control (uninjected) eye of the same nude mouse. Counts in the plot regions indicated by the ellipses were used for statistical analysis. There were no GFP+ counts in the cells from the uninjected eye. The eye with the xenograft had statistically reliable 3.5-fold and 41-fold increases in cells expressing CD4 and CD8 cell surface markers, respectively, relative to the control eye. The flow cytometry data were analyzed with FloJoTM software and the numbers on the panels represent the fractions of the total count in the elliptical regions. The Type 1 tumor was generated by injection of 500 cells; the corresponding growth curve is illustrated in Fig. 3A by filled orange circles. This experiment was replicated in a second mouse with similar results.

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