Histone H3 mutations—a special role for H3.3 in tumorigenesis?

Chromosoma

Volumn 124, Issue 2, 2015, Pages 177-189

  Kallappagoudar, Satish ^a   Yadav, Rajesh K ^a   Lowe, Brandon R ^a   Partridge, Janet F ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; HISTONE H3.3; POLYCOMB GROUP PROTEIN; UNCLASSIFIED DRUG; HISTONE; NUCLEOSOME;

CARCINOGENESIS; DISEASE COURSE; DNA DAMAGE; DNA END JOINING REPAIR; DNA REPAIR; DNA REPLICATION; DNA SYNTHESIS; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; NONHUMAN; PROTEIN PROCESSING; REVIEW; X CHROMOSOME INACTIVATION; AMINO ACID SEQUENCE; ANIMAL; BRAIN STEM NEOPLASMS; CHILD; GENETICS; GLIOMA; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOSOME;

AMINO ACID SEQUENCE; ANIMALS; BRAIN STEM NEOPLASMS; CARCINOGENESIS; CHILD; GLIOMA; HISTONES; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEOSOMES;

EID: 84929955270     PISSN: 00095915     EISSN: 14320886     Source Type: Journal    
DOI: 10.1007/s00412-015-0510-4     Document Type: Review

References (108)

1. Adam S, Polo SE, Almouzni G (2013) Transcription recovery after DNA damage requires chromatin priming by the H3.3 histone chaperone HIRA. Cell 155:94–106
2. Adam S, Polo SE, Almouzni G (2014) How to restore chromatin structure and function in response to DNA damage—let the chaperones play: delivered on 9 July 2013 at the 38th FEBS Congress in St Petersburg, Russia. FEBS J 281:2315–2323
3. Ahmad K, Henikoff S (2002) The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9:1191–1200
4. Banaszynski LA, Wen D, Dewell S, Whitcomb SJ, Lin M, Diaz N, Elsasser SJ, Chapgier A, Goldberg AD, Canaani E, Rafii S, Zheng D, Allis CD (2013) Hira-dependent histone H3.3 deposition facilitates PRC2 recruitment at developmental loci in ES cells. Cell 155:107–120
5. Bechet D, Gielen GG, Korshunov A, Pfister SM, Rousso C, Faury D, Fiset PO, Benlimane N, Lewis PW, Lu C, David AC, Kieran MW, Ligon KL, Pietsch T, Ellezam B, Albrecht S, Jabado N (2014) Specific detection of methionine 27 mutation in histone 3 variants (H3K27M) in fixed tissue from high-grade astrocytomas. Acta Neuropathol 128:733–741
6. Behjati S, Tarpey PS, Presneau N, Scheipl S, Pillay N, Van LP, Wedge DC, Cooke SL, Gundem G, Davies H, Nik-Zainal S, Martin S, McLaren S, Goodie V, Robinson B, Butler A, Teague JW, Halai D, Khatri B, Myklebost O, Baumhoer D, Jundt G, Hamoudi R, Tirabosco R, Amary MF, Futreal PA, Stratton MR, Campbell PJ, Flanagan AM (2013) Distinct H3F3A and H3F3B driver mutations define chondroblastoma and giant cell tumor of bone. Nat Genet 45:1479–1482
7. Bender S, Tang Y, Lindroth AM, Hovestadt V, Jones DT, Kool M, Zapatka M, Northcott PA, Sturm D, Wang W, Radlwimmer B, Hojfeldt JW, Truffaux N, Castel D, Schubert S, Ryzhova M, Seker-Cin H, Gronych J, Johann PD, Stark S, Meyer J, Milde T, Schuhmann M, Ebinger M, Monoranu CM, Ponnuswami A, Chen S, Jones C, Witt O, Collins VP, Von DA, Jabado N, Puget S, Grill J, Helin K, Korshunov A, Lichter P, Monje M, Plass C, Cho YJ, Pfister SM (2013) Reduced H3K27me3 and DNA hypomethylation are major drivers of gene expression in K27M mutant pediatric high-grade gliomas. Cancer Cell 24:660–672
8. Bengani H, Mendiratta S, Maini J, Vasanthi D, Sultana H, Ghasemi M, Ahluwalia J, Ramachandran S, Mishra RK, Brahmachari V (2013) Identification and validation of a putative polycomb responsive element in the human genome. PLoS ONE 8:e67217
9. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125:315–326
10. Bjerke L, Mackay A, Nandhabalan M, Burford A, Jury A, Popov S, Bax DA, Carvalho D, Taylor KR, Vinci M, Bajrami I, McGonnell IM, Lord CJ, Reis RM, Hargrave D, Ashworth A, Workman P, Jones C (2013) Histone H3.3 mutations drive pediatric glioblastoma through upregulation of MYCN. Cancer Discov
11. Brown ZZ, Muller MM, Jain SU, Allis CD, Lewis PW, Muir TW (2014) Strategy for “detoxification” of a cancer-derived histone mutant based on mapping its interaction with the methyltransferase PRC2. J Am Chem Soc 136:13498–13501
12. Buczkowicz P, Hoeman C, Rakopoulos P, Pajovic S, Letourneau L, Dzamba M, Morrison A, Lewis P, Bouffet E, Bartels U, Zuccaro J, Agnihotri S, Ryall S, Barszczyk M, Chornenkyy Y, Bourgey M, Bourque G, Montpetit A, Cordero F, Castelo-Branco P, Mangerel J, Tabori U, Ho KC, Huang A, Taylor KR, Mackay A, Bendel AE, Nazarian J, Fangusaro JR, Karajannis MA, Zagzag D, Foreman NK, Donson A, Hegert JV, Smith A, Chan J, Lafay-Cousin L, Dunn S, Hukin J, Dunham C, Scheinemann K, Michaud J, Zelcer S, Ramsay D, Cain J, Brennan C, Souweidane MM, Jones C, Allis CD, Brudno M, Becher O, Hawkins C (2014) Genomic analysis of diffuse intrinsic pontine gliomas identifies three molecular subgroups and recurrent activating ACVR1 mutations. Nat Genet 46:451–456
13. Calo E, Wysocka J (2013) Modification of enhancer chromatin: what, how, and why? Mol Cell 49:825–837
14. Carvalho S, Raposo AC, Martins FB, Grosso AR, Sridhara SC, Rino J, Carmo-Fonseca M, de Almeida SF (2013) Histone methyltransferase SETD2 coordinates FACT recruitment with nucleosome dynamics during transcription. Nucleic Acids Res 41:2881–2893
15. Carvalho S, Vitor AC, Sridhara SC, Martins FB, Raposo AC, Desterro JM, Ferreira J, de Almeida SF (2014) SETD2 is required for DNA double-strand break repair and activation of the p53-mediated checkpoint. Elife 3:e02482
16. Chan KM, Fang D, Gan H, Hashizume R, Yu C, Schroeder M, Gupta N, Mueller S, James CD, Jenkins R, Sarkaria J, Zhang Z (2013) The histone H3.3K27M mutation in pediatric glioma reprograms H3K27 methylation and gene expression. Genes Dev 27:985–990
17. Chen P, Zhao J, Wang Y, Wang M, Long H, Liang D, Huang L, Wen Z, Li W, Li X, Feng H, Zhao H, Zhu P, Li M, Wang QF, Li G (2013) H3.3 actively marks enhancers and primes gene transcription via opening higher-ordered chromatin. Genes Dev 27:2109–2124
18. Chow CM, Georgiou A, Szutorisz H, Silva ME, Pombo A, Barahona I, Dargelos E, Canzonetta C, Dillon N (2005) Variant histone H3.3 marks promoters of transcriptionally active genes during mammalian cell division. EMBO Rep 6:354–360
19. Cuddapah S, Roh TY, Cui K, Jose CC, Fuller MT, Zhao K, Chen X (2012) A novel human polycomb binding site acts as a functional polycomb response element in Drosophila. PLoS ONE 7:e36365
20. Di CL, Helin K (2013) Transcriptional regulation by Polycomb group proteins. Nat Struct Mol Biol 20:1147–1155
21. Drane P, Ouararhni K, Depaux A, Shuaib M, Hamiche A (2010) The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev 24:1253–1265
22. Duarte LF, Young AR, Wang Z, Wu HA, Panda T, Kou Y, Kapoor A, Hasson D, Mills NR, Ma’ayan A, Narita M, Bernstein E (2014) Histone H3.3 and its proteolytically processed form drive a cellular senescence programme. Nat Commun 5:5210
23. Duns G, van den Berg E, Van DI, Osinga J, Hollema H, Hofstra RM, Kok K (2010) Histone methyltransferase gene SETD2 is a novel tumor suppressor gene in clear cell renal cell carcinoma. Cancer Res 70:4287–4291
24. Elsasser SJ, Huang H, Lewis PW, Chin JW, Allis CD, Patel DJ (2012) DAXX envelops a histone H3.3-H4 dimer for H3.3-specific recognition. Nature 491:560–565
25. Filipescu D, Szenker E, Almouzni G (2013) Developmental roles of histone H3 variants and their chaperones. Trends Genet 29:630–640
26. Fontebasso AM, Schwartzentruber J, Khuong-Quang DA, Liu XY, Sturm D, Korshunov A, Jones DT, Witt H, Kool M, Albrecht S, Fleming A, Hadjadj D, Busche S, Lepage P, Montpetit A, Staffa A, Gerges N, Zakrzewska M, Zakrzewski K, Liberski PP, Hauser P, Garami M, Klekner A, Bognar L, Zadeh G, Faury D, Pfister SM, Jabado N, Majewski J (2013) Mutations in SETD2 and genes affecting histone H3K36 methylation target hemispheric high-grade gliomas. Acta Neuropathol 125:659–669
27. Fontebasso AM, Papillon-Cavanagh S, Schwartzentruber J, Nikbakht H, Gerges N, Fiset PO, Bechet D, Faury D, De JN, Ramkissoon LA, Corcoran A, Jones DT, Sturm D, Johann P, Tomita T, Goldman S, Nagib M, Bendel A, Goumnerova L, Bowers DC, Leonard JR, Rubin JB, Alden T, Browd S, Geyer JR, Leary S, Jallo G, Cohen K, Gupta N, Prados MD, Carret AS, Ellezam B, Crevier L, Klekner A, Bognar L, Hauser P, Garami M, Myseros J, Dong Z, Siegel PM, Malkin H, Ligon AH, Albrecht S, Pfister SM, Ligon KL, Majewski J, Jabado N, Kieran MW (2014) Recurrent somatic mutations in ACVR1 in pediatric midline high-grade astrocytoma. Nat Genet 46:462–466
28. Frank D, Doenecke D, Albig W (2003) Differential expression of human replacement and cell cycle dependent H3 histone genes. Gene 312:135–143
29. Franklin SG, Zweidler A (1977) Non-allelic variants of histones 2a, 2b and 3 in mammals. Nature 266:273–275
30. Frey A, Listovsky T, Guilbaud G, Sarkies P, Sale JE (2014) Histone H3.3 is required to maintain replication fork progression after UV damage. Curr Biol 24:2195–2201
31. Funato K, Major T, Lewis PW, Allis CD, Tabar V (2014) Use of human embryonic stem cells to model pediatric gliomas with H3.3K27M histone mutation. Science 346:1529–1533
32. Gabrielli F, Aden DP, Carrel SC, Von BC, Rane A, Angeletti CA, Hancock R (1984) Histone complements of human tissues, carcinomas, and carcinoma-derived cell lines. Mol Cell Biochem 65:57–66
33. Gaillard PH, Martini EM, Kaufman PD, Stillman B, Moustacchi E, Almouzni G (1996) Chromatin assembly coupled to DNA repair: a new role for chromatin assembly factor I. Cell 86:887–896
34. Gielen GH, Gessi M, Hammes J, Kramm CM, Waha A, Pietsch T (2013) H3F3A K27M mutation in pediatric CNS tumors: a marker for diffuse high-grade astrocytomas. Am J Clin Pathol 139:345–349
35. Goldberg AD, Banaszynski LA, Noh KM, Lewis PW, Elsaesser SJ, Stadler S, Dewell S, Law M, Guo X, Li X, Wen D, Chapgier A, DeKelver RC, Miller JC, Lee YL, Boydston EA, Holmes MC, Gregory PD, Greally JM, Rafii S, Yang C, Scambler PJ, Garrick D, Gibbons RJ, Higgs DR, Cristea IM, Urnov FD, Zheng D, Allis CD (2010) Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140:678–691
36. Grossniklaus U, Paro R (2014) Transcriptional silencing by Polycomb-group proteins. Cold Spring Harb Perspect Biol 6
37. Guo R, Zheng L, Park JW, Lv R, Chen H, Jiao F, Xu W, Mu S, Wen H, Qiu J, Wang Z, Yang P, Wu F, Hui J, Fu X, Shi X, Shi YG, Xing Y, Lan F, Shi Y (2014) BS69/ZMYND11 reads and connects histone H3.3 lysine 36 trimethylation-decorated chromatin to regulated Pre-mRNA processing. Mol Cell 56:298–310
38. Hake SB, Garcia BA, Duncan EM, Kauer M, Dellaire G, Shabanowitz J, Bazett-Jones DP, Allis CD, Hunt DF (2006) Expression patterns and post-translational modifications associated with mammalian histone H3 variants. J Biol Chem 281:559–568
39. Hashizume R, Andor N, Ihara Y, Lerner R, Gan H, Chen X, Fang D, Huang X, Tom MW, Ngo V, Solomon D, Mueller S, Paris PL, Zhang Z, Petritsch C, Gupta N, Waldman TA, James CD (2014) Pharmacologic inhibition of histone demethylation as a therapy for pediatric brainstem glioma. Nat Med 20:1394–1396
40. Heaphy CM, de Wilde RF, Jiao Y, Klein AP, Edil BH, Shi C, Bettegowda C, Rodriguez FJ, Eberhart CG, Hebbar S, Offerhaus GJ, McLendon R, Rasheed BA, He Y, Yan H, Bigner DD, Oba-Shinjo SM, Marie SK, Riggins GJ, Kinzler KW, Vogelstein B, Hruban RH, Maitra A, Papadopoulos N, Meeker AK (2011) Altered telomeres in tumors with ATRX and DAXX mutations. Science 333:425
41. Herz HM, Morgan M, Gao X, Jackson J, Rickels R, Swanson SK, Florens L, Washburn MP, Eissenberg JC, Shilatifard A (2014) Histone H3 lysine-to-methionine mutants as a paradigm to study chromatin signaling. Science 345:1065–1070
42. Hock H (2012) A complex Polycomb issue: the two faces of EZH2 in cancer. Genes Dev 26:751–755
43. Hodl M, Basler K (2009) Transcription in the absence of histone H3.3. Curr Biol 19:1221–1226
44. Huang C, Zhu B (2014) H3.3 turnover: a mechanism to poise chromatin for transcription, or a response to open chromatin? Bioessays 36:579–584
45. Huang C, Zhang Z, Xu M, Li Y, Li Z, Ma Y, Cai T, Zhu B (2013) H3.3-H4 tetramer splitting events feature cell-type specific enhancers. PLoS Genet 9:e1003558
46. Huether R, Dong L, Chen X, Wu G, Parker M, Wei L, Ma J, Edmonson MN, Hedlund EK, Rusch MC, Shurtleff SA, Mulder HL, Boggs K, Vadordaria B, Cheng J, Yergeau D, Song G, Becksfort J, Lemmon G, Weber C, Cai Z, Dang J, Walsh M, Gedman AL, Faber Z, Easton J, Gruber T, Kriwacki RW, Partridge JF, Ding L, Wilson RK, Mardis ER, Mullighan CG, Gilbertson RJ, Baker SJ, Zambetti G, Ellison DW, Zhang J, Downing JR (2014) The landscape of somatic mutations in epigenetic regulators across 1,000 paediatric cancer genomes. Nat Commun 5:3630
47. Jha DK, Strahl BD (2014) An RNA polymerase II-coupled function for histone H3K36 methylation in checkpoint activation and DSB repair. Nat Commun 5:3965
48. Jin C, Felsenfeld G (2006) Distribution of histone H3.3 in hematopoietic cell lineages. Proc Natl Acad Sci U S A 103:574–579
49. Jin C, Felsenfeld G (2007) Nucleosome stability mediated by histone variants H3.3 and H2A.Z. Genes Dev 21:1519–1529
50. Jones C, Baker SJ (2014) Unique genetic and epigenetic mechanisms driving paediatric diffuse high-grade glioma. Nat Rev Cancer 14
51. Khuong-Quang DA, Buczkowicz P, Rakopoulos P, Liu XY, Fontebasso AM, Bouffet E, Bartels U, Albrecht S, Schwartzentruber J, Letourneau L, Bourgey M, Bourque G, Montpetit A, Bourret G, Lepage P, Fleming A, Lichter P, Kool M, Von DA, Sturm D, Korshunov A, Faury D, Jones DT, Majewski J, Pfister SM, Jabado N, Hawkins C (2012) K27M mutation in histone H3.3 defines clinically and biologically distinct subgroups of pediatric diffuse intrinsic pontine gliomas. Acta Neuropathol 124:439–447
52. Kraushaar DC, Jin W, Maunakea A, Abraham B, Ha M, Zhao K (2013) Genome-wide incorporation dynamics reveal distinct categories of turnover for the histone variant H3.3. Genome Biol 14:R121
53. Kuo AJ, Cheung P, Chen K, Zee BM, Kioi M, Lauring J, Xi Y, Park BH, Shi X, Garcia BA, Li W, Gozani O (2011) NSD2 links dimethylation of histone H3 at lysine 36 to oncogenic programming. Mol Cell 44:609–620
54. Lewis PW, Allis CD (2013) Poisoning the “histone code” in pediatric gliomagenesis. Cell Cycle 12
55. Lewis PW, Elsaesser SJ, Noh KM, Stadler SC, Allis CD (2010) 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 107:14075–14080
56. Lewis PW, Muller MM, Koletsky MS, Cordero F, Lin S, Banaszynski LA, Garcia BA, Muir TW, Becher OJ, Allis CD (2013) Inhibition of PRC2 activity by a gain-of-function H3 mutation found in pediatric glioblastoma. Science 340:857–861
57. Li F, Mao G, Tong D, Huang J, Gu L, Yang W, Li GM (2013) The histone mark H3K36me3 regulates human DNA mismatch repair through its interaction with MutSalpha. Cell 153:590–600
58. Loppin B, Bonnefoy E, Anselme C, Laurencon A, Karr TL, Couble P (2005) The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature 437:1386–1390
59. Lovejoy CA, Li W, Reisenweber S, Thongthip S, Bruno J, De LT, De S, Petrini JH, Sung PA, Jasin M, Rosenbluh J, Zwang Y, Weir BA, Hatton C, Ivanova E, Macconaill L, Hanna M, Hahn WC, Lue NF, Reddel RR, Jiao Y, Kinzler K, Vogelstein B, Papadopoulos N, Meeker AK (2012) Loss of ATRX, genome instability, and an altered DNA damage response are hallmarks of the alternative lengthening of telomeres pathway. PLoS Genet 8:e1002772
60. Loyola A, Bonaldi T, Roche D, Imhof A, Almouzni G (2006) PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol Cell 24:309–316
61. McKittrick E, Gafken PR, Ahmad K, Henikoff S (2004) Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc Natl Acad Sci U S A 101:1525–1530
62. Mehta S, Huillard E, Kesari S, Maire CL, Golebiowski D, Harrington EP, Alberta JA, Kane MF, Theisen M, Ligon KL, Rowitch DH, Stiles CD (2011) The central nervous system-restricted transcription factor Olig2 opposes p53 responses to genotoxic damage in neural progenitors and malignant glioma. Cancer Cell 19:359–371
63. Mito Y, Henikoff JG, Henikoff S (2007) Histone replacement marks the boundaries of cis-regulatory domains. Science 315:1408–1411
64. Morris SA, Shibata Y, Noma K, Tsukamoto Y, Warren E, Temple B, Grewal SI, Strahl BD (2005) Histone H3 K36 methylation is associated with transcription elongation in Schizosaccharomyces pombe. Eukaryot Cell 4:1446–1454
65. Newbold RF, Mokbel K (2010) Evidence for a tumour suppressor function of SETD2 in human breast cancer: a new hypothesis. Anticancer Res 30:3309–3311
66. Osley MA (1991) The regulation of histone synthesis in the cell cycle. Annu Rev Biochem 60:827–861
67. O’Sullivan RJ, Almouzni G (2014) Assembly of telomeric chromatin to create ALTernative endings. Trends Cell Biol 24:675–685
68. Pai CC, Deegan RS, Subramanian L, Gal C, Sarkar S, Blaikley EJ, Walker C, Hulme L, Bernhard E, Codlin S, Bahler J, Allshire R, Whitehall S, Humphrey TC (2014) A histone H3K36 chromatin switch coordinates DNA double-strand break repair pathway choice. Nat Commun 5:4091
69. Pengelly AR, Copur O, Jackle H, Herzig A, Muller J (2013) A histone mutant reproduces the phenotype caused by loss of histone-modifying factor Polycomb. Science 339:698–699
70. Pfister SX, Ahrabi S, Zalmas LP, Sarkar S, Aymard F, Bachrati CZ, Helleday T, Legube G, La Thangue NB, Porter AC, Humphrey TC (2014) SETD2-dependent histone H3K36 trimethylation is required for homologous recombination repair and genome stability. Cell Rep 7:2006–2018
71. Pina B, Suau P (1987) Changes in histones H2A and H3 variant composition in differentiating and mature rat brain cortical neurons. Dev Biol 123:51–58
72. Plass C, Pfister SM, Lindroth AM, Bogatyrova O, Claus R, Lichter P (2013) Mutations in regulators of the epigenome and their connections to global chromatin patterns in cancer. Nat Rev Genet 14:765–780
73. Pryde F, Jain D, Kerr A, Curley R, Mariotti FR, Vogelauer M (2009) H3 k36 methylation helps determine the timing of cdc45 association with replication origins. PLoS ONE 4:e5882
74. Ray-Gallet D, Woolfe A, Vassias I, Pellentz C, Lacoste N, Puri A, Schultz DC, Pchelintsev NA, Adams PD, Jansen LE, Almouzni G (2011) Dynamics of histone H3 deposition in vivo reveal a nucleosome gap-filling mechanism for H3.3 to maintain chromatin integrity. Mol Cell 44:928–941
75. Sakai A, Schwartz BE, Goldstein S, Ahmad K (2009) Transcriptional and developmental functions of the H3.3 histone variant in Drosophila. Curr Biol 19:1816–1820
76. Santenard A, Ziegler-Birling C, Koch M, Tora L, Bannister AJ, Torres-Padilla ME (2010) Heterochromatin formation in the mouse embryo requires critical residues of the histone variant H3.3. Nat Cell Biol 12:853–862
77. Saratsis AM, Kambhampati M, Snyder K, Yadavilli S, Devaney JM, Harmon B, Hall J, Raabe EH, An P, Weingart M, Rood BR, Magge SN, MacDonald TJ, Packer RJ, Nazarian J (2014) Comparative multidimensional molecular analyses of pediatric diffuse intrinsic pontine glioma reveals distinct molecular subtypes. Acta Neuropathol 127:881–895
78. Schwartz BE, Ahmad K (2005) Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev 19:804–814
79. Schwartzentruber J, Korshunov A, Liu XY, Jones DT, Pfaff E, Jacob K, Sturm D, Fontebasso AM, Quang DA, Tonjes M, Hovestadt V, Albrecht S, Kool M, Nantel A, Konermann C, Lindroth A, Jager N, Rausch T, Ryzhova M, Korbel JO, Hielscher T, Hauser P, Garami M, Klekner A, Bognar L, Ebinger M, Schuhmann MU, Scheurlen W, Pekrun A, Fruhwald MC, Roggendorf W, Kramm C, Durken M, Atkinson J, Lepage P, Montpetit A, Zakrzewska M, Zakrzewski K, Liberski PP, Dong Z, Siegel P, Kulozik AE, Zapatka M, Guha A, Malkin D, Felsberg J, Reifenberger G, Von DA, Ichimura K, Collins VP, Witt H, Milde T, Witt O, Zhang C, Castelo-Branco P, Lichter P, Faury D, Tabori U, Plass C, Majewski J, Pfister SM, Jabado N (2012) Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature 482:226–231
80. Shibahara K, Stillman B (1999) Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 96:575–585
81. Sing A, Pannell D, Karaiskakis A, Sturgeon K, Djabali M, Ellis J, Lipshitz HD, Cordes SP (2009) A vertebrate Polycomb response element governs segmentation of the posterior hindbrain. Cell 138:885–897
82. Sturm D, Witt H, Hovestadt V, Khuong-Quang DA, Jones DT, Konermann C, Pfaff E, Tonjes M, Sill M, Bender S, Kool M, Zapatka M, Becker N, Zucknick M, Hielscher T, Liu XY, Fontebasso AM, Ryzhova M, Albrecht S, Jacob K, Wolter M, Ebinger M, Schuhmann MU, Van MT, Fruhwald MC, Hauch H, Pekrun A, Radlwimmer B, Niehues T, Von KG, Durken M, Kulozik AE, Madden J, Donson A, Foreman NK, Drissi R, Fouladi M, Scheurlen W, Von DA, Monoranu C, Roggendorf W, Herold-Mende C, Unterberg A, Kramm CM, Felsberg J, Hartmann C, Wiestler B, Wick W, Milde T, Witt O, Lindroth AM, Schwartzentruber J, Faury D, Fleming A, Zakrzewska M, Liberski PP, Zakrzewski K, Hauser P, Garami M, Klekner A, Bognar L, Morrissy S, Cavalli F, Taylor MD, Van SP, Koster J, Versteeg R, Volckmann R, Mikkelsen T, Aldape K, Reifenberger G, Collins VP, Majewski J, Korshunov A, Lichter P, Plass C, Jabado N, Pfister SM (2012) Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma. Cancer Cell 22:425–437
83. Swartling FJ, Savov V, Persson AI, Chen J, Hackett CS, Northcott PA, Grimmer MR, Lau J, Chesler L, Perry A, Phillips JJ, Taylor MD, Weiss WA (2012) Distinct neural stem cell populations give rise to disparate brain tumors in response to N-MYC. Cancer Cell 21:601–613
84. Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y (2004) Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116:51–61
85. Taylor KR, Mackay A, Truffaux N, Butterfield YS, Morozova O, Philippe C, Castel D, Grasso CS, Vinci M, Carvalho D, Carcaboso AM, De TC, Cruz O, Mora J, Entz-Werle N, Ingram WJ, Monje M, Hargrave D, Bullock AN, Puget S, Yip S, Jones C, Grill J (2014a) Recurrent activating ACVR1 mutations in diffuse intrinsic pontine glioma. Nat Genet 46:457–461
86. Taylor KR, Vinci M, Bullock AN, Jones C (2014b) ACVR1 mutations in DIPG: lessons learned from FOP. Cancer Res 74:4565–4570
87. Torres-Padilla ME, Bannister AJ, Hurd PJ, Kouzarides T, Zernicka-Goetz M (2006) Dynamic distribution of the replacement histone variant H3.3 in the mouse oocyte and preimplantation embryos. Int J Dev Biol 50:455–461
88. van der Heijden GW, Dieker JW, Derijck AA, Muller S, Berden JH, Braat DD, Van DV, De BP (2005) Asymmetry in histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote. Mech Dev 122:1008–1022
89. Venneti S, Garimella MT, Sullivan LM, Martinez D, Huse JT, Heguy A, Santi M, Thompson CB, Judkins AR (2013) Evaluation of histone 3 lysine 27 trimethylation (H3K27me3) and enhancer of Zest 2 (EZH2) in pediatric glial and glioneuronal tumors shows decreased H3K27me3 in H3F3A K27M mutant glioblastomas. Brain Pathol 23:558–564
90. Venneti S, Santi M, Felicella MM, Yarilin D, Phillips JJ, Sullivan LM, Martinez D, Perry A, Lewis PW, Thompson CB, Judkins AR (2014) A sensitive and specific histopathologic prognostic marker for H3F3A K27M mutant pediatric glioblastomas. Acta Neuropathol 128:743–753
91. Vermunt MW, Reinink P, Korving J, De BE, Creyghton PM, Basak O, Geeven G, Toonen PW, Lansu N, Meunier C, Van HS, Clevers H, De LW, Cuppen E, Creyghton MP (2014) Large-scale identification of coregulated enhancer networks in the adult human brain. Cell Rep 9:767–779
92. Viana-Pereira M, Lee A, Popov S, Bax DA, Al-Sarraj S, Bridges LR, Stavale JN, Hargrave D, Jones C, Reis RM (2011) Microsatellite instability in pediatric high grade glioma is associated with genomic profile and differential target gene inactivation. PLoS ONE 6:e20588
93. Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Diaz LA Jr, Kinzler KW (2013) Cancer genome landscapes. Science 339:1546–1558
94. Wagner EJ, Carpenter PB (2012) Understanding the language of Lys36 methylation at histone H3. Nat Rev Mol Cell Biol 13:115–126
95. Wells D, Kedes L (1985) Structure of a human histone cDNA: evidence that basally expressed histone genes have intervening sequences and encode polyadenylylated mRNAs. Proc Natl Acad Sci U S A 82:2834–2838
96. Wells D, Hoffman D, Kedes L (1987) Unusual structure, evolutionary conservation of non-coding sequences and numerous pseudogenes characterize the human H3.3 histone multigene family. Nucleic Acids Res 15:2871–2889
97. Wen D, Banaszynski LA, Liu Y, Geng F, Noh KM, Xiang J, Elemento O, Rosenwaks Z, Allis CD, Rafii S (2014a) Histone variant H3.3 is an essential maternal factor for oocyte reprogramming. Proc Natl Acad Sci U S A 111:7325–7330
98. Wen D, Banaszynski LA, Rosenwaks Z, Allis CD, Rafii S (2014b) H3.3 replacement facilitates epigenetic reprogramming of donor nuclei in somatic cell nuclear transfer embryos. Nucleus 5:369–375
99. Wen H, Li Y, Xi Y, Jiang S, Stratton S, Peng D, Tanaka K, Ren Y, Xia Z, Wu J, Li B, Barton MC, Li W, Li H, Shi X (2014c) ZMYND11 links histone H3.3K36me3 to transcription elongation and tumour suppression. Nature 508:263–268
100. Wong LH, McGhie JD, Sim M, Anderson MA, Ahn S, Hannan RD, George AJ, Morgan KA, Mann JR, Choo KH (2010) ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome Res 20:351–360
101. Woo CJ, Kharchenko PV, Daheron L, Park PJ, Kingston RE (2010) A region of the human HOXD cluster that confers polycomb-group responsiveness. Cell 140:99–110
102. Woo CJ, Kharchenko PV, Daheron L, Park PJ, Kingston RE (2013) Variable requirements for DNA-binding proteins at polycomb-dependent repressive regions in human HOX clusters. Mol Cell Biol 33:3274–3285
103. Workman JL, Kingston RE (1998) Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu Rev Biochem 67:545–579
104. Wu RS, Tsai S, Bonner WM (1982) Patterns of histone variant synthesis can distinguish G0 from G1 cells. Cell 31:367–374
105. Wu G, Broniscer A, McEachron TA, Lu C, Paugh BS, Becksfort J, Qu C, Ding L, Huether R, Parker M, Zhang J, Gajjar A, Dyer MA, Mullighan CG, Gilbertson RJ, Mardis ER, Wilson RK, Downing JR, Ellison DW, Zhang J, Baker SJ (2012) Somatic histone H3 alterations in pediatric diffuse intrinsic pontine gliomas and non-brainstem glioblastomas. Nat Genet 44:251–253
106. Wu G, Diaz AK, Paugh BS, Rankin SL, Ju B, Li Y, Zhu X, Qu C, Chen X, Zhang J, Easton J, Edmonson M, Ma X, Lu C, Nagahawatte P, Hedlund E, Rusch M, Pounds S, Lin T, Onar-Thomas A, Huether R, Kriwacki R, Parker M, Gupta P, Becksfort J, Wei L, Mulder HL, Boggs K, Vadodaria B, Yergeau D, Russell JC, Ochoa K, Fulton RS, Fulton LL, Jones C, Boop FA, Broniscer A, Wetmore C, Gajjar A, Ding L, Mardis ER, Wilson RK, Taylor MR, Downing JR, Ellison DW, Zhang J, Baker SJ (2014) The genomic landscape of diffuse intrinsic pontine glioma and pediatric non-brainstem high-grade glioma. Nat Genet 46:444–450
107. Yoh SM, Lucas JS, Jones KA (2008) The Iws1:Spt6:CTD complex controls cotranscriptional mRNA biosynthesis and HYPB/Setd2-mediated histone H3K36 methylation. Genes Dev 22:3422–3434
108. Zhang Q, Qi S, Xu M, Yu L, Tao Y, Deng Z, Wu W, Li J, Chen Z, Wong J (2013) Structure-function analysis reveals a novel mechanism for regulation of histone demethylase LSD2/AOF1/KDM1b. Cell Res 23:225–241