Genetic and epigenetic regulators of retinal Müller glial cell reprogramming

Xueqi Xiao; Zhiyong Liao; Jian Zou

doi:10.1016/j.aopr.2023.05.004

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Genetic and epigenetic regulators of retinal Müller glial cell reprogramming

Review | 更新时间：2023-11-15

- Genetic and epigenetic regulators of retinal Müller glial cell reprogramming
- Genetic and epigenetic regulators of retinal Müller glial cell reprogramming
- 眼科实践与研究新进展 2023年3卷第3期页码：126-133
- 作者机构：
  
  1. ,Wenzhou,China
  2. ,Hangzhou,China
  3. ,Hangzhou,China
- 作者简介：
- 基金信息：
- DOI：10.1016/j.aopr.2023.05.004
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Genetic and epigenetic regulators of retinal Müller glial cell reprogramming[J]. 眼科实践与研究新进展, 2023,3(3):126-133.

Xueqi Xiao, Zhiyong Liao, Jian Zou. Genetic and epigenetic regulators of retinal Müller glial cell reprogramming[J]. AOPR, 2023,3(3):126-133.
Genetic and epigenetic regulators of retinal Müller glial cell reprogramming[J]. 眼科实践与研究新进展, 2023,3(3):126-133. DOI： 10.1016/j.aopr.2023.05.004.

Xueqi Xiao, Zhiyong Liao, Jian Zou. Genetic and epigenetic regulators of retinal Müller glial cell reprogramming[J]. AOPR, 2023,3(3):126-133. DOI： 10.1016/j.aopr.2023.05.004.

摘要

Background,Retinal diseases characterized with irreversible loss of retinal nerve cells, such as optic atrophy and retinal degeneration, are the main causes of blindness. Current treatments for these diseases are very limited. An emerging treatment strategy is to induce the reprogramming of Müller glial cells to generate new retinal nerve cells, which could potentially restore vision.,Main text,Müller glial cells are the predominant glial cells in retinae and play multiple roles to maintain retinal homeostasis. In lower vertebrates, such as in zebrafish, Müller glial cells can undergo cell reprogramming to regenerate new retinal neurons in response to various damage factors, while in mammals, this ability is limited. Interestingly, with proper treatments, Müller glial cells can display the potential for regeneration of retinal neurons in mammalian retinae. Recent studies have revealed that dozens of genetic and epigenetic regulators play a vital role in inducing the reprogramming of Müller glial cells in vivo. This review summarizes these critical regulators for Müller glial cell reprogramming and highlights their differences between zebrafish and mammals.,Conclusions,A number of factors have been identified as the important regulators in Müller glial cell reprogramming. The early response of Müller glial cells upon acute retinal injury, such as the regulation in the exit from quiescent state, the initiation of reactive gliosis, and the re-entry of cell cycle of Müller glial cells, displays significant difference between mouse and zebrafish, which may be mediated by the diverse regulation of Notch and TGFβ (transforming growth factor-β) isoforms and different chromatin accessibility.

Abstract

关键词

Keywords

Müller glial cell reprogrammingGenetic regulationEpigenetic modificationretinal neuron regeneration

references

1 M. Hoon, H. Okawa, L. Della Santina, et al.Functional architecture of the retina: development and disease Prog Retin Eye Res, 42 (2014), pp. 44-84, 10.1016/j.preteyeres.2014.06.003

2 D.L. StenkampDevelopment of the vertebrate eye and retina Prog Mol Biol Transl Sci, 134 (2015), pp. 397-414, 10.1016/bs.pmbts.2015.06.006

3 Z.B. Jin, M.L. Gao, W.L. Deng, et al.Stemming retinal regeneration with pluripotent stem cells Prog Retin Eye Res, 69 (2019), pp. 38-56, 10.1016/j.preteyeres.2018.11.003

4 D. GoldmanMuller glial cell reprogramming and retina regeneration Nat Rev Neurosci, 15 (7) (2014), pp. 431-442, 10.1038/nrn3723

5 E. Newman, A. ReichenbachThe Muller cell: a functional element of the retina Trends Neurosci, 19 (8) (1996), pp. 307-312, 10.1016/0166-2236(96)10040-0

6 A. Reichenbach, A. BringmannNew functions of Muller cells Glia, 61 (5) (2013), pp. 651-678, 10.1002/glia.22477

7 T. LangmannMicroglia activation in retinal degeneration J Leukoc Biol, 81 (6) (2007), pp. 1345-1351, 10.1189/jlb.0207114

8 A. Chohan, U. Singh, A. Kumar, et al.Muller stem cell dependent retinal regeneration Clin Chim Acta, 464 (2017), pp. 160-164, 10.1016/j.cca.2016.11.030

9 J.R. Lenkowski, P.A. RaymondMuller glia: stem cells for generation and regeneration of retinal neurons in teleost fish Prog Retin Eye Res, 40 (2014), pp. 94-123, 10.1016/j.preteyeres.2013.12.007

10 R.A. Gorsuch, D.R. HydeRegulation of Muller glial dependent neuronal regeneration in the damaged adult zebrafish retina Exp Eye Res, 123 (2014), pp. 131-140, 10.1016/j.exer.2013.07.012

11 A.J. Fischer, T.A. RehMüller glia are a potential source of neural regeneration in the postnatal chicken retina Nat Neurosci, 4 (3) (2001), pp. 247-252, 10.1038/85090

12 M. Lahne, M. Nagashima, D.R. Hyde, et al.Reprogramming müller glia to regenerate retinal neurons Ann Rev Vis Sci, 6 (2020), pp. 171-193, 10.1146/annurev-vision-121219-081808

13 A.P. Jadhav, K. Roesch, C.L. CepkoDevelopment and neurogenic potential of Muller glial cells in the vertebrate retina Prog Retin Eye Res, 28 (4) (2009), pp. 249-262, 10.1016/j.preteyeres.2009.05.002

14 A. Bringmann, P. WiedemannMuller glial cells in retinal disease Ophthalmologica, 227 (1) (2012), pp. 1-19, 10.1159/000328979

15 A.B. Graca, C. Hippert, R.A. PearsonMuller glia reactivity and development of gliosis in response to pathological conditions Adv Exp Med Biol, 1074 (2018), pp. 303-308, 10.1007/978-3-319-75402-4_37

16 X. Liu, Y. Liu, H. Jin, et al.Reactive fibroblasts in response to optic nerve crush injury Mol Neurobiol, 58 (4) (2021), pp. 1392-1403, 10.1007/s12035-020-02199-4

17 F.M. Conedera, A.M.Q. Pousa, N. Mercader, et al.The TGFbeta/Notch axis facilitates Muller cell-to-epithelial transition to ultimately form a chronic glial scar Mol Neurodegener, 16 (1) (2021), p. 69, 10.1186/s13024-021-00482-z

18 J.L. Thomas, A.H. Ranski, G.W. Morgan, et al.Reactive gliosis in the adult zebrafish retina Exp Eye Res, 143 (2016), pp. 98-109, 10.1016/j.exer.2015.09.017

19 N.L. Jorstad, M.S. Wilken, L. Todd, et al.STAT signaling modifies Ascl1 chromatin binding and limits neural regeneration from muller glia in adult mouse retina Cell Rep, 30 (7) (2020), pp. 2195-2208 e5, 10.1016/j.celrep.2020.01.075

20 N.L. Jorstad, M.S. Wilken, W.N. Grimes, et al.Stimulation of functional neuronal regeneration from Muller glia in adult mice Nature, 548 (7665) (2017), pp. 103-107, 10.1038/nature23283

21 Y. Lu, B. Brommer, X. Tian, et al.Reprogramming to recover youthful epigenetic information and restore vision Nature, 588 (7836) (2020), pp. 124-129, 10.1038/s41586-020-2975-4

22 T. Hoang, J. Wang, P. Boyd, et al.Gene regulatory networks controlling vertebrate retinal regeneration Science, 370 (6519) (2020), Article eabb8598, 10.1126/science.abb8598

23 M.-S. Lee, J. Wan, D. GoldmanTgfb3 collaborates with PP2A and notch signaling pathways to inhibit retina regeneration Elife, 9 (2020), Article e55137, 10.7554/eLife.55137

24 J.R. Lenkowski, Z. Qin, C.J. Sifuentes, et al.Retinal regeneration in adult zebrafish requires regulation of TGFβ signaling Glia, 61 (10) (2013), pp. 1687-1697, 10.1002/glia.22549

25 C. Tappeiner, E. Maurer, P. Sallin, et al.Inhibition of the TGFβ pathway enhances retinal regeneration in adult zebrafish PLoS One, 11 (11) (2016), Article e0167073, 10.1371/journal.pone.0167073

26 F.M. Conedera, A.M. Quintela Pousa, D.M. Presby, et al.Diverse signaling by TGFβ isoforms in response to focal injury is associated with either retinal regeneration or reactive gliosis Cell Mol Neurobiol, 41 (1) (2021), pp. 43-62, 10.1007/s10571-020-00830-5

27 A. Angbohang, N. Wu, T. Charalambous, et al.Downregulation of the canonical WNT signaling pathway by TGFβ1 inhibits photoreceptor differentiation of adult human müller glia with stem cell characteristics Stem Cell Dev, 25 (1) (2016), pp. 1-12, 10.1089/scd.2015.0262

28 F. Elsaeidi, P. Macpherson, E.A. Mills, et al.Notch suppression collaborates with Ascl1 and Lin28 to unleash a regenerative response in fish retina, but not in mice J Neurosci, 38 (9) (2018), pp. 2246-2261, 10.1523/JNEUROSCI.2126-17.2018

29 C. Conner, K.M. Ackerman, M. Lahne, et al.Repressing notch signaling and expressing TNFalpha are sufficient to mimic retinal regeneration by inducing Muller glial proliferation to generate committed progenitor cells J Neurosci, 34 (43) (2014), pp. 14403-14419, 10.1523/JNEUROSCI.0498-14.2014

30 L.J. Campbell, J.S. Hobgood, M. Jia, et al.Notch3 and DeltaB maintain Muller glia quiescence and act as negative regulators of regeneration in the light-damaged zebrafish retina Glia, 69 (3) (2021), pp. 546-566, 10.1002/glia.23912

31 A. Sahu, S. Devi, J. Jui, et al.Notch signaling via Hey1 and Id2b regulates Muller glia's regenerative response to retinal injury Glia, 69 (12) (2021), pp. 2882-2898, 10.1002/glia.24075

32 S. Mitra, S. Devi, M.S. Lee, et al.Vegf signaling between Muller glia and vascular endothelial cells is regulated by immune cells and stimulates retina regeneration Proc Natl Acad Sci U S A, 119 (50) (2022), Article e2211690119, 10.1073/pnas.2211690119

33 S. Hayes, B.R. Nelson, B. Buckingham, et al.Notch signaling regulates regeneration in the avian retina Dev Biol, 312 (1) (2007), pp. 300-311, 10.1016/j.ydbio.2007.09.046

34 L.J. Campbell, J.L. Levendusky, S.A. Steines, et al.Retinal regeneration requires dynamic Notch signaling Neural Regenerat Res, 17 (6) (2022), pp. 1199-1209, 10.4103/1673-5374.327326

35 K. Eastlake, W.D.B. Lamb, J. Luis, et al.Prospects for the application of Muller glia and their derivatives in retinal regenerative therapies Prog Retin Eye Res, 85 (2021), Article 100970, 10.1016/j.preteyeres.2021.100970

36 H. Gao, A. L, X. Huang, et al.Muller glia-mediated retinal regeneration Mol Neurobiol, 58 (5) (2021), pp. 2342-2361, 10.1007/s12035-020-02274-w

37 D.M. Mitchell, A.G. Lovel, D.L. StenkampDynamic changes in microglial and macrophage characteristics during degeneration and regeneration of the zebrafish retina J Neuroinflammation, 15 (1) (2018), p. 163, 10.1186/s12974-018-1185-6

38 M. IribarneInflammation induces zebrafish regeneration Neural Regenerat Res, 16 (9) (2021), pp. 1693-1701, 10.4103/1673-5374.306059

39 M. Nagashima, P.F. HitchcockInflammation regulates the multi-step process of retinal regeneration in zebrafish Cells, 10 (4) (2021), p. 783, 10.3390/cells10040783

40 F.M. Conedera, A.M.Q. Pousa, N. Mercader, et al.Retinal microglia signaling affects Muller cell behavior in the zebrafish following laser injury induction Glia, 67 (6) (2019), pp. 1150-1166, 10.1002/glia.23601

41 N.J. Silva, M. Nagashima, J. Li, et al.Inflammation and matrix metalloproteinase 9 (Mmp-9) regulate photoreceptor regeneration in adult zebrafish Glia, 68 (7) (2020), pp. 1445-1465, 10.1002/glia.23792

42 D.T. White, S. Sengupta, M.T. Saxena, et al.Immunomodulation-accelerated neuronal regeneration following selective rod photoreceptor cell ablation in the zebrafish retina Proceed Nat Acad Sci USA, 114 (18) (2017), pp. E3719-E3728, 10.1073/pnas.1617721114

43 X. Hu, G.-L. Zhao, M.-X. Xu, et al.Interplay between Müller cells and microglia aggravates retinal inflammatory response in experimental glaucoma J Neuroinflammation, 18 (1) (2021), p. 303, 10.1186/s12974-021-02366-x

44 N.P.B. Au, Ma C.H. E. NeuroinflammationMicroglia and implications for retinal ganglion cell survival and axon regeneration in traumatic optic neuropathy Front Immunol, 13 (2022), Article 860070, 10.3389/fimmu.2022.860070

45 I. Palazzo, L.J. Todd, T.V. Hoang, et al.NFkB-signaling promotes glial reactivity and suppresses Müller glia-mediated neuron regeneration in the mammalian retina Glia, 70 (7) (2022), pp. 1380-1401, 10.1002/glia.24181

46 C.J. Sifuentes, J.-W. Kim, A. Swaroop, et al.Rapid, dynamic activation of müller glial stem cell responses in zebrafish Invest Ophthalmol Vis Sci, 57 (13) (2016), pp. 5148-5160, 10.1167/iovs.16-19973

47 I. Palazzo, K. Deistler, T.V. Hoang, et al.NF-κB signaling regulates the formation of proliferating Müller glia-derived progenitor cells in the avian retina Development (Cambridge, England), 147 (10) (2020), p. dev183418, 10.1242/dev.183418

48 I. Palazzo, L. Kelly, L. Koenig, et al.Patterns of NFkB activation resulting from damage, reactive microglia, cytokines, and growth factors in the mouse retina Exp Neurol, 359 (2023), Article 114233, 10.1016/j.expneurol.2022.114233

49 C.M. Nelson, K.M. Ackerman, P. O'Hayer, et al.Tumor necrosis factor-alpha is produced by dying retinal neurons and is required for Muller glia proliferation during zebrafish retinal regeneration J Neurosci, 33 (15) (2013), pp. 6524-6539, 10.1523/JNEUROSCI.3838-12.2013

50 L. Niu, Y. Fang, X. Yao, et al.TNFalpha activates MAPK and Jak-Stat pathways to promote mouse Muller cell proliferation Exp Eye Res, 202 (2021), Article 108353, 10.1016/j.exer.2020.108353

51 Q. Li, Y. Cheng, S. Zhang, et al.TRPV4-induced Müller cell gliosis and TNF-α elevation-mediated retinal ganglion cell apoptosis in glaucomatous rats via JAK2/STAT3/NF-κB pathway J Neuroinflammation, 18 (1) (2021), p. 271, 10.1186/s12974-021-02315-8

52 M. Ji, Q. Sun, G. Zhang, et al.Microglia-derived TNF-α mediates Müller cell activation by activating the TNFR1-NF-κB pathway Exp Eye Res, 214 (2022), Article 108852, 10.1016/j.exer.2021.108852

53 M. Völkner, F. Wagner, L.M. Steinheuer, et al.HBEGF-TNF induce a complex outer retinal pathology with photoreceptor cell extrusion in human organoids Nat Commun, 13 (1) (2022), p. 6183, 10.1038/s41467-022-33848-y

54 S.C. Kassen, R. Thummel, L.A. Campochiaro, et al.CNTF induces photoreceptor neuroprotection and Muller glial cell proliferation through two different signaling pathways in the adult zebrafish retina Exp Eye Res, 88 (6) (2009), pp. 1051-1064, 10.1016/j.exer.2009.01.007

55 X.F. Zhao, J. Wan, C. Powell, et al.Leptin and IL-6 family cytokines synergize to stimulate Muller glia reprogramming and retina regeneration Cell Rep, 9 (1) (2014), pp. 272-284, 10.1016/j.celrep.2014.08.047

56 P. Boyd, L.J. Campbell, D.R. HydeClcf1/Crlf1a-mediated signaling is neuroprotective and required for Müller glia proliferation in the light-damaged zebrafish retina Front Cell Dev Biol, 11 (2023), Article 1142586, 10.3389/fcell.2023.1142586

57 A.J. Fischer, M. Schmidt, G. Omar, et al.BMP4 and CNTF are neuroprotective and suppress damage-induced proliferation of Muller glia in the retina Mol Cell Neurosci, 27 (4) (2004), pp. 531-542, 10.1016/j.mcn.2004.08.007

58 Y. Wang, S.B. Smith, J.M. Ogilvie, et al.Ciliary neurotrophic factor induces glial fibrillary acidic protein in retinal Müller cells through the JAK/STAT signal transduction pathway Curr Eye Res, 24 (4) (2002), pp. 305-312, 10.1076/ceyr.24.4.305.8408

59 M. Kirsch, N. Trautmann, M. Ernst, et al.Involvement of gp130-associated cytokine signaling in Muller cell activation following optic nerve lesion Glia, 58 (7) (2010), pp. 768-779, 10.1002/glia.20961

60 K.D. Rhee, S. Nusinowitz, K. Chao, et al.CNTF-mediated protection of photoreceptors requires initial activation of the cytokine receptor gp130 in Muller glial cells Proc Natl Acad Sci U S A, 110 (47) (2013), pp. E4520-E4529, 10.1073/pnas.1303604110

61 J. Wan, R. Ramachandran, D. GoldmanHB-EGF is necessary and sufficient for Muller glia dedifferentiation and retina regeneration Dev Cell, 22 (2) (2012), pp. 334-347, 10.1016/j.devcel.2011.11.020

62 J. Wan, X.F. Zhao, A. Vojtek, et al.Retinal injury, growth factors, and cytokines converge on beta-catenin and pStat3 signaling to stimulate retina regeneration Cell Rep, 9 (1) (2014), pp. 285-297, 10.1016/j.celrep.2014.08.048

63 A.J.,M.C.R. Fischer, B.D. Dierks, et al.Insulin and fibroblast growth factor 2 activate a neurogenic program in Mü ller glia of the chicken retina J Neurosci, 22 (21) (2002), pp. 9387-9398, 10.1523/JNEUROSCI.22-21-09387.2002

64 E.R. Ritchey, C.P. Zelinka, J. Tang, et al.The combination of IGF1 and FGF2 and the induction of excessive ocular growth and extreme myopia Exp Eye Res, 99 (2012), pp. 1-16, 10.1016/j.exer.2012.03.019

65 L. Todd, L.I. Volkov, C. Zelinka, et al.Heparin-binding EGF-like growth factor (HB-EGF) stimulates the proliferation of Muller glia-derived progenitor cells in avian and murine retinas Mol Cell Neurosci, 69 (2015), pp. 54-64, 10.1016/j.mcn.2015.10.004

66 M. Goel, N.K. DhingrabFGF and insulin lead to migration of Muller glia to photoreceptor layer in rd1 mouse retina Neurosci Lett, 755 (2021), Article 135936, 10.1016/j.neulet.2021.135936

67 M. Nagashima, T.S. D'Cruz, A.E. Danku, et al.Midkine-a is required for cell cycle progression of müller glia during neuronal regeneration in the vertebrate retina J Neurosci : Off J Soc Neurosci, 40 (6) (2020), pp. 1232-1247, 10.1523/JNEUROSCI.1675-19.2019

68 W.A. Campbell, A. Fritsch-Kelleher, I. Palazzo, et al.Midkine is neuroprotective and influences glial reactivity and the formation of Müller glia-derived progenitor cells in chick and mouse retinas Glia, 69 (6) (2021), pp. 1515-1539, 10.1002/glia.23976

69 C.M. Nelson, R.A. Gorsuch, T.J. Bailey, et al.Stat3 defines three populations of Muller glia and is required for initiating maximal muller glia proliferation in the regenerating zebrafish retina J Comp Neurol, 520 (18) (2012), pp. 4294-4311, 10.1002/cne.23213

70 L. Todd, N. Squires, L. Suarez, et al.Jak/Stat signaling regulates the proliferation and neurogenic potential of Muller glia-derived progenitor cells in the avian retina Sci Rep, 6 (2016), Article 35703, 10.1038/srep35703

71 W.M. Peterson, Q. Wang, R. Tzekova, et al.Ciliary neurotrophic factor and stress stimuli activate the JakSTAT pathway in retinal neurons and glia J Neurosci, 20 (11) (2000), pp. 4081-4090, 10.1523/JNEUROSCI.20-11-04081.2000

72 R. Rodriguez Viales, N. Diotel, M. Ferg, et al.The helix-loop-helix protein id1 controls stem cell proliferation during regenerative neurogenesis in the adult zebrafish telencephalon Stem Cell, 33 (3) (2015), pp. 892-903, 10.1002/stem.1883

73 L. Tang, C. Zhang, L. Lu, et al.Melatonin maintains inner blood-retinal barrier by regulating microglia via inhibition of PI3K/Akt/Stat3/NF-κB signaling pathways in experimental diabetic retinopathy Front Immunol, 13 (2022), Article 831660, 10.3389/fimmu.2022.831660

74 B.A. Westerman, C. Murre, C.B. OudejansThe cellular Pax-Hox-helix connection Biochim Biophys Acta, 1629 (1-3) (2003), pp. 1-7, 10.1016/j.bbaexp.2003.08.002

75 S.R. Viswanathan, G.Q. Daley, R.I. GregorySelective blockade of microRNA processing by Lin28 Science, 320 (5872) (2008), pp. 97-100, 10.1126/science.1154040

76 B. Xu, K. Zhang, Y. HuangLin28 modulates cell growth and associates with a subset of cell cycle regulator mRNAs in mouse embryonic stem cells RNA, 15 (3) (2009), pp. 357-361, 10.1261/rna.1368009

77 R. Ramachandran, B.V. Fausett, D. GoldmanAscl1a regulates Muller glia dedifferentiation and retinal regeneration through a Lin-28-dependent, let-7 microRNA signalling pathway Nat Cell Biol, 12 (11) (2010), pp. 1101-1107, 10.1038/ncb2115

78 R. Ramachandran, X.F. Zhao, D. GoldmanAscl1a/Dkk/beta-catenin signaling pathway is necessary and glycogen synthase kinase-3beta inhibition is sufficient for zebrafish retina regeneration Proc Natl Acad Sci U S A, 108 (38) (2011), pp. 15858-15863, 10.1073/pnas.1107220108

79 Y. Ueki, M.S. Wilken, K.E. Cox, et al.Transgenic expression of the proneural transcription factor Ascl1 in Muller glia stimulates retinal regeneration in young mice Proc Natl Acad Sci U S A, 112 (44) (2015), pp. 13717-13722, 10.1073/pnas.1510595112

80 J. Pollak, M.S. Wilken, Y. Ueki, et al.ASCL1 reprograms mouse Muller glia into neurogenic retinal progenitors Development, 140 (12) (2013), pp. 2619-2631, 10.1242/dev.091355

81 L. Todd, M.J. Hooper, A.K. Haugan, et al.Efficient stimulation of retinal regeneration from Müller glia in adult mice using combinations of proneural bHLH transcription factors Cell Rep, 37 (3) (2021), Article 109857, 10.1016/j.celrep.2021.109857

82 L. Todd, W. Jenkins, C. Finkbeiner, et al.Reprogramming Müller glia to regenerate ganglion-like cells in adult mouse retina with developmental transcription factors Sci Adv, 8 (47) (2022), Article eabq7219, 10.1126/sciadv.abq7219

83 M.L. Kaufman, N.B. Goodson, K.U. Park, et al.Initiation of Otx2 expression in the developing mouse retina requires a unique enhancer and either Ascl1 or Neurog2 activity Development (Cambridge, England), 148 (12) (2021), 10.1242/dev.199399

84 R. Lourenco, A.S. Brandao, J. Borbinha, et al.Yap regulates muller glia reprogramming in damaged zebrafish retinas Front Cell Dev Biol, 9 (2021), Article 667796, 10.3389/fcell.2021.667796

85 A. Hamon, D. Garcia-Garcia, D. Ail, et al.Linking YAP to muller glia quiescence exit in the degenerative retina Cell Rep, 27 (6) (2019), pp. 1712-1725 e6, 10.1016/j.celrep.2019.04.045

86 E.M. Rueda, B.M. Hall, M.C. Hill, et al.The hippo pathway blocks mammalian retinal muller glial cell reprogramming Cell Rep, 27 (6) (2019), pp. 1637-1649 e6, 10.1016/j.celrep.2019.04.047

87 R.A. Gorsuch, M. Lahne, C.E. Yarka, et al.Sox2 regulates Muller glia reprogramming and proliferation in the regenerating zebrafish retina via Lin28 and Ascl1a Exp Eye Res, 161 (2017), pp. 174-192, 10.1016/j.exer.2017.05.012

88 P. Sharma, S. Gupta, M. Chaudhary, et al.Oct4 mediates Muller glia reprogramming and cell cycle exit during retina regeneration in zebrafish Life Sci Alliance, 2 (5) (2019), 10.26508/lsa.201900548

89 S. Mitra, P. Sharma, S. Kaur, et al.Dual regulation of lin28a by Myc is necessary during zebrafish retina regeneration J Cell Biol, 218 (2) (2019), pp. 489-507, 10.1083/jcb.201802113

90 N. Kastan, K. Gnedeva, T. Alisch, et al.Small-molecule inhibition of Lats kinases may promote Yap-dependent proliferation in postmitotic mammalian tissues Nat Commun, 12 (1) (2021), p. 3100, 10.1038/s41467-021-23395-3

91 N.R. Kastan, S. Oak, R. Liang, et al.Development of an improved inhibitor of Lats kinases to promote regeneration of mammalian organs Proceed Nat Acad Sci USA, 119 (28) (2022), Article e2206113119, 10.1073/pnas.2206113119

92 Z. Zhang, H. Hou, S. Yu, et al.Inflammation-induced mammalian target of rapamycin signaling is essential for retina regeneration Glia, 68 (1) (2020), pp. 111-127, 10.1002/glia.23707

93 S. Gupta, P. Sharma, M. Chaudhary, et al.Pten associates with important gene regulatory network to fine-tune Müller glia-mediated zebrafish retina regeneration Glia, 71 (2) (2023), pp. 259-283, 10.1002/glia.24270

94 N. Kara, M.R. Kent, D. Didiano, et al.The miR-216a-dot1l regulatory Axis is necessary and sufficient for muller glia reprogramming during retina regeneration Cell Rep, 28 (8) (2019), pp. 2037-2047 e4, 10.1016/j.celrep.2019.07.061

95 D. Gallina, I. Palazzo, L. Steffenson, et al.Wnt/β-catenin-signaling and the formation of Müller glia-derived progenitors in the chick retina Develop Neurobiol, 76 (9) (2016), pp. 983-1002, 10.1002/dneu.22370

96 K. Song, Z. Lin, L. Cao, et al.Sox11b regulates the migration and fate determination of Müller glia-derived progenitors during retina regeneration in zebrafish Neural Regenerat Res, 18 (2) (2023), pp. 445-450, 10.4103/1673-5374.346550

97 W. Niu, T. Zang, Y. Zou, et al.In vivo reprogramming of astrocytes to neuroblasts in the adult brain Nat Cell Biol, 15 (10) (2013), pp. 1164-1175, 10.1038/ncb2843

98 S. Reverdatto, A. Prasad, J.L. Belrose, et al.Developmental and injury-induced changes in DNA methylation in regenerative versus non-regenerative regions of the vertebrate central nervous system BMC Genom, 23 (1) (2022), p. 2, 10.1186/s12864-021-08247-0

99 P. Reddy, S. Memczak, J.C. Izpisua BelmonteUnlocking tissue regenerative potential by epigenetic reprogramming Cell Stem Cell, 28 (1) (2021), pp. 5-7, 10.1016/j.stem.2020.12.006

100 C. Powell, F. Elsaeidi, D. GoldmanInjury-dependent Muller glia and ganglion cell reprogramming during tissue regeneration requires Apobec2a and Apobec2b J Neurosci, 32 (3) (2012), pp. 1096-1109, 10.1523/JNEUROSCI.5603-11.2012

101 C. Powell, A.R. Grant, E. Cornblath, et al.Analysis of DNA methylation reveals a partial reprogramming of the Muller glia genome during retina regeneration Proc Natl Acad Sci U S A, 110 (49) (2013), pp. 19814-19819, 10.1073/pnas.1312009110

102 L.I. Reyes-Aguirre, M. LamasOct4 methylation-mediated silencing as an epigenetic barrier preventing muller glia dedifferentiation in a murine model of retinal injury Front Neurosci, 10 (2016), p. 523, 10.3389/fnins.2016.00523

103 J. Xiao, X. Li, L. Chen, et al.Apobec1 promotes neurotoxicity-induced dedifferentiation of muller glial cells Neurochem Res, 42 (4) (2017), pp. 1151-1164, 10.1007/s11064-016-2151-2

104 I.V. Gregoretti, Y.M. Lee, H.V. GoodsonMolecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis J Mol Biol, 338 (1) (2004), pp. 17-31, 10.1016/j.jmb.2004.02.006

105 S. Mitra, P. Sharma, S. Kaur, et al.Histone deacetylase-mediated muller glia reprogramming through Her4.1-Lin28a Axis is essential for retina regeneration in zebrafish iScience, 7 (2018), pp. 68-84, 10.1016/j.isci.2018.08.008

106 A. Saha, S. Tiwari, S. Dharmarajan, et al.Class I histone deacetylases in retinal progenitors and differentiating ganglion cells Gene Expr Patterns, 30 (2018), pp. 37-48, 10.1016/j.gep.2018.08.007

107 W.A. Campbell, H.M. El-Hodiri, D. Torres, et al.Chromatin access regulates the formation of Müller glia-derived progenitor cells in the retina Glia, 71 (7) (2023), pp. 1729-1754, 10.1002/glia.24366

108 W.P. Kloosterman, R.H. PlasterkThe diverse functions of microRNAs in animal development and disease Dev Cell, 11 (4) (2006), pp. 441-450, 10.1016/j.devcel.2006.09.009

109 C. Melton, R.L. Judson, R. BlellochOpposing microRNA families regulate self-renewal in mouse embryonic stem cells Nature, 463 (7281) (2010), pp. 621-626, 10.1038/nature08725

110 K. Rajaram, R.L. Harding, T. Bailey, et al.Dynamic miRNA expression patterns during retinal regeneration in zebrafish: reduced dicer or miRNA expression suppresses proliferation of Muller glia-derived neuronal progenitor cells Dev Dynam, 243 (12) (2014), pp. 1591-1605, 10.1002/dvdy.24188

111 Y. Xie, J. Zhou, B. ChenCritical examination of Ptbp1-mediated glia-to-neuron conversion in the mouse retina Cell Rep, 39 (11) (2022), Article 110960, 10.1016/j.celrep.2022.110960

112 S.G. Wohl, T.A. RehmiR-124-9-9* potentiates Ascl1-induced reprogramming of cultured Muller glia Glia, 64 (5) (2016), pp. 743-762, 10.1002/glia.22958

113 H. Zhou, J. Su, X. Hu, et al.Glia-to-Neuron conversion by CRISPR-CasRx alleviates symptoms of neurological disease in mice Cell, 181 (3) (2020), pp. 590-603 e16, 10.1016/j.cell.2020.03.024

114 E.V. Makeyev, J. Zhang, M.A. Carrasco, et al.The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing Mol Cell, 27 (3) (2007), pp. 435-448, 10.1016/j.molcel.2007.07.015

115 J. Hu, H. Qian, Y. Xue, et al.PTB/nPTB: master regulators of neuronal fate in mammals Biophys Rep, 4 (4) (2018), pp. 204-214, 10.1007/s41048-018-0066-y

116 X. QiThe role of miR-9 during neuron differentiation of mouse retinal stem cells Artif Cells, Nanomed Biotechnol, 44 (8) (2016), pp. 1883-1890, 10.3109/21691401.2015.1111231

117 K. Rajaram, R.L. Harding, D.R. Hyde, et al.miR-203 regulates progenitor cell proliferation during adult zebrafish retina regeneration Dev Biol, 392 (2) (2014), pp. 393-403, 10.1016/j.ydbio.2014.05.005

118 Y. Baba, Y. Aihara, S. WatanabeMicroRNA-7a regulates Muller glia differentiation by attenuating Notch3 expression Exp Eye Res, 138 (2015), pp. 59-65, 10.1016/j.exer.2015.06.022

119 H.P. Ji, Y. Xiong, W.T. Song, et al.MicroRNA-28 potentially regulates the photoreceptor lineage commitment of Muller glia-derived progenitors Sci Rep, 7 (1) (2017), Article 11374, 10.1038/s41598-017-11112-4

120 A. Jacobi, N.M. Tran, W. Yan, et al.Overlapping transcriptional programs promote survival and axonal regeneration of injured retinal ganglion cells Neuron, 110 (16) (2022), 10.1016/j.neuron.2022.06.002 2625-2645.e7

121 L. Li, F. Fang, X. Feng, et al.Single-cell transcriptome analysis of regenerating RGCs reveals potent glaucoma neural repair genes Neuron, 110 (16) (2022), 10.1016/j.neuron.2022.06.022 2646-2663.e6

122 F. Tian, Y. Cheng, S. Zhou, et al.Core transcription programs controlling injury-induced neurodegeneration of retinal ganglion cells Neuron, 110 (16) (2022), 10.1016/j.neuron.2022.06.003 2607-2624.e8

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