Intravital fluorescence facilitates measurement of multiple physiologic functions and gene expression in tumors of live animals

Disease Markers

Volumn 18, Issue 5-6, 2002, Pages 293-311

  Dewhirst, Mark W ^a,b   Shan, S ^a   Cao, Yiting ^a   Moeller, Benjamin ^a   Yuan, Fan ^b   Li, Chuan Yuan ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b Duke University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRADYKININ; CYTOKINE; FORMYLMETHIONYLLEUCYLPHENYLALANINE; INTERLEUKIN 2; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL MODEL; CELL INTERACTION; ENDOTHELIUM CELL; FLUORESCENCE; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GENE THERAPY; HYPOXIA; INTRAVITAL FLUORESCENCE MICROSCOPY; LEUKOCYTE; MEASUREMENT; METASTASIS; MICROVASCULATURE; NONHUMAN; ONCOLOGY; OXYGEN TRANSPORT; PH; PRIORITY JOURNAL; REPORTER GENE; REVIEW; TUMOR CELL;

ANIMALIA; MAMMALIA;

EID: 0346887124     PISSN: 02780240     EISSN: None     Source Type: Journal    
DOI: 10.1155/2002/820102     Document Type: Review

References (133)

1. R.M. Hoffman, Orthotopic transplant mouse models with green fluorescent protein-expressing cancer cells to visualize metastasis and angiogenesis, Cancer Metast Rev 17 (1998), 271-277.
2. R.M. Hoffman, Orthotopic metastatic mouse models for anticancer drug discovery and evaluation: a bridge to the clinic, Invest New Drugs 17 (1999), 343-359.
3. R.K. Jain, L.L. Munn and D. Fukumura, Dissecting tumour pathophysiology using intravital microscopy, Nat Rev Cancer 2 (2002), 266-276.
4. W.F. Jackson, Regional differences in mechanism of action of oxygen on hamster arterioles, Am J Physiol 265 (1993), H599-603.
5. B. Klitzman, A. Popel and B. Duling, Oxygen transport in resting and contracting hamster cremaster muscles: Experimental and theoretical microvascular studies, Microvasc Res 25 (1983), 108-131.
6. R.D. Braun, M.W. Dewhirst and D.L. Hatchell, Quantification of erythrocyte flow in the choroid of the albino rat, Am J Physiol 272 (1997), H1444-1453.
7. A.G. Tsai, B. Friesenecker, M.C. Mazzoni, H. Kerger, D.G. Buerk, P.C. Johnson and M. Intaglietta, Microvascular and tissue oxygen gradients in the rat mesentery, Proc Natl Acad Sci USA 95 (1998), 6590-6595.
8. R.D. Braun, A. Abbas, S.O. Bukhari and W. Wilson, 3rd, Hemodynamic parameters in blood vessels in choroidal melanoma xenografts and rat choroid, Invest Ophthalmol Vis Sci 43 (2002), 3045-3052.
9. N.J. Brown, S. Ali, M.W. Reed, R. Wiltrout and R.C. Rees, Trafficking of activated lymphocytes into the RENCA tumour microcirculation in vivo in mice, Br J Cancer 76 (1997), 1572-1578.
10. D.A. Schuschke, M.W. Reed, J.T. Saari, M.D. Olson, D.M. Ackermann and F.N. Miller, Short-term dietary copper deficiency does not inhibit angiogenesis in tumours implanted in striated muscle, Br J Cancer 66 (1992), 1059-1064.
11. E. Laemmel, O. Stucker, P.L. Darmon and E. Vicaut, Characterization of the specific response to serotonin of mouse tumour-feeding arterioles, Int J Radiat Biol 74 (1998), 379-386.
12. G.N. Naumov, S.M. Wilson, I.C. MacDonald, E.E. Schmidt, V.L. Morris, A.C. Groom, R.M. Hoffman and A.F. Chambers, Cellular expression of green fluorescent protein, coupled with high-resolution in vivo videomicroscopy, to monitor steps in tumor metastasis, J Cell Sci 112 (1999), 1835-1842.
13. G. Algire, Adaptation of transparent-chamber technique to mouse, J Natl Cancer Inst 4 (1943), 1-11.
14. D. Papenfuss, J. Gross, M. Intaglietta and F. Treese, A transparent access chamber for the rat dorsal skin fold, Microvasc Res 18 (1979), 311-318.
15. K. Ashaishi, G. Endlich, A. Gotz and K. Messmer, Quantitative analysis of microvascular structure and function in the amelanotic melanoma A-mel-3, Cancer Res 41 (1981), 1898-1904.
16. M. Leunig, F. Yuan, M. Menger, Y. Boucher, A. Goetz, K. Messmer and R. Jain, Angiogenesis, microvascular architecture, microhemodynamics and interstititial fluid pressure during early growth of human adenocarcinoma LS174T in SCID mice, Cancer Res 52 (1992), 6553-6560.
17. T. Dudar and R. Jain, Differential response of normal and tumor microcirculation to hyperthermia, Cancer Res 44 (1984), 605-612.
18. H. Eddy and G. Casarett, Development of the vascular system in the hamster malignant neurilemmoma, Microvasc Res 6 (1973), 63-82.
19. F. Yuan, H. Salehi, Y. Boucher, U. Vasthare, R. Tuma and R. Jain, Vascular permeability and microcirculation of gliomas and mammary carcinomas transplanted in rat and mouse cranial windows, Cancer Res 54 (1994), 4564-4568.
20. R.M. Foltz, R.E. McLendon, H.S. Friedman, R.K. Dodge, D.D. Bigner and M.W. Dewhirst, A pial window model for the intracranial study of human glioma microvascular function, Neurosurgery 36 (1995), 976-984; discussion 984-975.
21. Y. Tsuzuki, C. Mouta Carreira, M. Bockhorn, L. Xu, R.K. Jain and D. Fukumura, Pancreas microenvironment promotes VEGF expression and tumor growth: novel window models for pancreatic tumor angiogenesis and microcirculation, Lab Invest 81 (2001), 1439-1451.
22. B. Endrich, B. Zweifach, H. Reinhold and M. Intaglietta, Quantitative studies of microcirculatory function in malignant tissue: influence of temperature on microvascular hemodynamics during early growth of the BA1112 rat sarcoma, Int. Radiat Onc Biol Phys 5 (1979), 2021-2030.
23. M.W. Dewhirst, B. Klitzman, R.D. Braun, D.M. Brizel, Z.A. Haroon and T.W. Secomb, Review of methods used to study oxygen transport at the microcirculatory level, Int J Cancer 90 (2000), 237-255.
24. O. Shimomura, F.H. Johnson and Y. Saiga, Extraction, purification and properties of Aequorin, a bioluminescent protein from the luminous Hydromedusan, Aequorea, J Cell Comp Physiol 59 (1962), 223-239.
25. F.H. Johnson, O. Shimomura, Y. Saiga, L.C. Gershman, G.T. Reynolds and J.R. Waters, Quantum efficiency of cypridina luminescence, with a note on that of Aequorea, J Cell Comp Physiol 60 (1962), 85-103.
26. M. Chalfie, Y. Tu, G. Euskirchen, W.W. Ward and D.C. Prasher, Green fluorescent protein as a marker for gene expression, Science 263 (1994), 802-805.
27. B.P. Cormack, R.H. Valdivia and S. Falkow, FACS-optimized mutants of the green fluorescent protein (GFP), Gene 173 (1996), 33-38.
28. A. Terskikh, A. Fradkov, G. Ermakova, A. Zaraisky, P. Tan, A.V. Kajava, X. Zhao, S. Lukyanov, M. Matz, S. Kim, I. Weissman and P. Siebert, "Fluorescent Timer": protein that changes color with time [In Process Citation], Science 290 (2000), 1585-1588.
29. D. Vordermark, T. Shibata and J.M. Brown, Green fluorescent protein is a suitable reporter for tumor hypoxia despite an oxygen requirement for chromophore formation, Neoplasia 3 (2001), 527-534.
30. M. Ikawa, K. Kominami, Y. Yoshimura, K. Tanaka, Y. Nishimune and M. Okabe, A rapid and non-invasive selection of transgenic embryos before implantation using green fluorescent protein (GFP), FEBS Lett 375 (1995), 125-128.
31. Y.P. Wu, E. McMahon, M.R. Kraine, R. Tisch, A. Meyers, J. Frelinger, G.K. Matsushima and K. Suzuki, Distribution and characterization of GFP(+) donor hematogenous cells in Twitcher mice after bone marrow transplantation, Am J Pathol 156 (2000), 1849-1854.
32. S. Kawamoto, H. Niwa, F. Tashiro, S. Sano, G. Kondoh, J. Takeda, K. Tabayashi and J. Miyazaki, A novel reporter mouse strain that expresses enhanced green fluorescent protein upon Cre-mediated recombination, FEBS Lett 470 (2000), 263-268.
33. D. Tannahill, S. Bray and W.A. Harris, A Drosophila E(spl) gene is "neurogenic" in Xenopus: a green fluorescent protein study, Dev Biol 168 (1995), 694-697.
34. B.M. Tam, O.L. Moritz, L.B. Hurd and D.S. Papermaster, Identification of an outer segment targeting signal in the COOH terminus of rhodopsin using transgenic xenopus laevis, J Cell Biol 151 (2000), 1369-1380.
35. A. Amsterdam, S. Lin and N. Hopkins, The Aequorea victoria green fluorescent protein can be used as a reporter in live zebrafish embryos, Dev Biol 171 (1995), 123-129.
36. R. Rizzuto, M. Brini, P. Pizzo, M. Murgia and T. Pozzan, Chimeric green fluorescent protein as a tool for visualizing subcellular organelles in living cells, Curr Biol 5 (1995), 635-642.
37. V.G. Thackray, R.H. Young, J.E. Hooper and S.K. Nordeen, Estrogen agonist and antagonist action on the human estrogen receptor in Drosophila [In Process Citation], Endocrinology 141 (2000), 3912-3915.
38. C.M. Coburn and C.I. Bargmann, A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans, Neuron 17 (1996), 695-706.
39. C.R. Lim, Y. Kimata, M. Oka, K. Nomaguchi and K. Kohno, Thermosensitivity of green fluorescent protein fluorescence utilized to reveal novel nuclear-like compartments in a mutant nucleoporin NSP1, J Biochem (Tokyo) 118 (1995), 13-17.
40. P. De Wulf, L. Brambilla, M. Vanoni, D. Porro and L. Alberghina, Real-time flow cytometric quantification of GFP expression and gfp-fluorescence generation in saccharomyces cerevisiae [In Process Citation], J Microbiol Methods 42 (2000), 57-64.
41. J.R. Daum, N. Gomez-Ospina, M. Winey and D.J. Burke, The spindle checkpoint of saccharomyces cerevisiae responds to separable microtubule-dependent events [In Process Citation], Curr Biol 10 (2000), 1375-1378.
42. B.J. Feilmeier, G. Iseminger, D. Schroeder, H. Webber and G.J. Phillips, Green fluorescent protein functions as a reporter for protein localization in Escherichia coli, J Bacteriol 182 (2000), 4068-4076.
43. J.M. Mullaney, R.B. Thompson, Z. Gryczynski and L.W. Black, Green fluorescent protein as a probe of rotational mobility within bacteriophage T4 [In Process Citation], J Virol Methods 88 (2000), 35-40.
44. J. Chen, Y. Watanabe, N. Sako, K. Ohshima and Y. Okada, Complete nucleotide sequence and synthesis of infectious in vitro transcripts from a full-length cDNA clone of a rakkyo strain of tobacco mosaic virus, Arch Virol 141 (1996), 885-900.
45. D.M. Prescott, H.C. Charles, J.M. Poulson, R.L. Page, D.E. Thrall, Z. Vujaskovic and M.W. Dewhirst, The relationship between intracellular and extracellular pH in spontaneous canine tumors, Clin Cancer Res 6 (2000), 2501-2505.
46. R. Zhou, N. Bansal, D.B. Leeper and J.D. Glickson, Intracellular acidification of human melanoma xenografts by the respiratory inhibitor m-iodobenzylguanidine plus hyperglycemia: a 31P magnetic resonance spectroscopy study, Cancer Res 60 (2000), 3532-3536.
47. R.J. Gillies and R.M. Lynch, Frontiers in the measurement of cell and tissue pH, Novartis Found Symp 240 (2001), 7-19.
48. M. Okabe, M. Ikawa, K. Kominami, T. Nakanishi and Y. Nishimune, 'Green mice' as a source of ubiquitous green cells, FEBS Lett 407 (1997), 313-319.
49. M. Sato, Y. Yasuoka, H. Kodama, T. Watanabe, J.I. Miyazaki and M. Kimura, New approach to cell lineage analysis in mammals using the Cre-loxP system, Mol Reprod Dev 56 (2000), 34-44.
50. X.W. Yang, C. Wynder, M.L. Doughty and N. Heintz, BAC-mediated gene-dosage analysis reveals a role for Ziprol (Ru49/Zfp38) in progenitor cell proliferation in cerebellum and skin, Nat Genet 22 (1999), 327-335.
51. X.W. Yang, P. Model and N. Heintz, Homologous recombination based modification in Escherichia coli and germline transmission in transgenic mice of a bacterial artificial chromosome, Nat Biotechnol 15 (1997), 859-865.
52. J. Zuo, J. Treadaway, T.W. Buckner and B. Fritzsch, Visualization of alpha9 acetylcholine receptor expression in hair cells of transgenic mice containing a modified bacterial artificial chromosome, Proc Natl Acad Sci USA 96 (1999), 14100-14105.
53. S. Kupzig, Methods in Enzymology, (Vol. 302), Academic Press, San Diego, 1999.
54. S.J. Scales, R. Pepperkok and T.E. Kreis, Visualization of ER-to-Golgi transport in living cells reveals a sequential mode of action for COPII and COPI, Cell 90 (1997), 1137-1148.
55. A. Cornea, J.A. Janovick, X. Lin and P.M. Conn, Simultaneous and independent visualization of the gonadotropin-releasing hormone receptor and its ligand: evidence for independent processing and recycling in living cells [published erratum appears in Endocrinology 1999 Oct; 140(10):4771], Endocrinology 140 (1999), 4272-4280.
56. 2+ based on green fluorescent proteins and calmodulin [see comments], Nature 388 (1997), 882-887.
57. X. Xu, A.L. Gerard, B.C. Huang, D.C. Anderson, D.G. Payan and Y. Luo, Detection of programmed cell death using fluorescence energy transfer, Nucleic Acids Res 26 (1998), 2034-2035.
58. R. Heim and R.Y. Tsien, Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer, Curr Biol 6 (1996), 178-182.
59. G. Imreh, M. Beckman, K. Iverfeldt and E. Hallberg, Non-invasive monitoring of apoptosis versus necrosis in a neuroblastoma cell line expressing a nuclear pore protein tagged with the green fluorescent protein, Exp Cell Res 238 (1998), 371-376.
60. W. Zhang, S. Labrecque, E. Azoulay, R. Dudley and G. Matlashewski, Development of a p53 responsive GFP reporter; identification of live cells with p53 activity, J Biotechnol 84 (2000), 79-86.
61. C.Y. Li, S. Shan, Q. Huang, R.D. Braun, J. Lanzen, K. Hu, P. Lin and M.W. Dewhirst, Initial stages of tumor cell-induced angiogenesis: evaluation via skin window chambers in rodent models, J Natl Cancer Inst 92 (2000), 143-147.
62. D. Fukumura, R. Xavier, T. Sugiura, Y. Chen, E.C. Park, N. Lu, M. Selig, G. Nielsen, T. Taksir, R.K. Jain and B. Seed, Tumor induction of VEGF promoter activity in stromal cells, Cell 94 (1998), 715-725.
63. T. Motoike, S. Loughna, E. Perens, B.L. Roman, W. Liao, T.C. Chau, C.D. Richardson, T. Kawate, J. Kuno, B.M. Weinstein, D.Y. Stainier and T.N. Sato, Universal GFP reporter for the study of vascular development, Genesis 28 (2000), 75-81.
64. L. Xu, D. Fukumura and R.K. Jain, Acidic extracellular pH induces vascular endothelial growth factor (VEGF) in human glioblastoma cells via ERK1/ 2 MAPK signaling pathway: mechanism of low pH-induced VEGF, J Biol Chem 277 (2002), 11368-11374.
65. D. Fukumura, L. Xu, Y. Chen, T. Gohongi, B. Seed and R.K. Jain, Hypoxia and acidosis independently up-regulate vascular endothelial growth factor transcription in brain tumors in vivo, Cancer Res 61 (2001), 6020-6024.
66. M. Kneen, J. Farinas, Y. Li and A.S. Verkman, Green fluorescent protein as a noninvasive intracellular pH indicator, Biophys J 74 (1998), 1591-1599.
67. J.S. Condeelis, J. Wyckoff and J.E. Segall, Imaging of cancer invasion and metastasis using green fluorescent protein [In Process Citation], Eur J Cancer 36 (2000), 1671-1680.
68. T. Chishima, M. Yang, Y. Miyagi, L. Li, Y. Tan, E. Baranov, H. Shimada, A.R. Moossa, S. Penman and R.M. Hoffman, Governing step of metastasis visualized in vitro, Proc Natl Acad Sci USA 94 (1997), 11573-11576.
69. T. Chishima, Y. Miyagi, X. Wang, E. Baranov, Y. Tan, H. Shimada, A.R. Moossa and R.M. Hoffman, Metastatic patterns of lung cancer visualized live and in process by green fluorescence protein expression, Clin Exp Metastasis 15 (1997), 547-552.
70. T. Chishima, Y. Miyagi, X. Wang, Y. Tan, H. Shimada, A. Moossa and R.M. Hoffman, Visualization of the metastatic process by green fluorescent protein expression, Anticancer Res 17 (1997), 2377-2384.
71. T. Chishima, Y. Miyagi, X. Wang, H. Yamaoka, H. Shimada, A.R. Moossa and R.M. Hoffman, Cancer invasion and micrometastasis visualized in live tissue by green fluorescent protein expression, Cancer Res 57 (1997), 2042-2047.
72. S. Hasegawa, M. Yang, T. Chishima, Y. Miyagi, H. Shimada, A.R. Moossa and R.M. Hoffman, In vivo tumor delivery of the green fluorescent protein gene to report future occurrence of metastasis, Cancer Gene Ther 7 (2000), 1336-1340.
73. M. Yang, P. Jiang, Z. An, E. Baranov, L. Li, S. Hasegawa, M. Al-Tuwaijri, T. Chishima, H. Shimada, A.R. Moossa and R.M. Hoffman, Genetically fluorescent melanoma bone and organ metastasis models, Clin Cancer Res 5 (1999), 3549-3559.
74. M. Yang, P. Jiang, F.X. Sun, S. Hasegawa, E. Baranov, T. Chishima, H. Shimada, A.R. Moossa and R.M. Hoffman, A fluorescent orthotopic bone metastasis model of human prostate cancer, Cancer Res 59 (1999), 781-786.
75. M. Bouvet, J. Wang, S.R. Nardin, R. Nassirpour, M. Yang, E. Baranov, P. Jiang, A.R. Moossa and R.M. Hoffman, Real-time optical imaging of primary tumor growth and multiple metastatic events in a pancreatic cancer orthotopic model, Cancer Res 62 (2002), 1534-1540.
76. X. Li, J. Wang, Z. An, M. Yang, E. Baranov, P. Jiang, F. Sun, A.R. Moossa and R.M. Hoffman, Optically imageable metastatic model of human breast cancer, Clin Exp Metastasis 19 (2002), 347-350.
77. A.B. Al-Mehdi, K. Tozawa, A.B. Fisher, L. Shientag, A. Lee and R.J. Muschel, Intravascular origin of metastasis from the proliferation of endothelium-attached tumor cells: a new model for metastasis, Nat Med 6 (2000), 100-102.
78. C.W. Wong, C. Song, M.M. Grimes, W. Fu, M.W. Dewhirst, R.J. Muschel and A.B. Al-Mehdi, Intravascular location of breast cancer cells after spontaneous metastasis to the lung, Am J Pathol 161 (2002), 749-753.
79. Q. Huang, S. Shan, R.D. Braun, J. Lanzen, G. Anyrhambatla, G. Kong, M. Borelli, P. Corry, M.W. Dewhirst and C.Y. Li, Noninvasive visualization of tumors in rodent dorsal skin window chambers, Nat Biotechnol 17 (1999), 1033-1035.
80. F. Rolling, W.Y. Shen, N.L. Barnett, H. Tabarias, Y. Kanagasingam, I. Constable and P.E. Rakoczy, Long-term real-time monitoring of adeno-associated virus-mediated gene expression in the rat retina, Clin Experiment Ophthalmol 28 (2000), 382-386.
81. T.R. Flotte, S.E. Beck, K. Chesnut, M. Potter, A. Poirier and S. Zolotukhin, A fluorescence video-endoscopy technique for detection of gene transfer and expression, Gene Ther 5 (1998), 166-173.
82. C.Y. Li, J.B. Little, K. Hu, W. Zhang, L. Zhang, M.W. Dewhirst and Q. Huang, Persistent genetic instability in cancer cells induced by non-DNA-damaging stress exposures, Cancer Res 61 (2001), 428-432.
83. L.K. Fung and W.M. Saltzman, Polymeric implants for cancer chemotherapy, Advanced Drug Delivery Reviews 26 (1997), 209-230.
84. W. Dang, O.M. Colvin, H. Brem and W.M. Saltzman, Covalent coupling of methotrexate to dextran enhances the penetration of cytotoxicity into a tissue-like matrix, Cancer Res 54 (1994), 1729-1735.
85. F. Yuan, M. Leunig, D.A. Berk and R.K. Jain, Microvascular permeability of albumin, vascular surface area, and vascular volume measured in human adenocarcinoma LS174T using dorsal chamber in SCID mice, Microvasc Res 45 (1993), 269-289.
86. N.Z. Wu, B. Klitzman, G. Rosner, D. Needham and M.W. Dewhirst, Measurement of material extravasation in microvascular networks using fluorescence video-microscopy, Microvasc Res 46 (1993), 231-253.
87. L.E. Gerlowski and R.K. Jain, Microvascular permeability of normal and neoplastic tissues, Microvasc Res 31 (1986), 288-305.
88. H.C. Lichtenbeld, F. Yuan, C.C. Michel and R.K. Jain, Perfusion of single tumor microvessels: application to vascular permeability measurement, Microcirculation 3 (1996), 349-357.
89. D.A. Berk, F. Yuan, M. Leunig and R.K. Jain, Fluorescence photobleaching with spatial Fourier analysis: measurement of diffusion in light-scattering media, Biophys J 65 (1993), 2428-2436.
90. S.R. Chary and R.K. Jain, Direct measurement of interstitial diffusion and convection of albumin in normal and neoplastic tissues using fluorescence photobleaching, PNAS 86 (1989), 5385-5389.
91. L.J. Nugent and R.K. Jain, Plasma pharmacokinetics and interstitial diffusion of macromolecules in a capillary bed, Am J Physiol 246 (1984), H129-137.
92. A. Pluen, Y. Boucher, S. Ramanujan, T.D. McKee, T. Gohongi, E. di Tomaso, E.B. Brown, Y. Izumi, R.B. Campbell, D.A. Berk and R.K. Jain, Role of tumor-host interactions in interstitial diffusion of macromolecules: Cranial vs. subcutaneous tumors, Proc Natl Acad Sci USA 98 (2001), 4628-4633.
93. D.A. Berk, F. Yuan, M. Leunig and R.K. Jain, Direct in vivo measurement of targeted binding in a human tumor xenograft, Proc Natl Acad Sci USA 94 (1997), 1785-1790.
94. D. Brizel, B. Klitzman, J. Cook, J. Edwards, G. Rosner and M. Dewhirst, A comparison of tumor and normal tissue microvascular hematocrits and red cell fluxes in a rat window chamber model, Int. J Radia. Oncol Biol Phys 25 (1993), 269-276.
95. N.Z. Wu and A.L. Baldwin, Possible mechanism(s) for permeability recovery of venules during histamine application, Microvasc Res 44 (1992), 334-352.
96. N.Z. Wu and A.L. Baldwin, Transient venular permeability increase and endothelial gap formation induced by histamine, Am J Physiol 262 (1992), H1238-1247.
97. F.E. Curry, Regulation of water and solute exchange in microvessel endothelium: studies in single perfused capillaries, Microcirculation 1 (1994), 11-26.
98. R.H. Adamson, J.F. Lenz and F.E. Curry, Quantitative laser scanning confocal microscopy on single capillaries: permeability measurement, Microcirculation 1 (1994), 251-265.
99. E.B. Brown, R.B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura and R.K. Jain, In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy, Nat Med 7 (2001), 864-868.
100. D. Axelrod, D.E. Koppel, J. Schlessinger, E. Elson and W.W. Webb, Mobility measurement by analysis of fluorescence photobleaching recovery kinetics, Biophys J 16 (1976), 1055-1069.
101. L.J. Nugent and R.K. Jain, Extravascular diffusion in normal and neoplastic tissues, Cancer Res 44 (1984), 238-244.
102. D. Fukumura, F. Yuan, M. Endo and R.K. Jain, Role of nitric oxide in tumor microcirculation. Blood flow, vascular permeability, and leukocyte-endothelial interactions, Am J Pathol 150 (1997), 713-725.
103. D. Fukumura, F. Yuan, W.L. Monsky, Y. Chen and R.K. Jain, Effect of host microenvironment on the microcirculation of human colon adenocarcinoma, Am J Pathol 151 (1997), 679-688.
104. G. Kong, R.D. Braun and M.W. Dewhirst, Hyperthermia enables tumor-specific nanoparticle delivery: effect of particle size, Cancer Res 60 (2000), 4440-4445.
105. F. Yuan, M. Dellian, D. Fukumura, M. Leunig, D.A. Berk, V.P. Torchilin and R.K. Jain, Vascular permeability in a human tumor xenograft: molecular size dependence and cutoff size, Cancer Res 55 (1995), 3752-3756.
106. S.K. Hobbs, W. Monsky, F. Yuan, W.G. Roberts, L. Griffith, V.P. Torchillin and R.K. Jain, Regulation of transport pathways in tumor vessels: Role of tumor type and microenvironment. Proc Nat Acad Sci USA 95 (1998), 4607-4612.
107. G. Kong, R.D. Braun and M.W. Dewhirst, Characterization of the effect of hyperthermia on nanoparticle extravasation from tumor vasculature, Cancer Res 61 (2001), 3027-3032.
108. D.E. Meyer, G.A. Kong, M.W. Dewhirst, M.R. Zalutsky and A. Chilkoti, Targeting a genetically engineered elastin-like polypeptide to solid tumors by local hyperthermia, Cancer Res 61 (2001), 1548-1554.
109. M. Dewhirst, H. Kimura, S. Rehmus, R. Braun, D. Papahadjopoulos, K. Hong and T. Secomb, Microvascular studies on the origins of perfusion-limited hypoxia, Bri. J Cancer 74 (1996), S247-S251.
110. H. Kimura, R.D. Braun, E.T. Ong, R. Hsu, T.W. Secomb, D. Papahadjopoulos, K. Hong and M.W. Dewhirst, Fluctuations in red cell flux in tumor microvessels can lead to transient hypoxia and reoxygenation in tumor parenchyma, Cancer Res 56 (1996), 5522-5528.
111. J. Unthank, J. Lash, J. Nixon, R. Sidner and H. Bohlen, Evaluation of carbocyanine-labeled erythrocytes for microvascular measurements, Microvasc Res 45 (1993), 193-210.
112. G.R. Martin and R.K. Jain, Noninvasive measurement of interstitial pH profiles in normal and neoplastic tissue using fluorescence ratio imaging microscopy, Cancer Res 54 (1994), 5670-5674.
113. G.R. Martin and R.K. Jain, Fluorescence ratio imaging measurement of pH gradients: calibration and application in normal and tumor tissues, Microvasc Res 46 (1993), 216-230.
114. G. Helmlinger, F. Yuan, M. Dellian and R.K. Jain, Interstitial pH and pO2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation, Nat Med 3 (1997), 177-182.
115. S.A. Vinogradov and D.F. Wilson, Recovery of oxygen distributions in tissue from phosphorescence decay data, Adv Exp Med Biol 361 (1994), 67-73.
116. D.F. Wilson and S.A. Vinogradov, Recent advances in oxygen measurements using phosphorescence quenching, Adv Exp Med Biol 361 (1994), 61-66.
117. S.A. Vinogradov and D.F. Wilson, Phosphorescence lifetime analysis with a quadratic programming algorithm for determining quencher distributions in heterogeneous systems, Biophys J 67 (1994), 2048-2059.
118. S.A. Vinogradov, L.W. Lo, W.T. Jenkins, S.M. Evans, C. Koch and D.F. Wilson, Noninvasive imaging of the distribution in oxygen in tissue in vivo using near-infrared phosphors, Biophys J 70 (1996), 1609-1617.
119. I.P. Torres Filho, M. Leunig, F. Yuan, M. Intaglietta and R.K. Jain, Noninvasive measurement of microvascular and interstitial oxygen profiles in a human tumor in SCID mice, Proc Natl Acad Sci USA 91 (1994), 2081-2085.
120. M.W. Dewhirst, E.T. Ong, R.D. Braun, B. Smith, B. Klitzman, S.M. Evans and D. Wilson, Quantification of longitudinal tissue pO2 gradients in window chamber tumours: impact on tumour hypoxia, Br J Cancer 79 (1999), 1717-1722.
121. T.M. Carlos and J.M. Harlan, Leukocyte-endothelial adhesion molecules, Blood 84 (1994), 2068-2101.
122. M.J. Eppihimer and D.N. Granger, Ischemia/reperfusion-induced leukocyte-endothelial interactions in postcapillary venules, Shock 8 (1997), 16-25.
123. C. Ohkubo, D. Bigos and R.K. Jain, Interleukin 2 induced leukocyte adhesion to the normal and tumor microvascular endothelium in vivo and its inhibition by dextran sulfate: implications for vascular leak syndrome, Cancer Res 51 (1991), 1561-1563.
124. A. Sasaki, R.J. Melder, T.L. Whiteside, R.B. Herberman and R.K. Jain, Preferential localization of human adherent lymphokine-activated killer cells in tumor microcirculation, J Natl Cancer Inst 83 (1991), 433-437.
125. M.W. Dewhirst, R.Z. Vinuya, E.T. Ong, B. Klitzman, G. Rosner, T.W. Secomb and J.F. Gross, Effects of bradykinin on the hemodynamics of tumor and granulating normal tissue microvasculature, Radiat Res 130 (1992), 345-354.
126. N.Z. Wu, B.A. Ross, C. Gulledge, B. Klitzman, R. Dodge and M.W. Dewhirst, Differences in leucocyte-endothelium interactions between normal and adenocarcinoma bearing tissues in response to radiation, Br J Cancer 69 (1994), 883-889.
127. R.J. Melder, G.C. Koenig, B.P. Witwer, N. Safabakhsh, L.L. Munn and R.K. Jain, During angiogenesis, vascular endothelial growth factor and basic fibroblast growth factor regulate natural killer cell adhesion to tumor endothelium [see comments], Nat Med 2 (1996), 992-997.
128. D. Fukumura, F. Yuan, W.L. Monsky, Y. Chen and R.K. Jain, Effect of host microenvironment on the microcirculation of human colon adenocarcinoma, Am J Pathol 151 (1997), 679-688.
129. R.K. Jain, G.C. Koenig, M. Dellian, D. Fukumura, L.L. Munn and R.J. Melder, Leukocyte-endothelial adhesion and angiogenesis in tumors, Cancer Metast Rev 15 (1996), 195-204.
130. R.J. Melder, H.A. Salehi and R.K. Jain, Interaction of activated natural killer cells with normal and tumor vessels in cranial windows in mice, Microvasc Res 50 (1995), 35-44.
131. J.C. Acker, L.B. Marks, D.P. Spencer, W. Yang, M.A. Avery, R.K. Dodge, G.L. Rosner and M.W. Dewhirst, Serial in vivo observations of cerebral vasculature after treatment with a large single fraction of radiation, Radiat Res 149 (1998), 350-359.
132. H. Kimura, N.Z. Wu, R. Dodge, D.P. Spencer, B.M. Klitzman, T.M. McIntyre and M.W. Dewhirst, Inhibition of radiation-induced up-regulation of leukocyte adhesion to endothelial cells with the platelet-activating factor inhibitor, BN52021, Int J Radiat Oncol Biol Phys 33 (1995), 627-633.
133. N.Z. Wu, B. Klitzman, R. Dodge and M.W. Dewhirst, Diminished leukocyte-endothelium interaction in tumor microvessels, Cancer Res 52 (1992), 4265-4268.