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Rodent Models of Oxygen-Induced Retinopathy

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Book cover Retinal and Choroidal Angiogenesis

Abstract

Retinopathy of prematurity (ROP), a condition affecting premature infants, is characterized by pathological ocular angiogenesis, or retinal neovasculariztion (NV). Much of what is known about the development of the retinal vasculature and the progression of ROP has been acquired through the use of animal models of oxygen-induced retinopathy (OIR), which approximate ROP. Animal models of OIR have provided a wealth of information regarding the cellular and molecular pathogenesis of ROP. This information has contributed to a better understanding of other, non-ocular, neovascular conditions. The aim of this chapter is to explore the significance of the two most prevalent animal models of OIR, the mouse and the rat.

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References

  1. T. L. Terry, Extreme prematurity and fibroblastic overgrowth of persistent vascular sheath behind each crystalline lens: I, preliminary report, Am. J. Ophthalmol. 25, 203-204 (1942).

    Google Scholar 

  2. K. Campbell, Intensive oxygen therapy as a possible cause of retrolental fibroplasia; a clinical approach, Med. J. Austral. 2(2), 48-50 (1951).

    PubMed  CAS  Google Scholar 

  3. A. Patz, L. E. Hoeck, and E. De La Cruz, Studies on the effect of high oxygen administration in retrolental fibroplasia: I, nursery observations, Am. J. Ophthalmol. 35 (9), 1248-1253 (1952).

    PubMed  CAS  Google Scholar 

  4. L. J. Gyllensten and B. E. Hellstrom, Retrolental fibroplasias: animal experiments, Acta. Paediatr. 41 (6), 577-582 (1952).

    PubMed  CAS  Google Scholar 

  5. A. Patz, A. Eastham, D. Higginbotham, and T. Kleh, Oxygen studies in retrolental fibroplasia: II, the production of the microscopic changes of retrolental fibroplasia in experimental animals, Am. J. Ophthalmol. 36 (11), 1511-1522 (1953).

    PubMed  CAS  Google Scholar 

  6. N. Ashton, B. Ward, and G. Serpell, Role of oxygen in the genesis of retrolental fibroplasia: a preliminary report, Br. J. Ophthalmol. 37 (9), 513-520 (1953).

    Article  PubMed  CAS  Google Scholar 

  7. N. Ashton, B. Ward, and G. Serpell, Effect of oxygen on developing retinal vessels with particular reference to the problem of retrolental fibroplasias, Br. J. Ophthalmol. 38 (7), 397-432 (1954).

    Article  PubMed  CAS  Google Scholar 

  8. E. M. Hatfield, Blindness in infants and young children, Sight Sav. Rev. 42 (2), 69-89 (1972).

    Google Scholar 

  9. D. L. Gibson, S. B. Sheps, M. T. Schechter, S. Wiggins, and A. Q. McCormick, Retinopathy of prematurity: a new epidemic, Pediatrics 83 (4), 486-492 (1989).

    PubMed  CAS  Google Scholar 

  10. W. A. Silverman, Retrolental fibroplasia: a modern parable. New York: Grune and Stratton,

    Google Scholar 

  11. A. Madan, Angiogenesis and antiangiogenesis in the neonate: relevance to retinopathy, Neo. Reviews 4, 356-363 (2003).

    Google Scholar 

  12. A. Madan and J. S. Penn, Animal models of oxygen-induced retinopathy, Frontiers in Biosciences 8, 1030-1043 (2003).

    Article  Google Scholar 

  13. A. M. Roth, Retinal vascular development in premature infants, Am. J. Ophthalmol. 84 (5), 636-640 (1977).

    PubMed  CAS  Google Scholar 

  14. R. Foos and S. Kopelow, Development of retinal vasculature in paranatal infants, Surv. Ophthalmol. 18, 117-127 (1973).

    Google Scholar 

  15. I. Michaelson, The mode of development of the vascular system of the retina, with some observations in its significance for certain retinal diseases, Trans. Ophthalmol. Soc. U.K. 68, 137-180 (1948).

    Google Scholar 

  16. D. K. Coats, E. A. Paysse, and P. G. Steinkuller, Threshold retinopathy of prematurity in neonates less than 25 weeks’ estimated gestational age, J. AAPOS. 4 (3), 183-185 (2000).

    Article  PubMed  CAS  Google Scholar 

  17. M. Fruttiger, Development of the mouse retinal vasculature: angiogenesis versus vasculogenesis, Invest. Ophthalmol. Vis. Sci. 43 (2), 522-527 (2002).

    PubMed  Google Scholar 

  18. T. Chan-Ling, D. S. McLeod, S. Hughes, L. Baxter, Y. Chu, T Hasegawa, and G. A. Lutty, Astrocyte-endothelial cell relationships during human retinal vascular development, Invest. Ophthalmol. Vis. Sci. 45 (6), 2020-2032 (2004).

    Article  PubMed  Google Scholar 

  19. L. Gyllensten and B. Hellstrom, Experimental approach to the pathogenesis of retrolental fibroplasias: I. Changes of the eyes induced by exposure of newborn mice to concentrated oxygen, Acta. Pediat. 43 (100), 131-148 (1954).

    CAS  Google Scholar 

  20. L. Gyllensten and B. Hellstrom, Experimental approach to the pathogenesis of retrolental fibroplasia II. The influence of the developmental maturity in oxygen-induced changes in the mouse eye, Am. J. Ophthalmol. 39 (4, Part 1), 475-488 (1955).

    PubMed  CAS  Google Scholar 

  21. A. Patz, A. Eastham, D. H. Higgenbotham, and T. Kleh, Oxygen studies in retrolental fibroplasia II. The production of the microscopic changes of retrolental fibroplasia in experimental animals, Am. J. Ophthalmol. 36 (11), 1511-1522 (1953).

    PubMed  CAS  Google Scholar 

  22. P. M. Bischoff, S. D. Wajer, and R. W. Flower, Scanning electron microscopic studies of the hyaloid vascular system in newborn mice exposed to O2 and CO2, Graefes Arch. Clin. Exp. Ophthalmol. 220 (6), 257-263 (1983).

    Article  PubMed  CAS  Google Scholar 

  23. L. E. Smith, E. Wesolowski, A. McLellan, S. K. Kostyk, R. D’Amato, R. Sullivan, and P. A. D’Amore, Oxygen-induced retinopathy in the mouse, Invest. Ophthalmol. Vis. Sci. 35 (1), 101-111 (1994).

    PubMed  CAS  Google Scholar 

  24. R. M. Rohan, A. Fernandez, T. Udagawa, J. Yuan, and R. J. D’Amato, Genetic heterogeneity of angiogenesis in mice, FASEB J. 14 (7), 871-876 (2000).

    PubMed  CAS  Google Scholar 

  25. M. S. Rogers, R. M. Rohan, A. E. Birsner, and R. J. D’Amato, Genetic loci that control vascular endothelial growth factor-induced angiogenesis, FASEB J. 17 (4), 2112-2114 (2003).

    PubMed  CAS  Google Scholar 

  26. C. K. Chan, L. N. Pham, J. Zhou, C. Spee, S. J. Ryan, and D. R. Hinton, Differential expression of pro- and antiangiogenic factors in mouse strain-dependent hypoxia-induced retinal neovascularization, Lab. Invest. 85 (6), 721-733 (2005).

    Article  PubMed  CAS  Google Scholar 

  27. S. Claxton and M. Fruttiger, Role of arteries in oxygen induced vaso-obliteration, Exp. Eye Res 77 (3), 305-311 (2003).

    Article  PubMed  CAS  Google Scholar 

  28. G. A. Gole, Animal models of retinopathy of prematurity. In: Silverman WA, Flynn JT, eds. Contemporary Issues in Fetal and Neonatal Medicine 2: Retinopathy of Prematurity. Boston: Blackwell Scientific Publishers; 1985: 53-95.

    Google Scholar 

  29. A. Patz, Oxygen studies in retrolental fibroplasia IV: clinical and experimental observations, Am. J. Ophthalmol. 38 (3), 291-308 (1954).

    PubMed  CAS  Google Scholar 

  30. N. Ashton and R. Blach, Studies in developing retinal vessels VIII: effect of oxygen on the vessels of the ratling, Br. J. Ophthalmol. 45, 321-340 (1961).

    Article  PubMed  CAS  Google Scholar 

  31. J. S. Penn, B. L. Tolman, and L. A. Lowery, Variable oxygen exposure causes preretinal neovascularization in the newborn rat, Invest. Ophthalmol. Vis. Sci. 34 (3), 576-585 (1993).

    PubMed  CAS  Google Scholar 

  32. J. S. Penn, M. M. Henry, and B. L. Tolman, Exposure to alternating hypoxia and hyperoxia causes severe proliferative retinopathy in the newborn rat, Pediatr. Res. 36 (6), 724-731 (1994).

    Article  PubMed  CAS  Google Scholar 

  33. G. Gao, Y. Li, J. Fant, C. E. Crosson, S. P. Becerra, and J. X. Ma, Difference in ischemic regulation of vascular endothelial growth factor and pigment epithelium-derived factor in brown norway and sprague dawley rats contributing to different susceptibilities to retinal neovascularization, Diabetes 51 (4), 1218-1225 (2002).

    Article  PubMed  CAS  Google Scholar 

  34. S. X. Zhang, J. X. Ma, J. Sima, Y. Chen, M. S. Hu, A. Ottlecz, and G. N. Lambrou, Genetic difference in susceptibility to the blood-retina barrier breakdown in diabetes and oxygen-induced retinopathy, Am. J. Pathol. 166 (1), 313-321 (2005).

    PubMed  Google Scholar 

  35. B. N. Floyd, D. A. Leske, S. M. Wren, M. Mookadam, M. P. Fautsch, and J. M. Holmes, Differences between rat strains in models of retinopathy of prematurity, Mol. Vis. 11, 524-530 (2005).

    PubMed  CAS  Google Scholar 

  36. A. Kitzmann, D. A. Leske, Y. Chen, A. Kendall, W. Lanier, and J. Holmes, Incidence and severity of neovascularization in oxygen-and metabolic acidosis-induced retinopathy depend on rat source, Curr. Eye Res. 25, 215-220 (2002).

    Article  PubMed  Google Scholar 

  37. L. I. Larrazabal, and J. S. Penn, Study of ocular vasculature in the newborn rat by fluorescein angiography, J. Ophthal. Phot. 11, 49-52 (1989).

    Google Scholar 

  38. L. I. Larrazabal and J. S. Penn, Fluorescein angiography in the newborn rat: Implications in oxygen-induced retinopathy, Invest. Ophthalmol. Vis. Sci. 31 (5), 810-818 (1990).

    PubMed  CAS  Google Scholar 

  39. J. S. Penn and B. D. Johnson, Fluorescein angiography as a means of assessing retinal vascular pathology in oxygen-exposed newborn rats, Curr. Eye. Res. 12 (6), 561-570 (1993).

    Article  PubMed  CAS  Google Scholar 

  40. J. S. Penn, B. L. Tolman, L. A. Lowery, and C. A. Koutz, Oxygen-induced retinopathy in the rat: hemorrhages and dysplasias may lead to retinal detachment, Curr. Eye Res. 11 (10), 939-953 (1992).

    Article  PubMed  CAS  Google Scholar 

  41. I. C. Michaelson, N. Herz, E. Lewkowitz, and D. Kertesz, Effect of increased oxygen on the development of the retinal vessels, Brit. J. Ophthal. 38 (10), 577-587 (1954).

    Article  PubMed  CAS  Google Scholar 

  42. D. R. Senger, S. J. Galli, A. M. Dvorak, C. A. Perruzzi, V. S. Harvey, and H. F. Dvorak, Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid, Science 219 (4587), 983-985 (1983).

    Article  PubMed  CAS  Google Scholar 

  43. P. J. Keck, S. D. Hauser, G. Krivi, K. Sanzo, T. Warren, J. Feder, and D. T. Connolly, Vascular permeability factor, and endothelial cell mitogen related to PDGF, Science 246 (4935), 1309-1312 (1989).

    Article  PubMed  CAS  Google Scholar 

  44. D. W. Leung, G. Cachianes, W. J. Kuang, D. V. Goeddel, and N. Ferrara, Vascular endothelial growth factor is a secreted angiogenic mitogen, Science 246 (4935), 1306-1309 (1989).

    Article  PubMed  CAS  Google Scholar 

  45. N. Ferrara, K. Houck, L. Jakeman, and D. W. Leung, Molecular and biological properties of the vascular endothelial growth factor family of proteins, Endocr. Rev. 13 (1), 18-32 (1992).

    Article  PubMed  CAS  Google Scholar 

  46. K. J. Kim, B. Li, J. Winer J, M. Armanini, N. Gillett, H. S. Phillips, and N. Ferrara, Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo, Nature 362 (6423), 841-844 (1993).

    Google Scholar 

  47. N. Ferrara and T. Davis-Smyth, The biology of vascular endothelial growth factor, Endocr. Rev. 18 (1), 4-25 (1997).

    Article  PubMed  CAS  Google Scholar 

  48. A. P. Adamis, J. W. Miller, M. T. Bernal, D. J. D’Amico, J. Folkman, T. K. Yeo, and K. T. Yeo, Increased vascular endothelial growth factor levels in the vitreous of eyes with proliferative diabetic retinopathy, Am. J. Ophthalmol. 118 (4), 445-450 (1994).

    PubMed  CAS  Google Scholar 

  49. L. P. Aiello, R. L. Avery, P. G. Arrigg, B. A. Keyt, H. D. Jampel, S. T. Shah, L. R. Pasquale, H. Thieme, M. A. Iwamoto, and J. E. Park, Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders, N. Engl. J. Med. 331 (22), 1480-1487 (1994).

    Article  CAS  Google Scholar 

  50. G. Gao, Y. Li, D. Zhang, S. Gee, C. Crosson, and J. Ma, Unbalanced expression of VEGF and PEDF in ischemia-induced retinal neovascularization, FEBS Lett. 489 (2-3), 270-276 (2001).

    Article  PubMed  CAS  Google Scholar 

  51. E. A. Pierce, E. D. Foley, and L. E. Smith, Regulation of vascular endothelial cell growth factor by oxygen in a model of retinopathy of prematurity, Arch. Ophthalmol. 114 (10), 1219-1228 (1996).

    PubMed  CAS  Google Scholar 

  52. D. Shweiki, A. Itin, D. Soffer, and E. Keshet, Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis, Nature 359 (6398), 843-845 (1992).

    Article  PubMed  CAS  Google Scholar 

  53. E. A. Pierce, R. L. Avery, E. D. Foley, L. P. Aiello, and L. E. Smith, Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization, Proc. Natl. Acad. Sci. USA 92 (3), 905-909 (1995).

    Google Scholar 

  54. D. A. Simpson, G. M. Murphy, T. Bhaduri , T. A. Gardiner, D. B. Archer, and A. W. Stitt, Expression of the VEGF gene family during retinal vaso-obliteration and hypoxia, Biochem. Biophys. Res. Commun. 262 (2), 333-340 (1999).

    Article  PubMed  CAS  Google Scholar 

  55. H. Ozaki, H. Hayashi, S. A. Vinores, Y. Moromizato, P. A. Campochiaro, and K. Oshima, Intravitreal sustained release of VEGF causes retinal neovascularization in rabbits and breakdown of the blood-retinal barrier in rabbits and primates, Exp. Eye Res. 64 (4), 505-517 (1997).

    Article  PubMed  CAS  Google Scholar 

  56. H. Ozaki, A. Y. Yu, N. Della, K. Ozaki, J. D. Luna, H. Yamada, S. F. Hackett, N. Okamoto, D. J. Zack, G. L. Semenza, and P. A. Campochiaro, Hypoxia inducible factor-1alpha is increased in ischemic retina: temporal and spatial correlation with VEGF expression, Invest. Ophthalmol. Vis. Sci. 40 (1), 82-189 (1999).

    Google Scholar 

  57. L. P. Aiello, E. A. Pierce, E. D. Foley, H. Takagi, H. Chen, L. Riddle, N. Ferrara, G. L. King, and L. E. Smith, Suppression of retinal neovascularization in vivo by inhibition of vascular endothelial growth factor (VEGF) using soluble VEGF-receptor chimeric proteins, Proc. Natl. Acad. Sci. USA 92 (23), 10457-10461 (1995).

    Google Scholar 

  58. T. Tobe, N. Okamoto, M. A. Vinores, N. L. Derevjanik, S. A. Vinores, D. J. Zack, and P. A. Campochiaro, Evolution of neovascularization in mice with overexpresion of vascular endothelial growth factor in photoreceptors, Invest. Ophthalmol. Vis. Sci. 39 (1), 180-188 (1998).

    PubMed  CAS  Google Scholar 

  59. W. T. Deng, Z. Yan, A. Dinculescu, J. Pang, J. T. Teusner, N. G. Cortez, K. I. Berns, and W. W. Hauswirth, Adeno-associated virus mediated expression of vascular endothelial growth factor peptides inhibits retinal neovascularization in a mouse model of oxygen-induced retinopathy, Hum. Gene Ther. 16, 1247-1254 (2005).

    Article  PubMed  CAS  Google Scholar 

  60. A. P. Adamis, D. T. Shima, M. J. Tolentino, E. S. Gragoudas, N. Ferrara, J. Folkman, P. A. D’Amore, and J. W. Miller, Inhibition of vascular endothelial growth factor prevents retinal ischemia-associated iris neovasculariztion in a nonhuman primate, Arch. Ophthalmol. 114 (1), 66-71 (1996).

    PubMed  CAS  Google Scholar 

  61. F. Kinose, G. Roscilli, S. Lamartina, K. D. Anderson, F. Bonelli, S. G. Spence, G. Ciliberto, T. F. Vogt, D. J. Holder, C. Toniatti, and C. J. Thut, Inhibition of retinal and choroidal neovascularization by a novel KDR kinase inhibitor, Mol. Vis. 11, 366-373 (2005).

    PubMed  CAS  Google Scholar 

  62. R. Rota, T. Riccioni, M. Zaccarini, S. Lamartina, A. D. Gallo, A. Fusco, I. Kovesdi, E. Balestrazzi, D. C. Abeni, R. R. Ali, and M. C. Capogrossi, Marked inhibition of retinal neovascularization in rats following soluble-flt-1 gene transfer, J. Gene Med. 6(9), 992-1002 (2004).

    Article  PubMed  CAS  Google Scholar 

  63. E. W. Ng, D. T. Shima, P. Calias, E. T. Cunningham, D. R. Guyer, and A. P. Adamis, Pegaptanib, a targeted anti-VEGF aptamer for ocular vascular disease, Nat. Rev. Drug Discov. 5 (2), 123-132 (2006).

    Article  PubMed  CAS  Google Scholar 

  64. R. M. Rich, P. J. Rosenfeld, C. A. Puliafito, S. R. Dubovy, J. L. Davis, H. W. Flynn, S. Gonzalez, W. J. Feuer, R. C. Lin, G. A. Lalwani, J. K. Nguyen, and G. Kumar, Short-term safety and efficacy of intravitreal bevacizumab (Avastin) for neovascular age-related macular degeneration, Retina 26 (5), 495-511 (2006).

    Article  PubMed  Google Scholar 

  65. A. D. Wright, E. M. Kohner, N. W. Oakley, M. Hartog, G. F. Joplin, and T. R. Fraser, Serum growth hormone levels and the response of diabetic retinopathy to pituitary ablation, Br. Med. J. 2 (653), 346-348 (1969).

    Article  PubMed  CAS  Google Scholar 

  66. L. E. Smith, J. J. Kopchick, W. Chen, J. Knapp, F. Kinose, D. Daley, E. Foley, R. G. Smith, and J. M. Schaeffer, Essential role of growth hormone in ischemia-induced retinal neovascularization, Science 276 (5319), 1706-1709 (1997).

    Article  PubMed  CAS  Google Scholar 

  67. L. E. Smith, W. Shen, C. Perruzzi, S. Soker, F. Kinose, X. Xu, G. Rovinson, S. Driver, J. Bischoff, B. Zhang, J. M. Schaeffer, and D. R. Senger, Regulation of vascular endothelial growth factor-dependent retinal neovascularization by insulin-like growth factor-1 receptor, Nat. Med. 5 (12), 1390-1395 (1999).

    Article  PubMed  CAS  Google Scholar 

  68. T. Kondo, D. Vicent, K. Suzuma, M. Yanagisawa, G. L. King, M. Holzenberger, and C. R. Kahn, Knockout of insulin and IGF-1 receptors on vascular endothelial cells protects against retinal neovascularization, J. Clin. Invest. 111 (12), 1835-1842 (2003).

    Article  PubMed  CAS  Google Scholar 

  69. A. Das, A. McLamore, W. Song, and P. G. McGuire, Retinal neovascularization is suppressed with a matrix metalloproteinase inhibitor, Arch. Ophthalmol. 117 (4), 498-503 (1999).

    PubMed  CAS  Google Scholar 

  70. J. Luna, T. Tobe, S. A. Mousa, T. M. Reilly, and P. A. Campochiaro, Antagonists of integrin alpha v beta 3 inhibit retinal neovascularization in a murine model, Lab. Invest. 75 (4), 563-573 (1996).

    PubMed  CAS  Google Scholar 

  71. M. Friedlander, C. L. Theesfeld, M. Sugita, M. Fruttiger, M. A. Thomas, S. Chang, and D. A. Cheresh, Involvement of integrins alpha v beta 3 and alpha v beta 5 in ocular neovascular diseases, Proc. Natl. Acad. Sci. USA 93 (18), 9764-9769 (1996).

    Google Scholar 

  72. H. Hammes, M. Brownlee, A. Jonczyk, A. Sutter, and K. T. Preissner, Subcutaneous injection of a cyclic peptide antagonist of vitronectin receptor-type integrins inhibits retinal neovascularization, Nat. Med. 2 (5), 529-533 (1996).

    Article  PubMed  CAS  Google Scholar 

  73. S. Davis, T. H. Aldrich, and P. F. Jones, Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning, Cell 87 (7), 1161-1169 (1996).

    Article  PubMed  CAS  Google Scholar 

  74. P. C. Maisonpierre, C. Suri, P. F. Jones, S. Bartunkova, S. J. Wiegand, C. Radziejewski, D. Compton, J. McClain, T. H. Aldrich, N. Papadopoulos, T. J. Daly, S. Davis, T. N. Sato, G. D. Yancopoulos, Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis, Science 277, 55-60 (1997).

    Article  PubMed  CAS  Google Scholar 

  75. D. Hanahan, Signaling vascular morphogenesis and maintenance, Science 277(5322), 48-50 (1997).

    Article  PubMed  CAS  Google Scholar 

  76. J. Folkman and P. A. D’Amore, Blood vessel formation: What is its molecular basis, Cell 87 (7), 1153-1155 (1996).

    Article  PubMed  CAS  Google Scholar 

  77. N. W. Gale and G. D. Yancopoulos, Growth factors acting via endothelial cell-specific receptor tyrosine kinases: VEGFs, angiopoietins, and ephrins in vascular development, Genes Dev. 13 (9), 1055-1066 (1999).

    PubMed  CAS  Google Scholar 

  78. G. D. Yancoupolos, S. Davis, N. W. Gale, J. S. Rudge, S. J. Wiegand, and J. Holash, Vascular-specific growth factors and blood vessel formation, Nature 407 (6801), 242-248 (2000).

    Article  Google Scholar 

  79. H. Nambu, R. Nambu, Y. Oshima, S. F. Hackett, G. Okoye, S. Wiegand, G. Yancopoulos, D. J. Zack, and P. A. Campochiaro, Angiopoietin 1 inhibits ocular neovascularization and breakdown of the blood-retinal barrier, Gene Therapy 11 (10), 865-873 (2004).

    Article  PubMed  CAS  Google Scholar 

  80. H. Nambu, N. Umeda, S. Kachi, Y. Oshima, H. Akiyama, R. Nambu, and P. A. Campochiaro, Angiopoietin 1 prevents retinal detachment in an aggressive model of proliferative retinopathy, but has no effect on established neovascularization, J. Cell Phys. 204 (1), 227-235 (2005).

    Article  CAS  Google Scholar 

  81. S. Sarlos, B. Rizkalla, C. J. Moravski, Z. Cao, M. E. Cooper, and J. L. Wilkinson-Berka, Retinal angiogenesis is mediated by an interaction between the angiotensin type 2 receptor, VEGF, and angiopoietin, Am. J. Pathol. 163 (3), 879-887 (2003).

    PubMed  CAS  Google Scholar 

  82. S. F. Hackett, H. Ozaki, R. W. Strauss, K. Wahlin, C. Suri, P. Maisonpierre, G. Yancopoulos, and P. A. Campochiaro, Angiopoietin 2 expression in the retina: up-regulation during physiologic and pathologic neovascularization, J. Cell Physiol. 184(3), 275-284 (2000).

    Article  PubMed  CAS  Google Scholar 

  83. S. F. Hackett, S. Wiegand, G. Yancopoulos, and P. A. Campochiaro, Angiopoietin-2 plays an important role in retinal angiogenesis, J. Cell Physiol. 192 (2), 182-187 (2002).

    Google Scholar 

  84. N. Umeda, H. Ozaki, H. Hayashi, and K. Oshima, Expression of ephrinB2 and its receptors on fibroproliferative membranes in ocular angiogenic diseases, Am. J. Ophthalmol. 138 (2), 270-279 (2004).

    Article  PubMed  CAS  Google Scholar 

  85. J. J. Steinle, C. J. Meininger, U. Chowdhury, G. Wu, and H. J. Granger, Role of ephrin B2 in human retinal endothelial cell proliferation and migration, Cell Signal 15 (11), 1011-1017 (2003).

    Google Scholar 

  86. D. O. Zamora, M. H. Davies, S. R. Planck, J. T. Rosenbaum, and M. R. Powers, Soluble forms of ephrinB2 and EphB4 reduce retinal neovascularization in a model of proliferative retinopathy, Invest. Ophthalmol. Vis. Sci. 46 (6), 2175-2182 (2005).

    Article  PubMed  Google Scholar 

  87. N. Cheng, D. M. Brantley, H. Liu, W. Fanslow, D. P. Cerretti, K. N. Bussell, A. Reith, D. Jackson, and J. Chen, Blockade of EphA receptor tyrosine kinase activation inhibits VEGF-induced angiogenesis, Mol. Cancer Res. 1 (1), 2-11 (2002).

    Article  PubMed  CAS  Google Scholar 

  88. J. Chen, D. Hicks, D. Brantley-Sieders, N. Cheng, G. W. McCollum, X. Qi-Werdich, and J. Penn, Inhibition of retinal neovascularization by soluble EphA2 receptor, Exp. Eye Res. 82 (4), 664-673 (2006).

    Article  PubMed  CAS  Google Scholar 

  89. W. Smalley and R. N. DuBois, Colorectal cancer and nonsteroidal anti-inflammatory drugs, Adv. Pharmacol. 39, 1-20 (1997).

    Google Scholar 

  90. N. B. Nandgaonkar, T. Rotschild, K. Yu, and R. D. Higgins, Indomethacin improves oxygen-induced retinopathy in the mouse, Pediatr. Res. 46 (2), 184-188 (1999).

    Article  PubMed  CAS  Google Scholar 

  91. J. Sharma, S. M. Barr, Y. Geng, Y. Yun, and R. D. Higgins, Ibuprofen improves oxygen-induced retinopathy in a mouse model, Curr. Eye Res. 27 (5), 309-314 (2003).

    Article  PubMed  Google Scholar 

  92. K. Takahashi, Y. Saishin, Y. Saishin, K. Mori, A. Ando, S. Yamamoto, Y. Oshima, H. Nambu, M. B. Melia, D. P. Bingaman, and P. A. Campochiaro, Topical nepafenac inhibits ocular neovascularization, Invest. Ophthalmol. Vis. Sci. 44 (1), 409-415 (2003).

    Article  PubMed  Google Scholar 

  93. J. L. Wilkinson-Berka, N. S. Alousis, D. J. Kelly, and R. E. Gilbert, COX-2 inhibition and retinal angiogenesis in a mouse model of retinopathy of prematurity, Invest. Ophthalmol. Vis. Sci. 44 (3), 974-979 (2003).

    Article  PubMed  Google Scholar 

  94. C. J. Barnstable and J. Tombran-Tink, Neuroprotective and antiangiogenic actions of PEDF in the eye: molecular targets and therapeutic potential, Prog. Retin. Eye Res. 23 (5), 561-577 (2004).

    Article  PubMed  CAS  Google Scholar 

  95. D. W. Dawson, O. V. Volpert, P. Gillis, S. E. Crawford, H. Xu, W. Benedict, and N. P. Bouck, Pigment epithelium-derived factor: a potent inhibitor of angiogenesis, Science 285 (5425), 245-248 (1999).

    Google Scholar 

  96. R. Z. Renno, A. I. Youssri, N. Michaud, E. S. Gragoudas, and J. W. Miller, Expression of pigment epithelium-derived factor in experimental choroidal neovascularization, Invest. Ophthalmol. Vis. Sci. 43 (5), 1574-1580 (2002).

    PubMed  Google Scholar 

  97. E. J. Duh, H. S. Yang, I. Suzuma I, M. Miyagi, E. Youngman, K. Mori, M. Katai, L. Yan, K. Suzuma, K. West, S. Davarya, P. Tong, P. Gehlbach, J. Pearlman, J. W. Crabb, L. P. Aiello, P. A. Campochiaro, and D. J. Zack, Pigment epithelium-derived factor suppresses ischemia-induced retinal neovasculariztion and VEGF-induced migration and growth, Invest. Ophthalmol. Vis. Sci. 43 (3), 821-829 (2002).

    PubMed  Google Scholar 

  98. A. Auricchio, K. C. Behling, A. M. Maguire, E. M. O’Connor, J. Bennett, J. M. Wilson, and M. J. Tolentino, Inhibition of retinal neovascularization by intraocular viral-mediated delivery of anti-angiogenic agents, Mol. Ther. 6 (4), 490-494 (2002).

    Article  PubMed  CAS  Google Scholar 

  99. V. Stellmach, S. E. Crawford, W. Zhou, and N. Bouck, Prevention of ischemia-induced retinopathy by the natural ocular antiangiogenic agent pigment epithelium-derived factor, Proc. Natl. Acad. Sci. USA 98 (5), 2593-2597 (2001).

    Google Scholar 

  100. K. Mori, P. Gehlbach, A. Ando, D. McVey, L. Wei, and P. A. Campochiaro, Regression of ocular neovasculariztion in response to increased expression of pigment epithelium-derived factor, Invest. Ophthalmol. Vis. Sci. 43 (7), 2428-2434, (2002).

    PubMed  Google Scholar 

  101. A. W. Stitt, D. Graham, and T. A. Gardiner, Ocular wounding prevents pre-retinal neovascularization and upregulated PEDF expression in the inner retina, Mol. Vis. 10, 432-438 (2004).

    PubMed  CAS  Google Scholar 

  102. J. S. Penn, G. W. McCollum, J. M. Barnett JM, X. Q. Werdich, K. A. Koepke, and V. S. Rajaratnam, Angiostatic effect of penetrating ocular injury: role of pigment epithelium-derived factor , Invest. Ophthalmol. Vis. Sci. 47 (1), 405-414 (2006).

    Google Scholar 

  103. P.A. Campochiaro, Q. D. Nguyen, S. M. Shah, M. L. Klein, E. Holz, R. N. Frank, D. A. Saperstein, A. Gupta, J. T. Stout, J. Macko, R. DiBartolomeo, and L. L. Wei, Adenoviral vector-delivered pigment epithelium-derived factor for neovascular age-related macular degeneration: results of a phase I clinical trial , Hum. Gene Ther. 17 (2), 167-176 (2006).

    Article  PubMed  CAS  Google Scholar 

  104. C. A. May, A. V. Ohlmann, H. Hammes, and U. H. Spandau, Proteins with an endostatin-like domain in a mouse model of oxygen-induced retinopathy, Exp. Eye Res. 82 (2), 341-348 (2006).

    Article  PubMed  CAS  Google Scholar 

  105. T. A. Drixler, I. H. Borel Rinkes, E. D. Ritchie, F. W. Treffers, T. J. van Vroonhoven, M. F. Gebbink, and E. E. Voest, Angiostatin inhibits pathological but not physiological retinal angiogenesis, Invest. Ophthalmol. Vis. Sci. 42 (13), 3325-3330 (2001).

    PubMed  CAS  Google Scholar 

  106. T. Igarashi, K. Miyake, K. Kato, A Watanabe, M. Ishizaki, K. Ohara, and T. Shimada, Lenitivirus-mediated expression of angiostatin efficiently inhibits neovascularization in a murine proliferative retinopathy model, Gene Ther. 10 (3), 219-226 (2003).

    Article  PubMed  CAS  Google Scholar 

  107. A. Shafiee, J. S. Penn, H. C. Krutzsch, J. K. Inman, D. D. Roberts, D. A. Blake, Inhibition of retinal angiogenesis by peptides derived from thrombospondin-1, Invest. Ophthalmol. Vis. Sci. 41 (8), 2378-2388 (2000).

    PubMed  CAS  Google Scholar 

  108. J. Schlessinger, I. Lax, and M. Lemmon, Regulation of growth factor activation by proteoglycans: What is the role of the low affinity receptors? Cell 83 (3), 357–360 (1995).

    Article  PubMed  CAS  Google Scholar 

  109. F. Blasi, J. D. Vassalli, and K. Dano, Urokinase-type plasminogen activator: proenzyme, receptor, and inhibitors , J. Cell. Biol. 104 (4), 801-804 (1987).

    Article  PubMed  CAS  Google Scholar 

  110. O. Saksela, Plasminogen activation and regulation of pericellular proteolysis, Biochim. Biophys. Acta. 823 (1), 35-65 (1985).

    PubMed  CAS  Google Scholar 

  111. J. S. Penn and V. S. Rajaratnam, Inhibition of retinal neovascularization by intravitreal injection of human rPAI-1 in a rat model of retinopathy of prematurity, Invest. Ophthalmol. Vis. Sci. 44 (12), 5423-5429 (2003).

    Article  PubMed  Google Scholar 

  112. L. E. Bullard, X. Qi, and J.S. Penn, Role for extracellular signal-responsive kinase-1 and -2 in retinal angiogenesis, Invest. Ophthalmol. Vis. Sci. 44 (4), 1722-1731 (2003).

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Departments of Cell & Developmental Biology, Vanderbilt University School of Medicine, Nashville, Tennessee

    Susan E. Yanni & John S. Penn

  2. Ophthalmology and Visual Sciences, Vanderbilt University School of Medicine, Nashville, Tennessee

    Gary W. McCollum & John S. Penn

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  1. Susan E. Yanni
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  1. Vanderbilt University School of Medicine, Nashville, TN, U.S.A

    J.S. Penn

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Yanni, S.E., McCollum, G.W., Penn, J.S. (2008). Rodent Models of Oxygen-Induced Retinopathy. In: Penn, J. (eds) Retinal and Choroidal Angiogenesis. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6780-8_3

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