Histone modifications controlling native and induced neural stem cell identity

Current Opinion in Genetics and Development

Volumn 34, Issue , 2015, Pages 95-101

  Broccoli, Vania ^a,b   Colasante, Gaia ^a   Sessa, Alessandro ^a   Rubio, Alicia ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; HISTONE ACETYLTRANSFERASE; HISTONE H3; POLYCOMB REPRESSIVE COMPLEX 2; TRANSCRIPTION FACTOR; CHROMATIN;

CELL COMMUNICATION; CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL LINEAGE; CELL METABOLISM; CELL TRANSFORMATION; EPIGENETICS; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORK; HISTONE ACETYLATION; HISTONE MODIFICATION; HUMAN; INDUCED NEURAL STEM CELL; NEURAL STEM CELL; NONHUMAN; NUCLEAR REPROGRAMMING; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SOMATIC CELL; ANIMAL; CHROMATIN; CYTOLOGY; DROSOPHILA MELANOGASTER; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTONE CODE; METABOLISM; NERVE CELL; PLURIPOTENT STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CHROMATIN; DROSOPHILA MELANOGASTER; EPIGENESIS, GENETIC; GENE REGULATORY NETWORKS; HISTONE CODE; NEURAL STEM CELLS; NEURONS; PLURIPOTENT STEM CELLS;

EID: 84944406680     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2015.08.003     Document Type: Review

References (62)

1. Bernstein E., Duncan E.M., Masui O., Gil J., Heard E., Allis C.D. Mouse polycomb proteins bind differentially to methylated histone H3 and RNA and are enriched in facultative heterochromatin. Mol Cell Biol 2006, 26:2560-2569.
2. Hirabayashi Y., Gotoh Y. Epigenetic control of neural precursor cell fate during development. Nat Rev Neurosci 2010, 11:377-388.
3. Parsons X.H. Human stem cell derivatives retain more open epigenomic landscape when derived from pluripotent cells than from tissues. J Regen Med 2013, 1.
4. Han D.W., Tapia N., Hermann A., Hemmer K., Hoing S., Arauzo-Bravo M.J., Zaehres H., Wu G., Frank S., Moritz S., et al. Direct reprogramming of fibroblasts into neural stem cells by defined factors. Cell Stem Cell 2012, 10:465-472.
5. Kim J., Efe J.A., Zhu S., Talantova M., Yuan X., Wang S., Lipton S.A., Zhang K., Ding S. Direct reprogramming of mouse fibroblasts to neural progenitors. Proc Natl Acad Sci U S A 2011, 108:7838-7843.
6. Lu J., Liu H., Huang C.T., Chen H., Du Z., Liu Y., Sherafat M.A., Zhang S.C. Generation of integration-free and region-specific neural progenitors from primate fibroblasts. Cell Rep 2013, 3:1580-1591.
7. Lujan E., Chanda S., Ahlenius H., Sudhof T.C., Wernig M. Direct conversion of mouse fibroblasts to self-renewing, tripotent neural precursor cells. Proc Natl Acad Sci U S A 2012, 109:2527-2532.
8. Matsui T., Takano M., Yoshida K., Ono S., Fujisaki C., Matsuzaki Y., Toyama Y., Nakamura M., Okano H., Akamatsu W. Neural stem cells directly differentiated from partially reprogrammed fibroblasts rapidly acquire gliogenic competency. Stem Cells 2012, 30:1109-1119.
9. Ring K.L., Tong L.M., Balestra M.E., Javier R., Andrews-Zwilling Y., Li G., Walker D., Zhang W.R., Kreitzer A.C., Huang Y. Direct reprogramming of mouse and human fibroblasts into multipotent neural stem cells with a single factor. Cell Stem Cell 2012, 11:100-109.
10. Thier M., Worsdorfer P., Lakes Y.B., Gorris R., Herms S., Opitz T., Seiferling D., Quandel T., Hoffmann P., Nothen M.M., et al. Direct conversion of fibroblasts into stably expandable neural stem cells. Cell Stem Cell 2012, 10:473-479.
11. Rada-Iglesias A., Bajpai R., Swigut T., Brugmann S.A., Flynn R.A., Wysocka J. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 2011, 470:279-283.
12. Poletti V., Delli Carri A., Malagoli Tagliazucchi G., Faedo A., Petiti L., Mazza E.M., Peano C., De Bellis G., Bicciato S., Miccio A., et al. Genome-wide definition of promoter and enhancer usage during neural induction of human embryonic stem cells. PLoS One 2015, 10:e0126590.
13. Burgold T., Spreafico F., De Santa F., Totaro M.G., Prosperini E., Natoli G., Testa G. The histone H3 lysine 27-specific demethylase Jmjd3 is required for neural commitment. PLoS One 2008, 3:e3034.
14. Mikkelsen T.S., Ku M., Jaffe D.B., Issac B., Lieberman E., Giannoukos G., Alvarez P., Brockman W., Kim T.K., Koche R.P., et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007, 448:553-560.
15. Huang C., Chen J., Zhang T., Zhu Q., Xiang Y., Chen C.D., Jing N. The dual histone demethylase KDM7A promotes neural induction in early chick embryos. Dev Dyn 2010, 239:3350-3357.
16. Tsukada Y., Ishitani T., Nakayama K.I. KDM7 is a dual demethylase for histone H3 Lys 9 and Lys 27 and functions in brain development. Genes Dev 2010, 24:432-437.
17. Huang C., Xiang Y., Wang Y., Li X., Xu L., Zhu Z., Zhang T., Zhu Q., Zhang K., Jing N., et al. Dual-specificity histone demethylase KIAA1718 (KDM7A) regulates neural differentiation through FGF4. Cell Res 2010, 20:154-165.
18. Golebiewska A., Atkinson S.P., Lako M., Armstrong L. Epigenetic landscaping during hESC differentiation to neural cells. Stem Cells 2009, 27:1298-1308.
19. Ziller M.J., Edri R., Yaffe Y., Donaghey J., Pop R., Mallard W., Issner R., Gifford C.A., Goren A., Xing J., et al. Dissecting neural differentiation regulatory networks through epigenetic footprinting. Nature 2015, 518:355-359.
20. Cheutin T., Cavalli G. Polycomb silencing: from linear chromatin domains to 3D chromosome folding. Curr Opin Genet Dev 2014, 25:30-37.
21. 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. Mol Cell 2008, 32:503-518.
22. 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.
23. 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.
24. Hahn M.A., Qiu R., Wu X., Li A.X., Zhang H., Wang J., Jui J., Jin S.G., Jiang Y., Pfeifer G.P., et al. Dynamics of 5-hydroxymethylcytosine and chromatin marks in Mammalian neurogenesis. Cell Rep 2013, 3:291-300.
25. Piper M., Barry G., Harvey T.J., McLeay R., Smith A.G., Harris L., Mason S., Stringer B.W., Day B.W., Wray N.R., et al. NFIB-mediated repression of the epigenetic factor Ezh2 regulates cortical development. J Neurosci 2014, 34:2921-2930.
26. Akizu N., Estaras C., Guerrero L., Marti E., Martinez-Balbas M.A. H3K27me3 regulates BMP activity in developing spinal cord. Development 2010, 137:2915-2925.
27. Estaras C., Akizu N., Garcia A., Beltran S., de la Cruz X., Martinez-Balbas M.A. Genome-wide analysis reveals that Smad3 and JMJD3 HDM co-activate the neural developmental program. Development 2012, 139:2681-2691.
28. 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 2014.
29. Park D.H., Hong S.J., Salinas R.D., Liu S.J., Sun S.W., Sgualdino J., Testa G., Matzuk M.M., Iwamori N., Lim D.A. Activation of neuronal gene expression by the JMJD3 demethylase is required for postnatal and adult brain neurogenesis. Cell Rep 2014, 8:1290-1299.
30. Aloia L., Di Stefano B., Sessa A., Morey L., Santanach A., Gutierrez A., Cozzuto L., Benitah S.A., Graf T., Broccoli V., et al. Zrf1 is required to establish and maintain neural progenitor identity. Genes Dev 2014, 28:182-197.
31. Aloia L., Gutierrez A., Caballero J.M., Di Croce L. Direct interaction between Id1 and Zrf1 controls neural differentiation of embryonic stem cells. EMBO Rep 2015, 16:63-70.
32. Richly H., Rocha-Viegas L., Ribeiro J.D., Demajo S., Gundem G., Lopez-Bigas N., Nakagawa T., Rospert S., Ito T., Di Croce L. Transcriptional activation of polycomb-repressed genes by ZRF1. Nature 2010, 468:1124-1128.
33. Gao Z., Zhang J., Bonasio R., Strino F., Sawai A., Parisi F., Kluger Y., Reinberg D. PCGF homologs, CBX proteins, and RYBP define functionally distinct PRC1 family complexes. Mol Cell 2012, 45:344-356.
34. Gao Z., Lee P., Stafford J.M., von Schimmelmann M., Schaefer A., Reinberg D. An AUTS2-Polycomb complex activates gene expression in the CNS. Nature 2014, 516:349-354.
35. Lilja T., Heldring N., Hermanson O. Like a rolling histone: epigenetic regulation of neural stem cells and brain development by factors controlling histone acetylation and methylation. Biochim Biophys Acta 2013, 1830:2354-2360.
36. Verdin E., Ott M. 50 years of protein acetylation: from gene regulation to epigenetics, metabolism and beyond. Nat Rev Mol Cell Biol 2015, 16:258-264.
37. Iyer N.G., Ozdag H., Caldas C. p300/CBP and cancer. Oncogene 2004, 23:4225-4231.
38. Tanaka Y., Naruse I., Hongo T., Xu M., Nakahata T., Maekawa T., Ishii S. Extensive brain hemorrhage and embryonic lethality in a mouse null mutant of CREB-binding protein. Mech Dev 2000, 95:133-145.
39. Yao T.P., Oh S.P., Fuchs M., Zhou N.D., Ch'ng L.E., Newsome D., Bronson R.T., Li E., Livingston D.M., Eckner R. Gene dosage-dependent embryonic development and proliferation defects in mice lacking the transcriptional integrator p300. Cell 1998, 93:361-372.
40. Wang J., Weaver I.C., Gauthier-Fisher A., Wang H., He L., Yeomans J., Wondisford F., Kaplan D.R., Miller F.D. CBP histone acetyltransferase activity regulates embryonic neural differentiation in the normal and Rubinstein-Taybi syndrome brain. Dev Cell 2010, 18:114-125.
41. Liu P., Dou X., Liu C., Wang L., Xing C., Peng G., Chen J., Yu F., Qiao Y., Song L., et al. Histone deacetylation promotes mouse neural induction by restricting Nodal-dependent mesendoderm fate. Nat Commun 2015, 6:6830.
42. Gallagher D., Voronova A., Zander M.A., Cancino G.I., Bramall A., Krause M.P., Abad C., Tekin M., Neilsen P.M., Callen D.F., et al. Ankrd11 is a chromatin regulator involved in autism that is essential for neural development. Dev Cell 2015, 32:31-42.
43. Lo-Castro A., Brancati F., Digilio M.C., Garaci F.G., Bollero P., Alfieri P., Curatolo P. Neurobehavioral phenotype observed in KBG syndrome caused by ANKRD11 mutations. Am J Med Genet B Neuropsychiatr Genet 2013, 162B:17-23.
44. Marshall C.R., Noor A., Vincent J.B., Lionel A.C., Feuk L., Skaug J., Shago M., Moessner R., Pinto D., Ren Y., et al. Structural variation of chromosomes in autism spectrum disorder. Am J Hum Genet 2008, 82:477-488.
45. Sirmaci A., Spiliopoulos M., Brancati F., Powell E., Duman D., Abrams A., Bademci G., Agolini E., Guo S., Konuk B., et al. Mutations in ANKRD11 cause KBG syndrome, characterized by intellectual disability, skeletal malformations, and macrodontia. Am J Hum Genet 2011, 89:289-294.
46. Yang J., Tang Y., Liu H., Guo F., Ni J., Le W. Suppression of histone deacetylation promotes the differentiation of human pluripotent stem cells towards neural progenitor cells. BMC Biol 2014, 12:95.
47. Keramari M., Razavi J., Ingman K.A., Patsch C., Edenhofer F., Ward C.M., Kimber S.J. Sox2 is essential for formation of trophectoderm in the preimplantation embryo. PLoS One 2010, 5:e13952.
48. Sarkar P., Randall S.M., Collier T.S., Nero A., Russell T.A., Muddiman D.C., Rao B.M. Activin/nodal signaling switches the terminal fate of human embryonic stem cell-derived trophoblasts. J Biol Chem 2015, 290:8834-8848.
49. Wang Z., Oron E., Nelson B., Razis S., Ivanova N. Distinct lineage specification roles for NANOG, OCT4, and SOX2 in human embryonic stem cells. Cell Stem Cell 2012, 10:440-454.
50. Lodato M.A., Ng C.W., Wamstad J.A., Cheng A.W., Thai K.K., Fraenkel E., Jaenisch R., Boyer L.A. SOX2 co-occupies distal enhancer elements with distinct POU factors in ESCs and NPCs to specify cell state. PLoS Genet 2013, 9:e1003288.
51. Soufi A., Garcia M.F., Jaroszewicz A., Osman N., Pellegrini M., Zaret K.S. Pioneer transcription factors target partial DNA motifs on nucleosomes to initiate reprogramming. Cell 2015, 161:555-568.
52. Bergsland M., Ramskold D., Zaouter C., Klum S., Sandberg R., Muhr J. Sequentially acting Sox transcription factors in neural lineage development. Genes Dev 2011, 25:2453-2464.
53. Yu K.R., Shin J.H., Kim J.J., Koog M.G., Lee J.Y., Choi S.W., Kim H.S., Seo Y., Lee S., Shin T.H., et al. Rapid and efficient direct conversion of human adult somatic cells into neural stem cells by HMGA2/let-7b. Cell Rep 2015, 10:441-452.
54. Yaqubi M., Mohammadnia A., Fallahi H. Predicting involvement of polycomb repressive complex 2 in direct conversion of mouse fibroblasts into induced neural stem cells. Stem Cell Res Ther 2015, 6:42.
55. Ding X., Wang X., Sontag S., Qin J., Wanek P., Lin Q., Zenke M. The polycomb protein Ezh2 impacts on induced pluripotent stem cell generation. Stem Cells Dev 2014, 23:931-940.
56. Sher F., Boddeke E., Copray S. Ezh2 expression in astrocytes induces their dedifferentiation toward neural stem cells. Cell Reprogram 2011, 13:1-6.
57. Hansson J., Rafiee M.R., Reiland S., Polo J.M., Gehring J., Okawa S., Huber W., Hochedlinger K., Krijgsveld J. Highly coordinated proteome dynamics during reprogramming of somatic cells to pluripotency. Cell Rep 2012, 2:1579-1592.
58. Polo J.M., Anderssen E., Walsh R.M., Schwarz B.A., Nefzger C.M., Lim S.M., Borkent M., Apostolou E., Alaei S., Cloutier J., et al. A molecular roadmap of reprogramming somatic cells into iPS cells. Cell 2012, 151:1617-1632.
59. Lister R., Mukamel E.A., Nery J.R., Urich M., Puddifoot C.A., Johnson N.D., Lucero J., Huang Y., Dwork A.J., Schultz M.D., et al. Global epigenomic reconfiguration during mammalian brain development. Science 2013, 341:1237905.
60. Xie W., Schultz M.D., Lister R., Hou Z., Rajagopal N., Ray P., Whitaker J.W., Tian S., Hawkins R.D., Leung D., et al. Epigenomic analysis of multilineage differentiation of human embryonic stem cells. Cell 2013, 153:1134-1148.
61. Bar-Nur O., Verheul C., Sommer A.G., Brumbaugh J., Schwarz B.A., Lipchina I., Huebner A.J., Mostoslavsky G., Hochedlinger K. Lineage conversion induced by pluripotency factors involves transient passage through an iPSC stage. Nat Biotechnol 2015, 33:761-768.
62. Maza I., Caspi I., Zviran A., Chomsky E., Rais Y., Viukov S., Geula S., Buenrostro J.D., Weinberger L., Krupalnik V., et al. Transient acquisition of pluripotency during somatic cell transdifferentiation with iPSC reprogramming factors. Nat Biotechnol 2015, 33:769-774.