Ezh2 maintains retinal progenitor proliferation, transcriptional integrity, and the timing of late differentiation

Developmental Biology

Volumn 403, Issue 2, 2015, Pages 128-138

  Zhang, Jianmin ^a   Taylor, Russell J ^b   La Torre, Anna ^b   Wilken, Matthew S ^b   Cox, Kristen E ^b   Reh, Thomas A ^b   Vetter, Monica L ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Histone modification; Neurogenesis; PRC2; Proliferation; Retina

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; HISTONE H3; HOX PROTEIN; PROTEIN H3K27ME3; RNA; TRANSCRIPTION FACTOR EZH2; TRANSCRIPTION FACTOR PAX6; UNCLASSIFIED DRUG; EZH2 PROTEIN, MOUSE; POLYCOMB REPRESSIVE COMPLEX 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DISRUPTION; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; EMBRYO; ENZYME ACTIVE SITE; GENE LOCUS; GLIA CELL; HISTONE MODIFICATION; HOX GENE; MOLECULAR DYNAMICS; MOUSE; MUELLER CELL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PHOTORECEPTOR; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; REGULATOR GENE; RETINA DEVELOPMENT; RETINA NERVE CELL; RNA SEQUENCE; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; CELL DIFFERENTIATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; METABOLISM; RETINA; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENE EXPRESSION REGULATION; MICE; POLYCOMB REPRESSIVE COMPLEX 2; RETINA; STEM CELLS; TRANSCRIPTION, GENETIC;

EID: 84931560384     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2015.05.010     Document Type: Article

References (50)

1. Aldiri I., Vetter M.L. PRC2 during vertebrate organogenesis: a complex in transition. Dev. Biol. 2012, 367:91-99.
2. Aldiri I., Moore K.B., Hutcheson D.A., Zhang J., Vetter M.L. Polycomb repressive complex PRC2 regulates Xenopus retina development downstream of Wnt/beta-catenin signaling. Development 2013, 140:2867-2878.
3. Bassett E.A., Wallace V.A. Cell fate determination in the vertebrate retina. Trends Neurosci. 2012, 35:565-573.
4. Boyer L.A., Plath K., Zeitlinger J., Brambrink T., Medeiros L.A., Lee T.I., Levine S.S., Wernig M., Tajonar A., Ray M.K., Bell G.W., Otte A.P., Vidal M., Gifford D.K., Young R.A., Jaenisch R. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006, 441:349-353.
5. Brockdorff N. Noncoding RNA and Polycomb recruitment. RNA 2013, 19:429-442.
6. Conerly M.L., MacQuarrie K.L., Fong A.P., Yao Z., Tapscott S.J. Polycomb-mediated repression during terminal differentiation: what don't you want to be when you grow up?. Genes Dev. 2011, 25:997-1003.
7. Delgado-Olguin P., Huang Y., Li X., Christodoulou D., Seidman C.E., Seidman J.G., Tarakhovsky A., Bruneau B.G. Epigenetic repression of cardiac progenitor gene expression by Ezh2 is required for postnatal cardiac homeostasis. Nat. Genet. 2012, 44:343-347.
8. Ezhkova E., Pasolli H.A., Parker J.S., Stokes N., Su I.H., Hannon G., Tarakhovsky A., Fuchs E. Ezh2 orchestrates gene expression for the stepwise differentiation of tissue-specific stem cells. Cell 2009, 136:1122-1135.
9. Fasano C.A., Phoenix T.N., Kokovay E., Lowry N., Elkabetz Y., Dimos J.T., Lemischka I.R., Studer L., Temple S. Bmi-1 cooperates with Foxg1 to maintain neural stem cell self-renewal in the forebrain. Genes Dev. 2009, 23:561-574.
10. Furuta Y., Lagutin O., Hogan B.L., Oliver G.C. Retina- and ventral forebrain-specific Cre recombinase activity in transgenic mice. Genesis 2000, 26:130-132.
11. He A., Ma Q., Cao J., von Gise A., Zhou P., Xie H., Zhang B., Hsing M., Christodoulou D.C., Cahan P., Daley G.Q., Kong S.W., Orkin S.H., Seidman C.E., Seidman J.G., Pu W.T. Polycomb repressive complex 2 regulates normal development of the mouse heart. Circ. Res. 2012, 110:406-415.
12. Hirabayashi Y., Gotoh Y. Epigenetic control of neural precursor cell fate during development. Nat. Rev. Neurosci. 2010, 11:377-388.
13. Hirabayashi Y., Suzki N., Tsuboi M., Endo T.A., Toyoda T., Shinga J., Koseki H., Vidal M., Gotoh Y. Polycomb limits the neurogenic competence of neural precursor cells to promote astrogenic fate transition. Neuron 2009, 63:600-613.
14. Hwang W.W., Salinas R.D., Siu J.J., Kelley K.W., Delgado R.N., Paredes M.F., Alvarez-Buylla A., Oldham M.C., Lim D.A. Distinct and separable roles for EZH2 in neurogenic astroglia. eLife 2014, 3:e02439.
15. Iida A., Iwagawa T., Baba Y., Satoh S., Mochizuki Y., Nakauchi H., Furukawa T., Koseki H., Murakami A., Watanabe S. Roles of histone H3K27 trimethylase Ezh2 in retinal proliferation and differentiation. Dev. Neurobiol. Epub ahead of print 2014, 10.1002/dneu.22261.
16. Juan A.H., Derfoul A., Feng X., Ryall J.G., Dell'Orso S., Pasut A., Zare H., Simone J.M., Rudnicki M.A., Sartorelli V. Polycomb EZH2 controls self-renewal and safeguards the transcriptional identity of skeletal muscle stem cells. Genes dev. 2011, 25:789-794.
17. Katoh K., Yamazaki R., Onishi A., Sanuki R., Furukawa T. G9a histone methyltransferase activity in retinal progenitors is essential for proper differentiation and survival of mouse retinal cells. J. Neurosci.: Off. J. Soc. Neurosci. 2012, 32:17658-17670.
18. La Torre A., Georgi S., Reh T.A. Conserved microRNA pathway regulates developmental timing of retinal neurogenesis. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E2362-E2370.
19. Laugesen A., Helin K. Chromatin repressive complexes in stem cells, development, and cancer. Cell Stem Cell 2014, 14:735-751.
20. Lee T.I., Jenner R.G., Boyer L.A., Guenther M.G., Levine S.S., Kumar R.M., Chevalier B., Johnstone S.E., Cole M.F., Isono K., Koseki H., Fuchikami T., Abe K., Murray H.L., Zucker J.P., Yuan B., Bell G.W., Herbolsheimer E., Hannett N.M., Sun K., Odom D.T., Otte A.P., Volkert T.L., Bartel D.P., Melton D.A., Gifford D.K., Jaenisch R., Young R.A. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 2006, 125:301-313.
21. Margueron R., Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature 2011, 469:343-349.
22. Margueron R., Li G., Sarma K., Blais A., Zavadil J., Woodcock C.L., Dynlacht B.D., Reinberg D. Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms. Mole. Cell 2008, 32:503-518.
23. Marquardt T., Ashery-Padan R., Andrejewski N., Scardigli R., Guillemot F., Gruss P. Pax6 is required for the multipotent state of retinal progenitor cells. Cell 2001, 105:43-55.
24. Meola N., Pizzo M., Alfano G., Surace E.M., Banfi S. The long noncoding RNA Vax2os1 controls the cell cycle progression of photoreceptor progenitors in the mouse retina. RNA 2012, 18:111-123.
25. Pasini D., Bracken A.P., Hansen J.B., Capillo M., Helin K. The polycomb group protein Suz12 is required for embryonic stem cell differentiation. Mol. Cell. Biol. 2007, 27:3769-3779.
26. Pereira J.D., Sansom S.N., Smith J., Dobenecker M.W., Tarakhovsky A., Livesey F.J. Ezh2, the histone methyltransferase of PRC2, regulates the balance between self-renewal and differentiation in the cerebral cortex. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:15957-15962.
27. Popov N., Gil J. Epigenetic regulation of the INK4b-ARF-INK4a locus: in sickness and in health. Epigenetics: Off. J. DNA Methylation Soc. 2010, 5:685-690.
28. Popova E.Y., Barnstable C.J., Zhang S.S. Cell type-specific epigenetic signatures accompany late stages of mouse retina development. Adv. Exp. Med. Biol. 2014, 801:3-8.
29. Popova E.Y., Xu X., DeWan A.T., Salzberg A.C., Berg A., Hoh J., Zhang S.S., Barnstable C.J. Stage and gene specific signatures defined by histones H3K4me2 and H3K27me3 accompany mammalian retina maturation in vivo. PloS One 2012, 7:e46867.
30. Price J.D., Park K.Y., Chen J., Salinas R.D., Cho M.J., Kriegstein A.R., Lim D.A. The Ink4a/Arf locus is a barrier to direct neuronal transdifferentiation. J. Neurosci.: Off. J. Soc. Neurosci. 2014, 34:12560-12567.
31. Rapicavoli N.A., Poth E.M., Blackshaw S. The long noncoding RNA RNCR2 directs mouse retinal cell specification. BMC Dev. Biol. 2010, 10:49.
32. Rapicavoli N.A., Poth E.M., Zhu H., Blackshaw S. The long noncoding RNA Six3OS acts in trans to regulate retinal development by modulating Six3 activity. Neural Dev. 2011, 6:32.
33. Rhee K.D., Yu J., Zhao C.Y., Fan G., Yang X.J. Dnmt1-dependent DNA methylation is essential for photoreceptor terminal differentiation and retinal neuron survival. Cell Death Dis. 2012, 3:e427.
34. Rinn J.L., Kertesz M., Wang J.K., Squazzo S.L., Xu X., Brugmann S.A., Goodnough L.H., Helms J.A., Farnham P.J., Segal E., Chang H.Y. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 2007, 129:1311-1323.
35. Schuettengruber B., Chourrout D., Vervoort M., Leblanc B., Cavalli G. Genome regulation by polycomb and trithorax proteins. Cell 2007, 128:735-745.
36. Schwarz D., Varum S., Zemke M., Scholer A., Baggiolini A., Draganova K., Koseki H., Schubeler D., Sommer L. Ezh2 is required for neural crest-derived cartilage and bone formation. Development 2014, 141:867-877.
37. Shen X., Liu Y., Hsu Y.J., Fujiwara Y., Kim J., Mao X., Yuan G.C., Orkin S.H. EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Mol. Cell 2008, 32:491-502.
38. Sher F., Rossler R., Brouwer N., Balasubramaniyan V., Boddeke E., Copray S. Differentiation of neural stem cells into oligodendrocytes: involvement of the polycomb group protein Ezh2. Stem Cells 2008, 26:2875-2883.
39. Snitow M.E., Li S., Morley M.P., Rathi K., Lu M.M., Kadzik R.S., Stewart K.M., Morrisey E.E. Ezh2 represses the basal cell lineage during lung endoderm development. Development 2015, 142:108-117.
40. Sparmann A., van Lohuizen M. Polycomb silencers control cell fate, development and cancer. Nat. Rev. 2006, 6:846-856.
41. Srinivas S., Watanabe T., Lin C.S., William C.M., Tanabe Y., Jessell T.M., Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 2001, 1:4.
42. Su I.H., Basavaraj A., Krutchinsky A.N., Hobert O., Ullrich A., Chait B.T., Tarakhovsky A. Ezh2 controls B cell development through histone H3 methylation and Igh rearrangement. Nat. Immunol. 2003, 4:124-131.
43. Testa G. The time of timing: how Polycomb proteins regulate neurogenesis. BioEssays: News Rev. Mol. Cell. Dev. Biol. 2011, 33:519-528.
44. Voigt P., Tee W.W., Reinberg D. A double take on bivalent promoters. Genes Dev. 2013, 27:1318-1338.
45. Weishaupt H., Sigvardsson M., Attema J.L. Epigenetic chromatin states uniquely define the developmental plasticity of murine hematopoietic stem cells. Blood 2010, 115:247-256.
46. Wilczynska K.M., Singh S.K., Adams B., Bryan L., Rao R.R., Valerie K., Wright S., Griswold-Prenner I., Kordula T. Nuclear factor I isoforms regulate gene expression during the differentiation of human neural progenitors to astrocytes. Stem Cells 2009, 27:1173-1181.
47. Woodhouse S., Pugazhendhi D., Brien P., Pell J.M. Ezh2 maintains a key phase of muscle satellite cell expansion but does not regulate terminal differentiation. J. Cell Sci. 2013, 126:565-579.
48. Zeitlinger J., Stark A. Developmental gene regulation in the era of genomics. Dev. Biol. 2010, 339:230-239.
49. Zencak D., Lingbeek M., Kostic C., Tekaya M., Tanger E., Hornfeld D., Jaquet M., Munier F.L., Schorderet D.F., van Lohuizen M., Arsenijevic Y. Bmi1 loss produces an increase in astroglial cells and a decrease in neural stem cell population and proliferation. J. Neurosci.: Off. J. Soc. Neurosci. 2005, 25:5774-5783.
50. Zhang J., Fuhrmann S., Vetter M.L. A nonautonomous role for retinal frizzled-5 in regulating hyaloid vitreous vasculature development. Investig. Ophthalmol. Vis. Sci. 2008, 49:5561-5567.