Impairment of intrinsically photosensitive retinal ganglion cells associated with late stages of retinal degeneration

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 7, 2013, Pages 4605-4618

  Esquiva, Gema ^a   Lax, Pedro ^a   Cuenca, Nicolás ^a  

^a UNIVERSITY OF ALICANTE   (Spain)

Author keywords

Immunoperoxidase; ipRGCs; Melanopsin; P23H rats; Retinitis pigmentosa

Indexed keywords

MELANOPSIN; PEROXIDASE;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL STRUCTURE; CONTROLLED STUDY; DENDRITE; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IMMUNOPEROXIDASE STAINING; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHOTOSENSITIVITY; PRIORITY JOURNAL; RAT; RETINA DEGENERATION; RETINA GANGLION CELL; RETINITIS PIGMENTOSA; SOMATIC CELL;

IMMUNOPEROXIDASE; IPRGCS; MELANOPSIN; P23H RATS; RETINITIS PIGMENTOSA;

AGING; ANALYSIS OF VARIANCE; ANIMALS; DISEASE MODELS, ANIMAL; IMMUNOHISTOCHEMISTRY; RATS; RATS, SPRAGUE-DAWLEY; RETINAL GANGLION CELLS; RETINITIS PIGMENTOSA; ROD OPSINS;

EID: 84880056034     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-12120     Document Type: Article

References (73)

1. Provencio I, Rodriguez IR, Jiang G, et al. A novel human opsin in the inner retina. J Neurosci. 2000;20:600-605.
2. Provencio I, Rollag MD, Castrucci AM. Photoreceptive net in the mammalian retina. This mesh of cells may explain how some blind mice can still tell day from night. Nature. 2002; 415:493.
3. Hattar S, Liao HW, Takao M, et al. Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science. 2002;295:1065-1070.
4. Hannibal J, Fahrenkrug J. Melanopsin: a novel photopigment involved in the photoentrainment of the brain's biological clock? Ann Med. 2002;34:401-407.
5. Berson DM, Dunn FA, Takao M. Phototransduction by retinal ganglion cells that set the circadian clock. Science. 2002;295: 1070-1073.
6. Baver SB, Pickard GE, Sollars PJ. Two types of melanopsin retinal ganglion cell differentially innervate the hypothalamic suprachiasmatic nucleus and the olivary pretectal nucleus. Eur J Neurosci. 2008;27:1763-1770.
7. Berson DM, Castrucci AM, Provencio I. Morphology and mosaics of melanopsin-expressing retinal ganglion cell types in mice. J Comp Neurol. 2010;518:2405-2422.
8. Hattar S, Kumar M, Park A, et al. Central projections of melanopsin-expressing retinal ganglion cells in the mouse. J Comp Neurol. 2006;497:326-349.
9. Hu C, Hill DD, Wong KY. Intrinsic physiological properties of the five types of mouse ganglion-cell photoreceptors. J Neurophysiol. 2013;109:1876-1879.
10. Schmidt TM, Chen SK, Hattar S. Intrinsically photosensitive retinal ganglion cells: many subtypes, diverse functions. Trends Neurosci. 2011;34:572-580.
11. Lucas RJ, Hattar S, Takao M, et al. Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science. 2003;299:245-247.
12. Belenky MA, Smeraski CA, Provencio I, et al. Melanopsin retinal ganglion cells receive bipolar and amacrine cell synapses. J Comp Neurol. 2003;460:380-393.
13. Rollag MD, Berson DM, Provencio I. Melanopsin, ganglion-cell photoreceptors, and mammalian photoentrainment. J Biol Rhythms. 2003;18:227-234.
14. Berson DM. Strange vision: ganglion cells as circadian photoreceptors. Trends Neurosci. 2003;26:314-320.
15. Panda S, Sato TK, Castrucci AM, et al. Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science. 2002;298:2213-2216.
16. Ruby NF, Brennan TJ, Xie X, et al. Role of melanopsin in circadian responses to light. Science. 2002;298:2211-2213.
17. Panda S, Provencio I, Tu DC, et al. Melanopsin is required for non-image-forming photic responses in blind mice. Science. 2003;301:525-527.
18. Gooley JJ, Lu J, Chou TC, Scammell TE, Saper CB. Melanopsin in cells of origin of the retinohypothalamic tract. Nat Neurosci. 2001;4:1165.
19. Galindo-Romero C, Jimenez-Lopez M, Garcia-Ayuso D, et al. Number and spatial distribution of intrinsically photosensitive retinal ganglion cells in the adult albino rat. Exp Eye Res. 2013; 108:84-93.
20. Hannibal J, Hindersson P, Knudsen SM, et al. The photopigment melanopsin is exclusively present in pituitary adenylate cyclase-activating polypeptide-containing retinal ganglion cells of the retinohypothalamic tract. J Neurosci. 2002;22:RC191.
21. Foster RG, Provencio I, Hudson D, et al. Circadian photoreception in the retinally degenerate mouse (rd/rd). J Comp Physiol A. 1991;169:39-50.
22. Provencio I, Wong S, Lederman AB, et al. Visual and circadian responses to light in aged retinally degenerate mice. Vision Res. 1994;34:1799-1806.
23. Dryja TP, McGee TL, Reichel E, et al. A point mutation of the rhodopsin gene in one form of retinitis pigmentosa. Nature. 1990;343:364-366.
24. Dryja TP, McEvoy JA, McGee TL, et al. Novel rhodopsin mutations Gly114Val and Gln184Pro in dominant retinitis pigmentosa. Invest Ophthalmol Vis Sci. 2000;41:3124-3127.
25. Machida S, Kondo M, Jamison JA, et al. P23H rhodopsin transgenic rat: correlation of retinal function with histopathology. Invest Ophthalmol Vis Sci. 2000;41:3200-3209.
26. Cuenca N, Pinilla I, Sauve Y, et al. Regressive and reactive changes in the connectivity patterns of rod and cone pathways of P23H transgenic rat retina. Neuroscience. 2004;127:301-317.
27. Pinilla I, Lund RD, Sauve Y. Enhanced cone dysfunction in rats homozygous for the P23H rhodopsin mutation. Neurosci Lett. 2005;382:16-21.
28. Fernandez-Sanchez L, Lax P, Esquiva G, et al. Safranal, a saffron constituent, attenuates retinal degeneration in P23H rats. PLoS ONE. 2012;7:e43074.
29. Fernandez-Sanchez L, Lax P, Isiegas C, et al. Proinsulin slows retinal degeneration and vision loss in the P23H rat model of retinitis pigmentosa. Hum Gene Ther. 2012;23:1290-1300.
30. Fernandez-Sanchez L, Lax P, Pinilla I, et al. Tauroursodeoxycholic acid prevents retinal degeneration in transgenic P23H rats. Invest Ophthalmol Vis Sci. 2011;52:4998-5008.
31. Jones BW, Watt CB, Frederick JM, et al. Retinal remodeling triggered by photoreceptor degenerations. J Comp Neurol. 2003;464:1-16.
32. Kolomiets B, Dubus E, Simonutti M, et al. Late histological and functional changes in the P23H rat retina after photoreceptor loss. Neurobiol Dis. 2010;38:47-58.
33. Garcia-Ayuso D, Salinas-Navarro M, Agudo M, et al. Retinal ganglion cell numbers and delayed retinal ganglion cell death in the P23H rat retina. Exp Eye Res. 2010;91:800-810.
34. Lax P, Otalora BB, Esquiva G, et al. Circadian dysfunction in P23H rhodopsin transgenic rats: effects of exogenous melatonin. J Pineal Res. 2011;50:183-191.
35. Kardon R, Anderson SC, Damarjian TG, et al. Chromatic pupillometry in patients with retinitis pigmentosa. Ophthalmology. 2011;118:376-381.
36. Moldrup ML, Georg B, Falktoft B, et al. Light induces Fos expression via extracellular signal-regulated kinases 1/2 in melanopsin-expressing PC12 cells. J Neurochem. 2010;112: 797-806.
37. Hannibal J, Georg B, Fahrenkrug J. Melanopsin changes in neonatal albino rat independent of rods and cones. Neuroreport. 2007;18:81-85.
38. Hannibal J, Georg B, Fahrenkrug J. Differential expression of melanopsin mRNA and protein in Brown Norwegian rats. Exp Eye Res. 2013;106:55-63.
39. Cuenca N, De Juan J, Kolb H. Substance P-immunoreactive neurons in the human retina. J Comp Neurol. 1995;356:491-504.
40. Cuenca N, Kolb H. Circuitry and role of substance Pimmunoreactive neurons in the primate retina. J Comp Neurol. 1998;393:439-456.
41. Langhammer CG, Previtera ML, Sweet ES, et al. Automated Sholl analysis of digitized neuronal morphology at multiple scales: whole cell Sholl analysis versus Sholl analysis of arbor subregions. Cytometry A. 2010;77:1160-1168.
42. Sholl DA. Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat. 1953;87:387-406.
43. Viney TJ, Balint K, Hillier D, et al. Local retinal circuits of melanopsin-containing ganglion cells identified by transsynaptic viral tracing. Curr Biol. 2007;17:981-988.
44. Schmidt TM, Kofuji P. Functional and morphological differences among intrinsically photosensitive retinal ganglion cells. J Neurosci. 2009;29:476-482.
45. Dacey DM, Liao HW, Peterson BB, et al. Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature. 2005;433:749-754.
46. Jusuf PR, Lee SC, Hannibal J, et al. Characterization and synaptic connectivity of melanopsin-containing ganglion cells in the primate retina. Eur J Neurosci. 2007;26:2906-2921.
47. Engelund A, Fahrenkrug J, Harrison A, et al. Vesicular glutamate transporter 2 (VGLUT2) is co-stored with PACAP in projections from the rat melanopsin-containing retinal ganglion cells. Cell Tissue Res. 2010;340:243-255.
48. Schmidt TM, Taniguchi K, Kofuji P. Intrinsic and extrinsic light responses in melanopsin-expressing ganglion cells during mouse development. J Neurophysiol. 2008;100:371-384.
49. Pires SS, Hughes S, Turton M, et al. Differential expression of two distinct functional isoforms of melanopsin (Opn4) in the mammalian retina. J Neurosci. 2009;29:12332-12342.
50. Spear PD. Neural bases of visual deficits during aging. Vision Res. 1993;33:2589-2609.
51. Katz ML, Robison WG Jr. Evidence of cell loss from the rat retina during senescence. Exp Eye Res. 1986;42:293-304.
52. Weisse I. Changes in the aging rat retina. Ophthalmic Res. 1995;27(suppl 1):154-163.
53. Aggarwal P, Nag TC, Wadhwa S. Age-related decrease in rod bipolar cell density of the human retina: an immunohistochemical study. J Biosci. 2007;32:293-298.
54. Samuel MA, Zhang Y, Meister M, et al. Age-related alterations in neurons of the mouse retina. J Neurosci. 2011;31:16033-16044.
55. Turek FW, Penev P, Zhang Y, et al. Effects of age on the circadian system. Neurosci Biobehav Rev. 1995;19:53-58.
56. Zhang Y, Kornhauser JM, Zee PC, et al. Effects of aging on light-induced phase-shifting of circadian behavioral rhythms, fos expression and CREB phosphorylation in the hamster suprachiasmatic nucleus. Neuroscience. 1996;70:951-961.
57. Herbst K, Sander B, Lund-Andersen H, et al. Intrinsically photosensitive retinal ganglion cell function in relation to age: a pupillometric study in humans with special reference to the age-related optic properties of the lens. BMC Ophthalmol. 2012;12:4.
58. Gonzalez-Menendez I, Contreras F, Cernuda-Cernuda R, et al. No loss of melanopsin-expressing ganglion cells detected during postnatal development of the mouse retina. Histol Histopathol. 2010;25:73-82.
59. Kim CB, Tom BW, Spear PD. Effects of aging on the densities, numbers, and sizes of retinal ganglion cells in rhesus monkey. Neurobiol Aging. 1996;17:431-438.
60. Vugler AA, Semo M, Joseph A, et al. Survival and remodeling of melanopsin cells during retinal dystrophy. Vis Neurosci. 2008; 25:125-138.
61. Semo M, Lupi D, Peirson SN, et al. Light-induced c-fos in melanopsin retinal ganglion cells of young and aged rodless/coneless (rd/rd cl) mice. Eur J Neurosci. 2003;18:3007-3017.
62. Ionescu D, Driver HS, Heon E, et al. Sleep and daytime sleepiness in retinitis pigmentosa patients. J Sleep Res. 2001; 10:329-335.
63. Gordo MA, Recio J, Sanchez-Barcelo EJ. Decreased sleep quality in patients suffering from retinitis pigmentosa. J Sleep Res. 2001;10:159-164.
64. Cugini P, Cruciani F, De Rosa R, et al. Alterations of blood pressure and heart rate circadian rhythmic structure in nonblind patients affected by retinitis pigmentosa. J Hum Hypertens. 2001;15:577-581.
65. Robinson GA, Madison RD. Axotomized mouse retinal ganglion cells containing melanopsin show enhanced survival, but not enhanced axon regrowth into a peripheral nerve graft. Vision Res. 2004;44:2667-2674.
66. Li RS, Chen BY, Tay DK, et al. Melanopsin-expressing retinal ganglion cells are more injury-resistant in a chronic ocular hypertension model. Invest Ophthalmol Vis Sci. 2006;47: 2951-2958.
67. Li SY, Yau SY, Chen BY, et al. Enhanced survival of melanopsinexpressing retinal ganglion cells after injury is associated with the PI3 K/Akt pathway. Cell Mol Neurobiol. 2008;28:1095-1107.
68. Jones BW, Marc RE. Retinal remodeling during retinal degeneration. Exp Eye Res. 2005;81:123-137.
69. Marc RE, Jones BW, Watt CB, et al. Neural remodeling in retinal degeneration. Prog Retin Eye Res. 2003;22:607-655.
70. Lopez-del Hoyo N, Fazioli L, Lopez-Begines S, et al. Overexpression of guanylate cyclase activating protein 2 in rod photoreceptors in vivo leads to morphological changes at the synaptic ribbon. PLoS ONE. 2012;7:e42994.
71. Dorfman AL, Cuenca N, Pinilla I, et al. Immunohistochemical evidence of synaptic retraction, cytoarchitectural remodeling, and cell death in the inner retina of the rat model of oygeninduced retinopathy (OIR). Invest Ophthalmol Vis Sci. 2011; 52:1693-1708.
72. Marc RE, Jones BW, Anderson JR, et al. Neural reprogramming in retinal degeneration. Invest Ophthalmol Vis Sci. 2007;48: 3364-3371.
73. Phillips MJ, Otteson DC, Sherry DM. Progression of neuronal and synaptic remodeling in the rd10 mouse model of retinitis pigmentosa. J Comp Neurol. 2010;518:2071-2089.