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Documenta Ophthalmologica

, Volume 118, Issue 1, pp 37–54 | Cite as

The effect of oxygen and light on the structure and function of the neonatal rat retina

  • A. L. Dorfman
  • S. Joly
  • P. Hardy
  • S. Chemtob
  • P. LachapelleEmail author
Review Paper

Abstract

The neonatal rat is born with its eyes closed and an immature visual system, that some say is equivalent to that of a human fetus at 26 weeks of gestation. From birth, the visual system of the newborn rat will gradually mature, the first manifestation of that being the opening of the eye which usually take place at postnatal day 14. Complete maturation of the retina and visual pathways is normally reached at the end of the first month of life. The neonatal rat model thus represents a unique paradigm to study the normal and abnormal maturation of the primary visual pathways that normally occurs in utero in human subjects. Our laboratory has, over the past decade, developed two animal models of postnatally induced retinopathy, namely the Oxygen-Induced Retinopathy (OIR) that share several common features with the human Retinopathy of Prematurity (ROP) and the Light-Induced Retinopathy that is viewed by some as a valid model of some forms of Retinitis Pigmentosa (RP). The following pages review what is known of the pathophysiological processes taking place and suggest possible therapeutic avenues that could be explored in order to halt the degenerative process.

Keywords

Retinopathy Oxygen Light Neonatal rat Electroretinogram Histology 

Notes

Acknowledgments

This study was supported by a research grant (MOP-13383) from the Canadian Institutes of Health Research (CIHR), from the FRSQ-Réseau Vision as well as from the McGill University-Montreal Children’s Hospital Research Institute. A.L. Dorfman and S. Joly equally contributed to this manuscript and should therefore be considered as equal first authors.

References

  1. 1.
    Dorfman A, Dembinska O, Chemtob S, Lachapelle P (2008) Early manifestations of postnatal hyperoxia on the retinal structure and function of the neonatal rat. Invest Ophthalmol Vis Sci 49:458–466PubMedCrossRefGoogle Scholar
  2. 2.
    Moore A (1990) Retinopathy of prematurity. In: Taylor D (ed) Pediatric ophthalmology. Blackwell Scientific, Boston, pp 365–375Google Scholar
  3. 3.
    Patz A, Payne JW (1998) Retinopathy of prematurity (retrolental fibroplasia). In: Tasman W, Jaegen EA (eds). Duane’s foundations of clinical ophthalmology. Lippincott Williams & Wilkins, Philadelphia, pp 1–19Google Scholar
  4. 4.
    Chan-Ling T, Tout S, Hollander H, Stone J (1992) Vascular changes and their mechanisms in the feline model of retinopathy of prematurity. Invest Ophthalmol Vis Sci 33:2128–2147PubMedGoogle Scholar
  5. 5.
    Smith LE, Wesolowski E, McLellan A, Kostyk SK, D’Amato R, Sullivan R, D’Amore PA (1994) Oxygen-induced retinopathy in the mouse. Invest Ophthalmol Vis Sci 35:101–111PubMedGoogle Scholar
  6. 6.
    McLeod DS, Brownstein R, Lutty GA (1996) Vaso-obliteration in the canine model of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 37:300–311PubMedGoogle Scholar
  7. 7.
    McLeod DS, Crone SN, Lutty GA (1996) Vasoproliferation in the neonatal dog model of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 37:1322–1333PubMedGoogle Scholar
  8. 8.
    Ricci B (1990) Oxygen-induced retinopathy in the rat model. Doc Ophthalmol 74(3):171–177Google Scholar
  9. 9.
    Penn JS, Tolman BL, Henry MM (1994) Oxygen-induced retinopathy in the rat: relationship of retinal nonperfusion to subsequent neovascularization. Invest Ophthalmol Vis Sci 35:3429–3435PubMedGoogle Scholar
  10. 10.
    Reynaud X, Dorey CK (1994) Extraretinal neovascularization induced by hypoxic episodes in the neonatal rat. Invest Ophthalmol Vis Sci 35:3169–3177PubMedGoogle Scholar
  11. 11.
    Madan A, Penn JS (2003) Animal models of oxygen-induced retinopathy. Front Biosci 8:d1030–d1043PubMedCrossRefGoogle Scholar
  12. 12.
    Hardy P, Beauchamp M, Sennlaub F, Gobeil F Jr, Tremblay L, Mwaikambo B, Lachapelle P, Chemtob S (2005) New insights into the retinal circulation: inflammatory lipid mediators in ischemic retinopathy. Prostaglandins Leukot Essent Fatty Acids 72:301–325PubMedCrossRefGoogle Scholar
  13. 13.
    Hardy P, Beauchamp M, Sennlaub F Jr Gobeil F, Mwaikambo B, Lachapelle P, Chemtob S (2005) Inflammatory lipid mediators in ischemic retinopathy. Pharmacol Rep 57(Suppl):169–190PubMedGoogle Scholar
  14. 14.
    Penn JS, Thum LA, Naash MI (1992) Oxygen-induced retinopathy in the rat: vitamins C and E as potential therapies. Invest Ophthalmol Vis Sci 33:1836–1845PubMedGoogle Scholar
  15. 15.
    Penn JS, Tolman BL, Bullard LE (1997) Effect of a water-soluble vitamin E analog, trolox C, on retinal vascular development in an animal model of retinopathy of prematurity. Free Radic Biol Med 22:977–984PubMedCrossRefGoogle Scholar
  16. 16.
    Beauchamp MH, Martinez-Bermudez AK, Gobeil F Jr, Marrache AM, Hou X, Speranza G, Abran D, Quiniou C, Lachapelle P, Roberts J 2nd, Almazan G, Varma DR, Chemtob S (2001) Role of thromboxane in retinal microvascular degeneration in oxygen-induced retinopathy. J Appl Physiol 90:2279–2288PubMedGoogle Scholar
  17. 17.
    Beauchamp MH, Sennlaub F, Speranza G, Gobeil F Jr, Checchin D, Kermorvant-Duchemin E, Abran D, Hardy P, Lachapelle P, Varma DR, Chemtob S (2004) Redox-dependent effects of nitric oxide on microvascular integrity in oxygen-induced retinopathy. Free Radic Biol Med 37:1885–1894PubMedCrossRefGoogle Scholar
  18. 18.
    Hardy P, Peri KG, Lahaie I, Varma DR, Chemtob S (1996) Increased nitric oxide synthesis and action preclude choroidal vasoconstriction to hyperoxia in newborn pigs. Circ Res 79:504–511PubMedGoogle Scholar
  19. 19.
    Hardy P, Dumont I, Bhattacharya M, Hou X, Lachapelle P, Varma DR, Chemtob S (2000) Oxidants, nitric oxide and prostanoids in the developing ocular vasculature: a basis for ischemic retinopathy. Cardiovasc Res 47:489–509PubMedCrossRefGoogle Scholar
  20. 20.
    Beauchamp MH, Marrache AM, Hou X, Gobeil F Jr, Bernier SG, Lachapelle P, Abran D, Quiniou C, Brault S, Peri KG, Roberts J 2nd, Almazan G, Varma DR, Chemtob S (2002) Platelet-activating factor in vasoobliteration of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 43:3327–3337PubMedGoogle Scholar
  21. 21.
    Cunningham S, Fleck BW, Elton RA, McIntosh N (1995) Transcutaneous oxygen levels in retinopathy of prematurity. Lancet 346:1464–1465PubMedCrossRefGoogle Scholar
  22. 22.
    Gibson AT (2007) Outcome following preterm birth. Best Pract Res Clin Obstet Gynaecol 21:869–882PubMedCrossRefGoogle Scholar
  23. 23.
    Penn JS, Henry MM, Tolman BL (1994) Exposure to alternating hypoxia and hyperoxia causes severe proliferative retinopathy in the newborn rat. Pediatr Res 36:724–731PubMedCrossRefGoogle Scholar
  24. 24.
    Penn JS, Henry MM, Wall PT, Tolman BL (1995) The range of PaO2 variation determines the severity of oxygen-induced retinopathy in newborn rats. Invest Ophthalmol Vis Sci 36:2063–2070PubMedGoogle Scholar
  25. 25.
    Lachapelle P, Dembinska O, Rojas LM, Benoit J, Almazan G, Chemtob S (1999) Persistent functional and structural retinal anomalies in newborn rats exposed to hyperoxia. Can J Physiol Pharmacol 77:48–55PubMedCrossRefGoogle Scholar
  26. 26.
    Dembinska O, Rojas LM, Varma DR, Chemtob S, Lachapelle P (2001) Graded contribution of retinal maturation to the development of oxygen-induced retinopathy in rats. Invest Ophthalmol Vis Sci 42:1111–1118PubMedGoogle Scholar
  27. 27.
    Dembinska O, Rojas LM, Chemtob S, Lachapelle P (2002) Evidence for a brief period of enhanced oxygen susceptibility in the rat model of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 43:2481–2490PubMedGoogle Scholar
  28. 28.
    Dorfman AL, Dembinska O, Chemtob S, Lachapelle P (2006) Structural and functional consequences of trolox C treatment in the rat model of postnatal hyperoxia. Invest Ophthalmol Vis Sci 47:1101–1108PubMedCrossRefGoogle Scholar
  29. 29.
    Penn JS (1990) Oxygen-induced retinopathy in the rat: possible contribution of peroxidation reactions. Doc Ophthalmol 74:179–186PubMedCrossRefGoogle Scholar
  30. 30.
    D’Amore PA, Sweet E (1987) Effects of hyperoxia on microvascular cells in vitro. In Vitro Cell Dev Biol 23:123–128PubMedCrossRefGoogle Scholar
  31. 31.
    Augé N, Pieraggi MT, Thiers JC, Nègre-Salvayre A, Salvayre R (1995) Proliferative and cytotoxic effects of mildly oxidized low-density lipoproteins on vascular smooth-muscle cells. Biochem J 309(Pt 3):1015–1020PubMedGoogle Scholar
  32. 32.
    Kondo T, Kinouchi H, Kawase M, Yoshimoto T (1996) Differential response in the release of hydrogen peroxide between astroglial cells and endothelial cells following hypoxia/reoxygenation. Neurosci Lett 215:103–106PubMedCrossRefGoogle Scholar
  33. 33.
    Benjamin LE, Hemo I, Keshet E (1998) A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development 125:1591–1598PubMedGoogle Scholar
  34. 34.
    Stone J, Itin A, Alon T, Pe’er J, Gnessin H, Chan-Ling T, Keshet E (1995) Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci 15(7 Pt 1):4738–4747PubMedGoogle Scholar
  35. 35.
    Alon T, Hemo I, Itin A, Peter J, Stone J, Keshet E (1995) Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nat Med 1:1024–1028PubMedCrossRefGoogle Scholar
  36. 36.
    Gu X, Samuel S, El-Shabrawey M, Caldwell RB, Bartoli M, Marcus DM, Brooks SE (2002) Effects of sustained hyperoxia on revascularization in experimental retinopathy of prematurity. Invest Ophthalmol Vis Sci 43:496–502PubMedGoogle Scholar
  37. 37.
    Fulton AB, Hansen RM, Findl O (1995) The development of the rod photoresponse from dark-adapted rats. Invest Ophthalmol Vis Sci 36:1038–1045PubMedGoogle Scholar
  38. 38.
    Fulton AB, Hansen RM (1996) Photoreceptor function in infants and children with a history of mild retinopathy of prematurity. J Opt Soc Am A Opt Image Sci Vis 13:566–571PubMedCrossRefGoogle Scholar
  39. 39.
    Fulton AB, Hansen RM, Petersen RA, Vanderveen DK (2001) The rod photoreceptors in retinopathy of prematurity: an electroretinographic study. Arch Ophthalmol 119:499–505Google Scholar
  40. 40.
    Hansen RM, Fulton AB (2000) Background adaptation in children with a history of mild retinopathy of prematurity. Invest Ophthalmol Vis Sci 41:320–324PubMedGoogle Scholar
  41. 41.
    Reisner DS, Hansen RM, Findl O, Petersen RA, Fulton AB (1997) Dark adapted thresholds in children with histories of mild retinopathy of prematurity. Invest Ophthalmol Vis Sci 38:1175–1183PubMedGoogle Scholar
  42. 42.
    Barnaby AM, Hansen RM, Moskowitz A, Fulton AB (2007) Development of scotopic visual thresholds in retinopathy of prematurity. Invest Ophthalmol Vis Sci 48:4854–4860PubMedCrossRefGoogle Scholar
  43. 43.
    Fulton AB, Hansen RM, Moskowitz A, Barnaby AM (2005) Multifocal ERG in subjects with a history of retinopathy of prematurity. Doc Ophthalmol 111:7–13PubMedCrossRefGoogle Scholar
  44. 44.
    Liu K, Akula JD, Falk C, Hansen RM, Fulton AB (2006) The retinal vasculature and function of the neural retina in a rat model of retinopathy of prematurity. Invest Ophthalmol Vis Sci 47:2639–2647PubMedCrossRefGoogle Scholar
  45. 45.
    Liu K, Akula JD, Hansen RM, Moskowitz A, Kleinman MS, Fulton AB (2006) Development of the electroretinographic oscillatory potentials in normal and ROP rats. Invest Ophthalmol Vis Sci 47:5447–5452PubMedCrossRefGoogle Scholar
  46. 46.
    Penn JS, Thum LA, Rhem MN, Dell SJ (1988) Effects of oxygen rearing on the electroretinogram and GFA-protein in the rat. Invest Ophthalmol Vis Sci 29:1623–1630PubMedGoogle Scholar
  47. 47.
    Akula JD, Hansen RM, Martinez-Perez ME, Fulton AB (2007) Rod photoreceptor function predicts blood vessel abnormality in retinopathy of prematurity. Invest Ophthalmol Vis Sci 48:4351–4359PubMedCrossRefGoogle Scholar
  48. 48.
    Reynaud X, Hansen RM, Fulton AB (1995) Effect of prior oxygen exposure on the electroretinographic responses of infant rats. Invest Ophthalmol Vis Sci 36:2071–2079PubMedGoogle Scholar
  49. 49.
    Weidman TA, Kuwabara T (1968) Postnatal development of the rat retina. An electron microscopic study. Arch Ophthalmol T79T:470–484Google Scholar
  50. 50.
    Fulton AB, Reynaud X, Hansen RM, Lemere CA, Parker C, Williams TP (1999) Rod photoreceptors in infant rats with a history of oxygen exposure. Invest Ophthalmol Vis Sci 40:168–174PubMedGoogle Scholar
  51. 51.
    Joly S, Dorfman AL, Chemtob S, Moukhles H, Lachapelle P (2006) Structural and functional consequences of bright light exposure on the retina of neonatal rats. Doc Ophthalmol 113:93–103PubMedCrossRefGoogle Scholar
  52. 52.
    Gole GA, Browning J, Elts SM (1990) The mouse model of oxygen-induced retinopathy: a suitable animal model for angiogenesis research. Doc Ophthalmol 74:163–169PubMedCrossRefGoogle Scholar
  53. 53.
    Aiello LP, Pierce EA, Foley ED, Takagi H, Chen H, Riddle L, Ferrara N, King GL, Smith LE (1995) 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 92:10457–10461PubMedCrossRefGoogle Scholar
  54. 54.
    Holmes JM, Duffner LA (1996) The effect of postnatal growth retardation on abnormal neovascularization in the oxygen exposed neonatal rat. Curr Eye Res 15:403–409PubMedCrossRefGoogle Scholar
  55. 55.
    Graymore C (1959) Metabolism of the developing retina, 1: aerobic and anaerobic glycolysis in the developing rat retina. Br J Ophthalmol 43:34–39PubMedCrossRefGoogle Scholar
  56. 56.
    Graymore C (1960) Metabolism of the developing retina, III: respiration in the developing rat retina and the effect of an inherited degeneration of the retinal neuro-epithelium. Br J Ophthalmol 44:363–369PubMedCrossRefGoogle Scholar
  57. 57.
    Bougle D, Vert P, Reichart E, Hartemann D Heng EL (1982) Retinal superoxide dismutase activity in newborn kittens exposed to normobaric hyperoxia: effect of vitamin E. Pediatr Res 16:400–402PubMedCrossRefGoogle Scholar
  58. 58.
    DeVito V, Reynolds JW, Benda GI, Carlson C (1986) Serum vitamin E levels in very low-birth weight infants receiving vitamin E in parenteral nutrition solutions. JPEN J Parenter Enteral Nutr 10:63–65PubMedCrossRefGoogle Scholar
  59. 59.
    Nielsen JC, Naash MI, Anderson RE (1988) The regional distribution of vitamins E and C in mature and premature human retinas. Invest Ophthalmol Vis Sci 29:22–26PubMedGoogle Scholar
  60. 60.
    Katz ML, Robison WG Jr (1988) Autoxidative damage to the retina: potential role in retinopathy of prematurity. Birth Defects Orig Artic 24:237–248Google Scholar
  61. 61.
    Flower RW, Hall MO, Patz A (1984) Oxygen. In: Sears ML (ed) Pharmacology of the eye. Springer, Verlag, New York, pp 627–638Google Scholar
  62. 62.
    McColm JR, Fleck BW (2001) Retinopathy of prematurity: causation. Semin Neonatol 6:453–460PubMedCrossRefGoogle Scholar
  63. 63.
    Phelps DL, Rosenbaum AL, Isenberg SJ, Leake RD, Dorey FJ (1987) Tocopherol efficacy and safety for preventing retinopathy of prematurity: a randomized, controlled, double-masked trial. Pediatrics 79:489–500PubMedGoogle Scholar
  64. 64.
    Johnson L, Quinn GE, Abbasi S, Gerdes J, Bowen FW, Bhutani V (1995) Severe retinopathy of prematurity in infants with birth weights less than 1250 grams: incidence and outcome of treatment with pharmacologic serum levels of vitamin E in addition to cryotherapy from 1985 to 1991. J Pediatr 127:632–639PubMedCrossRefGoogle Scholar
  65. 65.
    Liu PM, Fang PC, Huang CB, Kou HK, Chung MY, Yang YH, Chung CH (2005) Risk factors of retinopathy of prematurity in premature infants weighing less than 1600 g. Am J Perinatol 22:115–120PubMedCrossRefGoogle Scholar
  66. 66.
    Dyatlov VA, Makovetskaia VV, Leonhardt R, Lawrence DA, Carpenter DO (1998) Vitamin E enhances Ca(2+)-mediated vulnerability of immature cerebellar granule cells to ischemia. Free Radic Biol Med 25:793–802PubMedCrossRefGoogle Scholar
  67. 67.
    Moncada S, Higgs A, Furchgott R (1997) International Union of Pharmacology Nomenclature in Nitric Oxide Research. Pharmacol Rev 49:137–142PubMedGoogle Scholar
  68. 68.
    Stamler JS, Singel DJ, Loscalzo J (1992) Biochemistry of nitric oxide and its redox-activated forms. Science 258:1898–1902PubMedCrossRefGoogle Scholar
  69. 69.
    Morrow JD, Awad JA, Boss HJ, Blair IA, Roberts LJ (1992) Non-cyclooxygenase-derived prostanoids (F2-isoprostanes) are formed in situ on phospholipids. Proc Natl Acad Sci USA 89:10721–10725PubMedCrossRefGoogle Scholar
  70. 70.
    Morrow JD, Minton TA, Mukundan CR, Campbell MD, Zackert WE, DanielVC, Badr KF, Blair IA, Roberts LJ (1994) Free radical-induced generation of isoprostanes in vivo. Evidence for the formation of D-ring and E-ring isoprostanes. J Biol Chem 269:4317–4326PubMedGoogle Scholar
  71. 71.
    Morrow JD, Chen Y, Brame CJ, Yang J, Sanchez SC, Xu J, Zackert WE, Awad JA, Roberts LJ (1999) The isoprostanes: unique prostaglandin-like products of free-radical-initiated lipid peroxidation. Drug Metab Rev 31:117–139PubMedCrossRefGoogle Scholar
  72. 72.
    Lahaie I, Hardy P, Hou X, Hassessian H, Asselin P, Lachapelle P, Almazan G, Varma DR, Morrow JD, Roberts LJ, Chemtob S (1998) A novel mechanism for vasoconstrictor action of 8-isoprostaglandin F2 alpha on retinal vessels. Am J Physiol 274:R1406–R1416PubMedGoogle Scholar
  73. 73.
    Alloatti G, Montrucchio G, Camussi G (1994) Role of platelet-activating factor (PAF) in oxygen radical-induced cardiac dysfunction. J Pharmacol Exp Ther 269:766–771PubMedGoogle Scholar
  74. 74.
    Cluzel J, Doly M, Bazan NG, Bonhomme B, Braquet P (1995) Inhibition of platelet-activating factor-induced retinal impairments by cholera and pertussis toxins. Ophthalmic Res 27:153–157PubMedCrossRefGoogle Scholar
  75. 75.
    Liu XH, Eun BL, Silverstein FS, Barks JD (1996) The platelet-activating factor antagonist BN 52021 attenuates hypoxic-ischemic brain injury in the immature rat. Pediatr Res 40:797–803PubMedCrossRefGoogle Scholar
  76. 76.
    Akisu M, Kultursay N, Coker I, Huseyinov A (1998) Platelet-activating factor is an important mediator in hypoxic ischemic brain injury in the newborn rat. Flunarizine and Ginkgo biloba extract reduce PAF concentration in the brain. Biol Neonate 74:439–444PubMedCrossRefGoogle Scholar
  77. 77.
    Montrucchio G, Alloatti G, Camussi G (2000) Role of platelet-activating factor in cardiovascular pathophysiology. Physiol Rev 80:1669–1699PubMedGoogle Scholar
  78. 78.
    Rui T, Cepinskas G, Feng Q, Ho YS, Kvietys PR (2001) Cardiac myocytes exposed to anoxia-reoxygenation promote neutrophil transendothelial migration. Am J Physiol Heart Circ.Physiol 281:H440–H447PubMedGoogle Scholar
  79. 79.
    Chanez P, Dent G, Yukawa T, Barnes PJ, Chung KF (1990) Generation of oxygen free radicals from blood eosinophils from asthma patients after stimulation with PAF or phorbol ester. Eur Respir J 3:1002–1007PubMedGoogle Scholar
  80. 80.
    Kinnula VL, Adler KB, Ackley NJ, Crapo JD (1992) Release of reactive oxygen species by guinea pig tracheal epithelial cells in vitro. Am J Physiol 262:L708–L712PubMedGoogle Scholar
  81. 81.
    Simm A, Bertsch G, Frank H, Zimmermann U, Hoppe J (1997) Cell death of AKR-2B fibroblasts after serum removal: a process between apoptosis and necrosis. J Cell Sci 110(Pt 7):819–828PubMedGoogle Scholar
  82. 82.
    Lemasters JJ (1999) V. Necrapoptosis and the mitochondrial permeability transition: shared pathways to necrosis and apoptosis. Am J Physiol 276:G1–G6PubMedGoogle Scholar
  83. 83.
    Hou X, Gobeil F Jr., Marrache AM, Quiniou C, Brault S, Checchin D, Bernier SG, Sennlaub F, Joyal JS, Abran D, Peri K, Varma DR, Chemtob S (2003) Increased platelet-activating factor-induced periventricular brain microvascular constriction associated with immaturity. Am J Physiol Regul Integr Comp Physiol 284:R928–R935PubMedGoogle Scholar
  84. 84.
    Abran D, Varma DR, Chemtob S (1995) Increased thromboxane-mediated contractions of retinal vessels of newborn pigs to peroxides. Am J Physiol 268:H628–H632PubMedGoogle Scholar
  85. 85.
    Chemtob S, Hardy P, Abran D, Li DY, Peri K, Cuzzani O, Varma DR (1995) Peroxide-cyclooxygenase interactions in postasphyxial changes in retinal and choroidal hemodynamics. J Appl Physiol 78:2039–2046PubMedGoogle Scholar
  86. 86.
    Flower RW, McLeod DS, Wajer SD, Sendi GS, Egner PG, Dubin NH (1984) Prostaglandins as mediators of vasotonia in the immature retina. Pediatrics 73:440–444PubMedGoogle Scholar
  87. 87.
    Zhu Y, Park TS, Gidday JM (1998) Mechanisms of hyperoxia-induced reductions in retinal blood flow in newborn pig. Exp Eye Res 67:357–369PubMedCrossRefGoogle Scholar
  88. 88.
    De La Cruz JP, Moreno A, Ruiz-Ruiz MI, Sanchez De La Cuesta F (2000) Effect of DT-TX 30, a combined thromboxane synthase inhibitor and thromboxane receptor antagonist, on retinal vascularity in experimental diabetes mellitus. Thromb Res 97:125–131PubMedCrossRefGoogle Scholar
  89. 89.
    Ashton N (1966) Oxygen and the growth and development of retinal vessels. In vivo and in vitro studies. The XX Francis I. Proctor Lecture. Am J Ophthalmol 62:412–435PubMedGoogle Scholar
  90. 90.
    Chan-Ling T, Stone J (1992) Retinopathy of prematurity: Origins in the architecture of the retina. Prog Retinal Eye Res 12:155–178CrossRefGoogle Scholar
  91. 91.
    Ashton N (1963) Studies of the retinal capillaries in relation to diabetic and other retinopathies. Br J Ophthalmol. 47:521–538PubMedCrossRefGoogle Scholar
  92. 92.
    Abran D, Li DY, Varma DR, Chemtob S (1995) Characterization and ontogeny of PGE2 and PGF2 alpha receptors on the retinal vasculature of the pig. Prostaglandins 50:253–267PubMedCrossRefGoogle Scholar
  93. 93.
    Ashton AW, Yokota R, John G, Zhao S, Suadicani SO, Spray DC, Ware JA (1999) Inhibition of endothelial cell migration, intercellular communication, and vascular tube formation by thromboxane A(2). J Biol Chem 274:35562–35570PubMedCrossRefGoogle Scholar
  94. 94.
    Quiniou C, Sennlaub F, Beauchamp MH, Checchin D, Lahaie I, Brault S, Gobeil F Jr, Sirinyan M, Kooli A, Hardy P, Pshezhetsky A, Chemtob S (2006) Dominant role for calpain in thromboxane-induced neuromicrovascular endothelial cytotoxicity. J Pharmacol ExpTher 316:618–627Google Scholar
  95. 95.
    Orrenius S, McCabe MJ Jr, Nicotera P (1992) Ca(2+)-dependent mechanisms of cytotoxicity and programmed cell death. Toxicol Lett 64–65. Spec No: 357–364Google Scholar
  96. 96.
    Trump BF, Berezesky IK (1995) Calcium-mediated cell injury and cell death. FASEB J 9:219–228PubMedGoogle Scholar
  97. 97.
    Chakraborti T, Das S, Mondal M, Roychoudhury S, Chakraborti S (1999) Oxidant, mitochondria and calcium: an overview. Cell Signal 11:77–85PubMedCrossRefGoogle Scholar
  98. 98.
    Gu X, El-Remessy AB, Brooks SE, Al-Shabrawey M, Tsai NT, Caldwell RB (2003) Hyperoxia induces retinal vascular endothelial cell apoptosis through formation of peroxynitrite. Am J Physiol Cell Physiol 285:C546–C554PubMedGoogle Scholar
  99. 99.
    Brooks SE, Gu X, Samuel S, Marcus DM, Bartoli M, Huang PL, Caldwell RB (2001) Reduced severity of oxygen-induced retinopathy in eNOS-deficient mice. Invest Ophthalmol Vis Sci 42:222–228PubMedGoogle Scholar
  100. 100.
    El-Remessy AB, Abou-Mohamed G, Caldwell RW, Caldwell RB (2003) High glucose-induced tyrosine nitration in endothelial cells: role of eNOS uncoupling and aldose reductase activation. Invest Ophthalmol Vis Sci 44:3135–3143PubMedCrossRefGoogle Scholar
  101. 101.
    Jiang H, Kruger N, Lahiri DR, Wang D, Vatele JM, Balazy M (1999) Nitrogen dioxide induces cis-trans-isomerization of arachidonic acid within cellular phospholipids. Detection of trans-arachidonic acids in vivo. J Biol Chem 274:16235–16241PubMedCrossRefGoogle Scholar
  102. 102.
    Balazy M, Poff CD (2004) Biological nitration of arachidonic acid. Curr Vasc Pharmacol 2:81–93PubMedCrossRefGoogle Scholar
  103. 103.
    Kermorvant-Duchemin E, Sennlaub F, Sirinyan M, Brault S, Andelfinger G, Kooli A, Germain S, Ong H, Orleans-Juste P, Gobeil F Jr., Zhu T, Boisvert C, Hardy P, Jain K, Falck JR, Balazy M, Chemtob S (2005) Trans-arachidonic acids generated during nitrative stress induce a thrombospondin-1-dependent microvascular degeneration. Nat Med 11:1339–1345PubMedCrossRefGoogle Scholar
  104. 104.
    Dawson DW, Pearce SF, Zhong R, Silverstein RL, Frazier WA, Bouck NP (1997) CD36 mediates the In vitro inhibitory effects of thrombospondin-1 on endothelial cells. J Cell Biol 138:707–717PubMedCrossRefGoogle Scholar
  105. 105.
    Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N (2000) Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 6:41–48PubMedCrossRefGoogle Scholar
  106. 106.
    Flynn JT, Bancalari E, Snyder ES, Goldberg RN, Feuer W, Cassady J, Schiffman J, Feldman HI, Bachynski B, Buckley E et al (1992) A cohort study of transcutaneous oxygen tension and the incidence and severity of retinopathy of prematurity. N Engl J Med 326:1050–1054PubMedGoogle Scholar
  107. 107.
    Mann RM, Riva CE, Stone RA, Barnes GE, Cranstoun SD (1995) Nitric oxide and choroidal blood flow regulation. Invest Ophthalmol Vis Sci 36:925–930PubMedGoogle Scholar
  108. 108.
    Stone WL, Farnsworth CC, Dratz EA (1979) A reinvestigation of the fatty acid content of bovine, rat and frog retinal rod outer segments. Exp Eye Res 28:387–397PubMedCrossRefGoogle Scholar
  109. 109.
    Organisciak DT, Jiang YL, Wang HM, Pickford M, Blanks JC (1989) Retinal light damage in rats exposed to intermittent light. Comparison with continuous light exposure. Invest Ophthalmol Vis Sci 30:795–805PubMedGoogle Scholar
  110. 110.
    De La Paz MA, Anderson RE (1992) Lipid peroxidation in rod outer segments. Role of hydroxyl radical and lipid hydroperoxides. Invest Ophthalmol Vis Sci 33:2091–2096PubMedGoogle Scholar
  111. 111.
    Demontis GC, Longoni B, Marchiafava PL (2002) Molecular steps involved in light-induced oxidative damage to retinal rods. Invest Ophthalmol Vis Sci 43:2421–2427PubMedGoogle Scholar
  112. 112.
    Organisciak DT, Winkler BS (1994) Retinal light damage: Practical and theoretical considerations. Prog Retin Eye Res 13:1–29CrossRefGoogle Scholar
  113. 113.
    Hanna N, Peri KG, Abran D, Hardy P, Doke A, Lachapelle P, Roy MS, Orquin J, Varma DR, Chemtob S (1997) Light induces peroxidation in retina by activating prostaglandin G/H synthase. Free Radic Biol Med 23:885–897PubMedCrossRefGoogle Scholar
  114. 114.
    Boulton M, Rozanowska M, Rozanowski B (2001) Retinal photodamage. J Photochem Photobiol B Biol 64:144–161CrossRefGoogle Scholar
  115. 115.
    Remé CE, Bush R, Hafezi F, Wenzel A, Grimm C (1998) Photostasis and beyond- Where adaptation ends. In: Williams TP, Thistle AB (eds) Photostasis and related phenomena. Plenum Press, New York, pp 199–206Google Scholar
  116. 116.
    Penn JS, Williams TP (1986) Photostasis: regulation of daily photon-catch by rat retinas in response to various cyclic illuminances. Exp Eye Res 43:915–928PubMedCrossRefGoogle Scholar
  117. 117.
    Fulton AB, Hansen RM, Dodge J, Williams TP (1998) Photoreceptor development and photostasis. In: Williams TP, Thistle AB (eds) Photostasis and Related Phenomena. Plenum Press, New YorkGoogle Scholar
  118. 118.
    Penn JS (1998) Early studies of the photostasis phenomenon- Retinal adaptation to the light environment. In: Williams TP, Thistle AB (eds) Photostasis and related phenomena. Plenum Press, New York London, pp 1Google Scholar
  119. 119.
    Williams TP (1998) Light history and photostasis- What is a “normal”rat retina? In: Williams TP, Thistle AB (eds) Photostasis and related phenomena. Plenum Press, New York, pp 17–32Google Scholar
  120. 120.
    Noell WK, Walker VS, Kang BS, Berman S (1966) Retinal damage by light in rats. Invest Ophthalmol 5:450–473PubMedGoogle Scholar
  121. 121.
    Grimm C, Wenzel A, Hafezi F, Remé CE (2000) Gene expression in the mouse retina: the effect of damaging light. Mol Vis 6:252–260PubMedGoogle Scholar
  122. 122.
    Gorn RA, Kuwabara T (1967) Retinal damage by visible light. A physiologic study. Arch Ophthalmol 77:115–118PubMedGoogle Scholar
  123. 123.
    Kuwabara T, Gorn RA (1968) Retinal damage by visible light. An electron microscopic study. Arch Ophthalmol 79:69–78PubMedGoogle Scholar
  124. 124.
    O’Steen WK, Anderson KV, Shear CR (1974) Photoreceptor degeneration in albino rats: dependency on age. Invest Ophthalmol 13:334–339PubMedGoogle Scholar
  125. 125.
    Penn JS, Thum LA (1987) A comparison of the retinal effects of light damage and high illuminance light history. Prog Clin Biol Res 247:425–438PubMedGoogle Scholar
  126. 126.
    Penn JS, Thum LA, Naash MI (1989) Photoreceptor physiology in the rat is governed by the light environment. Exp Eye Res 49:205–215PubMedCrossRefGoogle Scholar
  127. 127.
    Li F, Cao W, Anderson RE (2001) Protection of photoreceptor cells in adult rats from light-induced degeneration by adaptation to bright cyclic light. Exp Eye Res 73:569–577PubMedCrossRefGoogle Scholar
  128. 128.
    Marc RE, Jones BW, Watt CB, Strettoi E (2003) Neural remodeling in retinal degeneration. Prog Retin Eye Res 22:607–655PubMedCrossRefGoogle Scholar
  129. 129.
    Organisciak DT, Darrow RM, Barsalou LS (2003) Light-induced retinal degeneration. In: Levin LA, Di Polo A (eds) Ocular neuroprotection. Marcel Dekker Inc, New York, Basel, pp 85–107Google Scholar
  130. 130.
    Wenzel A, Grimm C, Samardzija M, Remé CE (2005) Molecular mechanisms of light-induced photoreceptor apoptosis and neuroprotection for retinal degeneration. Prog Retin Eye Res 24:275–306PubMedCrossRefGoogle Scholar
  131. 131.
    Grignolo A, Orzalesi N, Castellazzo R, Vittone P (1969) Retinal damage by visible light in albino rats. An electron microscope study. Ophthalmologica 157:43–59PubMedCrossRefGoogle Scholar
  132. 132.
    O’Steen WK, Shear CR, Anderson KV (1972) Retinal damage after prolonged exposure to visible light. A light and electron microscopic study. Am J Anat 134:5–21PubMedCrossRefGoogle Scholar
  133. 133.
    Remé CE, Wolfrum U, Imsand C, Hafezi F, Williams TP (1999) Photoreceptor autophagy: effects of light history on number and opsin content of degradative vacuoles. Invest Ophthalmol Vis Sci 40:2398–2404PubMedGoogle Scholar
  134. 134.
    Remé CE (2005) The dark side of light: rhodopsin and the silent death of vision the proctor lecture. Invest Ophthalmol Vis Sci 46:2671–2682PubMedCrossRefGoogle Scholar
  135. 135.
    Rapp LM (1995) Retinal Phototoxicity. In: Chang LW, Dyer RS (eds) Handbook of neurotoxicology. Marcel Dekker, New York, pp 963–1003Google Scholar
  136. 136.
    Zhang C, Lei B, Lam TT, Yang F, Sinha D, Tso MO (2004) Neuroprotection of photoreceptors by minocycline in light-induced retinal degeneration. Invest Ophthalmol Vis Sci 45:2753–2759PubMedCrossRefGoogle Scholar
  137. 137.
    Li F, Cao W, Anderson RE (2003) Alleviation of constant-light-induced photoreceptor degeneration by adaptation of adult albino rat to bright cyclic light. Invest Ophthalmol Vis Sci 44:4968–4975PubMedCrossRefGoogle Scholar
  138. 138.
    Kuwabara T, Funahashi M (1976) Light damage in the developing rat retina. Arch Ophthalmol 94:1369–1374PubMedGoogle Scholar
  139. 139.
    Malik S, Cohen D, Meyer E, Perlman I (1986) Light damage in the developing retina of the albino rat: an electroretinographic study. Invest Ophthalmol Vis Sci 27:164–167PubMedGoogle Scholar
  140. 140.
    Joly S, Pernet V, Dorfman AL, Chemtob S, Lachapelle P (2006) Light-induced retinopathy: comparing adult and juvenile rats. Invest Ophthalmol Vis Sci 47:3202–12PubMedCrossRefGoogle Scholar
  141. 141.
    Rapp LM, Williams TP (1980) A parametric study of retinal light damage in albino and pigmented rats. In: Williams TP, Baker BN (eds) The effects of constant light on visual processes. Plenum Press, New York, pp 135–159Google Scholar
  142. 142.
    Rapp LM, Naash MI, Wiegand RD, Joel CD, Nielson JC, Anderson RE (1985) Morphological and biochemical comparisons between retinal regions having differing susceptibility to photoreceptor degeneration. In: Liss AR (ed) Retinal degeneration: experimental and clinical studies, pp 421–437Google Scholar
  143. 143.
    LaVail MM, Matthes MT, Yasumura D, Steinberg RH (1997) Variability in rate of cone degeneration in the retinal degeneration (rd/rd) mouse. Exp Eye Res 65:45–50PubMedCrossRefGoogle Scholar
  144. 144.
    Gordon WC, Casey DM, Lukiw WJ, Bazan NG (2002) DNA damage and repair in light-induced photoreceptor degeneration. Invest Ophthalmol Vis Sci 43:3511–3521PubMedGoogle Scholar
  145. 145.
    Faktorovich EG, Steinberg RH, Yasumura D, Matthes MT, LaVail MM (1992) Basic fibroblast growth factor and local injury protect photoreceptors from light damage in the rat. J Neurosci 12:3554–3567PubMedGoogle Scholar
  146. 146.
    LaVail MM, Unoki K, Yasumura D, Matthes MT, Yancopoulos GD, Steinberg RH (1992) Multiple growth factors, cytokines, and neurotrophins rescue photoreceptors from the damaging effects of constant light. Proc Natl Acad Sci USA 89:11249–11253PubMedCrossRefGoogle Scholar
  147. 147.
    Masuda K, Watanabe I, Unoki K, Ohba N, Muramatsu T (1995) Functional Rescue of photoreceptors from the damaging effects of constant light by survival-promoting factors in the rat. Invest Ophthalmol Vis Sci 36:2142–2146PubMedGoogle Scholar
  148. 148.
    Cao W, Li F, Steinberg RH, Lavail MM (2001) Development of normal and injury-induced gene expression of aFGF, bFGF, CNTF, BDNF, GFAP and IGF-I in the rat retina. Exp Eye Res 72:591–604PubMedCrossRefGoogle Scholar
  149. 149.
    Lau D, Flannery J (2003) Viral-mediated FGF-2 treatment of the constant light damage model of photoreceptor degeneration. Doc Ophthalmol 106:89–98PubMedCrossRefGoogle Scholar
  150. 150.
    Ikeda K, Tanihara H, Tatsuno T, Noguchi H, Nakayama C (2003) Brain-derived neurotrophic factor shows a protective effect and improves recovery of the ERG b-wave response in light-damage. J Neurochem 87:290–296PubMedCrossRefGoogle Scholar
  151. 151.
    Gao H, Hollyfield JG (1996) Basic fibroblast growth factor: increased gene expression in inherited and light-induced photoreceptor degeneration. Exp Eye Res 62:181–189PubMedCrossRefGoogle Scholar
  152. 152.
    Wen R, Cheng T, Song Y, Matthes MT, Yasumura D, LaVail MM, Steinberg RH (1998) Continuous exposure to bright light upregulates bFGF and CNTF expression in the rat retina. Curr Eye Res 17:494–500PubMedCrossRefGoogle Scholar
  153. 153.
    Walsh N, Valter K, Stone J (2001) Cellular and subcellular patterns of expression of bFGF and CNTF in the normal and light stressed adult rat retina. Exp Eye Res 72:495–501PubMedCrossRefGoogle Scholar
  154. 154.
    Joly S, Pernet V, Chemtob S, Di Polo A, Lachapelle P (2007) Neuroprotection in the juvenile rat model of light-induced retinopathy: evidence suggesting a role for FGF-2 and CNTF. Invest Ophthalmol Vis Sci 48:2311–20PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • A. L. Dorfman
    • 1
    • 2
  • S. Joly
    • 2
  • P. Hardy
    • 3
  • S. Chemtob
    • 1
    • 3
  • P. Lachapelle
    • 2
    Email author
  1. 1.Departments of Pharmacology and TherapeuticsMcGill University-Montreal Children’s Hospital Research InstituteMontrealCanada
  2. 2.Departments of Ophthalmology (D-164)/Neurology-NeurosurgeryMcGill University-Montreal Children’s Hospital Research InstituteMontrealCanada
  3. 3.Department of Pediatrics, Ophthalmology and Pharmacology, Research Center-Hôpital Ste. JustineUniversity of MontrealMontrealCanada

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