Top

Published in:

01-07-2012 | Review

Retinal remodeling

Authors: B. W. Jones, M. Kondo, H. Terasaki, Y. Lin, M. McCall, R. E. Marc

Published in: Japanese Journal of Ophthalmology | Issue 4/2012

Abstract

Retinal photoreceptor degeneration takes many forms. Mutations in rhodopsin genes or disorders of the retinal pigment epithelium, defects in the adenosine triphosphate binding cassette transporter, ABCR gene defects, receptor tyrosine kinase defects, ciliopathies and transport defects, defects in both transducin and arrestin, defects in rod cyclic guanosine 3′,5′-monophosphate phosphodiesterase, peripherin defects, defects in metabotropic glutamate receptors, synthetic enzymatic defects, defects in genes associated with signaling, and many more can all result in retinal degenerative disease like retinitis pigmentosa (RP) or RP-like disorders. Age-related macular degeneration (AMD) and AMD-like disorders are possibly due to a constellation of potential gene targets and gene/gene interactions, while other defects result in diabetic retinopathy or glaucoma. However, all of these insults as well as traumatic insults to the retina result in retinal remodeling. Retinal remodeling is a universal finding subsequent to retinal degenerative disease that results in deafferentation of the neural retina from photoreceptor input as downstream neuronal elements respond to loss of input with negative plasticity. This negative plasticity is not passive in the face of photoreceptor degeneration, with a phased revision of retinal structure and function found at the molecular, synaptic, cell, and tissue levels involving all cell classes in the retina, including neurons and glia. Retinal remodeling has direct implications for the rescue of vision loss through bionic or biological approaches, as circuit revision in the retina corrupts any potential surrogate photoreceptor input to a remnant neural retina. However, there are a number of potential opportunities for intervention that are revealed through the study of retinal remodeling, including therapies that are designed to slow down photoreceptor loss, interventions that are designed to limit or arrest remodeling events, and optogenetic approaches that target appropriate classes of neurons in the remnant neural retina.

Aleman TS, Cideciyan AV, Sumaroka A, Schwartz SB, Roman AJ, Windsor EAM, et al. Inner retinal abnormalities in X-linked retinitis pigmentosa with RPGR mutations. Invest Ophthalmol Vis Sci. 2007;48:4759–65.PubMedCrossRef

Cuenca N, Pinilla I, Sauvé Y, Lu B, Wang S, Lund RD. Regressive and reactive changes in the connectivity patterns of rod and cone pathways of P23H transgenic rat retina. Neuroscience. 2004;127:301–17.PubMedCrossRef

Cuenca N, Pinilla I, Sauvé Y, Lund RD. Early changes in synaptic connectivity following progressive photoreceptor degeneration in RCS rats. Eur J Neurosci. 2005;22:1057–72.PubMedCrossRef

de Raad S, Szczesny PJ, Munz K, Remé CE. Light damage in the rat retina: glial fibrillary acidic protein accumulates in Müller cells in correlation with photoreceptor damage. Ophthalmic Res. 1996;28:99–107.PubMedCrossRef

Fariss RN, Li ZY, Milam AH. Abnormalities in rod photoreceptors, amacrine cells, and horizontal cells in human retinas with retinitis pigmentosa. Am J Ophthalmol. 2000;129:215–23.PubMedCrossRef

Fletcher EL, Kalloniatis M. Neurochemical architecture of the normal and degenerating rat retina. J Comp Neurol. 1996;376:343–60.PubMedCrossRef

Jones BW, Marc RE. Retinal remodeling during retinal degeneration. Exp Eye Res. 2005;81:123–37.PubMedCrossRef

Jones BW, Marc RE, Watt CB, Vaughan DK, Organisciak DT. Neural plasticity revealed by light-induced photoreceptor lesions. Adv Exp Med Biol. 2006;572:405–10.PubMedCrossRef

Jones BW, Watt CB, Marc RE. Retinal remodelling. Clin Exp Optom. 2005;88:282–91.PubMedCrossRef

10.

Marc RE, Jones BW. Molecular phenotyping of retinal ganglion cells. J Neurosci. 2002;22:413–27.PubMed

11.

Marc RE, Jones BW. Retinal remodeling in inherited photoreceptor degenerations. Mol Neurobiol. 2003;28:139–47.PubMedCrossRef

12.

Marc RE, Jones BW, Watt CB, Strettoi E. Neural remodeling in retinal degeneration. Prog Retin Eye Res. 2003;22:607–55.PubMedCrossRef

13.

Marc RE, Jones BW, Vazquez-Chona F, Vaughan DK, Organisciak DT. Extreme retinal remodeling triggered by light damage: implications for age related macular degeneration. Mol Vis. 2008;14:782–805.PubMed

14.

Kolb H, Gouras P. Electron microscopic observations of human retinitis pigmentosa, dominantly inherited. Invest Ophthalmol. 1974;13:487–98.PubMed

15.

Li ZY, Kljavin IJ, Milam AH. Rod photoreceptor neurite sprouting in retinitis pigmentosa. J Neurosci. 1995;15:5429–38.PubMed

16.

Machida S, Kondo M, Jamison JA, Khan NW, Kononen LT, Sugawara T, et al. P23H rhodopsin transgenic rat: correlation of retinal function with histopathology. Invest Ophthalmol Vis Sci. 2000;41:3200–9.PubMed

17.

Pu M, Xu L, Zhang H. Visual response properties of retinal ganglion cells in the Royal College of Surgeons dystrophic rat. Invest Ophthalmol Vis Sci. 2006;47:3579–85.

18.

Specht D, Tom Dieck S, Ammermüller J, Regus-Leidig H, Gundelfinger ED, Brandstätter JH. Structural and functional remodeling in the retina of a mouse with a photoreceptor synaptopathy: plasticity in the rod and degeneration in the cone system. Eur J Neurosci. 2007;26:2506–15.PubMedCrossRef

19.

Stasheff SF. Emergence of sustained spontaneous hyperactivity and temporary preservation of OFF responses in ganglion cells of the retinal degeneration (rd1) mouse. J Neurophysiol. 2008;99:1408–21.PubMedCrossRef

20.

Strettoi E, Pignatelli V. Modifications of retinal neurons in a mouse model of retinitis pigmentosa. Proc Natl Acad Sci USA. 2000;97:11020–5.PubMedCrossRef

21.

Strettoi E, Pignatelli V, Rossi C, Porciatti V, Falsini B. Remodeling of second-order neurons in the retina of rd/rd mutant mice. Vision Res. 2003;43:867–77.PubMedCrossRef

22.

Strettoi E, Porciatti V, Falsini B, Pignatelli V, Rossi C. Morphological and functional abnormalities in the inner retina of the rd/rd mouse. J Neurosci. 2002;22:5492–504.PubMed

23.

Sullivan RK, Woldemussie E, Pow DV. Dendritic and synaptic plasticity of neurons in the human age-related macular degeneration retina. Invest Ophthalmol Vis Sci. 2007;48:2782–9.PubMedCrossRef

24.

Jones BW, Watt CB, Frederick JM, Baehr W, Chen CK, Levine EM, et al. Retinal remodeling triggered by photoreceptor degenerations. J Comp Neurol. 2003;464:1–16.PubMedCrossRef

25.

Sullivan R, Penfold P, Pow DV. Neuronal migration and glial remodeling in degenerating retinas of aged rats and in nonneovascular AMD. Invest Ophthalmol Vis Sci. 2003;44:856–65.PubMedCrossRef

26.

Marc RE, Jones BW, Anderson JR, Kinard K, Marshak DW, Wilson JH, et al. Neural reprogramming in retinal degeneration. Invest Ophthalmol Vis Sci. 2007;48:3364–71.PubMedCrossRef

27.

Baehr W, Frederick JM. Naturally occurring animal models with outer retina phenotypes. Vision Res. 2009;49:2636–52.PubMedCrossRef

28.

Chang CJ, Lai WW, Edward DP, Tso MOM. Apoptotic photoreceptor cell death after traumatic retinal detachment in humans. Arch Ophthalmol. 1995;113:880–6.PubMedCrossRef

29.

Frederick JM, Krasnoperova NV, Hoffmann K, Church-Kopish J, Rüther K, Howes K, et al. Mutant rhodopsin transgene expression on a null background. Invest Ophthalmol Vis Sci. 2001;42:826–33.PubMed

30.

Humphries MM, Rancourt D, Farrar GJ, Kenna P, Hazel M, Bush RA, et al. Retinopathy induced in mice by targeted disruption of the rhodopsin gene. Nat Genet. 1997;15:216–9.PubMedCrossRef

31.

Aguirre GD, Baldwin V, Pearce-Kelling S, Narfström K, Ray K, Acland GM. Congenital stationary night blindness in the dog: common mutation in the RPE65 gene indicates founder effect. Mol Vis. 1998;4:23.PubMed

32.

Gu SM, Thompson DA, Srikumari CR, Lorenz B, Finckh U, Nicoletti A, et al. Mutations in RPE65 cause autosomal recessive childhood-onset severe retinal dystrophy. Nat Genet. 1997;17:194–7.PubMedCrossRef

33.

Morimura H, Fishman GA, Grover SA, Fulton AB, Berson EL, Dryja TP. Mutations in the RPE65 gene in patients with autosomal recessive retinitis pigmentosa or Leber congenital amaurosis. Proc Natl Acad Sci USA. 1998;95:3088–93.PubMedCrossRef

34.

Allikmets R, Singh N, Sun H, Shroyer NF, Hutchinson A, Chidambaram A, et al. A photoreceptor cell-specific ATP-binding transporter gene (ABCR) is mutated in recessive Stargardt macular dystrophy. Nat Genet. 1997;15:236–46.PubMedCrossRef

35.

Allikmets R. Simple and complex ABCR: genetic predisposition to retinal disease. Am J Hum Genet. 2000;67:793–9.PubMedCrossRef

36.

Allikmets R, Shroyer NF, Singh N, Seddon JM, Lewis RA, Bernstein PS, et al. Mutation of the Stargardt disease gene (ABCR) in age-related macular degeneration. Science. 1997;277:1805–7.PubMedCrossRef

37.

Cremers FP, van de Pol DJ, van Driel M, den Hollander AI, van Haren FJ, Knoers NV, et al. Autosomal recessive retinitis pigmentosa and cone-rod dystrophy caused by splice site mutations in the Stargardt’s disease gene ABCR. Hum Mol Genet. 1998;7:355–62.PubMedCrossRef

38.

Molday LL, Rabin AR, Molday RS. ABCR expression in foveal cone photoreceptors and its role in Stargardt macular dystrophy. Nat Genet. 2000;25:257–8.PubMedCrossRef

39.

D’Cruz PM, Yasumura D, Weir J, Matthes MT, Abderrahim H, LaVail MM, et al. Mutation of the receptor tyrosine kinase gene Mertk in the retinal dystrophic RCS rat. Hum Mol Genet. 2000;9:645–51.PubMedCrossRef

40.

Duncan JL, Yang H, Vollrath D, Yasumura D, Matthes MT, Trautmann N, et al. Inherited retinal dystrophy in Mer knockout mice. Adv Exp Med Biol. 2003;533:165–72.PubMedCrossRef

41.

Li JB, Gerdes JM, Haycraft CJ, Fan Y, Teslovich TM, May-Simera H, et al. Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell. 2004;117:541–52.PubMedCrossRef

42.

Yen HJ, Tayeh MK, Mullins RF, Stone EM, Sheffield VC, Slusarski DC. Bardet–Biedl syndrome genes are important in retrograde intracellular trafficking and Kupffer’s vesicle cilia function. Hum Mol Genet. 2006;15:667–77.PubMedCrossRef

43.

Dryja TP, Berson EL, Rao VR, Oprian DD. Heterozygous missense mutation in the rhodopsin gene as a cause of congenital stationary night blindness. Nat Genet. 1993;4:280–3.PubMedCrossRef

44.

Zeitz C, Gross AK, Leifert D, Kloeckener-Gruissem B, McAlear SD, Lemke J, et al. Identification and functional characterization of a novel rhodopsin mutation associated with autosomal dominant CSNB. Invest Ophthalmol Vis Sci. 2008;49:4105–14.PubMedCrossRef

45.

Sommer ME, Farrens DL. Arrestin can act as a regulator of rhodopsin photochemistry. Vision Res. 2006;46:4532–46.PubMedCrossRef

46.

Sommer ME, Smith WC, Farrens DL. Dynamics of arrestin–rhodopsin interactions: acidic phospholipids enable binding of arrestin to purified rhodopsin in detergent. J Biol Chem. 2006;281:9407–17.PubMedCrossRef

47.

Huang SH, Pittler SJ, Huang X, Oliveira L, Berson EL, Dryja TP. Autosomal recessive retinitis pigmentosa caused by mutations in the alpha subunit of rod cGMP phosphodiesterase. Nat Genet. 1995;11:468–71.PubMedCrossRef

48.

McLaughlin ME, Ehrhart TL, Berson EL, Dryja TP. Mutation spectrum of the gene encoding the beta subunit of rod phosphodiesterase among patients with autosomal recessive retinitis pigmentosa. Proc Natl Acad Sci USA. 1995;92:3249–53.PubMedCrossRef

49.

McLaughlin ME, Sandberg MA, Berson EL, Dryja TP. Recessive mutations in the gene encoding the beta-subunit of rod phosphodiesterase in patients with retinitis pigmentosa. Nat Genet. 1993;4:130–4.PubMedCrossRef

50.

Clarke G, Goldberg AF, Vidgen D, Collins L, Ploder L, Schwarz L, et al. Rom-1 is required for rod photoreceptor viability and the regulation of disk morphogenesis. Nat Genet. 2000;25:67–73.PubMedCrossRef

51.

Dryja TP, McGee TL, Berson EL, Fishman GA, Sandberg MA, Alexander KR, et al. Night blindness and abnormal cone electroretinogram ON responses in patients with mutations in the GRM6 gene encoding mGluR6. Proc Natl Acad Sci USA. 2005;102:4884–9.PubMedCrossRef

52.

Zeitz C, van Genderen M, Neidhardt J, Luhmann UF, Hoeben F, Forster U, et al. Mutations in GRM6 cause autosomal recessive congenital stationary night blindness with a distinctive scotopic 15-Hz flicker electroretinogram. Invest Ophthalmol Vis Sci. 2005;46:4328–35.PubMedCrossRef

53.

Vasireddy V, Uchida Y, Salem N Jr, Kim SY, Mandal MNA, Reddy GB, et al. Loss of functional ELOVL4 depletes very long-chain fatty acids (≥C28) and the unique ω-O-acylceramides in skin leading to neonatal death. Hum Mol Genet. 2007;16:471–82.PubMedCrossRef

54.

Zhang K, Kniazeva M, Han M, Li W, Yu Z, Yang Z, et al. A 5-bp deletion in ELOVL4 is associated with two related forms of autosomal dominant macular dystrophy. Nat Genet. 2001;27:89–93.PubMed

55.

Chen CK, Burns ME, He W, Wensel TG, Baylor DA, Simon MI. Slowed recovery of rod photoresponse in mice lacking the GTPase accelerating protein RGS9-1. Nature. 2000;403:557–60.PubMedCrossRef

56.

Hu G, Wensel TG. R9AP, a membrane anchor for the photoreceptor GTPase accelerating protein, RGS9-1. Proc Natl Acad Sci USA. 2002;99:9755–60.PubMedCrossRef

57.

Hu G, Zhang Z, Wensel TG. Activation of RGS9-1GTPase acceleration by its membrane anchor, R9AP. J Biol Chem. 2003;278:14550–4.PubMedCrossRef

58.

Wensel TG. Signal transducing membrane complexes of photoreceptor outer segments. Vision Res. 2008;48:2052–61.PubMedCrossRef

59.

Boon CJF, Klevering BJ, Hoyng CB, Zonneveld-Vrieling MN, Nabuurs SB, Blokland E, et al. Basal laminar drusen caused by compound heterozygous variants in the CFH gene. Am J Hum Genet. 2008;82:516–23.PubMedCrossRef

60.

Cameron DJ, Yang Z, Gibbs D, Chen H, Kaminoh Y, Jorgensen A, et al. HTRA1 variant confers similar risks to geographic atrophy and neovascular age-related macular degeneration. Cell Cycle. 2007;6:1122–5.PubMedCrossRef

61.

Chen H, Yang Z, Gibbs D, Yang X, Hau V, Zhao P, et al. Association of HTRA1 polymorphism and bilaterality in advanced age-related macular degeneration. Vision Res. 2008;48:690–4.PubMedCrossRef

62.

Dewan A, Liu M, Hartman S, Zhang SS, Liu DT, Zhao C, et al. HTRA1 promoter polymorphism in wet age-related macular degeneration. Science. 2006;314:989–92.PubMedCrossRef

63.

Edwards AO, Ritter R III, Abel KJ, Manning A, Panhuysen C, Farrer LA. Complement factor H polymorphism and age-related macular degeneration. Science. 2005;308:421–4.PubMedCrossRef

64.

Gold B, Merriam JE, Zernant J, Hancox LS, Taiber AJ, Gehrs K, et al. Variation in factor B (BF) and complement component 2 (C2) genes is associated with age-related macular degeneration. Nat Genet. 2006;38:458–62.PubMedCrossRef

65.

Hageman GS, Anderson DH, Johnson LV, Hancox LS, Taiber AJ, Hardisty LI, et al. A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration. Proc Natl Acad Sci USA. 2005;102:7227–32.PubMedCrossRef

66.

Jakobsdottir J, Conley YP, Weeks DE, Mah TS, Ferrell RE, Gorin MB. Susceptibility genes for age-related maculopathy on chromosome 10q26. Am J Hum Genet. 2005;77:389–407.PubMedCrossRef

67.

Kaplan J, Gerber S, Larget-Piet D, Rozet JM, Dollfus H, Dufier JL, et al. A gene for Stargardt’s disease (fundus flavimaculatus) maps to the short arm of chromosome 1. Nat Genet. 1993;5:308–11.PubMedCrossRef

68.

Maller JB, Fagerness JA, Reynolds RC, Neale BM, Daly MJ, Seddon JM. Variation in complement factor 3 is associated with risk of age-related macular degeneration. Nat Genet. 2007;39:1200–1.PubMedCrossRef

69.

Stone EM, Braun TA, Russell SR, Kuehn MH, Lotery AJ, Moore PA, et al. Missense variations in the fibulin 5 gene and age-related macular degeneration. N Engl J Med. 2004;351:346–53.PubMedCrossRef

70.

Yates JRW, Sepp T, Matharu BK, Khan JC, Thurlby DA, Shahid H, et al. Complement C3 variant and the risk of age-related macular degeneration. N Engl J Med. 2007;357:553–61.PubMedCrossRef

71.

Phipps JA, Yee P, Fletcher EL, Vingrys AJ. Rod photoreceptor dysfunction in diabetes: activation, deactivation, and dark adaptation. Invest Ophthalmol Vis Sci. 2006;47:3187–94.PubMedCrossRef

72.

Choi SS, Zawadzki RJ, Lim MC, Brandt JD, Keltner JL, Doble N, et al. Evidence of outer retinal changes in glaucoma patients as revealed by ultrahigh-resolution in vivo retinal imaging. Br J Ophthalmol. 2011;95:131–41.PubMedCrossRef

73.

Milam AH, Li ZY, Fariss RN. Histopathology of the human retina in retinitis pigmentosa. Prog Retin Eye Res. 1998;17:175–205.PubMedCrossRef

74.

Jones BW, Kondo M, Terasaki H, Watt CB, Rapp K, Anderson J, et al. Retinal remodeling in the Tg p347l rabbit, a large-eye model of retinal degeneration. J Comp Neurol. 2011;519:2713–33.PubMedCrossRef

75.

Varela C, Igartua I, De la Rosa EJ, De la Villa P. Functional modifications in rod bipolar cells in a mouse model of retinitis pigmentosa. Vision Res. 2003;43:879–85.PubMedCrossRef

76.

Chua J, Fletcher EL, Kalloniatis M. Functional remodeling of glutamate receptors by inner retinal neurons occurs from an early stage of retinal degeneration. J Comp Neurol. 2009;514:473–91.PubMedCrossRef

77.

Peng YW, Hao Y, Petters RM, Wong F. Ectopic synaptogenesis in the mammalian retina caused by rod photoreceptor-specific mutations. Nat Neurosci. 2000;3:1121–7.PubMedCrossRef

78.

Park SJ, Kim IB, Choi KR, Moon JI, Oh SJ, Chung JW, et al. Reorganization of horizontal cell processes in the developing FVB/N mouse retina. Cell Tissue Res. 2001;306:341–6.PubMedCrossRef

79.

Marc RE, Jones BW, Watt CB. Retinal remodeling: circuitry revisions triggered by photoreceptor degeneration. In: Pinaud R, Tremere L, De Weerd P, editors. Plasticity in the visual system: from genes to circuits. New York: Springer; 2006. p. 33–54.

80.

Li ZY, Possin DE, Milam AH. Histopathology of bone spicule pigmentation in retinitis pigmentosa. Ophthalmology. 1995;102:805–16.PubMed

81.

Spraul CW, Lang GE, Grossniklaus HE, Lang GK. Histologic and morphometric analysis of the choroid, Bruch’s membrane, and retinal pigment epithelium in postmortem eyes with age-related macular degeneration and histologic examination of surgically excised choroidal neovascular membranes. Surv Ophthalmol. 1999;44(Suppl 1):S10–32.PubMedCrossRef

82.

Carter-Dawson LD, LaVail MM, Sidman RL. Differential effect of the rd mutation on rods and cones in the mouse retina. Invest Ophthalmol Vis Sci. 1978;17:489–98.PubMed

83.

Margolis DJ, Detwiler PB. Cellular origin of spontaneous ganglion cell spike activity in animal models of retinitis pigmentosa. J Ophthalmol. 2011. doi:10.1155/2011/507037.PubMed

84.

Sekirnjak C, Hulse C, Jepson LH, Hottowy P, Sher A, Dabrowski W, et al. Loss of responses to visual but not electrical stimulation in ganglion cells of rats with severe photoreceptor degeneration. J Neurophysiol. 2009;102:3260–9.PubMedCrossRef

85.

Lewis GP, Linberg KA, Fisher SK. Neurite outgrowth from bipolar and horizontal cells after experimental retinal detachment. Invest Ophthalmol Vis Sci. 1998;39:424–34.PubMed

86.

Linberg KA, Lewis GP, Matsumoto B, Fisher SK. Immunocytochemical evidence that rod-connected horizontal cell axon terminals remodel in response to experimental retinal detachment in the cat. Mol Vis. 2006;12:1674–86.PubMed

87.

Wong RO, Herrmann K, Shatz CJ. Remodeling of retinal ganglion cell dendrites in the absence of action potential activity. J Neurobiol. 1991;22:685–97.PubMedCrossRef

88.

Beltran WA, Hammond P, Acland GM, Aguirre GD. A frameshift mutation in RPGR exon ORF15 causes photoreceptor degeneration and inner retina remodeling in a model of X-linked retinitis pigmentosa. Invest Ophthalmol Vis Sci. 2006;47:1669–81.PubMedCrossRef

89.

Ray A, Sun GJ, Chan L, Grzywacz NM, Weiland J, Lee EJ. Morphological alterations in retinal neurons in the S334ter-line3 transgenic rat. Cell Tissue Res. 2010;339:481–91.PubMedCrossRef

90.

Iandiev I, Uckermann O, Pannicke T, Wurm A, Tenckhoff S, Pietsch UC, et al. Glial cell reactivity in a porcine model of retinal detachment. Invest Ophthalmol Vis Sci. 2006;47:2161–71.PubMedCrossRef

91.

Ross JW, Fernandez de Castro JP, Zhao J, Samuel M, Walters E, Rios C, et al. Generation of an inbred miniature pig model of retinitis pigmentosa. Invest Ophthalmol Vis Sci. 2012;53:501–7.PubMedCrossRef

92.

Anderson JR, Bones JW, Watt CB, Shaw MV, Yang JH, Demill D, et al. Exploring the retinal connectome. Mol Vis. 2011;17:355–79.PubMed

93.

Cuenca N, Pinilla I, Fernández-Sánchez L, Salinas-Navarro M, Alarcón-Martínez L, Avilés-Trigueros M, et al. Changes in the inner and outer retinal layers after acute increase of the intraocular pressure in adult albino Swiss mice. Exp Eye Res. 2010;91:273–85.PubMedCrossRef

94.

Yefimova MG, Messaddeq N, Karam A, Jacquard C, Weber C, Jonet L, et al. Polyglutamine toxicity induces rod photoreceptor division, morphological transformation or death in spinocerebellar ataxia 7 mouse retina. Neurobiol Dis. 2010;40:311–24.PubMedCrossRef

95.

Firth SI, Feller MB. Dissociated GABAergic retinal interneurons exhibit spontaneous increases in intracellular calcium. Vis Neurosci. 2006;23:807–14.PubMedCrossRef

96.

Voigt T, Wassle H. Dopaminergic innervation of A II amacrine cells in mammalian retina. J Neurosci. 1987;7:4115–28.PubMed

97.

Kolb H, Cuenca N, Dekorver L. Postembedding immunocytochemistry for GABA and glycine reveals the synaptic relationships of the dopaminergic amacrine cell of the cat retina. J Comp Neurol. 1991;310:267–84.PubMedCrossRef

98.

Feigenspan A, Gustincich S, Bean BP, Raviola E. Spontaneous activity of solitary dopaminergic cells of the retina. J Neurosci. 1998;18:6776–89.PubMed

99.

Jones BW, Marc RE, Watt CB. Dopaminergic amacrine and interplexiform cells exhibit glutamatergic signatures. Invest Ophthalmol Vis Sci. 2004;45:E (abstract 5435).

100.

VanLeeuwen JE, Petzinger GM, Walsh JP, Akopian GK, Vuckovic M, Jakowec MW. Altered AMPA receptor expression with treadmill exercise in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned mouse model of basal ganglia injury. J Neurosci Res. 2010;88:650–68.PubMed

101.

Kim M, Carman CV, Springer TA. Bidirectional transmembrane signaling by cytoplasmic domain separation in integrins. Science. 2003;301:1720–5.PubMedCrossRef

102.

Shimaoka M, Takagi J, Springer TA. Conformational regulation of integrin structure and function. Annu Rev Biophys Biomol Struct. 2002;31:485–516.PubMedCrossRef

103.

Cukierman E, Pankov R, Stevens DR, Yamada KM. Taking cell-matrix adhesions to the third dimension. Science. 2001;294:1708–12.PubMedCrossRef

104.

Kremer H, van Wijk E, Märker T, Wolfrum U, Roepman R. Usher syndrome: molecular links of pathogenesis, proteins and pathways. Hum Mol Genet. 2006;15(Spec No 2):R262–70.

105.

Lin Y, Jones BW, Liu A, Tucker JF, Rapp K, Luo L, et al. Retinoid receptors trigger neuritogenesis in retinal degenerations. FASEB J. 2011;36:81–92.

106.

Lin Y, Jones BW, Rapp K, Shaw MV, Yang J-H, Watt CB, et al. Roles of retinoic acid signaling in neuritogenesis during light-induced retinal degeneration. ARVO Meeting Abstracts. 2010;51:5592.

107.

Lin Y, Jones BW, Rapp K, Shaw MV, Yang J-H, Watt CB, et al. CaMKII signaling is contributive to neuritogenesis in light-induced retinal degeneration. ARVO Meeting Abstracts. 2011;52:1846.

108.

Marc RE, Liu W. Fundamental GABAergic amacrine cell circuitries in the retina: nested feedback, concatenated inhibition, and axosomatic synapses. J Comp Neurol. 2000;425:560–82.PubMedCrossRef

109.

Anderson JR, Jones BW, Yang J-H, Shaw MV, Watt CB, Koshevoy P, et al. A computational framework for ultrastructural mapping of neural circuitry. PLoS Biol. 2009;7:e1000074.PubMedCrossRef

110.

Kondo M, Sakai T, Komeima K, Kurimoto Y, Ueno S, Nishizawa Y, et al. Generation of a transgenic rabbit model of retinal degeneration. Invest Ophthalmol Vis Sci. 2009;50:1371–7.PubMedCrossRef

111.

Gal A, Li Y, Thompson DA, Weir J, Orth U, Jacobson SG, et al. Mutations in MERTK, the human orthologue of the RCS rat retinal dystrophy gene, cause retinitis pigmentosa. Nat Genet. 2000;26:270–1.PubMedCrossRef

112.

Seiler MJ, Aramant RB, Thomas BB, Peng Q, Sadda SR, Keirstead HS. Visual restoration and transplant connectivity in degenerate rats implanted with retinal progenitor sheets. Eur J Neurosci. 2010;31:508–20.PubMedCrossRef

113.

Baloyannis SJ. Dendritic pathology in Alzheimer’s disease. J Neurol Sci. 2009;283:153–7.PubMedCrossRef

114.

Bywood PT, Johnson SM. Dendrite loss is a characteristic early indicator of toxin-induced neurodegeneration in rat midbrain slices. Exp Neurol. 2000;161:306–16.PubMedCrossRef

115.

Prince DA, Parada I, Scalise K, Graber K, Shen F. Epilepsy following cortical injury: cellular and molecular mechanisms as targets for potential prophylaxis. Epilepsia. 2009;50(Suppl 2):30–40.PubMedCrossRef

116.

Duncan T, Wiggert B, Whittaker N, Darrow R, Organisciak DT. Effect of visible light on normal and p23h-3 transgenic rat retinas: characterization of a novel retinoic acid derivative present in the p23h-3 retina. Photochem Photobiol. 2006;82:741–5.PubMedCrossRef

117.

Clagett-Dame M, McNeill E, Muley P. Role of all-trans retinoic acid in neurite outgrowth and axonal elongation. J Neurobiol. 2006;66:739–56.PubMedCrossRef

118.

Thiagarajan TC, Piedras-Renteria ES, Tsien RW. Alpha and beta CAMKII: inverse regulation by neuronal activity and opposing effects on synaptic strength. Neuron. 2002;36:1103–14.PubMedCrossRef

119.

Jiang L, Boye SL, Dizhoor A, Hauswirth WW, Baehr W. Knock-down of GCAP1 by RNA interference delays photoreceptor degeneration in GCAP1-Y99C transgenic mice. Invest Ophthalmol Vis Sci. 2011;51:4488.

120.

Terada N, Hamazaki T, Oka M, Hoki M, Mastalerz DM, Nakano Y, et al. Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature. 2002;416:542–5.PubMedCrossRef

121.

Canola K, Angénieux B, Tekaya M, Quiambao A, Naash MI, Munier FL, et al. Retinal stem cells transplanted into models of late stages of retinitis pigmentosa preferentially adopt a glial or a retinal ganglion cell fate. Invest Ophthalmol Vis Sci. 2007;48:446–54.PubMedCrossRef

122.

Bull ND, Limb GA, Martin KR. Human Muller stem cell (MIO-M1) transplantation in a rat model of glaucoma: survival, differentiation, and integration. Invest Ophthalmol Vis Sci. 2008;49:3449–56.PubMedCrossRef

123.

Busskamp V, Duebel J, Balya D, Fradot M, Viney TJ, Siegert S, et al. Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa. Science. 2010;329:413–7.PubMedCrossRef

124.

Lagali P, Balya D, Awatramani GB, Münch TA, Kim DS, Busskamp V, et al. Light-activated channels targeted to ON bipolar cells restore visual function in retinal degeneration. Nat Neurosci. 2008;11:667–75.PubMedCrossRef

125.

Doroudchi MM, Greenberg KP, Liu J, Silka KA, Boyden ES, Lockridge JA, et al. Virally delivered channelrhodopsin-2 safely and effectively restores visual function in multiple mouse models of blindness. Mol Ther. 2011;19:1220–9.PubMedCrossRef

126.

Marc R. Injury and repair: retinal remodeling. In: Dana R, editor. Encyclopedia of the eye. Amsterdam: Elsevier; 2009.

127.

Ivanova E, Pan Z-H. Evaluation of the adeno-associated virus mediated long-term expression of channelrhodopsin-2 in the mouse retina. Mol Vis. 2009;15:1680–9.PubMed

Title: Retinal remodeling
Authors: B. W. Jones
M. Kondo
H. Terasaki
Y. Lin
M. McCall
R. E. Marc
Publication date: 01-07-2012
Publisher: Springer Japan
Published in: Japanese Journal of Ophthalmology / Issue 4/2012
Print ISSN: 0021-5155
Electronic ISSN: 1613-2246
DOI: https://doi.org/10.1007/s10384-012-0147-2

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Retinal remodeling

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2012

Estimating retinal nerve fiber layer thickness in normal schoolchildren with spectral-domain optical coherence tomography

Novel compound heterozygous mutations in the MFRP gene in a Japanese patient with posterior microphthalmos

Detection of visual field defects in pre-perimetric glaucoma using fundus-oriented small-target perimetry

The usefulness of infraorbital nerve enlargement on MRI imaging in clinical diagnosis of IgG4-related orbital disease

Comparison of efficacy of four prostaglandin analogues by bilateral treatment in healthy subjects

Risk factors for primary open-angle glaucoma in South Korea: the Namil study