Mechanism of cancer: Oncohistones in action

a.
Department of Abdominal Oncology, State Key Laboratory of Biotherapy and Cancer Center, West China Hospital, Sichuan University and Collaborative Innovation Center, Chengdu 610041, China
b.
Department of Biomedical Sciences, City University of Hong Kong, Hong Kong 999077, China

More Information

Corresponding author: E-mail address: hjunhong@scu.edu.cn (Junhong Han)

摘要

- /
- /
- /
Abstract: Oncohistones are histones with high-frequency point mutations that are associated with tumorigenesis. Although each histone variant is encoded by multiple genes, a single mutation in one allele of one gene seems to have a dominant effect over global histone H3 methylation level at the relevant amino acid residue. These oncohistones are highly tumor type specific. For example, H3K27M and H3G34V/R mutations occur only in pediatric brain cancers, whereas H3K36M and H3G34W/L have only been found in pediatric bone tumors. H1 mutations also seem to be exclusively linked to lymphomas. In this review, we discuss the occurrence, frequency and potential functional mechanisms of each oncohistone in tumorigenesis of its relevant cancer. We believe that further investigation into the mechanism regarding their tumor type specificity and cancer-related functions will shed new light on their application in cancer diagnosis and targeted therapy development.
- Oncohistone /
- Histone modification /
- Tumorigenesis /
- Pediatric cancer

HTML全文

参考文献(86)

[1]	Abedalthagafi, M., Phillips, J.J., Kim, G.E. et al. The alternative lengthening of telomere phenotype is significantly associated with loss of ATRX expression in high-grade pediatric and adult astrocytomas: a multi-institutional study of 214 astrocytomas Mod. Pathol., 26 (2013),pp. 1425-1432
[2]	Adam, S., Polo, S.E., Almouzni, G. Transcription recovery after DNA damage requires chromatin priming by the H3.3 histone chaperone HIRA Cell, 155 (2013),pp. 94-106
[3]	Adam, S., Polo, S.E., Almouzni, G. 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 (2014),pp. 2315-2323
[4]	Aihara, K., Mukasa, A., Gotoh, K. et al. Neuro. Oncol., 16 (2014),pp. 140-146
[5]	Amanatullah, D.F., Clark, T.R., Lopez, M.J. et al. Giant cell tumor of bone Orthopedics, 37 (2014),pp. 112-120
[6]	Amary, F., Berisha, F., Ye, H. et al. Am. J. Surg. Pathol., 41 (2017),pp. 1059-1068
[7]	Amary, M.F., Berisha, F., Mozela, R. et al. Histopathology, 69 (2016),pp. 121-127
[8]	Banaszynski, L.A., Wen, D., Dewell, S. et al. Hira-dependent histone H3.3 deposition facilitates PRC2 recruitment at developmental loci in ES cells Cell, 155 (2013),pp. 107-120
[9]	Baubec, T., Colombo, D.F., Wirbelauer, C. et al. Genomic profiling of DNA methyltransferases reveals a role for DNMT3B in genic methylation Nature, 520 (2015),pp. 243-247
[10]	Bechet, D., Gielen, G.G., Korshunov, A. et al. Specific detection of methionine 27 mutation in histone 3 variants (H3K27M) in fixed tissue from high-grade astrocytomas Acta Neuropathol., 128 (2014),pp. 733-741
[11]	Behjati, S., Tarpey, P.S., Presneau, N. et al. Nat. Genet., 45 (2013),pp. 1479-1482
[12]	Bender, S., Tang, Y., Lindroth, A.M. et al. Reduced H3K27me3 and DNA hypomethylation are major drivers of gene expression in K27M mutant pediatric high-grade gliomas Cancer Cell, 24 (2013),pp. 660-672
[13]	Bjerke, L., Mackay, A., Nandhabalan, M. et al. Histone H3.3. mutations drive pediatric glioblastoma through upregulation of MYCN Cancer Discov., 3 (2013),pp. 512-519
[14]	Broniscer, A., Baker, S.J., West, A.N. et al. Clinical and molecular characteristics of malignant transformation of low-grade glioma in children J. Clin. Oncol., 25 (2007),pp. 682-689
[15]	Brown, Z.Z., Muller, M.M., Jain, S.U. et al. Strategy for “detoxification” of a cancer-derived histone mutant based on mapping its interaction with the methyltransferase PRC2 J. Am. Chem. Soc., 136 (2014),pp. 13498-13501
[16]	Buczkowicz, P., Bartels, U., Bouffet, E. et al. Histopathological spectrum of paediatric diffuse intrinsic pontine glioma: diagnostic and therapeutic implications Acta Neuropathol., 128 (2014),pp. 573-581
[17]	Buczkowicz, P., Hoeman, C., Rakopoulos, P. et al. Nat. Genet., 46 (2014),pp. 451-456
[18]	Camelo-Piragua, S., Kesari, S. Further understanding of the pathology of glioma: implications for the clinic Expert Rev. Neurother., 16 (2016),pp. 1055-1065
[19]	Castel, D., Philippe, C., Calmon, R. et al. Acta Neuropathol., 130 (2015),pp. 815-827
[20]	Chan, K.M., Fang, D., Gan, H. et al. The histone H3.3K27M mutation in pediatric glioma reprograms H3K27 methylation and gene expression Genes Dev., 27 (2013),pp. 985-990
[21]	Chan, K.M., Han, J., Fang, D. et al. Cell Cycle, 12 (2013),pp. 2546-2552
[22]	Chheda, Z.S., Kohanbash, G., Okada, K. et al. Novel and shared neoantigen derived from histone 3 variant H3.3K27M mutation for glioma T cell therapy J. Exp. Med., 215 (2018),pp. 141-157
[23]	Chiang, J.C., Ellison, D.W. Molecular pathology of paediatric central nervous system tumours J. Pathol., 241 (2017),pp. 159-172
[24]	Creyghton, M.P., Cheng, A.W., Welstead, G.G. et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state Proc. Natl. Acad. Sci. U. S. A., 107 (2010),pp. 21931-21936
[25]	Diaz, A.K., Baker, S.J. The genetic signatures of pediatric high-grade glioma: no longer a one-act play Semin. Radiat. Oncol., 24 (2014),pp. 240-247
[26]	Duns, G., van den Berg, E., van Duivenbode, I. et al. Cancer Res., 70 (2010),pp. 4287-4291
[27]	Elsaesser, S.J., Goldberg, A.D., Allis, C.D. New functions for an old variant: no substitute for histone H3.3 Curr. Opin. Genet. Dev., 20 (2010),pp. 110-117
[28]	Fan, Y., Nikitina, T., Zhao, J. et al. Histone H1 depletion in mammals alters global chromatin structure but causes specific changes in gene regulation Cell, 123 (2005),pp. 1199-1212
[29]	Fang, D., Gan, H., Lee, J.H. et al. The histone H3.3K36M mutation reprograms the epigenome of chondroblastomas Science, 352 (2016),pp. 1344-1348
[30]	Fang, R., Barbera, A.J., Xu, Y. et al. Human LSD2/KDM1b/AOF1 regulates gene transcription by modulating intragenic H3K4me2 methylation Mol. Cell, 39 (2010),pp. 222-233
[31]	Feng, J., Hao, S., Pan, C. et al. The H3.3 K27M mutation results in a poorer prognosis in brainstem gliomas than thalamic gliomas in adults Hum. Pathol., 46 (2015),pp. 1626-1632
[32]	Fontebasso, A.M., Liu, X.Y., Sturm, D. et al. Chromatin remodeling defects in pediatric and young adult glioblastoma: a tale of a variant histone 3 tail Brain Pathol., 23 (2013),pp. 210-216
[33]	Fontebasso, A.M., Papillon-Cavanagh, S., Schwartzentruber, J. et al. Nat. Genet., 46 (2014),pp. 462-466
[34]	Fontebasso, A.M., Schwartzentruber, J., Khuong-Quang, D.A. et al. Acta Neuropathol., 125 (2013),pp. 659-669
[35]	Fullgrabe, J., Kavanagh, E., Joseph, B. Histone onco-modifications Oncogene, 30 (2011),pp. 3391-3403
[36]	Funato, K., Major, T., Lewis, P.W. et al. Use of human embryonic stem cells to model pediatric gliomas with H3.3K27M histone mutation Science, 346 (2014),pp. 1529-1533
[37]	Guo, R., Zheng, L., Park, J.W. et al. BS69/ZMYND11 reads and connects histone H3.3 lysine 36 trimethylation-decorated chromatin to regulated pre-mRNA processing Mol. Cell, 56 (2014),pp. 298-310
[38]	Hake, S.B., Garcia, B.A., Duncan, E.M. et al. Expression patterns and post-translational modifications associated with mammalian histone H3 variants J. Biol. Chem., 281 (2006),pp. 559-568
[39]	Haque, F., Varlet, P., Puntonet, J. et al. Evaluation of a novel antibody to define histone 3.3 G34R mutant brain tumours Acta Neuropathol. Commun., 5 (2017),p. 45
[40]	Hashizume, R., Andor, N., Ihara, Y. et al. Pharmacologic inhibition of histone demethylation as a therapy for pediatric brainstem glioma Nat. Med., 20 (2014),pp. 1394-1396
[41]	Herz, H.M., Mohan, M., Garruss, A.S. et al. Genes Dev., 26 (2012),pp. 2604-2620
[42]	Herz, H.M., Morgan, M., Gao, X. et al. Histone H3 lysine-to-methionine mutants as a paradigm to study chromatin signaling Science, 345 (2014),pp. 1065-1070
[43]	Jones, C., Baker, S.J. Unique genetic and epigenetic mechanisms driving paediatric diffuse high-grade glioma Nat. Rev. Cancer, 14 (2014),pp. 651-661
[44]	Jones, S., Li, M., Parsons, D.W. et al. Hum. Mutat., 33 (2012),pp. 100-103
[45]	Jones, S., Wang, T.L., Shih Ie, M. et al. Science, 330 (2010),pp. 228-231
[46]	Justin, N., Zhang, Y., Tarricone, C. et al. Structural basis of oncogenic histone H3K27M inhibition of human polycomb repressive complex 2 Nat. Commun., 7 (2016),p. 11316
[47]	Kallappagoudar, S., Yadav, R.K., Lowe, B.R. et al. Histone H3 mutations–a special role for H3.3 in tumorigenesis? Chromosoma, 124 (2015),pp. 177-189
[48]	Karytinos, A., Forneris, F., Profumo, A. et al. A novel mammalian flavin-dependent histone demethylase J. Biol. Chem., 284 (2009),pp. 17775-17782
[49]	Khorasanizadeh, S. The nucleosome: from genomic organization to genomic regulation Cell, 116 (2004),pp. 259-272
[50]	Khuong-Quang, D.A., Buczkowicz, P., Rakopoulos, P. et al. K27M mutation in histone H3.3 defines clinically and biologically distinct subgroups of pediatric diffuse intrinsic pontine gliomas Acta Neuropathol., 124 (2012),pp. 439-447
[51]	Khuong-Quang, D.A., Gerges, N., Jabado, N. Mutations in histone H3.3 and chromatin remodeling genes drive pediatric and young adult glioblastomas Med. Sci. (Paris), 28 (2012),pp. 809-812
[52]	Kuo, A.J., Cheung, P., Chen, K. et al. NSD2 links dimethylation of histone H3 at lysine 36 to oncogenic programming Mol. Cell, 44 (2011),pp. 609-620
[53]	Lewis, P.W., Muller, M.M., Koletsky, M.S. et al. Inhibition of PRC2 activity by a gain-of-function H3 mutation found in pediatric glioblastoma Science, 340 (2013),pp. 857-861
[54]	Li, F., Mao, G., Tong, D. et al. The histone mark H3K36me3 regulates human DNA mismatch repair through its interaction with MutSalpha Cell, 153 (2013),pp. 590-600
[55]	Li, H., Kaminski, M.S., Li, Y. et al. Blood, 123 (2014),pp. 1487-1498
[56]	Lindroth, A.M., Plass, C. Recurrent H3.3 alterations in childhood tumors Nat. Genet., 45 (2013),pp. 1413-1414
[57]	Liu, X., McEachron, T.A., Schwartzentruber, J. et al. Histone H3 mutations in pediatric brain tumors Cold Spring Harb. Perspect. Biol., 6 (2014)
[58]	Lohr, J.G., Stojanov, P., Lawrence, M.S. et al. Discovery and prioritization of somatic mutations in diffuse large B-cell lymphoma (DLBCL) by whole-exome sequencing Proc. Natl. Acad. Sci. U. S. A., 109 (2012),pp. 3879-3884
[59]	Lu, C., Jain, S.U., Hoelper, D. et al. Histone H3K36 mutations promote sarcomagenesis through altered histone methylation landscape Science, 352 (2016),pp. 844-849
[60]	Luger, K., Mader, A.W., Richmond, R.K. et al. Crystal structure of the nucleosome core particle at 2.8 A resolution Nature, 389 (1997),pp. 251-260
[61]	Maze, I., Noh, K.M., Soshnev, A.A. et al. Every amino acid matters: essential contributions of histone variants to mammalian development and disease Nat. Rev. Genet., 15 (2014),pp. 259-271
[62]	Mehta, S., Huillard, E., Kesari, S. et al. The central nervous system-restricted transcription factor Olig2 opposes p53 responses to genotoxic damage in neural progenitors and malignant glioma Cancer Cell, 19 (2011),pp. 359-371
[63]	Mohammad, F., Weissmann, S., Leblanc, B. et al. EZH2 is a potential therapeutic target for H3K27M-mutant pediatric gliomas Nat. Med., 23 (2017),pp. 483-492
[64]	Morgan, M.A., Shilatifard, A. (Poly)combing the pediatric cancer genome for answers Science, 340 (2013),pp. 823-824
[65]	Morin, R.D., Mungall, K., Pleasance, E. et al. Mutational and structural analysis of diffuse large B-cell lymphoma using whole-genome sequencing Blood, 122 (2013),pp. 1256-1265
[66]	Neri, F., Rapelli, S., Krepelova, A. et al. Intragenic DNA methylation prevents spurious transcription initiation Nature, 543 (2017),pp. 72-77
[67]	Newbold, R.F., Mokbel, K. Evidence for a tumour suppressor function of SETD2 in human breast cancer: a new hypothesis Anticancer Res., 30 (2010),pp. 3309-3311
[68]	Nikbakht, H., Panditharatna, E., Mikael, L.G. et al. Spatial and temporal homogeneity of driver mutations in diffuse intrinsic pontine glioma Nat. Commun., 7 (2016),p. 11185
[69]	Okosun, J., Bodor, C., Wang, J. et al. Integrated genomic analysis identifies recurrent mutations and evolution patterns driving the initiation and progression of follicular lymphoma Nat. Genet., 46 (2014),pp. 176-181
[70]	Pai, C.C., Deegan, R.S., Subramanian, L. et al. A histone H3K36 chromatin switch coordinates DNA double-strand break repair pathway choice Nat. Commun., 5 (2014),p. 4091
[71]	Pathania, M., De Jay, N., Maestro, N. et al. Cancer Cell, 32 (2017)
[72]	Piunti, A., Hashizume, R., Morgan, M.A. et al. Therapeutic targeting of polycomb and BET bromodomain proteins in diffuse intrinsic pontine gliomas Nat. Med., 23 (2017),pp. 493-500
[73]	Pugh, T.J., Weeraratne, S.D., Archer, T.C. et al. Medulloblastoma exome sequencing uncovers subtype-specific somatic mutations Nature, 488 (2012),pp. 106-110
[74]	Schwartzentruber, J., Korshunov, A., Liu, X.Y. et al. Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma Nature, 482 (2012),pp. 226-231
[75]	Sturm, D., Witt, H., Hovestadt, V. et al. Cancer Cell, 22 (2012),pp. 425-437
[76]	Swartling, F.J., Savov, V., Persson, A.I. et al. Distinct neural stem cell populations give rise to disparate brain tumors in response to N-MYC Canc. Cell, 21 (2012),pp. 601-613
[77]	Talbert, P.B., Henikoff, S. Histone variants–ancient wrap artists of the epigenome Nat. Rev. Mol. Cell Biol., 11 (2010),pp. 264-275
[78]	Venneti, S., Garimella, M.T., Sullivan, L.M. et al. Brain Pathol., 23 (2013),pp. 558-564
[79]	Wagner, E.J., Carpenter, P.B. Understanding the language of Lys36 methylation at histone H3 Nat. Rev. Mol. Cell Biol., 13 (2012),pp. 115-126
[80]	Wen, H., Li, Y., Xi, Y. et al. ZMYND11 links histone H3.3K36me3 to transcription elongation and tumour suppression Nature, 508 (2014),pp. 263-268
[81]	Wu, G., Broniscer, A., McEachron, T.A. et al. Somatic histone H3 alterations in pediatric diffuse intrinsic pontine gliomas and non-brainstem glioblastomas Nat. Genet., 44 (2012),pp. 251-253
[82]	Wu, G., Diaz, A.K., Paugh, B.S. et al. The genomic landscape of diffuse intrinsic pontine glioma and pediatric non-brainstem high-grade glioma Nat. Genet., 46 (2014),pp. 444-450
[83]	Yang, S., Zheng, X., Lu, C. et al. Molecular basis for oncohistone H3 recognition by SETD2 methyltransferase Genes Dev., 30 (2016),pp. 1611-1616
[84]	Yang, S.M., Kim, B.J., Norwood Toro, L. et al. H1 linker histone promotes epigenetic silencing by regulating both DNA methylation and histone H3 methylation Proc. Natl. Acad. Sci. U. S. A., 110 (2013),pp. 1708-1713
[85]	Yuen, B.T., Knoepfler, P.S. Histone H3.3 mutations: a variant path to cancer Cancer Cell, 24 (2013),pp. 567-574
[86]	Zhang, Q., Qi, S., Xu, M. et al. Structure-function analysis reveals a novel mechanism for regulation of histone demethylase LSD2/AOF1/KDM1b Cell Res., 23 (2013),pp. 225-241