Retinal regeneration in Zebrafish

doi:10.16098/j.issn.0529-1356.2015.05.025

Abstract

Abstract:

After retinal injury or disease, mammals exhibit very limited capacity to repair a damaged retina. In contrast, teleost fish such asZebrafishmount a robust regenerative response that recovers all types of lost neurons and glia and restores visual function. The source of cells responsible for this regeneration has been identified as Müller glia. Recent studies have revealed many important signaling and molecular mechanisms regulating Müller glia dedifferentiation and proliferation. In this review, we summarize the history of retinal regeneration research, models of injury, source of cells for regeneration, and its underlying molecular mechanisms.

Key words: Retina, Regeneration, Dedifferentiation, Müller glia, Zebrafish

ZHANG Shu-qiang LIU Dong XU Hui*. Retinal regeneration in Zebrafish[J]. AAS, 2015, 46(5): 715-719.

References

［1］Lamba D, Karl M, Reh T. Neural regeneration and cell replacement: a view from the eye［J］. Cell Stem Cell, 2008, 2(6): 538-549.
［2］Bernardos RL, Barthel LK, Meyers JR, et al. Late-stage neuronal progenitors in the retina are radial Muller glia that function as retinal stem cells ［J］. J Neurosci, 2007, 27(26):7028-7040.
［3］Ramachandran R, Reifler A, Parent JM, et al. Conditional gene expression and lineage tracing of tuba1a expressing cells during zebrafish development and retina regeneration［J］. J Comp Neurol, 2010, 518(20): 4196-4212.
［4］Lenkowski JR, Raymond PA. Muller glia: stem cells for generation and regeneration of retinal neurons in teleost fish［J］. Prog Retin Eye Res, 2014, 40: 94-123.
［5］Hitchcock PF, Lindsey Myhr KJ, Easterm SS Jr, et al. Local regeneration in the retina of the goldfish［J］. J Neurobiol, 1992, 23(2): 187-203.
［6］Hitchcock PF, Vanderyt JT. Regeneration of the dopamine-cell mosaic in the retina of the goldfish［J］. Vis Neurosci, 1994, 11(2):209-217.
［7］Cameron DA. Cellular proliferation and neurogenesis in the injured retina of adult zebrafish［J］. Vis Neurosci, 2000, 17(5):789-797.
［8］Goldman D, Hankin M, Li Z, et al. Transgenic zebrafish for studying nervous system development and regeneration［J］. Transgenic Res, 2001, 10(1): 21-33.
［9］Liu Q, Londraville RL, Azodi E, et al. Up-regulation of cadherin-2 and cadherin-4 in regenerating visual structures of adult zebrafish［J］. Exp Neurol, 2002, 177(2): 396-406.
［10］Faillace MP, Julian D, Korenbrot JI. Mitotic activation of proliferative cells in the inner nuclear layer of the mature fish retina: regulatory signals and molecular markers［J］. J Comp Neurol, 2002, 451(2): 127-141.
［11］Hitchcock PF, Cirenza P. Synaptic organization of regenerated retina in the goldfish［J］. J Comp Neurol, 1994, 343(4): 609-616.
［12］Maier W, Wolburg H. Regeneration of the goldfish retina after exposure to different doses of ouabain［J］. Cell Tissue Res, 1979, 202(1): 99-118.
［13］Raymond PA, Reifler MJ, Rivlin PK. Regeneration of goldfish retina: rod precursors are a likely source of regenerated cells［J］. J Neurobiol, 1988, 19(5): 431-463.
［14］Fimbel SM, Montgomery JE, Burket CT, et al. Regeneration of inner retinal neurons after intravitreal injection of ouabain in zebrafish［J］. J Neurosci, 2007, 27(7): 1712-1724.［15］Nagashima M, Barthel LK, Raymond PA. A self-renewing division of zebrafish Muller glial cells generates neuronal progenitors that require N-cadherin to regenerate retinal neurons［J］. Development, 2013, 140(22): 4510-4521.
［16］Fausett BV, Goldman D. A role for alpha1 tubulin-expressing Muller glia in regeneration of the injured zebrafish retina［J］. J Neurosci, 2006, 26(23): 6303-6313.
［17］Thummel R, Kassen SC, Enright JM, et al. Characterization of Muller glia and neuronal progenitors during adult zebrafish retinal regeneration［J］. Exp Eye Res, 2008, 87(5): 433-444.
［18］Lindsey AE, Powers MK. Visual behavior of adult goldfish with regenerating retina［J］. Vis Neurosci, 2007, 24(3): 247-255.
［19］Mensinger AF, Powers MK. Visual function in regenerating teleost retina following cytotoxic lesioning［J］. Vis Neurosci, 1999, 16(2): 241-251.
［20］Sherpa T, Fimbel SM, Mallory DE, et al. Ganglion cell regeneration following whole-retina destruction in zebrafish［J］. Dev Neurobiol, 2008, 68(2): 166-181.
［21］Marc RE, Sperling HG. The chromatic organization of the goldfish cone mosaic［J］. Vision Res, 1976, 16(11): 1211-1224.
［22］Cameron DA, Cornwall MC, MacNichol EF, et al. Visual pigment assignments in regenerated retina［J］. J Neurosci, 1997, 17(3): 917-923.
［23］Stenkamp DL, Powers MK, Carney LH, et al. Evidence for two distinct mechanisms of neurogenesis and cellular pattern formation in regenerated goldfish retinas［J］. J Comp Neurol, 2001, 431(4): 363-381.
［24］Raymond PA, Barthel LK, Bernardos RL, et al. Molecular characterization of retinal stem cells and their niches in adult zebrafish［J］. BMC Dev Biol, 2006, 6:-36.
［25］Thummel R, Enright JM, Kassen SC, et al. Pax6a and Pax6b are required at different points in neuronal progenitor cell proliferation during zebrafish photoreceptor regeneration［J］. Exp Eye Res, 2010, 90(5): 572-582.
［26］Powell C, Grant AR, Cornblath E, et al. Analysis of DNA methylation reveals a partial reprogramming of the Muller glia genome during retina regeneration［J］. Proc Natl Acad Sci USA, 2013, 110(49): 19814-19819.
［27］Ramachandran R, Reifler A, Wan J, et al. Application of Cre-loxP recombination for lineage tracing of adult zebrafish retinal stem cells［J］. Methods Mol Biol, 2012, 884: 129-140.
［28］Bringmann A, Iandiev I, Pannicke T, et al. Cellular signaling and factors involved in Muller cell gliosis: neuroprotective and detrimental effects［J］. Prog Retin Eye Res, 2009, 28(6): 423-451.
［29］Nelson CM, Ackerman KM, O’Hayer P, et al. Tumor necrosis factoralpha is produced by dying retinal neurons and is required for Muller glia proliferation during zebrafish retinal regeneration［J］. J Neurosci, 2013, 33(15): 6524-6539.
［30］Close JL, Liu J, Gumuscu B, et al. Epidermal growth factor receptor expression regulates proliferation in the postnatal rat retina［J］. Glia, 2006, 54(2): 94-104.
［31］Fischer AJ, Bongini R. Turning Müller glia into neural progenitors in the retina［J］. Mol Neurobiol, 2010, 42(3): 199-209.
［32］Karl MO, Hayes S, Nelson BR, et al. Stimulation of neural regeneration in the mouse retina［J］. Proc Natl Acad Sci USA, 2008, 105(49): 19508-19513.
［33］Wan J, Ramachandran R, Goldman D. HB-EGF is necessary and sufficient for Müller glia dedifferentiation and retina regeneration［J］. Dev Cell, 2012, 22(2): 334-347.
［34］Hochmann S, Kaslin J, Hans S, et al. Fgf signaling is required for photoreceptor maintenance in the adult zebrafish retina［J］. PLoS One, 2012, 7(1): e30365.
［35］Qin Z, Kidd AR 3rd, Thomas JL, et al. FGF signaling regulates rod photoreceptor cell maintenance and regeneration in zebrafish［J］. Exp Eye Res, 2011, 93(5): 726-734.
［36］Bonni A, Sun Y, Nadal-Vicens M, et al. Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway ［J］. Science, 1997, 278(5337):477-483.
［37］Zhang C, Li H, Liu MG, et al. STAT3 activation protects retinal ganglion cell layer neurons in response to stress［J］. Exp Eye Res, 2008, 86(6): 991-997.
［38］Niwa H, Burdon T, Chambers I, et al. Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3［J］. Genes Dev, 1998, 12(13): 2048-2060.
［39］Zhao XF, Wan J, Powell C, et al. Leptin and IL-6 family cytokines synergize to stimulate Muller glia reprogramming and retina regeneration［J］. Cell Rep, 2014, 9(1): 272-284.［40］Fausett BV, Gumerson JD, Goldman D. The proneural basic helix-loop-helix gene ascl1a is required for retina regeneration［J］. J Neurosci, 2008, 28(5): 1109-1117.
［41］Ramachandran R, Fausett BV, Goldman D. Ascl1a regulates Muller glia dedifferentiation and retinal regeneration through a Lin-28-dependent, let-7 microRNA signalling pathway［J］. Nat Cell Biol, 2010, 12(11): 1101-1107.
［42］Ramachandran R, Zhao XF, Goldman D. Ascl1a/Dkk/beta-catenin signaling pathway is necessary and glycogen synthase kinase-3beta inhibition is sufficient for zebrafish retina regeneration［J］. Proc Natl Acad Sci USA, 2011, 108(38): 15858-15863.
［43］Pollak J, Wilken MS, Ueki Y, et al. ASCL1 reprograms mouse Muller glia into neurogenic retinal progenitors［J］. Development, 2013, 140(12): 2619-2631.

[1]	FENG Li-ping XU Yi-lin CHEN Xun LIU Da-hai WANG Jun-yong WANG Xiao-ying LIN Jin-xing. Retinal microstructure and developmental characteristics in Zebrafish [J]. Acta Anatomica Sinica, 2024, 55(1): 105-112.
[2]	YAO Su-hua YAN Jun XIE Fang LIN Chun-hua HUANG Zheng-chun. Nerve repair effect of olanzapine-mediated cyclic AMP response element binding protein/brain-derived neurotrophic factor/receptor tyrosine kinase receptors B pathway on schizophrenic rats [J]. Acta Anatomica Sinica, 2023, 54(6): 660-667.
[3]	ZHANG Xiao-li ZHANG Shu-qiang XU Hui . Research progress in the reprogramming of retinal Müller glia cells [J]. Acta Anatomica Sinica, 2023, 54(4): 484-489.
[4]	XUE Qi-jie CHANG Cui-fang WANG Zi-hui ZANG Xia-yan LIN Kai-lin ZHANG Chun-bo HAN Lu YE Bing-yu XU Cun-shuan . Expression change and role of myeloma cancer gene mRNA and the non-coding RNA in the hepatocyte cycle initiation and termination during the rat liver regeneration [J]. Acta Anatomica Sinica, 2023, 54(4): 414-419.
[5]	LIN Kai-lin YANG Xian-guang WANG Zi-hui ZANG Xia-yan XUE Qi-jie HAN Lu ZHANG Chun-bo ZHAO Zhi-hu XU Cun-shuan. Expression change and role of Kruppel-like factor 4 mRNA, microRNA-881-3p, circular RNA_20298 and circular RNA_14826 in the hepatocyte apoptosis during the rat liver regeneration [J]. Acta Anatomica Sinica, 2023, 54(4): 420-424.
[6]	WANG Zi-hui GUO Jian-lin ZANG Xia-yan XUE Qi-jie LIN Kai-lin ZHANG Chun-bo HAN Lu LIN Jun-tang XU Cun-shuan . Expression change and role of sex determining region box transcription factor 2 mRNA and the non-coding RNA in the hepatocyte stem changes during the rat liver regeneration [J]. Acta Anatomica Sinica, 2023, 54(2): 202-207.
[7]	ZHANG Chun-bo WANG Gai-ping WANG Zi-hui ZANG Xia-yan XUE Qi-jie LIN Kai-lin HAN Lu WANG Qi-wen XU Cun-shuan. Expression change and role of myeloma cancer gene mRNA, microRNA-540-3p, circular RNA_04996 in the liver inflammatory reaction during the rat liver regeneration [J]. Acta Anatomica Sinica, 2023, 54(1): 70-74.
[8]	HU Xiao-jing ZHANG Ming-min Lü Guang-ming. Preliminary analysis of mRNA and microRNA differential expression profiles in spinal cord regeneration of Gekko japonicus after tail amputation [J]. Acta Anatomica Sinica, 2023, 54(1): 6-12.
[9]	BIAN Wei LI Meng-yi ZHOU Peng LI Jun-wei ZHANG Ting WU An-ting QI Shuang-shuang CUI Huai-rui SUN Chen-you. Effects of activating mTORC2/Akt signaling pathway on dopaminergic neurons and behaviors in 6-hydroxydopamin model mice [J]. Acta Anatomica Sinica, 2023, 54(1): 13-22.
[10]	YAO Yuan DU Jing-yi ZHOU Wen-juan . Protective effect and mechanism of ginsenoside Rb1 on repairing sciatic nerve injury in mice [J]. Acta Anatomica Sinica, 2022, 53(1): 19-27.
[11]	ZANG Xia-yan WANG Zi-hui LI Ya-fei GUO Jian-lin JIN WeiCHANG Cui-fang XU Cun-shuan. Expression and role of CCAAT enhancer binding protein α mRNA, microRNA-144-3p and three kinds of circular RNAs of hepatocytes during the rat liver regeneration initiation [J]. Acta Anatomica Sinica, 2021, 52(6): 901-908.
[12]	ZANG Xia-yan WANG Zi-hui GAO Han GUO Jian-lin JIN Wei CHANG Cui-fang XU Cun-shuan. Expression and role of CCAAT enhancer binding protein α mRNA, microRNA-144-3p and three kinds of circular RNAs of hepatocytes during the rat liver regeneration termination [J]. Acta Anatomica Sinica, 2021, 52(6): 909-912.
[13]	BAI Ge WANG Zi-hui SONG Ya-ping ZANG Xia-yan LI Ya-fei YE Bing-yu ZHAO Zhi-hu XU Cun-shuan . Expression and role of CCAAT enhancer binding protein β mRNA, microRNA-369-3p and rno-Rmdn2_0006 of hepatocytes during the rat liver regeneration initiation [J]. Acta Anatomica Sinica, 2021, 52(6): 913-916.
[14]	LI Ya-fei WANG Zi-hui ZANG Xia-yan JIN Wei CHANG Cui-fang GUO Jian-lin XU Cun-shuan. Expression and role of CCAAT enhancer binding protein δ mRNA, microRNA-3553 and rno-Acad8_0002 of hepatocytes during the rat liver regeneration initiation [J]. Acta Anatomica Sinica, 2021, 52(6): 917-920.
[15]	GAO Han WANG Zi-hui ZANG Xia-yan JIN Wei CHANG Cui-fang GUO Jian-lin XU Cun-shuan. Expression and role of CCAAT enhancer binding protein ζ mRNA, microRNA-136-3p and four kinds of circular RNAs of hepatocytes during the rat liver regeneration initiation [J]. Acta Anatomica Sinica, 2021, 52(6): 921-624.