Neuroprotective actions of progesterone in an in vivo model of retinitis pigmentosa

Pharmacological Research

Volumn 99, Issue , 2015, Pages 276-288

  Sanchez Vallejo V ^a   Benlloch Navarro, S ^a   Lopez Pedrajas R ^a   Romero, F J ^b   Miranda, M ^a  

^a UNIVERSIDAD CEU CARDENAL HERRERA   (Spain)

^b UNIVERSIDAD CATÓLICA DE VALENCIA SAN VICENTE MÁRTIR   (Spain)

Author keywords

Gliosis; Glutamate; Glutathione; Progesterone; Retinitis pigmentosa

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE AMMONIA LIGASE; GLUTAMATE CYSTEINE LIGASE; PROGESTERONE; ANTIOXIDANT; GLUTAMIC ACID; NEUROPROTECTIVE AGENT;

ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; CRYOPROTECTION; ELECTRORETINOGRAPHY; ENZYME ACTIVITY; EXCITOTOXICITY; HORMONE SYNTHESIS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VIVO STUDY; MOUSE; NEUROPROTECTION; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; RETINA INNER NUCLEAR LAYER; RETINITIS PIGMENTOSA; STEROIDOGENESIS; ANIMAL; C3H MOUSE; CELL DEATH; DISEASE MODEL; DRUG EFFECTS; METABOLISM; RETINA;

ANIMALS; ANTIOXIDANTS; CELL DEATH; DISEASE MODELS, ANIMAL; GLUTAMATE-CYSTEINE LIGASE; GLUTAMIC ACID; MICE; MICE, INBRED C3H; NEUROPROTECTIVE AGENTS; PROGESTERONE; RETINA; RETINITIS PIGMENTOSA;

EID: 84938071713     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2015.06.019     Document Type: Article

References (92)

1. S. Usui, K. Komeima, S.Y. Lee, Y.J. Jo, S. Ueno, B.S. Rogers, Z. Wu, J. Shen, L. Lu, B.C. Oveson, P.S. Rabinovitch, and P.A. Campochiaro Increased expression of catalase and superoxide dismutase 2 reduces cone cell death in retinitis pigmentosa Mol. Ther. 17 2009 778 786
2. F. Paquet-Durand, S. Azadi, S.M. Hauck, M. Ueffing, T. van Veen, and P. Ekström Calpain is activated in degenerating photoreceptors in the rd1 mouse J. Neurochem. 96 2006 802 814
3. A. Kennan, A. Aherne, and P. Humphries Light in retinitis pigmentosa Trends Genet. 21 2005 103 110
4. D. Dalkara, and J.A. Sahel Gene therapy for inherited retinal degenerations C R Biol. 337 2014 185 192
5. Y. He, Y. Zhang, and G. Su Recent advances in treatment of retinitis pigmentosa Curr. Stem Cell. Res. Ther. 10 2015 258 265
6. K. Komeima, B.S. Rogers, and P.A. Campochiaro Antioxidants slow photoreceptor cell death in mouse models of retinitis pigmentosa J Cell. Physiol 213 2007 809 815
7. M. Miranda, E. Arnal, S. Ahuja, R. Alvarez-Nölting, R. López-Pedrajas, P. Ekström, F. Bosch-Morell, T. van Veen, and F.J. Romero Antioxidants rescue photoreceptors in rd1 mice: relationship with thiol metabolism Free Radic. Biol. Med. 48 2010 216 222
8. E.G. Faktorovich, R.H. Steinberg, D. Yasumura, M.T. Matthes, and M.M. LaVail Basic fibroblast growth factor and local injury protect photoreceptors from light damage in the rat J. Neurosci. 12 1992 3554 3567
9. M. Cayouette, D. Behn, M. Sendtner, P. Lachapelle, and C. Gravel Intraocular gene transfer of ciliary neurotrophic factor prevents death and increases responsiveness of rod photoreceptors in the retinal degeneration slow mouse J. Neurosci. 18 1998 9282 9293
10. D. Bok, D. Yasumura, M.T. Matthes, A. Ruiz, J.L. Duncan, A.V. Chappelow, S. Zolutukhin, W. Hauswirth, and M.M. LaVail Effects of adeno-associated virus-vectored ciliary neurotrophic factor on retinal structure and function in mice with a P216L rds/peripherin mutation Exp. Eye Res. 74 2002 719 735
11. F. Doonan, C. O'Driscoll, P. Kenna, and T.G. Cotter Enhancing survival of photoreceptor cells in vivo using the synthetic progestin Norgestrel J. Neurochem. 118 2011 915 927
12. M. Singh, and C. Su Progesterone and neuroprotection Horm. Behav. 63 2013 284 290
13. J.Y. Hwang, R.S. Duncan, C. Madry, M. Singh, and P. Koulen Progesterone potentiates calcium release through IP3 receptors by an Akt-mediated mechanism in hippocampal neurons Cell Calcium 45 2009 233 242
14. S.L. Petersen, K.A. Intlekofer, P.J. Moura-Conlon, D.N. Brewer, J. Del Pino Sans, and J.A. Lopez Novel progesterone receptors: neural localization and possible functions Front. Neurosci. 7 2013 164
15. B. Lei, B. Mace, H.N. Dawson, D.S. Warner, D.T. Laskowitz, and M.L. James Anti-inflammatory effects of progesterone in lipopolysaccharide-stimulated BV-2 microglia PLoS One 9 2014 e103969
16. D.W. Wright, A.L. Kellermann, V.S. Hertzberg, P.L. Clark, M. Frankel, F.C. Goldstein, J.P. Salomone, L.L. Dent, O.A. Harris, D.S. Ander, D.W. Lowery, M.M. Patel, D.D. Denson, A.B. Gordon, M.M. Wald, S. Gupta, S.W. Hoffman, and D.G. Stein ProTECT: a randomized clinical trial of progesterone for acute traumatic brain injury Ann. Emerg. Med. 49 2007 391 402
17. G. Xiao, J. Wei, W. Yan, W. Wang, and Z. Lu Improved outcomes from the administration of progesterone for patients with acute severe traumatic brain injury: a randomized controlled trial Crit. Care 12 2008 R61
18. D.G. Stein Progesterone exerts neuroprotective effects after brain injury Brain Res. Rev. 57 2008 386 397
19. R.L. Roof, S.W. Hoffman, and D.G. Stein Progesterone protects against lipid peroxidation following traumatic brain injury in rats Mol. Chem. Neuropathol. 31 1997 1 11
20. R. Aggarwal, B. Medhi, A. Pathak, V. Dhawan, and A. Chakrabarti Neuroprotective effect of progesterone on acute phase changes induced by partial global cerebral ischaemia in mice J. Pharm. Pharmacol. 60 2008 731 737
21. M. Liu, M.H. Kelley, P.S. Herson, and P.D. Hurn Neuroprotection of sex steroids Minerva Endocrinol. 35 2010 127 143
22. K.J. Grossman, C.W. Goss, and D.G. Stein Effects of progesterone on the inflammatory response to brain injury in the rat Brain Res. 1008 2004 29 39
23. X.L. Yao, J. Liu, E. Lee, G.S. Ling, and J.T. McCabe Progesterone differentially regulates pro- and antiapoptotic gene expression in cerebral cortex following traumatic brain injury in rats J. Neurotrauma. 22 2005 656 668
24. M. Djebaili, S.W. Hoffman, and D.G. Stein Allopregnanolone and progesterone decrease cell death and cognitive deficits after a contusion of the rat pre-frontal cortex Neuroscience 123 2004 349 359
25. P. Kaur, P.K. Jodhka, W.A. Underwood, C.A. Bowles, N.C. de Fiebre, C.M. de Fiebre, and M. Singh Progesterone increases brain-derived neuroptrophic factor expression and protects against glutamate toxicity in a mitogen-activated protein kinase- and phosphoinositide-3 kinase-dependent manner in cerebral cortical explants J. Neurosci. Res. 85 2007 2441 2449
26. P. Guarneri, C. Cascio, D. Russo, S. D'Agostino, G. Drago, G. Galizzi, G. De Leo, F. Piccoli, M. Guarneri, and R. Guarneri Neurosteroids in the retina: neurodegenerative and neuroprotective agents in retinal degeneration Ann. N. Y. Acad. Sci. 1007 2003 117 128
27. T. Nakazawa, H. Takahashi, and M. Shimura Estrogen has a neuroprotective effect on axotomized RGCs through ERK signal transduction pathway Brain Res. 1093 2006 141 149
28. W.K. O'Steen Ovarian steroid effects on light-induced retinal photoreceptor damage Exp. Eye Res. 25 1977 361 369
29. I. Káldi, and A. Berta Progesterone administration fails to protect albino male rats against photostress-induced retinal degeneration Eur. J. Ophthalmol. 14 2004 306 314
30. N. Lu, C. Li, Y. Cheng, A.L. DU. Protective effects of progesterone against high intraocular pressure-induced retinal ischemia-reperfusion in rats. Nan Fang Yi Ke Da Xue Xue Bao 2008, 28, 2026-2029.
31. N. Miyamoto, M. Mandai, I. Suzuma, K. Suzuma, K. Kobayashi, and Y. Honda Estrogen protects against cellular infiltration by reducing the expressions of E-selectin and IL-6 in endotoxin-induced uveitis J. Immunol. 163 1999 374 379
32. Y. Wang, X. Li, J. Wang, H. Shi, W. Bi, W. Hou, and X. Zhang 17β-estradiol mediates upregulation of stromal cell-derived factor-1 in the retina through activation of estrogen receptor in an ischemia-reperfusion injury model Graefes Arch. Clin. Exp. Ophthalmol. 253 2015 17 23
33. C. Li, Y. Tang, F. Li, S. Turner, K. Li, X. Zhou, M. Centola, X. Yan, and W. Cao 17beta-estradiol (betaE2) protects human retinal Müller cell against oxidative stress in vitro: evaluation of its effects on gene expression by cDNA microarray Glia 53 2006 392 400
34. D.M. Kumar, E. Perez, Z.Y. Cai, P. Aoun, A.M. Brun-Zinkernagel, D.F. Covey, J.W. Simpkins, and N. Agarwal Role of nonfeminizing estrogen analogues in neuroprotection of rat retinal ganglion cells against glutamate-induced cytotoxicity Free Radic. Biol. Med. 38 2005 1152 1163
35. E. Nixon, and J.W. Simpkins Neuroprotective effects of nonfeminizing estrogens in retinal photoreceptor neurons Invest. Ophthalmol. Vis. Sci. 53 2012 4739 4747
36. T. Nakazawa, H. Takahashi, and M. Shimura Estrogen hasa neuroprotective effect on axotomized RGCs through ERK signal transduction pathway Brain Res. 1093 2006 141 149
37. C.L. Robertson, and M. Saraswati Progesterone protects mitochondrial function in a rat model of pediatric traumatic brain injury J. Bioenerg Biomembr. 47 2015 43 51
38. S. Liu, H. Wu, G. Xue, X. Ma, J. Wu, Y. Qin, and Y. Hou Metabolic alteration of neuroactive steroids and protective effect of progesterone in Alzheimer's disease-like rats Neural Regen. Res. 8 2013 2800 2810
39. F.F. Xu, S. Sun, A.S. Ho, D. Lee, K.M. Kiang, X.Q. Zhang, A.M. Wang, E.X. Wu, W.M. Lui, B.Y. Liu, and G.K. Leung Effects of progesterone vs. dexamethasone on brain oedema and inflammatory responses following experimental brain resection Brain Inj. 28 2014 1594 1601
40. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and J.R. Randall Protein measurement with the Folin phenol reagent J. Biol. Chem. 193 1951 265 275
41. D.J. Reed, J.R. Babson, P.W. Beatty, A.E. Brodie, W.W. Ellis, and D.W. Potter High performance liquid chromatography analysis of nanomole levels of glutathione, glutathione disulfide, and related thiols and disulfides Anal. Biochem. 106 1980 55 62
42. K. Komeima, B.S. Rogers, L. Lu, and P.A. Campochiaro Antioxidants reduce cone cell death in a model of retinitis pigmentosa Proc. Natl. Acad. Sci. U. S. A. 103 2006 11300 11305
43. N. Sanvicens, and T.G. Cotter Ceramide is the key mediator of oxidative stress-induced apoptosis in retinal photoreceptor cells J. Neurochem. 98 2006 1432 1444
44. F. Paquet-Durand, S.M. Hauck, T. van Veen, M. Ueffing, and P. Ekström PKG activity causes photoreceptor cell death in two retinitis pigmentosa models J. Neurochem. 108 2009 796 810
45. M. Mancini, M.V. Soldovieri, G. Gessner, B. Wissuwa, V. Barrese, F. Boscia, A. Secondo, F. Miceli, C. Franco, P. Ambrosino, L.M. Canzoniero, M. Bauer, T. Hoshi, S.H. Heinemann, and M. Taglialatela Critical role of large-conductance calcium- and voltage-activated potassium channels in leptin-induced neuroprotection of N-methyl-d-aspartate-exposed cortical neurons Pharmacol. Res. 87 2014 80 86
46. R. Crupi, I. Paterniti, M. Campolo, R. Di Paola, S. Cuzzocrea, and E. Esposito Exogenous T3 administration provides neuroprotection in a murine model of traumatic brain injury Pharmacol. Res. 70 2013 80 89
47. T.S. Rex, M. Allocca, L. Domenici, E.M. Surace, A.M. Maguire, A. Lyubarsky, A. Cellerino, J. Bennett, and A. Auricchio Systemic but not intraocular Epo gene transfer protects the retina from light-and genetic-induced degeneration Mol. Ther. 10 2004 855 861
48. S. Corrochano, R. Barhoum, P. Boya, A.I. Arroba, N. Rodríguez-Muela, V. Gómez-Vicente, F. Bosch, F. de Pablo, P. de la Villa, and E.J. de la Rosa Attenuation of vision loss and delay in apoptosis of photoreceptors induced by proinsulin in a mouse model of retinitis pigmentosa Invest Ophthalmol. Vis. Sci. 49 2008 4188 4194
49. M. Indaram, W. Ma, L. Zhao, R.N. Fariss, I.R. Rodriguez, and W.T. Wong 7-Ketocholesterol increases retinal microglial migration, activation, and angiogenicity: a potential pathogenic mechanism underlying age-related macular degeneration Sci. Rep. 5 2015 9144
50. A.I. Arroba, N. Alvarez-Lindo, N. van Rooijen, and E.J. de la Rosa Microglia-Müller glia crosstalk in the rd10 mouse model of retinitis pigmentosa Adv. Exp. Med. Biol. 801 2014 373 379
51. N. Gupta, K.E. Brown, and A.H. Milam Activated microglia in human retinitis pigmentosa, late-onset retinal degeneration, and age-related macular degeneration Exp. Eye Res. 76 2003 463 471
52. F. Ghosh, and K. Johansson Neuronal and glial alterations in complex long-term rhegmatogenous retinal detachment Curr. Eye Res. 37 2012 704 711
53. R.S. Chong, and K.R. Martin Glial cell interactions and glaucoma Curr. Opin. Ophthalmol. 26 2015
54. T.S. Kern Interrelationships between the retinal neuroglia and vasculature in diabetes Diabetes Metab. J. 38 2014 163 170
55. R.J. Collier, Y. Wang, S.S. Smith, E. Martin, R. Ornberg, K. Rhoades, and C. Romano Complement deposition and microglial activation in the outer retina in light-induced retinopathy: inhibition by a 5-HT1A agonist Invest Ophthalmol. Vis. Sci. 52 2011 8108 8116
56. M. Rutar, R. Natoli, and J.M. Provis Small interfering RNA-mediated suppression of Ccl2 in Müller cells attenuates microglial recruitment and photoreceptor death following retinal degeneration J. Neuroinflammation 9 2012 221
57. M. Karlstetter, R. Scholz, M. Rutar, W.T. Wong, J.M. Provis, and T. Langmann Retinal microglia: just bystander or target for therapy Prog. Retin. Eye Res. 45 2015 30 57
58. K. Roesch, M.B. Stadler, and C.L. Cepko Gene expression changes within Müller glial cells in retinitis pigmentosa Mol. Vis. 18 2012 1197 1214
59. E.K. Michaelis Molecular biology of glutamate receptors in the central nervous system and their role in excitotoxicity, oxidative stress and aging Prog. Neurobiol. 54 1998 369 415
60. M.N. Delyfer, V. Forster, N. Neveux, S. Picaud, T. Léveillard, and J.A. Sahel Evidence for glutamate-mediated excitotoxic mechanisms during photoreceptor degeneration in the rd1 mouse retina Mol. Vis. 11 2005 688 696
61. J.E. Pulido, J.S. Pulido, J.C. Erie, J. Arroyo, K. Bertram, M.J. Lu, and S.A. Shippy A role for excitatory amino acids in diabetic eye disease Exp. Diabetes Res. 2007 2007 36150
62. R.J. Ulshafer, D.M. Sherry, R. Dawson Jr, and D.R. Wallace Excitatory amino acid involvement in retinal degeneration Brain Res. 531 1990 350 354
63. E.L. Fletcher, and M. Kalloniatis Neurochemical architecture of the normal and degenerating rat retina J. Comp. Neurol. 376 1996 343 360
64. M. Kalloniatis, and G. Tomisich Amino acid neurochemistry of the vertebrate retina Prog. Retin. Eye Res. 18 1999 811 866
65. E.L. Fletcher Alterations in neurochemistry during retinal degeneration Microsc. Res. Tech. 50 2000 89 102
66. M. Liu, M.H. Kelley, P.S. Herson, and P.D. Hurn Neuroprotection of sex steroids Minerva Endocrinol. 35 2010 127 143
67. J. Nilsen, and R.D. Brinton Impact of progestins on estradiol potentiation of the glutamate calcium response Neuroreport 13 2002 825 830
68. P. Kaur, P.K. Jodhka, W.A. Underwood, C.A. Bowles, N.C. de Fiebre, C.M. de Fiebre, and M. Singh Progesterone increases brain-derived neuroptrophic factor expression and protects against glutamate toxicity in a mitogen-activated protein kinase- and phosphoinositide-3 kinase-dependent manner in cerebral cortical explants J. Neurosci. Res. 85 2007 2441 2449
69. J. Hwang, R.S. Duncan, C. Madry, M. Singh, and P. Koulen Progesterone potentiates calcium release through ip3receptor by an akt-mediated mechanism in hippocampal neurons Cell Calcium 45 2009 233 242
70. M.S. Ola, K. Hosoya, and K.F. LaNoue Regulation of glutamate metabolism by hydrocortisone and branched chain keto acids in cultured rat retinal Müller cells (TR-MUL) Neurochem. Int. 59 2011 656 663
71. R. Gorovits, N. Avidan, N. Avisar, I. Shaked, and L. Vardimon Glutamine synthetase protects against neuronal degeneration in injured retinal tissue Proc. Natl. Acad. Sci. U. S. A. 1997 7024 7029
72. L. Gu, H. Xu, F. Wang, G. Xu, D. Sinha, J. Wang, J.Y. Xu, H. Tian, F. Gao, W. Li, L. Lu, J. Zhang, and G.T. Xu Erythropoietin exerts a neuroprotective function against glutamate neurotoxicity in experimental diabetic retina Invest. Ophthalmol. Vis. Sci. 55 October 21 2014 8208 8222
73. L. Verdier, Y. Boirie, S. Van Drieesche, M. Mignon, R.J. Begue, and D. Meynial-Denis Do sex steroids regulate glutamine synthesis with age Am. J. Physiol. Endocrinol. Metab. 282 2002 E215 E221
74. M. Meyer, M.C. Gonzalez Deniselle, L.I. Garay, G.G. Monachelli, A. Lima, P. Roig, R. Guennoun, M. Schumacher, and A.F. De Nicola Stage dependent effects of progesterone on motoneurons and glial cells of wobbler mouse spinal cord degeneration Cell Mol. Neurobiol. 30 2010 123 135
75. J. Shen, X. Yang, A. Dong, R.M. Petters, Y.W. Peng, F. Wong, and P.A. Campochiaro Oxidative damage is a potential cause of cone cell death retinitis pigmentosa J. Cell Physiol. 203 2005 457 464
76. K. Komeima, B.S. Rogers, L. Lu, and P.A. Campochiaro Antioxidants reduce cone cell death in a model of retinitis pigmentosa Proc. Natl. Acad. Sci. U. S. A. 103 2006 11300 11305
77. M. Miranda, E. Arnal, S. Ahuja, R. Alvarez-Nölting, R. López-Pedrajas, P. Ekström, F. Bosch-Morell, T. van Veen, and F.J. Romero Antioxidants rescue photoreceptors in rd1 mice: relationship with thiol metabolism Free Radic. Biol. Med. 48 2010 216 222
78. D.Y. Yu, S.J. Cringle, E.N. Su, and P.K. Yu Intraretinal oxygen levels before and after photoreceptor loss in the RCS rat Invest. Ophthalmol. Vis. Sci. 41 2000 3999 4006
79. S. Usui, K. Komeima, S.Y. Lee, Y.J. Jo, S. Ueno, B.S. Rogers, Z. Wu, J. Shen, L. Lu, B.C. Oveson, P.S. Rabinovitch, and P.A. Campochiaro Increased expression of catalase and superoxide dismutase 2 reduces cone cell death in retinitis pigmentosa Mol. Ther. 17 2009 778 786
80. A.G. Hall The role of glutathione in the regulation of apoptosis Eur. J. Clin. Invest. 29 1999 238 245
81. T.L. Perry, D.V. Godin, and S. Hansen Parkinson's disease: a disorder due to nigral glutathione deficiency? Neurosci. Len. 33 1982 30510
82. C.D. Smith, J.M. Camey, P.E. Starke-Reed, C.N. Oliver, E.R. Stadtrnan, R.A. Floyd, and W.R. Markesberry Excess brain protein oxidation and enzyme dysfunction in normal ageing and in Alzheimer's disease Proc. Natl. Acad. Sci. 88 1991 10540 10543
83. E. Sotic, K.W. Lange, K. Jellinger, and P. Riederer Reduced and oxidized glutathione in the substantia nigra of patients with Parkinson's disease Neurosci. Len. 142 1992 128 130
84. S. Jiang, S.E. Moriarty-Craige, M. Orr, J. Cai, P. Sternberg Jr, and D.P. Jones Oxidant-induced apoptosis in human retinal pigment epithelial cells: dependence on extracellular redox state Invest. Ophthalmol. Vis. Sci. 46 2005 1054 1061
85. H. Hermann, and S.G. Moses Content and state of glutathione in the tissues of the eye J. Biol. Chem. 158 1945 33 45
86. D.V. Pow, and D.K. Crook Immunocytochemical evidence for the presence of high levels of reduced glutathione in radial glial cells and horizontal cells in the rabbit retina Neurosci. Lett. 193 1995 25 28
87. M. Schuette, and P. Werner Redistribution of glutathione in the ischemic rat retina Neurosci. Lett. 246 1998 53 56
88. E. Gouix, A. Buisson, A. Nieoullon, L. Kerkerian-Le Goff, J.S. Tauskela, N. Blondeau, and L. Had-Aissouni Oxygen glucose deprivation-induced astrocyte dysfunction provokes neuronal death through oxidative stress Pharmacol. Res. 87 2014 8 17
89. E. Gouix, A. Buisson, A. Nieoullon, L. Kerkerian-Le Goff, J.S. Tauskela, N. Blondeau, and L. Had-Aissouni Oxygen glucose deprivation-induced astrocyte dysfunction provokes neuronal death through oxidative stress Pharmacol. Res. 87 2014 8 17
90. Y.D. Hoang, B.N. Nakamura, and U. Luderer Follicle-stimulating hormone and estradiol interact to stimulate glutathione synthesis in rat ovarian follicles and granulosa cells Biol. Reprod. 81 2009 636 646
91. H. Yang, N. Magilnick, C. Lee, D. Kalmaz, X. Ou, J.Y. Chan, and S.C. Lu Nrf1 and Nrf2 regulate rat glutamate-cysteine ligase catalytic subunit transcription indirectly via NF-kappaB and AP-1 Mol. Cell Biol. 25 2005 5933 5946
92. M.M. Sanz, L.E. Johnson, S. Ahuja, P.A. Ekström, J. Romero, and T. van Veen Significant photoreceptor rescue by treatment with a combination of antioxidants in an animal model for retinal degeneration Neuroscience 145 2015 1120 1129