Histone variants and cellular plasticity

Trends in Genetics

Volumn 31, Issue 9, 2015, Pages 516-527

  Santoro, Stephen W ^a   Dulac, Catherine ^b  

^a UNIVERSITY OF WYOMING   (United States)

^b HARVARD UNIVERSITY   (United States)

Author keywords

Brain; Cellular plasticity; Development; Epigenetics; Histone variants; Neuron

Indexed keywords

DEOXYRIBONUCLEASE I; HISTONE; HISTONE H2A; HISTONE H3; OCTAMER TRANSCRIPTION FACTOR 4; CHROMATIN; MUTANT PROTEIN;

BLASTOCYST; BRAIN TUMOR; CELL DIFFERENTIATION; CHROMATIN; CHROMATIN STRUCTURE; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; ENZYME ACTIVITY; GENE CONTROL; GENE EXPRESSION; GENETIC VARIABILITY; HUMAN; IMMUNOFLUORESCENCE; MEMORY; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOSOME; OOCYTE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN LOCALIZATION; REVIEW; SENSORY NERVE CELL; TETRAHYMENA THERMOPHILA; TISSUE DIFFERENTIATION; UPREGULATION; ADULT; ANIMAL; CELL PLASTICITY; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENETIC EPIGENESIS; GENETIC VARIATION; GENETICS; METABOLISM; PHYSIOLOGY;

ADULT; ANIMALS; CELL PLASTICITY; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; EPIGENESIS, GENETIC; GENETIC VARIATION; HISTONES; HUMANS; MUTANT PROTEINS;

EID: 84940895327     PISSN: 01689525     EISSN: 13624555     Source Type: Journal    
DOI: 10.1016/j.tig.2015.07.005     Document Type: Review

References (114)

1. Marzluff W.F., et al. Two chemically and metabolically distinct forms of calf thymus histone F3. J. Biol. Chem. 1972, 247:2026-2033.
2. Marzluff W.F., et al. The human and mouse replication-dependent histone genes. Genomics 2002, 80:487-498.
3. Talbert P.B., et al. A unified phylogeny-based nomenclature for histone variants. Epigenet. Chromatin 2012, 5:7.
4. Marzluff W.F., et al. Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nat. Rev. Genet. 2008, 9:843-854.
5. Burgess R.J., Zhang Z. Histone chaperones in nucleosome assembly and human disease. Nat. Struct. Mol. Biol. 2013, 20:14-22.
6. Yuan J., et al. Focus on histone variant H2AX: to be or not to be. FEBS Lett. 2010, 584:3717-3724.
7. Montellier E., et al. Chromatin-to-nucleoprotamine transition is controlled by the histone H2B variant TH2B. Genes Dev. 2013, 27:1680-1692.
8. De Rop V., et al. CENP-A: the key player behind centromere identity, propagation, and kinetochore assembly. Chromosoma 2012, 121:527-538.
9. Huang H., et al. Quantitative proteomic analysis of histone modifications. Chem. Rev. 2015, 115:2376-2418.
10. Campos E.I., Reinberg D. Histones: annotating chromatin. Annu. Rev. Genet. 2009, 43:559-599.
11. Ausio J. Histone variants - the structure behind the function. Brief. Funct. Genomics Proteomics 2006, 5:228-243.
12. Hake S.B., et al. Serine 31 phosphorylation of histone variant H3.3 is specific to regions bordering centromeres in metaphase chromosomes. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:6344-6349.
13. Elsasser S.J., et al. DAXX envelops a histone H3.3-H4 dimer for H3.3-specific recognition. Nature 2012, 491:560-565.
14. Wen H., et al. ZMYND11 links histone H3.3K36me3 to transcription elongation and tumour suppression. Nature 2014, 508:263-268.
15. Akiyama T., et al. Dynamic replacement of histone H3 variants reprograms epigenetic marks in early mouse embryos. PLoS Genet. 2011, 7:e1002279.
16. Britton L.M., et al. Breaking the histone code with quantitative mass spectrometry. Expert Rev. Proteomics 2011, 8:631-643.
17. Zentner G.E., Henikoff S. High-resolution digital profiling of the epigenome. Nat. Rev. Genet. 2014, 15:814-827.
18. Pehrson J.R., et al. Mice without macroH2A histone variants. Mol. Cell. Biol. 2014, 34:4523-4533.
19. Tang M.C., et al. Contribution of the two genes encoding histone variant h3.3 to viability and fertility in mice. PLoS Genet. 2015, 11:e1004964.
20. Banaszynski L.A., et al. Histone variants in metazoan development. Dev. Cell 2010, 19:662-674.
21. Sanchez Alvarado A., Yamanaka S. Rethinking differentiation: stem cells, regeneration, and plasticity. Cell 2014, 157:110-119.
22. Dulac C. Brain function and chromatin plasticity. Nature 2010, 465:728-735.
23. West A.E., Greenberg M.E. Neuronal activity-regulated gene transcription in synapse development and cognitive function. Cold Spring Harb. Perspect. Biol. 2011, 3:a005744.
24. Schrode N., et al. Anatomy of a blastocyst: cell behaviors driving cell fate choice and morphogenesis in the early mouse embryo. Genesis 2013, 51:219-233.
25. Rojas-Rios P., Gonzalez-Reyes A. Concise review: the plasticity of stem cell niches: a general property behind tissue homeostasis and repair. Stem Cells 2014, 32:852-859.
26. Hemberger M., et al. Epigenetic dynamics of stem cells and cell lineage commitment: digging Waddington's canal. Nat. Rev. Mol. Cell Biol. 2009, 10:526-537.
27. Trostle-Weige P.K., et al. Isolation and characterization of TH2A, a germ cell-specific variant of histone 2A in rat testis. J. Biol. Chem. 1982, 257:5560-5567.
28. Shires A., et al. A cysteine-containing H2B-like histone found in mature mammalian testis. J. Biol. Chem. 1976, 251:4155-4158.
29. Shinagawa T., et al. Histone variants enriched in oocytes enhance reprogramming to induced pluripotent stem cells. Cell Stem Cell 2014, 14:217-227.
30. Gaspar-Maia A., et al. Open chromatin in pluripotency and reprogramming. Nat. Rev. Mol. Cell Biol. 2011, 12:36-47.
31. Allis C.D., et al. Histone variants specific to the transcriptionally active, amitotically dividing macronucleus of the unicellular eucaryote, Tetrahymena thermophila. Cell 1980, 20:609-617.
32. Talbert P.B., Henikoff S. Histone variants - ancient wrap artists of the epigenome. Nat. Rev. Mol. Cell Biol. 2010, 11:264-275.
33. Gaspar-Maia A., et al. MacroH2A histone variants act as a barrier upon reprogramming towards pluripotency. Nat. Commun. 2013, 4:1565.
34. Hu G., et al. H2A.Z. facilitates access of active and repressive complexes to chromatin in embryonic stem cell self-renewal and differentiation. Cell Stem Cell 2013, 12:180-192.
35. Creyghton M.P., et al. H2AZ is enriched at polycomb complex target genes in ES cells and is necessary for lineage commitment. Cell 2008, 135:649-661.
36. Li Z., et al. Foxa2 and H2A.Z. mediate nucleosome depletion during embryonic stem cell differentiation. Cell 2012, 151:1608-1616.
37. Ku M., et al. H2A.Z. landscapes and dual modifications in pluripotent and multipotent stem cells underlie complex genome regulatory functions. Genome Biol. 2012, 13:R85.
38. Voigt P., et al. A double take on bivalent promoters. Genes Dev. 2013, 27:1318-1338.
39. Nichols J., et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998, 95:379-391.
40. Amat R., Gudas L.J. RARgamma is required for correct deposition and removal of Suz12 and H2A.Z. in embryonic stem cells. J. Cell. Physiol. 2011, 226:293-298.
41. Li G., Reinberg D. Chromatin higher-order structures and gene regulation. Curr. Opin. Genet. Dev. 2011, 21:175-186.
42. Suto R.K., et al. Crystal structure of a nucleosome core particle containing the variant histone H2A.Z. Nat. Struct. Biol. 2000, 7:1121-1124.
43. Bonisch C., Hake S.B. Histone H2A variants in nucleosomes and chromatin: more or less stable?. Nucleic Acids Res. 2012, 40:10719-10741.
44. Subramanian V., et al. H2A.Z. acidic patch couples chromatin dynamics to regulation of gene expression programs during ESC differentiation. PLoS Genet. 2013, 9:e1003725.
45. Soboleva T.A., et al. Histone variants at the transcription start-site. Trends Genet. 2014, 30:199-209.
46. Zlatanova J., Thakar A. H2A.Z: view from the top. Structure 2008, 16:166-179.
47. Weber C.M., et al. H2A.Z. nucleosomes enriched over active genes are homotypic. Nat. Struct. Mol. Biol. 2010, 17:1500-1507.
48. Weber C.M., Henikoff S. Histone variants: dynamic punctuation in transcription. Genes Dev. 2014, 28:672-682.
49. Nekrasov M., et al. Histone H2A.Z. inheritance during the cell cycle and its impact on promoter organization and dynamics. Nat. Struct. Mol. Biol. 2012, 19:1076-1083.
50. Jin C., et al. H3.3/H2A.Z. double variant-containing nucleosomes mark 'nucleosome-free regions' of active promoters and other regulatory regions. Nat. Genet. 2009, 41:941-945.
51. Thambirajah A.A., et al. New developments in post-translational modifications and functions of histone H2A variants. Biochem. Cell Biol. 2009, 87:7-17.
52. Franklin S.G., Zweidler A. Non-allelic variants of histones 2a, 2b and 3 in mammals. Nature 1977, 266:273-275.
53. Filipescu D., et al. Histone H3 variants and their chaperones during development and disease: contributing to epigenetic control. Annu. Rev. Cell Dev. Biol. 2014, 30:615-646.
54. Wen D., et al. Histone variant H3.3 is an essential maternal factor for oocyte reprogramming. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:7325-7330.
55. Szenker E., et al. A developmental requirement for HIRA-dependent H3.3 deposition revealed at gastrulation in Xenopus. Cell Rep. 2012, 1:730-740.
56. Couldrey C., et al. A retroviral gene trap insertion into the histone 3.3A gene causes partial neonatal lethality, stunted growth, neuromuscular deficits and male sub-fertility in transgenic mice. Hum. Mol. Genet. 1999, 8:2489-2495.
57. Bush K.M., et al. Endogenous mammalian histone H3.3 exhibits chromatin-related functions during development. Epigenet. Chromatin 2013, 6:7.
58. Lin C.J., et al. Histone variant H3.3 maintains a decondensed chromatin state essential for mouse preimplantation development. Development 2013, 140:3624-3634.
59. Bell O., et al. Localized H3K36 methylation states define histone H4K16 acetylation during transcriptional elongation in Drosophila. EMBO J. 2007, 26:4974-4984.
60. Li X., et al. The histone acetyltransferase MOF is a key regulator of the embryonic stem cell core transcriptional network. Cell Stem Cell 2012, 11:163-178.
61. Goldberg A.D., et al. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 2010, 140:678-691.
62. Banaszynski L.A., et al. Hira-dependent histone H3.3 deposition facilitates PRC2 recruitment at developmental loci in ES cells. Cell 2013, 155:107-120.
63. Elsasser S.J., et al. Histone H3.3 is required for endogenous retroviral element silencing in embryonic stem cells. Nature 2015, 522:240-244.
64. Jullien J., et al. HIRA dependent H3.3 deposition is required for transcriptional reprogramming following nuclear transfer to Xenopus oocytes. Epigenet. Chromatin 2012, 5:17.
65. Celeste A., et al. Genomic instability in mice lacking histone H2AX. Science 2002, 296:922-927.
66. Wu T., et al. Histone variant H2A.X. deposition pattern serves as a functional epigenetic mark for distinguishing the developmental potentials of iPSCs. Cell Stem Cell 2014, 15:281-294.
67. Buganim Y., et al. The developmental potential of iPSCs is greatly influenced by reprogramming factor selection. Cell Stem Cell 2014, 15:295-309.
68. Pehrson J.R., Fried V.A. MacroH2A, a core histone containing a large nonhistone region. Science 1992, 257:1398-1400.
69. Costanzi C., Pehrson J.R. MACROH2A2, a new member of the MARCOH2A core histone family. J. Biol. Chem. 2001, 276:21776-21784.
70. Buschbeck M., et al. The histone variant macroH2A is an epigenetic regulator of key developmental genes. Nat. Struct. Mol. Biol. 2009, 16:1074-1079.
71. Buschbeck M., Di Croce L. Approaching the molecular and physiological function of macroH2A variants. Epigenetics 2010, 5:118-123.
72. Pasque V., et al. Histone variant macroH2A marks embryonic differentiation in vivo and acts as an epigenetic barrier to induced pluripotency. J. Cell Sci. 2012, 125:6094-6104.
73. Barrero M.J., et al. Macrohistone variants preserve cell identity by preventing the gain of H3K4me2 during reprogramming to pluripotency. Cell Rep. 2013, 3:1005-1011.
74. Tanasijevic B., Rasmussen T.P. X chromosome inactivation and differentiation occur readily in ES cells doubly-deficient for macroH2A1 and macroH2A2. PLoS ONE 2011, 6:e21512.
75. Creppe C., et al. MacroH2A1 regulates the balance between self-renewal and differentiation commitment in embryonic and adult stem cells. Mol. Cell. Biol. 2012, 32:1442-1452.
76. Gurdon J.B., Melton D.A. Nuclear reprogramming in cells. Science 2008, 322:1811-1815.
77. Pasque V., et al. Histone variant macroH2A confers resistance to nuclear reprogramming. EMBO J. 2011, 30:2373-2387.
78. Friedmann-Morvinski D., Verma I.M. Dedifferentiation and reprogramming: origins of cancer stem cells. EMBO Rep. 2014, 15:244-253.
79. Sporn J.C., et al. Histone macroH2A isoforms predict the risk of lung cancer recurrence. Oncogene 2009, 28:3423-3428.
80. Kapoor A., et al. The histone variant macroH2A suppresses melanoma progression through regulation of CDK8. Nature 2010, 468:1105-1109.
81. Novikov L., et al. QKI-mediated alternative splicing of the histone variant MacroH2A1 regulates cancer cell proliferation. Mol. Cell. Biol. 2011, 31:4244-4255.
82. Sporn J.C., Jung B. Differential regulation and predictive potential of MacroH2A1 isoforms in colon cancer. Am. J. Pathol. 2012, 180:2516-2526.
83. Millar C.B. Organizing the genome with H2A histone variants. Biochem. J. 2013, 449:567-579.
84. Changolkar L.N., et al. Genome-wide distribution of macroH2A1 histone variants in mouse liver chromatin. Mol. Cell. Biol. 2010, 30:5473-5483.
85. Gamble M.J., et al. The histone variant macroH2A1 marks repressed autosomal chromatin, but protects a subset of its target genes from silencing. Genes Dev. 2010, 24:21-32.
86. Hubel D.H., Wiesel T.N. Ferrier lecture. Functional architecture of macaque monkey visual cortex. Proc. R. Soc. Lond. B: Biol. Sci. 1977, 198:1-59.
87. Hensch T.K. Critical period regulation. Annu. Rev. Neurosci. 2004, 27:549-579.
88. May A. Experience-dependent structural plasticity in the adult human brain. Trends Cogn. Sci. 2011, 15:475-482.
89. Cortes-Mendoza J., et al. Shaping synaptic plasticity: the role of activity-mediated epigenetic regulation on gene transcription. Int. J. Dev. Neurosci. 2013, 31:359-369.
90. Guan J.S., et al. The role of epigenetic regulation in learning and memory. Exp. Neurol. 2014, 268:30-36.
91. Pina B., Suau P. Changes in histones H2A and H3 variant composition in differentiating and mature rat brain cortical neurons. Dev. Biol. 1987, 123:51-58.
92. Michod D., et al. Calcium-dependent dephosphorylation of the histone chaperone DAXX regulates H3.3 loading and transcription upon neuronal activation. Neuron 2012, 74:122-135.
93. Drane P., et al. The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev. 2010, 24:1253-1265.
94. Lewis P.W., et al. Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:14075-14080.
95. Maze I., et al. Critical role of histone turnover in neuronal transcription and plasticity. Neuron 2015, 87:77-94.
96. Schwartzentruber J., et al. Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature 2012, 482:226-231.
97. Wu G., et al. Somatic histone H3 alterations in pediatric diffuse intrinsic pontine gliomas and non-brainstem glioblastomas. Nat. Genet. 2012, 44:251-253.
98. Lewis P.W., et al. Inhibition of PRC2 activity by a gain-of-function H3 mutation found in pediatric glioblastoma. Science 2013, 340:857-861.
99. Holtmaat A., Svoboda K. Experience-dependent structural synaptic plasticity in the mammalian brain. Nat. Rev. Neurosci. 2009, 10:647-658.
100. Zovkic I.B., et al. Histone H2A.Z. subunit exchange controls consolidation of recent and remote memory. Nature 2014, 515:582-586.
101. Ming G.L., Song H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 2011, 70:687-702.
102. Brann J.H., Firestein S.J. A lifetime of neurogenesis in the olfactory system. Front. Neurosci. 2014, 8:182.
103. Watt W.C., et al. Odorant stimulation enhances survival of olfactory sensory neurons via MAPK and CREB. Neuron 2004, 41:955-967.
104. Santoro S.W., Dulac C. The activity-dependent histone variant H2BE modulates the life span of olfactory neurons. Elife 2012, 1:e00070.
105. Wang Z., et al. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet. 2008, 40:897-903.
106. Thomas-Danguin T., et al. The perception of odor objects in everyday life: a review on the processing of odor mixtures. Front. Psychol. 2014, 5:504.
107. Wiedemann S.M., et al. Identification and characterization of two novel primate-specific histone H3 variants, H3.X and H3.Y. J. Cell Biol. 2010, 190:777-791.
108. Telese F., et al. 'Seq-ing' insights into the epigenetics of neuronal gene regulation. Neuron 2013, 77:606-623.
109. Itzkovitz S., van Oudenaarden A. Validating transcripts with probes and imaging technology. Nat. Methods 2011, 8(Suppl. 4):S12-S19.
110. Zhou V.W., et al. Charting histone modifications and the functional organization of mammalian genomes. Nat. Rev. Genet. 2011, 12:7-18.
111. Sarcinella E., et al. Monoubiquitylation of H2A.Z. distinguishes its association with euchromatin or facultative heterochromatin. Mol. Cell. Biol. 2007, 27:6457-6468.
112. Hon G., et al. Discovery and annotation of functional chromatin signatures in the human genome. PLoS Comput. Biol. 2009, 5:e1000566.
113. Mori K., Sakano H. How is the olfactory map formed and interpreted in the mammalian brain?. Annu. Rev. Neurosci. 2011, 34:467-499.
114. Dalton R.P., et al. Co-opting the unfolded protein response to elicit olfactory receptor feedback. Cell 2013, 155:321-332.