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H3K36 trimethylation-mediated biological functions in cancer

Xiao, Chu, Fan, Tao, Tian, He, Zheng, Yujia, Zhou, Zheng, Li, Shuofeng, Li, Chunxiang, He, Jie·2021·Clinical Epigenetics

Abstract

Histone modification is an important form of epigenetic regulation. Thereinto, histone methylation is a critical determination of chromatin states, participating in multiple cellular processes. As a conserved histone methylation mark, histone 3 lysine 36 trimethylation (H3K36me3) can mediate multiple transcriptional-related events, such as the regulation of transcriptional activity, transcription elongation, pre-mRNA alternative splicing, and RNA m 6 A methylation. Additionally, H3K36me3 also contributes to DNA damage repair. Given the crucial function of H3K36me3 in genome regulation, the roles of H3K36me3 and its sole methyltransferase SETD2 in pathogenesis, especially malignancies, have been emphasized in many studies, and it is conceivable that disruption of histone methylation regulatory network composed of “writer”, “eraser”, “reader”, and the mutation of H3K36me3 codes have the capacity of powerfully modulating cancer initiation and development. Here we review H3K36me3-mediated biological processes and summarize the latest findings regarding its role in cancers. We highlight the significance of epigenetic combination therapies in cancers.

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  1. Yu Y, Chen J, Gao Y, Gao J, Liao R, Wang Y, Oyang C, Li E, Zeng C, Zhou S, et al. Quantitative profiling of combinational K27/K36 modifications on histone H3 variants in mouse organs. J Proteome Res. 2016;15(3):1070–9. · DOI
  2. Henikoff S, Smith MM. Histone variants and epigenetics. Cold Spring Harb Perspect Biol. 2015;7(1):a019364. · DOI
  3. Delbarre E, Jacobsen BM, Reiner AH, Sørensen AL, Küntziger T, Collas P. Chromatin environment of histone variant H3.3 revealed by quantitative imaging and genome-scale chromatin and DNA immunoprecipitation. Mol Biol Cell. 2010;21(11):1872–84. · DOI
  4. Li J, Ahn JH, Wang GG. Understanding histone H3 lysine 36 methylation and its deregulation in disease. Cell Mol Life Sci. 2019;76(15):2899–916. · DOI
  5. Kouzarides T. Chromatin modifications and their function. Cell. 2007;128(4):693–705. · DOI · Paper page
  6. Madani Tonekaboni SA, Haibe-Kains B, Lupien M. Large organized chromatin lysine domains help distinguish primitive from differentiated cell populations. Nat Commun. 2021;12(1):499. · DOI
  7. Wagner EJ, Carpenter PB. Understanding the language of Lys36 methylation at histone H3. Nat Rev Mol Cell Biol. 2012;13(2):115–26. · DOI
  8. Nojima T, Tellier M, Foxwell J, et al. Deregulated expression of mammalian lncRNA through loss of SPT6 induces R-loop formation, replication stress, and cellular senescence. Mol Cell. 2018;72(6):970-984.e977. · DOI
  9. Bannister AJ, Schneider R, Myers FA, Thorne AW, Crane-Robinson C, Kouzarides T. Spatial distribution of di- and tri-methyl lysine 36 of histone H3 at active genes. J Biol Chem. 2005;280(18):17732–6. · DOI
  10. Sun Z, Zhang Y, Jia J, Fang Y, Tang Y, Wu H, Fang D. H3K36me3, message from chromatin to DNA damage repair. Cell Biosci. 2020;10:9. · DOI · Paper page
  11. Chen R, Zhao WQ, Fang C, Yang X, Ji M. Histone methyltransferase SETD2: a potential tumor suppressor in solid cancers. J Cancer. 2020;11(11):3349–56. · DOI
  12. Sessa A, Fagnocchi L, Mastrototaro G, Massimino L, Zaghi M, Indrigo M, Cattaneo S, Martini D, Gabellini C, Pucci C, et al. SETD5 regulates chromatin methylation state and preserves global transcriptional fidelity during brain development and neuronal wiring. Neuron. 2019;104(2):271-289.e213. · DOI
  13. Kizer KO, Phatnani HP, Shibata Y, Hall H, Greenleaf AL, Strahl BD. A novel domain in Set2 mediates RNA polymerase II interaction and couples histone H3 K36 methylation with transcript elongation. Mol Cell Biol. 2005;25(8):3305–16. · DOI
  14. Bhattacharya S, Workman JL. Regulation of SETD2 stability is important for the fidelity of H3K36me3 deposition. Epigenetics Chromatin. 2020;13(1):40. · DOI
  15. Bhattacharya S, Levy MJ, Zhang N, Li H, Florens L, Washburn MP, Workman JL. The methyltransferase SETD2 couples transcription and splicing by engaging mRNA processing factors through its SHI domain. Nat Commun. 2021;12(1):1443. · DOI
  16. Park IY, Powell RT, Tripathi DN, Dere R, Ho TH, Blasius TL, Chiang YC, Davis IJ, Fahey CC, Hacker KE, et al. Dual chromatin and cytoskeletal remodeling by SETD2. Cell. 2016;166(4):950–62. · DOI
  17. Chen K, Liu J, Liu S, Xia M, Zhang X, Han D, Jiang Y, Wang C, Cao X. Methyltransferase SETD2-mediated methylation of STAT1 Is critical for interferon antiviral activity. Cell. 2017;170(3):492-506.e414. · DOI
  18. Cloos PA, Christensen J, Agger K, Helin K. Erasing the methyl mark: histone demethylases at the center of cellular differentiation and disease. Genes Dev. 2008;22(9):1115–40. · DOI
  19. Klose RJ, Yamane K, Bae Y, Zhang D, Erdjument-Bromage H, Tempst P, Wong J, Zhang Y. The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36. Nature. 2006;442(7100):312–6. · DOI
  20. Yamamoto S, Tateishi K, Kudo Y, Yamamoto K, Isagawa T, Nagae G, Nakatsuka T, Asaoka Y, Ijichi H, Hirata Y, et al. Histone demethylase KDM4C regulates sphere formation by mediating the cross talk between Wnt and Notch pathways in colonic cancer cells. Carcinogenesis. 2013;34(10):2380–8. · DOI
  21. Liu G, Bollig-Fischer A, Kreike B, van de Vijver MJ, Abrams J, Ethier SP, Yang ZQ. Genomic amplification and oncogenic properties of the GASC1 histone demethylase gene in breast cancer. Oncogene. 2009;28(50):4491–500. · DOI
  22. Berry WL, Janknecht R. KDM4/JMJD2 histone demethylases: epigenetic regulators in cancer cells. Can Res. 2013;73(10):2936–42. · DOI
  23. Maurer-Stroh S, Dickens NJ, Hughes-Davies L, Kouzarides T, Eisenhaber F, Ponting CP. The tudor domain “royal family”: tudor, plant agenet, chromo, PWWP and MBT domains. Trends Biochem Sci. 2003;28(2):69–74. · DOI
  24. Wu H, Zeng H, Lam R, Tempel W, Amaya MF, Xu C, Dombrovski L, Qiu W, Wang Y, Min J. Structural and histone binding ability characterizations of human PWWP domains. PLoS ONE. 2011;6(6):e18919. · DOI
  25. Ballare C, Lange M, Lapinaite A, Martin GM, Morey L, Pascual G, Liefke R, Simon B, Shi Y, Gozani O, et al. Phf19 links methylated Lys36 of histone H3 to regulation of polycomb activity. Nat Struct Mol Biol. 2012;19(12):1257–65. · DOI
  26. Qin S, Guo Y, Xu C, Bian C, Fu M, Gong S, Min J. Tudor domains of the PRC2 components PHF1 and PHF19 selectively bind to histone H3K36me3. Biochem Biophys Res Commun. 2013;430(2):547–53. · DOI
  27. Keogh MC, Kurdistani SK, Morris SA, Ahn SH, Podolny V, Collins SR, Schuldiner M, Chin K, Punna T, Thompson NJ, et al. Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell. 2005;123(4):593–605. · DOI
  28. Yu S, Li J, Ji G, Long Ng Z, Siew J, Ning Lo W, Ye Y, Yuan Chew Y, Chau Long Y, Zhang W, et al. Npac is a Co-factor of histone H3K36me3 and regulates transcriptional elongation in mouse embryonic stem cells. Genomics Proteomics Bioinform. 2021. https://doi.org/10.1016/j.gpb.2020.08.004. · DOI
  29. Fei J, Ishii H, Hoeksema MA, Meitinger F, Kassavetis GA, Glass CK, Ren B, Kadonaga JT. NDF, a nucleosome-destabilizing factor that facilitates transcription through nucleosomes. Genes Dev. 2018;32(9–10):682–94. · DOI
  30. Lin LJ, Minard LV, Johnston GC, Singer RA, Schultz MC. Asf1 can promote trimethylation of H3 K36 by Set2. Mol Cell Biol. 2010;30(5):1116–29. · DOI
  31. Yoh SM, Lucas JS, Jones KA. The Iws1:Spt6:CTD complex controls cotranscriptional mRNA biosynthesis and HYPB/Setd2-mediated histone H3K36 methylation. Genes Dev. 2008;22(24):3422–34. · DOI
  32. Zhang T, Cooper S, Brockdorff N. The interplay of histone modifications—writers that read. EMBO Rep. 2015;16(11):1467–81. · DOI
  33. Tanaka H, Igata T, Etoh K, Koga T, Takebayashi SI, Nakao M. The NSD2/WHSC1/MMSET methyltransferase prevents cellular senescence-associated epigenomic remodeling. Aging Cell. 2020;19(7):e13173. · DOI
  34. García-Carpizo V, Sarmentero J, Han B, Graña O, Ruiz-Llorente S, Pisano DG, Serrano M, Brooks HB, Campbell RM, Barrero MJ. NSD2 contributes to oncogenic RAS-driven transcription in lung cancer cells through long-range epigenetic activation. Sci Rep. 2016;6:32952. · DOI
  35. Yuan W, Xie J, Long C, Erdjument-Bromage H, Ding X, Zheng Y, Tempst P, Chen S, Zhu B, Reinberg D. Heterogeneous nuclear ribonucleoprotein L Is a subunit of human KMT3a/Set2 complex required for H3 Lys-36 trimethylation activity in vivo. J Biol Chem. 2009;284(23):15701–7. · DOI
  36. Zhao Y, Zhou J, He L, Li Y, Yuan J, Sun K, Chen X, Bao X, Esteban MA, Sun H, et al. MyoD induced enhancer RNA interacts with hnRNPL to activate target gene transcription during myogenic differentiation. Nat Commun. 2019;10(1):5787. · DOI
  37. Strahl BD, Grant PA, Briggs SD, Sun ZW, Bone JR, Caldwell JA, Mollah S, Cook RG, Shabanowitz J, Hunt DF, et al. Set2 is a nucleosomal histone H3-selective methyltransferase that mediates transcriptional repression. Mol Cell Biol. 2002;22(5):1298–306. · DOI
  38. Chantalat S, Depaux A, Hery P, Barral S, Thuret JY, Dimitrov S, Gerard M. Histone H3 trimethylation at lysine 36 is associated with constitutive and facultative heterochromatin. Genome Res. 2011;21(9):1426–37. · DOI
  39. Veloso A, Kirkconnell KS, Magnuson B, Biewen B, Paulsen MT, Wilson TE, Ljungman M. Rate of elongation by RNA polymerase II is associated with specific gene features and epigenetic modifications. Genome Res. 2014;24(6):896–905. · DOI · Paper page
  40. Kadosh D, Struhl K. Targeted recruitment of the Sin3-Rpd3 histone deacetylase complex generates a highly localized domain of repressed chromatin in vivo. Mol Cell Biol. 1998;18(9):5121–7. · DOI
  41. Xu C, Cui G, Botuyan MV, Mer G. Structural basis for the recognition of methylated histone H3K36 by the Eaf3 subunit of histone deacetylase complex Rpd3S. Structure. 2008;16(11):1740–50. · DOI
  42. Govind CK, Qiu H, Ginsburg DS, Ruan C, Hofmeyer K, Hu C, Swaminathan V, Workman JL, Li B, Hinnebusch AG. Phosphorylated Pol II CTD recruits multiple HDACs, including Rpd3C(S), for methylation-dependent deacetylation of ORF nucleosomes. Mol Cell. 2010;39(2):234–46. · DOI
  43. Georgescu PR, Capella M, Fischer-Burkart S, Braun S. The euchromatic histone mark H3K36me3 preserves heterochromatin through sequestration of an acetyltransferase complex in fission yeast. Microb Cell. 2020;7(3):80–92. · DOI
  44. Yuan W, Xu M, Huang C, Liu N, Chen S, Zhu B. H3K36 methylation antagonizes PRC2-mediated H3K27 methylation. J Biol Chem. 2011;286(10):7983–9. · DOI
  45. Zheng Y, Sweet SM, Popovic R, Martinez-Garcia E, Tipton JD, Thomas PM, Licht JD, Kelleher NL. Total kinetic analysis reveals how combinatorial methylation patterns are established on lysines 27 and 36 of histone H3. Proc Natl Acad Sci USA. 2012;109(34):13549–54. · DOI
  46. Yuan H, Han Y, Wang X, Li N, Liu Q, Yin Y, Wang H, Pan L, Li L, Song K, et al. SETD2 Restricts Prostate Cancer Metastasis by Integrating EZH2 and AMPK Signaling Pathways. Cancer Cell. 2020;38(3):350-365.e357. · DOI
  47. Xie L, Pelz C, Wang W, Bashar A, Varlamova O, Shadle S, Impey S. KDM5B regulates embryonic stem cell self-renewal and represses cryptic intragenic transcription. EMBO J. 2011;30(8):1473–84. · DOI
  48. Xu Q, Xiang Y, Wang Q, Wang L, Brind’Amour J, Bogutz AB, Zhang Y, Zhang B, Yu G, Xia W, et al. SETD2 regulates the maternal epigenome, genomic imprinting and embryonic development. Nat Genet. 2019;51(5):844–56. · DOI
  49. Shirane K, Miura F, Ito T, Lorincz MC. NSD1-deposited H3K36me2 directs de novo methylation in the mouse male germline and counteracts Polycomb-associated silencing. Nat Genet. 2020;52(10):1088–98. · DOI
  50. Teissandier A, Bourc’his D. Gene body DNA methylation conspires with H3K36me3 to preclude aberrant transcription. EMBO J. 2017;36(11):1471–3. · DOI
  51. Dhayalan A, Rajavelu A, Rathert P, Tamas R, Jurkowska RZ, Ragozin S, Jeltsch A. The Dnmt3a PWWP domain reads histone 3 lysine 36 trimethylation and guides DNA methylation. J Biol Chem. 2010;285(34):26114–20. · DOI
  52. Duymich CE, Charlet J, Yang X, Jones PA, Liang G. DNMT3B isoforms without catalytic activity stimulate gene body methylation as accessory proteins in somatic cells. Nat Commun. 2016;7:11453. · DOI
  53. Stewart KR, Veselovska L, Kim J, Huang J, Saadeh H, Tomizawa S, Smallwood SA, Chen T, Kelsey G. Dynamic changes in histone modifications precede de novo DNA methylation in oocytes. Genes Dev. 2015;29(23):2449–62. · DOI
  54. Masalmeh RHA, Taglini F, Rubio-Ramon C, Musialik KI, Higham J, Davidson-Smith H, Kafetzopoulos I, Pawlicka KP, Finan HM, Clark R, et al. De novo DNA methyltransferase activity in colorectal cancer is directed towards H3K36me3 marked CpG islands. Nat Commun. 2021;12(1):694. · DOI
  55. Bell JS, Kagey JD, Barwick BG, Dwivedi B, McCabe MT, Kowalski J, Vertino PM. Factors affecting the persistence of drug-induced reprogramming of the cancer methylome. Epigenetics. 2016;11(4):273–87. · DOI
  56. Nilsen TW, Graveley BR. Expansion of the eukaryotic proteome by alternative splicing. Nature. 2010;463(7280):457–63. · DOI
  57. Luco RF, Pan Q, Tominaga K, Blencowe BJ, Pereira-Smith OM, Misteli T. Regulation of alternative splicing by histone modifications. Science (New York, NY). 2010;327(5968):996–1000. · DOI
  58. Pradeepa MM, Sutherland HG, Ule J, Grimes GR, Bickmore WA. Psip1/Ledgf p52 binds methylated histone H3K36 and splicing factors and contributes to the regulation of alternative splicing. PLoS Genet. 2012;8(5):e1002717. · DOI
  59. Daugaard M, Baude A, Fugger K, Povlsen LK, Beck H, Sørensen CS, Petersen NH, Sorensen PH, Lukas C, Bartek J, et al. LEDGF (p75) promotes DNA-end resection and homologous recombination. Nat Struct Mol Biol. 2012;19(8):803–10. · DOI
  60. Sanidas I, Polytarchou C, Hatziapostolou M, Ezell SA, Kottakis F, Hu L, Guo A, Xie J, Comb MJ, Iliopoulos D, et al. Phosphoproteomics screen reveals akt isoform-specific signals linking RNA processing to lung cancer. Mol Cell. 2014;53(4):577–90. · DOI
  61. Kolasinska-Zwierz P, Down T, Latorre I, Liu T, Liu XS, Ahringer J. Differential chromatin marking of introns and expressed exons by H3K36me3. Nat Genet. 2009;41(3):376–81. · DOI
  62. Dhamodharan S, Rose MM, Chakkarappan SR, Umadharshini KV, Arulmurugan R, Subbiah S, Inoue I, Munirajan AK. Genetic variant rs10251977 (G>A) in EGFR-AS1 modulates the expression of EGFR isoforms A and D. Sci Rep. 2021;11(1):8808. · DOI
  63. Li X-W, Shi B-Y, Yang Q-L, Wu J, Wu H-M, Wang Y-F, Wu Z-J, Fan Y-M, Wang Y-P. Epigenetic regulation of CDH1 exon 8 alternative splicing in gastric cancer. BMC Cancer. 2015;15(1):1–8. · DOI
  64. Guo R, Zheng L, Park JW, Lv R, Chen H, Jiao F, Xu W, Mu S, Wen H, Qiu J, et al. BS69/ZMYND11 reads and connects histone H3.3 lysine 36 trimethylation-decorated chromatin to regulated pre-mRNA processing. Mol Cell. 2014;56(2):298–310. · DOI
  65. de Almeida SF, Grosso AR, Koch F, Fenouil R, Carvalho S, Andrade J, Levezinho H, Gut M, Eick D, Gut I, et al. Splicing enhances recruitment of methyltransferase HYPB/Setd2 and methylation of histone H3 Lys36. Nat Struct Mol Biol. 2011;18(9):977–83. · DOI
  66. Huang H, Weng H, Chen J. The biogenesis and precise control of RNA m(6)A methylation. Trends Genet. 2020;36(1):44–52. · DOI
  67. Zhang Y, Yuan F, Presnell SR, Tian K, Gao Y, Tomkinson AE, Gu L, Li GM. Reconstitution of 5’-directed human mismatch repair in a purified system. Cell. 2005;122(5):693–705. · DOI
  68. Li F, Mao G, Tong D, Huang J, Gu L, Yang W, Li GM. The histone mark H3K36me3 regulates human DNA mismatch repair through its interaction with MutSalpha. Cell. 2013;153(3):590–600. · DOI
  69. Aska EM, Dermadi D, Kauppi L. Single-cell sequencing of mouse thymocytes reveals mutational landscape shaped by replication errors, mismatch repair, and H3K36me3. iScience. 2020;23(9):101452. · DOI
  70. Huang Y, Gu L, Li GM. H3K36me3-mediated mismatch repair preferentially protects actively transcribed genes from mutation. J Biol Chem. 2018;293(20):7811–23. · DOI
  71. Fang J, Huang Y, Mao G, Yang S, Rennert G, Gu L, Li H, Li GM. Cancer-driving H3G34V/R/D mutations block H3K36 methylation and H3K36me3-MutSalpha interaction. Proc Natl Acad Sci USA. 2018;115(38):9598–603. · DOI
  72. Li L, Wang Y. Cross-talk between the H3K36me3 and H4K16ac histone epigenetic marks in DNA double-strand break repair. J Biol Chem. 2017;292(28):11951–9. · DOI
  73. Chen Y, Lyu R, Rong B, Zheng Y, Lin Z, Dai R, Zhang X, Xie N, Wang S, Tang F, et al. Refined spatial temporal epigenomic profiling reveals intrinsic connection between PRDM9-mediated H3K4me3 and the fate of double-stranded breaks. Cell Res. 2020;30(3):256–68. · DOI
  74. Black JC, Manning AL, Van Rechem C, Kim J, Ladd B, Cho J, Pineda CM, Murphy N, Daniels DL, Montagna C, et al. KDM4A lysine demethylase induces site-specific copy gain and rereplication of regions amplified in tumors. Cell. 2013;154(3):541–55. · DOI
  75. Zhang LQ, Li QZ, Jin W, Zuo Y, Guo SC. Genome-wide analysis of H3K36me3 and its regulations to cancer-related genes expression in human cell lines. Biosystems. 2018;171:59–65. · DOI
  76. Al Sarakbi W, Sasi W, Jiang WG, Roberts T, Newbold RF, Mokbel K. The mRNA expression of SETD2 in human breast cancer: correlation with clinico-pathological parameters. BMC Cancer. 2009;9:290. · DOI
  77. Behjati S, Tarpey PS, Presneau N, Scheipl S, Pillay N, Van Loo P, Wedge DC, Cooke SL, Gundem G, Davies H, et al. Distinct H3F3A and H3F3B driver mutations define chondroblastoma and giant cell tumor of bone. Nat Genet. 2013;45(12):1479–82. · DOI · Paper page
  78. Yu W, Wang Z, Zhang K, Chi Z, Xu T, Jiang D, Chen S, Li W, Yang X, Zhang X, et al. One-carbon metabolism supports s-adenosylmethionine and histone methylation to drive inflammatory macrophages. Mol Cell. 2019;75(6):1147-1160.e1145. · DOI
  79. Newman AC, Maddocks ODK. Serine and functional metabolites in cancer. Trends Cell Biol. 2017;27(9):645–57. · DOI
  80. Pfister SX, Markkanen E, Jiang Y, Sarkar S, Woodcock M, Orlando G, Mavrommati I, Pai CC, Zalmas LP, Drobnitzky N, et al. Inhibiting WEE1 selectively kills histone H3K36me3-deficient cancers by dNTP starvation. Cancer Cell. 2015;28(5):557–68. · DOI
  81. Mar BG, Bullinger LB, McLean KM, Grauman PV, Harris MH, Stevenson K, Neuberg DS, Sinha AU, Sallan SE, Silverman LB, et al. Mutations in epigenetic regulators including SETD2 are gained during relapse in paediatric acute lymphoblastic leukaemia. Nat Commun. 2014;5:3469. · DOI
  82. Zhang LQ, Fan GL, Liu JJ, Liu L, Li QZ, Lin H. Identification of key histone modifications and their regulatory regions on gene expression level changes in chronic myelogenous leukemia. Front Cell Dev Biol. 2020;8:621578. · DOI
  83. Zhu X, He F, Zeng H, Ling S, Chen A, Wang Y, Yan X, Wei W, Pang Y, Cheng H, et al. Identification of functional cooperative mutations of SETD2 in human acute leukemia. Nat Genet. 2014;46(3):287–93. · DOI
  84. Zhang YL, Sun JW, Xie YY, Zhou Y, Liu P, Song JC, Xu CH, Wang L, Liu D, Xu AN, et al. Setd2 deficiency impairs hematopoietic stem cell self-renewal and causes malignant transformation. Cell Res. 2018;28(4):476–90. · DOI
  85. Chen BY, Song J, Hu CL, Chen SB, Zhang Q, Xu CH, Wu JC, Hou D, Sun M, Zhang YL, et al. SETD2 deficiency accelerates MDS-associated leukemogenesis via S100a9 in NHD13 mice and predicts poor prognosis in MDS. Blood. 2020;135(25):2271–85. · DOI
  86. Skucha A, Ebner J, Grebien F. Roles of SETD2 in leukemia-transcription, DNA-damage, and beyond. Int J Mol Sci. 2019;20(5):1029. · DOI
  87. Li J, Galbo PM Jr, Gong W, Storey AJ, Tsai YH, Yu X, Ahn JH, Guo Y, Mackintosh SG, Edmondson RD, et al. ZMYND11-MBTD1 induces leukemogenesis through hijacking NuA4/TIP60 acetyltransferase complex and a PWWP-mediated chromatin association mechanism. Nat Commun. 2021;12(1):1045. · DOI
  88. Wu X, Li R, Song Q, Zhang C, Jia R, Han Z, Zhou L, Sui H, Liu X, Zhu H, et al. JMJD2C promotes colorectal cancer metastasis via regulating histone methylation of MALAT1 promoter and enhancing beta-catenin signaling pathway. J Exp Clin Cancer Res. 2019;38(1):435. · DOI
  89. Yuan H, Li N, Fu D, Ren J, Hui J, Peng J, Liu Y, Qiu T, Jiang M, Pan Q, et al. Histone methyltransferase SETD2 modulates alternative splicing to inhibit intestinal tumorigenesis. J Clin Invest. 2017;127(9):3375–91. · DOI
  90. Wang XM, Lu Y, Song YM, Dong J, Li RY, Wang GL, Wang X, Zhang SD, Dong ZH, Lu M, et al. Integrative genomic study of Chinese clear cell renal cell carcinoma reveals features associated with thrombus. Nat Commun. 2020;11(1):739. · DOI
  91. Dizman N, Philip EJ, Pal SK. Genomic profiling in renal cell carcinoma. Nat Rev Nephrol. 2020;16(8):435–51. · DOI
  92. Varela I, Tarpey P, Raine K, Huang D, Ong CK, Stephens P, Davies H, Jones D, Lin ML, Teague J, et al. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature. 2011;469(7331):539–42. · DOI
  93. Guo G, Gui Y, Gao S, Tang A, Hu X, Huang Y, Jia W, Li Z, He M, Sun L, et al. Frequent mutations of genes encoding ubiquitin-mediated proteolysis pathway components in clear cell renal cell carcinoma. Nat Genet. 2011;44(1):17–9. · DOI
  94. Zbar B, Brauch H, Talmadge C, Linehan M. Loss of alleles of loci on the short arm of chromosome 3 in renal cell carcinoma. Nature. 1987;327(6124):721–4. · DOI
  95. Carvalho S, Vitor AC, Sridhara SC, Martins FB, Raposo AC, Desterro JM, Ferreira J, de Almeida SF. SETD2 is required for DNA double-strand break repair and activation of the p53-mediated checkpoint. Elife. 2014;3:e02482. · DOI
  96. Rao H, Li X, Liu M, Liu J, Feng W, Tang H, Xu J, Gao WQ, Li L. Multilevel regulation of β-catenin activity by SETD2 suppresses the transition from polycystic kidney disease to clear cell renal cell carcinoma. Can Res. 2021;81(13):3554–67. · DOI
  97. Hingorani SR, Petricoin EF, Maitra A, Rajapakse V, King C, Jacobetz MA, Ross S, Conrads TP, Veenstra TD, Hitt BA, et al. Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell. 2003;4(6):437–50. · DOI · Paper page
  98. Niu N, Lu P, Yang Y, He R, Zhang L, Shi J, Wu J, Yang M, Zhang ZG, Wang LW, et al. Loss of Setd2 promotes Kras-induced acinar-to-ductal metaplasia and epithelia-mesenchymal transition during pancreatic carcinogenesis. Gut. 2020;69(4):715–26. · DOI
  99. Zhou Y, Zheng X, Xu B, Deng H, Chen L, Jiang J. Histone methyltransferase SETD2 inhibits tumor growth via suppressing CXCL1-mediated activation of cell cycle in lung adenocarcinoma. Aging. 2020;12(24):25189–206. · DOI
  100. Walter DM, Venancio OS, Buza EL, Tobias JW, Deshpande C, Gudiel AA, Kim-Kiselak C, Cicchini M, Yates TJ, Feldser DM. Systematic in vivo inactivation of chromatin-regulating enzymes identifies Setd2 as a potent tumor suppressor in lung adenocarcinoma. Can Res. 2017;77(7):1719–29. · DOI
  101. Garrido-Castro AC, Spurr LF, Hughes ME, Li YY, Cherniack AD, Kumari P, Lloyd MR, Bychkovsky B, Barroso-Sousa R, Di Lascio S, et al. Genomic characterization of de novo metastatic breast cancer. Clin Cancer Res Off J Am Assoc Cancer Res. 2021;27(4):1105–18. · DOI
  102. Hateboer G, Gennissen A, Ramos YF, Kerkhoven RM, Sonntag-Buck V, Stunnenberg HG, Bernards R. BS69, a novel adenovirus E1A-associated protein that inhibits E1A transactivation. Embo J. 1995;14(13):3159–69. · DOI
  103. Wen H, Li Y, Xi Y, Jiang S, Stratton S, Peng D, Tanaka K, Ren Y, Xia Z, Wu J, et al. ZMYND11 links histone H3.3K36me3 to transcription elongation and tumour suppression. Nature. 2014;508(7495):263–8. · DOI
  104. Tsang JY, Lai ST, Ni YB, Shao Y, Poon IK, Kwan JS, Chow C, Shea KH, Tse GM. SETD2 alterations and histone H3K36 trimethylation in phyllodes tumor of breast. Breast Cancer Res Treat. 2021;187(2):339–47. · DOI
  105. Vranic S, Palazzo J, Sanati S, Florento E, Contreras E, Xiu J, Swensen J, Gatalica Z. Potential novel therapy targets in neuroendocrine carcinomas of the breast. Clin Breast Cancer. 2019;19(2):131–6. · DOI
  106. Yuen BT, Knoepfler PS. Histone H3.3 mutations: a variant path to cancer. Cancer Cell. 2013;24(5):567–74. · DOI
  107. Mohammad F, Helin K. Oncohistones: drivers of pediatric cancers. Genes Dev. 2017;31(23–24):2313–24. · DOI
  108. Chan KM, Fang D, Gan H, Hashizume R, Yu C, Schroeder M, Gupta N, Mueller S, James CD, Jenkins R, et al. The histone H3.3K27M mutation in pediatric glioma reprograms H3K27 methylation and gene expression. Genes Dev. 2013;27(9):985–90. · DOI · Paper page
  109. Bjerke L, Mackay A, Nandhabalan M, Burford A, Jury A, Popov S, Bax DA, Carvalho D, Taylor KR, Vinci M, et al. Histone H3.3 mutations drive pediatric glioblastoma through upregulation of MYCN. Cancer Discov. 2013;3(5):512–9. · DOI
  110. Li M, Cheng J, Ma Y, Guo H, Shu H, Huang H, Kuang Y, Yang T. The histone demethylase JMJD2A promotes glioma cell growth via targeting Akt-mTOR signaling. Cancer Cell Int. 2020;20:101. · DOI
  111. Lu C, Jain SU, Hoelper D, Bechet D, Molden RC, Ran L, Murphy D, Venneti S, Hameed M, Pawel BR, et al. Histone H3K36 mutations promote sarcomagenesis through altered histone methylation landscape. Science (New York, NY). 2016;352(6287):844–9. · DOI
  112. Papillon-Cavanagh S, Lu C, Gayden T, Mikael LG, Bechet D, Karamboulas C, Ailles L, Karamchandani J, Marchione DM, Garcia BA, et al. Impaired H3K36 methylation defines a subset of head and neck squamous cell carcinomas. Nat Genet. 2017;49(2):180–5. · DOI
  113. Wang L, Zehir A, Nafa K, Zhou N, Berger MF, Casanova J, Sadowska J, Lu C, Allis CD, Gounder M, et al. Genomic aberrations frequently alter chromatin regulatory genes in chordoma. Genes Chromosom Cancer. 2016;55(7):591–600. · DOI
  114. Zhu GG, Ramirez D, Chen W, Lu C, Wang L, Frosina D, Jungbluth A, Ntiamoah P, Nafa K, Boland PJ, et al. Chromosome 3p loss of heterozygosity and reduced expression of H3K36me3 correlate with longer relapse-free survival in sacral conventional chordoma. Hum Pathol. 2020;104:73–83. · DOI
  115. Li XJ, Li QL, Ju LG, Zhao C, Zhao LS, Du JW, Wang Y, Zheng L, Song BL, Li LY, et al. Deficiency of histone methyltransferase SET domain-containing 2 in liver leads to abnormal lipid metabolism and HCC. Hepatology. 2020;73:1797. · DOI
  116. Hu F, Li H, Liu L, Xu F, Lai S, Luo X, Hu J, Yang X. Histone demethylase KDM4D promotes gastrointestinal stromal tumor progression through HIF1β/VEGFA signalling. Mol Cancer. 2018;17(1):107. · DOI
  117. Singh S, Abu-Zaid A, Lin W, Low J, Abdolvahabi A, Jin H, Wu Q, Cooke B, Fang J, Bowling J, et al. 17-DMAG dually inhibits Hsp90 and histone lysine demethylases in alveolar rhabdomyosarcoma. iScience. 2021;24(1):101996. · DOI
  118. Zhou M, Li Y, Lin S, Chen Y, Qian Y, Zhao Z, Fan H. H3K9me3, H3K36me3, and H4K20me3 expression correlates with patient outcome in esophageal squamous cell carcinoma as epigenetic markers. Dig Dis Sci. 2019;64(8):2147–57. · DOI
  119. Shen X, Li Y, Xu Y, Liu M, Zhang Q, Yin R, Zhou M, Lin S, Fan H. Hypoxia-inducible factor-1α cooperates with histone Lys methylation to predict prognosis in esophageal squamous cell carcinoma. Biomark Med. 2021;15(7):509–22. · DOI
  120. Kim HG, Sung JY, Na K, Kim SW. Low H3K9me3 expression is associated with poor prognosis in patients with distal common bile duct cancer. In Vivo. 2020;34(6):3619–26. · DOI
  121. Kim KH, Roberts CW. Targeting EZH2 in cancer. Nat Med. 2016;22(2):128–34. · DOI · Paper page
  122. Bates SE. Epigenetic therapies for cancer. N Engl J Med. 2020;383(7):650–63. · DOI
  123. Zheng W, Ibanez G, Wu H, Blum G, Zeng H, Dong A, Li F, Hajian T, Allali-Hassani A, Amaya MF, et al. Sinefungin derivatives as inhibitors and structure probes of protein lysine methyltransferase SETD2. J Am Chem Soc. 2012;134(43):18004–14. · DOI
  124. Bajusz D, Bognar Z, Ebner J, Grebien F, Keseru GM. Discovery of a non-nucleoside SETD2 methyltransferase inhibitor against acute myeloid leukemia. Int J Mol Sci. 2021;22(18):10055. · DOI
  125. Yang H, Cui W, Wang L. Epigenetic synthetic lethality approaches in cancer therapy. Clin Epigenetics. 2019;11(1):136. · DOI
  126. Chen YK, Bonaldi T, Cuomo A, Del Rosario JR, Hosfield DJ, Kanouni T, Kao SC, Lai C, Lobo NA, Matuszkiewicz J, et al. Design of KDM4 Inhibitors with antiproliferative effects in cancer models. ACS Med Chem Lett. 2017;8(8):869–74. · DOI
  127. Jones PA, Ohtani H, Chakravarthy A, De Carvalho DD. Epigenetic therapy in immune-oncology. Nat Rev Cancer. 2019;19(3):151–61. · DOI
  128. Sheng W, LaFleur MW, Nguyen TH, Chen S, Chakravarthy A, Conway JR, Li Y, Chen H, Yang H, Hsu PH, et al. LSD1 ablation stimulates anti-tumor immunity and enables checkpoint blockade. Cell. 2018;174(3):549-563.e519. · DOI · Paper page
  129. Yang R, Cheng S, Luo N, Gao R, Yu K, Kang B, Wang L, Zhang Q, Fang Q, Zhang L, et al. Distinct epigenetic features of tumor-reactive CD8+ T cells in colorectal cancer patients revealed by genome-wide DNA methylation analysis. Genome Biol. 2019;21(1):2. · DOI
  130. Li X, Zhang Y, Chen M, Mei Q, Liu Y, Feng K, Jia H, Dong L, Shi L, Liu L, et al. Increased IFNgamma(+) T cells are responsible for the clinical responses of low-dose DNA-demethylating agent decitabine antitumor therapy. Clin Cancer Res Off J Am Assoc Cancer Res. 2017;23(20):6031–43. · DOI
  131. Pan X, Zheng L. Epigenetics in modulating immune functions of stromal and immune cells in the tumor microenvironment. Cell Mol Immunol. 2020;17(9):940–53. · DOI
  132. Ghoneim HE, Fan Y, Moustaki A, Abdelsamed HA, Dash P, Dogra P, Carter R, Awad W, Neale G, Thomas PG, et al. De novo epigenetic programs inhibit PD-1 blockade-mediated T cell rejuvenation. Cell. 2017;170(1):142-157.e119. · DOI
  133. Wang J, Hasan F, Frey AC, Li HS, Park J, Pan K, Haymaker C, Bernatchez C, Lee DA, Watowich SS, et al. Histone deacetylase inhibitors and IL21 cooperate to reprogram human effector CD8(+) T cells to memory T cells. Cancer Immunol Res. 2020;8(6):794–805. · DOI
  134. Jenke R, Ressing N, Hansen FK, Aigner A, Buch T. Anticancer therapy with HDAC inhibitors: mechanism-based combination strategies and future perspectives. Cancers (Basel). 2021;13(4):634. · DOI
  135. McAnena P, Brown JA, Kerin MJ. Circulating nucleosomes and nucleosome modifications as biomarkers in cancer. Cancers (Basel). 2017;9(1):5. · DOI
  136. Vad-Nielsen J, Meldgaard P, Sorensen BS, Nielsen AL. Cell-free chromatin immunoprecipitation (cfChIP) from blood plasma can determine gene-expression in tumors from non-small-cell lung cancer patients. Lung Cancer. 2020;147:244–51. · DOI
  137. Ferrari AC, Alumkal JJ, Stein MN, Taplin ME, Babb J, Barnett ES, Gomez-Pinillos A, Liu X, Moore D, DiPaola R, et al. Epigenetic therapy with panobinostat combined with bicalutamide rechallenge in castration-resistant prostate cancer. Clin Cancer Res Off J Am Assoc Cancer Res. 2019;25(1):52–63. · DOI
  138. Witta SE, Jotte RM, Konduri K, Neubauer MA, Spira AI, Ruxer RL, Varella-Garcia M, Bunn PA Jr, Hirsch FR. Randomized phase II trial of erlotinib with and without entinostat in patients with advanced non-small-cell lung cancer who progressed on prior chemotherapy. J Clin Oncol. 2012;30(18):2248–55. · DOI
  139. Lee V, Wang J, Zahurak M, Gootjes E, Verheul HM, Parkinson R, Kerner Z, Sharma A, Rosner G, De Jesus-Acosta A, et al. A phase I trial of a guadecitabine (SGI-110) and irinotecan in metastatic colorectal cancer patients previously exposed to irinotecan. Clin Cancer Res Off J Am Assoc Cancer Res. 2018;24(24):6160–7. · DOI
  140. Duan YC, Ma YC, Qin WP, Ding LN, Zheng YC, Zhu YL, Zhai XY, Yang J, Ma CY, Guan YY. Design and synthesis of tranylcypromine derivatives as novel LSD1/HDACs dual inhibitors for cancer treatment. Eur J Med Chem. 2017;140:392–402. · DOI
  141. Kalin JH, Wu M, Gomez AV, Song Y, Das J, Hayward D, Adejola N, Wu M, Panova I, Chung HJ, et al. Targeting the CoREST complex with dual histone deacetylase and demethylase inhibitors. Nat Commun. 2018;9(1):53. · DOI
  142. Cheng C, Yun F, Ullah S, Yuan Q. Discovery of novel cyclin-dependent kinase (CDK) and histone deacetylase (HDAC) dual inhibitors with potent in vitro and in vivo anticancer activity. Eur J Med Chem. 2020;189:112073. · DOI
  143. Xie R, Li Y, Tang P, Yuan Q. Rational design, synthesis and preliminary antitumor activity evaluation of a chlorambucil derivative with potent DNA/HDAC dual-targeting inhibitory activity. Bioorg Med Chem Lett. 2017;27(18):4415–20. · DOI
  144. Bian Y, Li W, Kremer DM, Sajjakulnukit P, Li S, Crespo J, Nwosu ZC, Zhang L, Czerwonka A, Pawlowska A, et al. Cancer SLC43A2 alters T cell methionine metabolism and histone methylation. Nature. 2020;585(7824):277–82. · DOI

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Metadata

Authors
Xiao, C., Fan, T., Tian, H., Zheng, Y., Zhou, Z., Li, S., Li, C., & He, J.
Venue
Clinical Epigenetics
Published
2021-10-29
Volume
13
Issue
1
ISSN
  • 1868-7075
  • 1868-7083
Cited by
63
References
15
Language
en
Funders
  • National Natural Science Foundation of China (81972196)
  • National Key R&D Program of China (2020AAA0109505)
  • R&D Program of Beijing Municipal Education Commission (KJZD20191002302)

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