Immunohistochemical evidence of synaptic retraction, cytoarchitectural remodeling, and cell death in the inner retina of the rat model of oygen-induced retinopathy (OIR)

Investigative Ophthalmology and Visual Science

Volumn 52, Issue 3, 2011, Pages 1693-1708

  Dorfman, Allison Lindsay ^a   Cuenca, Nicolás ^b   Pinilla, Isabel ^c   Chemtob, Sylvain ^d   Lachapelle, Pierre ^a  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b UNIVERSITY OF ALICANTE   (Spain)

^c INSTITUTO ARAGONÉS DE CIENCIAS DE LA SALUD   (Spain)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BASSOON PROTEIN; CALBINDIN; GAMMA TRANSDUCIN; MEMBRANE PROTEIN; METABOTROPIC RECEPTOR 6; OXYGEN; PARVALBUMIN; PROTEIN KINASE C ALPHA; RECOVERIN; SYNAPTOPHYSIN; TRANSDUCIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EUTHANASIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COMMUNICATION; CELL DEATH; CONTROLLED STUDY; CYTOARCHITECTURE; DENDRITE; HYPEROXIA; IMMUNOHISTOCHEMISTRY; NERVE PROJECTION; NEWBORN; NICK END LABELING; NONHUMAN; PERINATAL PERIOD; PHOTORECEPTOR; PRIORITY JOURNAL; RAT; RETINA; RETINA BIPOLAR GANGLION CELL; RETINA CONE; RETINA INNER PLEXIFORM LAYER; RETINA OUTER MOLECULAR LAYER; RETINA ROD; RETINOPATHY; SYNAPSE; SYNAPTOSOME;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BIOLOGICAL MARKERS; DISEASE MODELS, ANIMAL; EYE PROTEINS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; HUMANS; HYPEROXIA; IN SITU NICK-END LABELING; INFANT, NEWBORN; MALE; MICROSCOPY, CONFOCAL; NEURONAL PLASTICITY; OXYGEN; PRESYNAPTIC TERMINALS; RATS; RATS, LONG-EVANS; RATS, SPRAGUE-DAWLEY; RETINAL NEURONS; RETINOPATHY OF PREMATURITY;

EID: 79955934873     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.10-6197     Document Type: Article

References (65)

1. Holmström G, van Wijngaarden P, Coster DJ, Williams KA. Genetic susceptibility to retinopathy of prematurity: the evidence from clinical and experimental animal studies. Br J Ophthalmol. 2007; 91:1704-1708.
2. Holmström G. Retinopathy of prematurity. BMJ. 1993;307:694-695.
3. Brown BA, Thach AB, Song JC, Marx JL, Kwun RC, Frambach DA. Retinopathy of prematurity: evaluation of risk factors. Int Ophthalmol. 1998;22:279-283.
4. Monos T, Rosen SD, Karplus M, Yassur Y. Fundus pigmentation in retinopathy of prematurity. Pediatrics. 1996;97:343-348.
5. Shohat M, Reisner SH, Krikler R, Nissenkorn I, Yassur Y, Ben-Sira I. Retinopathy of prematurity: incidence and risk factors. Pediatrics. 1983;72:159-163.
6. Lang DM, Blackledge J, Arnold RW. Is Pacific race a retinopathy of prematurity risk factor? Arch Pediatr Adolesc Med. 2005;159:771-773.
7. Tadesse M, Dhanireddy R, Mittal M, Higgins RD. Race, Candida sepsis, and retinopathy of prematurity. Biol Neonate. 2002;81:86-90.
8. Saunders RA, Donahue ML, Christmann LM, et al. Racial variation in retinopathy of prematurity: the Cryotherapy for Retinopathy of Prematurity Cooperative Group. Arch Ophthalmol. 1997;115: 604-608.
9. Arnold RW, Kesler K, Avila E. Susceptibility to retinopathy of prematurity in Alaskan Natives. J Pediatr Ophthalmol Strabismus. 1994;31:192-194.
10. Schaffer DB, Palmer EA, Plotsky DF, et al. Prognostic factors in the natural course of retinopathy of prematurity: the Cryotherapy for Retinopathy of Prematurity Cooperative Group. Ophthalmology. 1993;100:230-237.
11. Weidman TA, Kuwabara T. Development of the rat retina. Invest Ophthalmol Vis Sci. 1969;8:60-69.
12. Patz A, Payne JW. Retinopathy of prematurity (retrolental fibroplasia). In: Tasman W, Jaegen EA, eds. Duane's Foundations of Clinical Ophthalmology. Philadelphia: Lippincott Williams & Wilkins; 1998:1-19.
13. Penn JS, Tolman BL, Henry MM. Oxygen-induced retinopathy in the rat: relationship of retinal nonperfusion to subsequent neovascularization. Invest Ophthalmol Vis Sci. 1994;35:3429-3435.
14. Reynaud X, Dorey CK. Extraretinal neovascularization induced by hypoxic episodes in the neonatal rat. Invest Ophthalmol Vis Sci. 1994;35:3169-77.
15. Moore A. Retinopathy of prematurity. In: Taylor D, ed. Pediatric Ophthalmology. Boston: Blackwell Scientific; 1990:365-375.
16. Safa R, Osborne NN. Retinas from albino rats are more susceptible to ischaemic damage than age-matched pigmented animals. Brain Res. 2000;862:36-42.
17. Gao G, Li Y, Fant J, Crosson CE, Becerra SP, Ma JX. 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. 2002;51:1218-1225.
18. Zhang D, Kaufman PL, Gao G, Saunders RA, Ma JX. Intravitreal injection of plasminogen kringle 5, an endogenous angiogenic inhibitor, arrests retinal neovascularization in rats. Diabetologia. 2001;44:757-765.
19. Dorfman AL, Polosa A, Joly S, Chemtob S, Lachapelle P. Functional and structural changes resulting from strain differences in the rat model of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci. 2009;50:2436-2450.
20. Dorfman A, Dembinska O, Chemtob S, Lachapelle P. Early manifestations of postnatal hyperoxia on the retinal structure and function of the neonatal rat. Invest Ophthalmol Vis Sci. 2008;49: 458-466.
21. Dorfman AL, Dembinska O, Chemtob S, Lachapelle P. Structural and functional consequences of trolox C treatment in the rat model of postnatal hyperoxia. Invest Ophthalmol Vis Sci. 2006; 47:1101-1108.
22. Dembinska O, Rojas LM, Chemtob S, Lachapelle P. Evidence for a brief period of enhanced oxygen susceptibility in the rat model of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci. 2002;43: 2481-2490.
23. Dembinska O, Rojas LM, Varma DR, Chemtob S, Lachapelle P. Graded contribution of retinal maturation to the development of oxygen-induced retinopathy in rats. Invest Ophthalmol Vis Sci. 2001;42:1111-1118.
24. Lachapelle P, Dembinska O, Rojas LM, Benoit J, Almazan G, Chemtob S. Persistent functional and structural retinal anomalies in newborn rats exposed to hyperoxia. Can J Physiol Pharmacol. 1999;77:48-55.
25. Cangiano L, Gargini C, Della Santina L, Demontis GC, Cervetto L. High-pass filtering of input signals by the Ih current in a nonspiking neuron, the retinal rod bipolar cell. PLoS ONE. 2007;12: e1327.
26. Cuenca N, Pinilla I, Sauvé Y, Wang S, Lu B, Lund RD. Regressive and reactive changes in the connectivity patterns of rod and cone pathways of P23H transgenic rat retina. Neuroscience. 2004;127: 301-317.
27. Nakajima Y, Iwakabe H, Akazawa C et al. Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. J Biol Chem. 1993;268:11868-11873.
28. Barhoum R, Martínez-Navarrete G, Corrochano S, et al. Functional and structural modifications during retinal degeneration in the rd10 mouse. Neuroscience. 2008;26:155:698-713.
29. Oh EC, Khan N, Novelli E, Khanna H, Strettoi E, Swaroop A. Transformation of cone precursors to functional rod photoreceptors by bZIP transcription factor NRL. Proc Natl Acad Sci U S A. 2007;104:1679-1684.
30. Cuenca N, Pinilla I, Sauvé Y, Lund R. Early changes in synaptic connectivity following progressive photoreceptor degeneration in RCS rats. Eur J Neurosci. 2005;22:1057-1072.
31. Pinilla I, Cuenca N, Martínez-Navarrete G, Lund RD, Sauve ́ Y. Intraretinal processing following photoreceptor rescue by nonretinal cells. Vision Res. 2009;49:2067-2077.
32. Johnson J, Tian N, Caywood MS, Reimer RJ, Edwards RH, Copenhagen DR. Vesicular neurotransmitter transporter expression in developing postnatal rodent retina: GABA and glycine precede glutamate. J Neurosci. 2003;23:518-529.
33. Gong J, Jellali A, Forster V, et al. The toxicity of the PrP106-126 prion peptide on cultured photoreceptors correlates with the prion protein distribution in the mammalian and human retina. Am J Pathol. 2007;170:1314-1324.
34. McGinnis JF, Stepanik PL, Chen W, Elias R, Cao W, Lerious V. Unique retina cell phenotypes revealed by immunological analysis of recoverin expression in rat retina cells. J Neurosci Res. 1999; 55:252-260.
35. Chen W, Elias R, Cao W, Lerious V, McGinnis JF. Anti-recoverin antibodies cause the apoptotic death of mammalian photoreceptor cells in vitro. J Neurosci Res. 1999;57:706-718.
36. Martínez-Navarrete GC, Martín-Nieto J, Esteve-Rudd J, Angulo A, Cuenca N. Alpha synuclein gene expression profile in the retina of vertebrates. Mol Vis. 2007;13:949-961.
37. Zhang L, Fina ME, Vardi N. Regulation of KCC2 and NKCC during development: membrane insertion and differences between cell types. J Comp Neurol. 2006;499:132-143.
38. Zhang H, Li S, Doan T, et al. Deletion of PrBP/_ impedes transport of GRK1 and PDE6 catalytic subunits to photoreceptor outer segments. Proc Natl Acad Sci U S A. 2007;104:8857-8862.
39. Nagar S, Krishnamoorthy V, Cherukuri P, Jain V, Dhingra NK. Early remodeling in an inducible animal model of retinal degeneration. Neuroscience. 2009;160:517-529.
40. Pinilla I, Cuenca N, Sauve ́ Y, Wang S, Lund RD. Preservation of outer retina and its synaptic connectivity following subretinal injections of human RPE cells in the Royal College of Surgeons rat. Exp Eye Res. 2007;85:381-392.
41. Euler T, Wässle H. Immunocytochemical identification of cone bipolar cells in the rat retina. J Comp Neurol. 1995;361:461-478.
42. Endo T, Kobayashi M, Kobayashi S, Onaya T. Immunocytochemical and biochemical localization of parvalbumin in the retina. Cell Tissue Res. 1986;243:213-217.
43. Hamano K, Kiyama H, Emson PC, Manabe R, Nakauchi M, Tohyama M. Localization of two calcium binding proteins, calbindin (28 kD) and parvalbumin (12 kD), in the vertebrate retina. J Comp Neurol. 1990;302:417-424.
44. Cuenca N, Deng P, Linberg KA, Lewis GP, Fisher SK, Kolb H. The neurons of the ground squirrel retina as revealed by immunostains for calcium binding proteins and neurotransmitters. J Neurocytol. 2002;31:649-666.
45. Wiedenmann B, Franke WW. Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell. 1985;41:1017-1028.
46. O'Driscoll C, Donovan M, Cotter TG. Analysis of apoptotic and survival mediators in the early post-natal and mature retina. Exp Eye Res. 2006;83:1482-1492.
47. Wallace DM, Donovan M, Cotter TG. Histone deacetylase activity regulates apaf-1 and caspase 3 expression in the developing mouse retina. Invest Ophthalmol Vis Sci. 2006;47:2765-2772.
48. Joly S, Dorfman AL, Chemtob S, Moukhles H, Lachapelle P. Structural and functional consequences of bright light exposure on the retina of neonatal rats. Doc Ophthalmol. 2006;113:93-103.
49. Penn JS, Thum LA, Rhem MN, Dell SJ. Effects of oxygen rearing on the electroretinogram and GFA-protein in the rat. Invest Ophthalmol Vis Sci. 1988;29:1623-1630.
50. Cringle SJ, Yu PK, Su EN, Yu DY. Oxygen distribution and consumption in the developing rat retina. Invest Ophthalmol Vis Sci. 2006;47:4072-4076.
51. Graymore C. 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. 1960;44: 363-369.
52. Graymore C. Metabolism of the developing retina, 1: aerobic and anaerobic glycolysis in the developing rat retina. Br J Ophthalmol. 1959;43:34-39.
53. Pignatelli V, Cepko CL, Strettoi E. Inner retinal abnormalities in a mouse model of Leber's congenital amaurosis. J Comp Neurol. 2004;469:351-359.
54. Sarna T, Burke JM, Korytowski W, et al. Loss of melanin from human RPE with aging: possible role of melanin photooxidation. Exp Eye Res. 2003;76:89-98.
55. Sarna T. Properties and function of the ocular melanin-a photobiophysical view. J Photochem Photobiol B. 1992;12:215-258.
56. Kolb H. How the retina works. Am Sci. 2003;91:28-35.
57. Valter K, Bisti S, Gargini C, et al. Time course of neurotrophic factor upregulation and retinal protection against light-induced damage after optic nerve section. Invest Ophthalmol Vis Sci. 2005;46:1748-1754.
58. Wen R, Song Y, Cheng T, et al. Injury-induced upregulation of bFGF and CNTF mRNAS in the rat retina. J Neurosci. 1995;15: 7377-7385.
59. Faktorovich EG, Steinberg RH, Yasumura D, Matthes MT, LaVail MM. Photoreceptor degeneration in inherited retinal dystrophy delayed by basic fibroblast growth factor. Nature. 1990;347:83-86.
60. Fulton AB, Hansen RM, Moskowitz A, Akula JD. The neurovascular retina in retinopathy of prematurity. Prog Retin Eye Res. 2009;28: 452-482.
61. Gariano RF, Gardner TW. Retinal angiogenesis in development and disease. Nature. 2005;438:960-966.
62. Gogat K, Le Gat L, Van Den Berghe L, et al. VEGF and KDR gene expression during human embryonic and fetal eye development. Invest Ophthalmol Vis Sci. 2004;45:7-14.
63. Reynaud X, Hansen RM, Fulton AB. Effect of prior oxygen exposure on the electroretinographic responses of infant rats. Invest Ophthalmol Vis Sci. 1995;36:2071-2079.
64. Chan-Ling T, Tout S, Holländer H, Stone J. Vascular changes and their mechanisms in the feline model of retinopathy of prematurity. Invest Ophthalmol Vis Sci. 1992;33:2128-2147.
65. Fulton AB, Hansen RM, Moskowitz A, Barnaby AM. Multifocal ERG in subjects with a history of retinopathy of prematurity. Doc Ophthalmol. 2005;111:7-13.