Modifications of H3K4 methylation levels are associated with DNA hypermethylation in acute myeloid leukemia.


Journal

The FEBS journal
ISSN: 1742-4658
Titre abrégé: FEBS J
Pays: England
ID NLM: 101229646

Informations de publication

Date de publication:
03 2020
Historique:
received: 05 04 2019
revised: 02 08 2019
accepted: 06 10 2019
pubmed: 11 10 2019
medline: 20 1 2021
entrez: 11 10 2019
Statut: ppublish

Résumé

The 'instructive model' of aberrant DNA methylation in human tumors is based on the observation that CpG islands prone to hypermethylation in cancers are embedded in chromatin enriched in H3K27me3 in human embryonic stem cells (hESC). Recent studies also link methylation of CpG islands to the methylation status of H3K4, where H3K4me3 is inversely correlated with DNA methylation. To provide insight into these conflicting findings, we generated DNA methylation profiles for acute myeloid leukemia samples from patients and leukemic cell lines and integrated them with publicly available ChIp-seq data, containing H3K4me3 and H3K27me3 CpG island occupation in hESC, or hematopoietic stem or progenitor cells (hHSC/MPP). Hypermethylated CpG islands in AML samples displayed H3K27me3 enrichments in hESC and hHSC/MPP; however, ChIp analysis of specific hypermethylated CpG islands revealed a significant reduction in H3K4me3 signal with a concomitant increase in H3K4me0 levels as opposed to a nonsignificant increase in H3K27me3 marks. The integration of AML DNA methylation profiles with the ChIp-seq data in hESC and hHSC/MPP also led to the identification of Iroquois homeobox 2 (IRX2) as a previously unknown factor promoting differentiation of leukemic cells. Our results indicate that in contrast to the 'instructive model', H3K4me3 levels are strongly associated with DNA methylation patterns in AML and have a role in the regulation of critical genes, such as the putative tumor suppressor IRX2.

Identifiants

pubmed: 31599112
doi: 10.1111/febs.15086
doi:

Substances chimiques

Histones 0
Homeodomain Proteins 0
IRX2 protein, human 0
Transcription Factors 0
histone H3 trimethyl Lys4 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1155-1175

Informations de copyright

© 2019 Federation of European Biochemical Societies.

Références

Ehrlich M (2009) DNA hypomethylation in cancer cells. Epigenomics 1, 239-259.
Gaudet F, Hodgson JG, Eden A, Jackson-Grusby L, Dausman J, Gray JW, Leonhardt H & Jaenisch R (2003) Induction of tumors in mice by genomic hypomethylation. Science 300, 489-492.
Eden A, Gaudet F, Waghmare A & Jaenisch R (2003) Chromosomal instability and tumors promoted by DNA hypomethylation. Science 300, 455-455.
Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, Onyango P, Cui H, Gabo K, Rongione M, Webster M et al. (2009) The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet 41, 178-186.
Landau DA, Clement K, Ziller MJ, Boyle P, Fan J, Gu H, Stevenson K, Sougnez C, Wang L, Li S et al. (2014) Locally disordered methylation forms the basis of intratumor methylome variation in chronic lymphocytic leukemia. Cancer Cell 26, 813-825.
Mudbhary R, Hoshida Y, Chernyavskaya Y, Jacob V, Villanueva A, Fiel M, Chen X, Kojima K, Thung S, Bronson RT et al. (2014) UHRF1 overexpression drives DNA hypomethylation and hepatocellular carcinoma. Cancer Cell 25, 196-209.
Helman E, Lawrence MS, Stewart C, Sougnez C, Getz G & Meyerson M (2014) Somatic retrotransposition in human cancer revealed by whole- genome and exome sequencing. Genome Res 24, 1053-1063.
Tubio JM, Li Y, Ju YS, Martincorena I, Cooke SL, Tojo M,Gundem G, Pipinikas CP, Zamora J, Raine K et al. (2014) Mobile DNA in cancer. Extensive transduction of nonrepetitive DNA mediated by L1 retrotransposition in cancer genomes. Science 345, 1251343.
Pfeifer GP (2018) Defining driver DNA methylation changes in human cancer. Int J Mol Sci 19, pii: E1166. https://doi.org/10.3390/ijms19041166
Taberlay PC, Statham AL, Kelly TK, Clark SJ & Jones PA (2014) Reconfiguration of nucleosome-depleted regions at distal regulatory elements accompanies DNA methylation of enhancers and insulators in cancer. Genome Res 9, 1421-1432.
Doi A, Park IH, Wen B, Murakami P, Aryee MJ, Irizarry R, Herb B, Ladd- Acosta C, Rho J, Loewer S et al. (2009) Differential methylation of tissue- and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat Genet 41, 1350-1353.
Ji H, Ehrlich LI, Seita J, Murakami P, Doi A, Lindau P, Lee H, Aryee MJ, Irizarry RA, Kim K et al. (2010) Comprehensive methylome map of lineage commitment from haematopoietic progenitors. Nature 467, 338-342.
Greger V, Debus N, Lohmann D, Höpping W, Passarge E & Horsthemke B (1994) Frequency and parental origin of hypermethylated RB1 alleles in retinoblastoma. Hum Genet 94, 491-496.
Herman JG, Latif F, Weng Y, Lerman MI, Zbar B, Liu S, Samid D, Duan DS, Gnarra JR & Linehan WM (1994) Silencing of the VHL tumor-suppressor gene by DNA methylation in renal carcinoma. Proc Natl Acad Sci USA 91, 9700-9704.
Stirzaker C, Millar DS, Paul CL, Warnecke PM, Harrison J, Vincent PC, Frommer M & Clark SJ (1997) Extensive DNA methylation spanning the Rb promoter in retinoblastoma tumors. Cancer Res 57, 2229-2237.
Graff JR, Gabrielson E, Fujii H, Baylin SB & Herman JG (2000) Methylation patterns of the E-cadherin 5' CpG island are unstable and reflect the dynamic, heterogeneous loss of E-cadherin expression during metastatic progression. J Biol Chem 275, 2727-2732.
Costello JF, Futscher BW, Kroes RA & Pieper RO (1994) Methylation-related chromatin structure is associated with exclusion of transcription factors from and suppressed expression of the O-6-methylguanine DNA methyltransferase gene in human glioma cell lines. Mol Cell Biol 14, 6515-6521.
Herman JG, Umar A, Polyak K, Graff JR, Ahuja N, Issa JP, Markowitz S, Willson JK, Hamilton SR, Kinzler KW et al. (1998) Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc Natl Acad Sci USA 95, 6870-6875.
Weinberg RA (2007) The Biology of Cancer. Garland Science, New York, NY.
Sproul D & Meehan RR (2013) Genomic insights into cancer-associated aberrant CpG island hypermethylation. Brief Funct Genomics 12, 174-190.
Baylin SB, Herman JG, Graff JR, Vertino PM & Issa JP (1998) Alterations in DNA methylation: a fundamental aspect of neoplasia. Adv Cancer Res 72, 141-196.
Eads CA, Danenberg KD, Kawakami K, Saltz LB, Danenberg PV & Laird PW (1999) CpG island hypermethylation in human colorectal tumors is not associated with DNA methyltransferase overexpression. Cancer Res 59, 2302-2306.
Di Croce L, Raker VA, Corsaro M, Fazi F, Fanelli M, Faretta M, Fuks F, Lo Coco F, Kouzarides T, Nervi C et al. (2002) Methyltransferase recruitment and DNA hypermethylation of target promoters by an oncogenic transcription factor. Science 295, 1079-1082.
Wu X & Zhang Y (2017) TET-mediated active DNA demethylation: mechanism, function and beyond. Nat Rev Genet 18, 517-534.
Atlasi Y & Stunnenberg HG (2017) The interplay of epigenetic marks during stem cell differentiation and development. Nat Rev Genet 18, 643-658.
Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, Zimmerman J, Eden E, Yakhini Z, Ben-Shushan E, Reubinoff BE et al. (2007) Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet 39, 232-236.
Widschwendter M, Fiegl H, Egle D, Mueller-Holzner E, Spizzo G, Marth C, Weisenberger DJ, Campan M, Young J, Jacobs I et al. (2007) Epigenetic stem cell signature in cancer. Nat Genet 39, 157-158.
Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, Cope L, Mohammad HP, Chen W, Daniel VC, Yu W et al. (2007) A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet 39, 237-242.
Easwaran H, Johnstone SE, Van Neste L, Ohm J, Mosbruger T, Wang Q, Aryee MJ, Joyce P, Ahuja N, Weisenberger D et al. (2012) A DNA hypermethylation module for the stem/progenitor cell signature of cancer. Genome Res 22, 837-849.
Hinoue T, Weisenberger DJ, Lange CP, Shen H, Byun HM, Van Den Berg D, Malik S, Pan F, Noushmehr H, van Dijk CM et al. (2012) Genome-scale analysis of aberrant DNA methylation in colorectal cancer. Genome Res 22, 271-282.
Viré E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C, Morey L, Van Eynde A, Bernard D, Vanderwinden JM et al. (2006) The Polycomb group protein EZH2 directly controls DNA methylation. Nature 439, 871-874.
Wu X, Gong Y, Yue J, Qiang B, Yuan J & Peng X (2008) Cooperation between EZH2, NSPc1-mediated histone H2A ubiquitination and Dnmt1 in HOX gene silencing. Nucleic Acids Res 36, 3590-3599.
Brinkman AB, Gu H, Bartels SJ, Zhang Y, Matarese F, Simmer F, Marks H, Bock C, Gnirke A, Meissner A et al. (2012) Sequential ChIP- bisulfite sequencing enables direct genome-scale investigation of chromatin and DNA methylation cross-talk. Genome Res 22, 1128-1138.
Court F & Arnaud P (2017) An annotated list of bivalent chromatin regions in human ES cells: a new tool for cancer epigenetic research. Oncotarget 8, 4110-4124.
Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP et al. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448, 553-560.
Chinaranagari S, Sharma P & Chaudhary J (2014) EZH2 dependent H3K27me3 is involved in epigenetic silencing of ID4 in prostate cancer. Oncotarget 5, 7172-7182.
Stern JL, Paucek RD, Huang FW, Ghandi M, Nwumeh R, Costello JC & Cech TR (2017) Allele-specific DNA methylation and its interplay with repressive histone marks at promoter-mutant TERT. Genes Cell Rep 21, 3700-3707.
Statham AL, Robinson MD, Song JZ, Coolen MW, Stirzaker C & Clark SJ (2012) Bisulfite sequencing of chromatin immunoprecipitated DNA (BisChIP- seq) directly informs methylation status of histone-modified DNA. Genome Res 22, 1120-1127.
Cai Y, Lin JR, Zhang Q, O'Brien K, Montagna C & Zhang ZD (2018) Epigenetic alterations to Polycomb targets precede malignant transition in a mouse model of breast cancer. Sci Rep 8, 5535.
Neri F, Incarnato D, Krepelova A, Rapelli S, Pagnani A, Zecchina R, Parlato C & Oliviero S (2013) Genome-wide analysis identifies a functional association of Tet1 and Polycomb repressive complex 2 in mouse embryonic stem cells. Genome Biol 14, R91.
Kong L, Tan L, Lv R, Shi Z, Xiong L, Wu F, Rabidou K, Smith M, He C, Zhang L et al. (2016) A primary role of TET proteins in establishment and maintenance of De Novo bivalency at CpG islands. Nucleic Acids Res 44, 8682-8692.
Weber M, Hellmann I, Stadler MB, Ramos L, Pääbo S, Rebhan M & Schübeler D (2007) Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 39, 457-466.
Okitsu CY & Hsieh CL (2007) DNA methylation dictates histone H3K4 methylation. Mol Cell Biol 27, 2746-2757.
Thomson JP, Skene PJ, Selfridge J, Clouaire T, Guy J, Webb S, Kerr AR, Deaton A, Andrews R, James KD et al. (2010) CpG islands influence chromatin structure via the CpG-binding protein Cfp1. Nature 464, 1082-1086.
Ooi SK, Qiu C, Bernstein E, Li K, Jia D, Yang Z, Erdjument-Bromage H, Tempst P, Lin SP, Allis CD et al. (2007) DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448, 714-717.
Otani J, Nankumo T, Arita K, Inamoto S, Ariyoshi M & Shirakawa M (2009) Structural basis for recognition of H3K4 methylation status by the DNA methyltransferase 3A ATRX-DNMT3-DNMT3L domain. EMBO Rep 10, 1235-1241.
Guo X, Wang L, Li J, Ding Z, Xiao J, Yin X, He S, Shi P, Dong L, Li G et al. (2015) Structural insight into autoinhibition and histone H3-induced activation of DNMT3A. Nature 517, 640-644.
Costello JF, Smiraglia DJ & Plass C (2002) Restriction landmark genome scanning. Methods 27, 144-149.
Zardo G, Tiirikainen M, Hong C, Misra A, Feuerstein BG, Volik S, Collins CC, Lamborn KR, Bollen A, Pinkel D et al. (2002) Integrated genomic and epigenomic analyses pinpoint biallelic gene inactivation in tumors. Nat Genet 32, 453-458.
Pan G, Tian S, Nie J, Yang C, Ruotti V, Wei H, Jonsdottir GA, Stewart R & Thomson JA (2007) Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 1, 299-312.
Zhao XD, Han X, Chew JL, Liu J, Chiu KP, Choo A, Orlov YL, Sung WK, Shahab A, Kuznetsov VA et al. (2007) Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells. Cell Stem Cell 1, 286-298.
Cui K, Zang C, Roh TY, Schones DE, Childs RW, Peng W & Zhao K (2009) Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell 4, 80-93.
Peng JC, Valouev A, Swigut T, Zhang J, Zhao Y, Sidow A & Wysocka J (2009) Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. Cell 139, 1290-1302.
Adamowicz M, Radlwimmer B, Rieker RJ, Mertens D, Schwarzbach M, Schraml P, Benner A, Lichter P, Mechtersheimer G & Joos S (2006) Frequent amplifications and abundant expression of TRIO, NKD2, and IRX2 in soft tissue sarcomas. Genes Chromosomes Cancer 45, 829-838.
Liu T, Zhou W, Zhang F, Shi G, Teng H, Xiao J & Wang Y (2014) Knockdown of IRX2 inhibits osteosarcoma cell proliferation and invasion by the AKT/MMP9 signaling pathway. Mol Med Rep 10, 169-174.
Kang H, Wilson CS, Harvey RC, Chen IM, Murphy MH, Atlas SR, Bedrick EJ, Devidas M, Carroll AJ, Robinson BW et al. (2012) Gene expression profiles predictive of outcome and age in infant acute lymphoblastic leukemia: a Children's Oncology Group study. Blood 119, 1872-1881.
Rauch TA, Wang Z, Wu X, Kernstine KH, Riggs AD & Pfeifer GP (2012) DNA methylation biomarkers for lung cancer. Tumour Biol 33, 287-296.
Sato T, Arai E, Kohno T, Takahashi Y, Miyata S, Tsuta K, Watanabe S, Soejima K, Betsuyaku T & Kanai Y (2014) Epigenetic clustering of lung adenocarcinomas based on DNA methylation profiles in adjacent lung tissue: its correlation with smoking history and chronic obstructive pulmonary disease. Int J Cancer 135, 319-334.
Kamalakaran S, Varadan V, Giercksky Russnes HE, Levy D, Kendall J, Janevski A, Riggs M, Banerjee N, Synnestvedt M, Schlichting E et al. (2011) DNA methylation patterns in luminal breast cancers differ from non- luminal subtypes and can identify relapse risk independent of other clinical variables. Mol Oncol 5, 77-92.
Werner S, Brors B, Eick J, Marques E, Pogenberg V, Parret A, Kemming D, Wood AW, Edgren H, Neubauer H et al. (2015) Suppression of early hematogenous dissemination of human breast cancer cells to bone marrow by retinoic Acid-induced. Cancer Discov 5, 506-519.
Werner S, Stamm H, Pandjaitan M, Kemming D, Brors B, Pantel K & Wikman H (2015) Iroquois homeobox 2 suppresses cellular motility and chemokine expression in breast cancer cells. BMC Cancer 15. https://doi.org/10.1186/s12885-015-1907-4
Fazi F, Rosa A, Fatica A, Gelmetti V, De Marchis ML, Nervi C & Bozzoni I (2005) A minicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBPalpha regulates human granulopoiesis. Cell 123, 819-831.
Fazi F, Racanicchi S, Zardo G, Starnes LM, Mancini M, Travaglini L, Diverio D, Ammatuna E, Cimino G, Lo-Coco F et al. (2007) Epigenetic silencing of the myelopoiesis regulator microRNA-223 by the AML1/ETO oncoprotein. Cancer Cell 12, 457-466.
Bennett JM, Catovsky D, Daniel MT, Flandrin G, Galton DA, Gralnick HR & Sultan C (1985) Proposed revised criteria for the classification of acute myeloid leukemia: a report of the French-American-British Cooperative Group. Ann Intern Med 103, 620-625.
Zardo G, Ciolfi A, Vian L, Starnes LM, Billi M, Racanicchi S, Maresca C, Fazi F, Travaglini L, Noguera N et al. (2012) Polycombs and microRNA-223 regulate human granulopoiesis by transcriptional control of target gene expression. Blood 119, 4034-4046.

Auteurs

Stefania Scalea (S)

Department of Experimental Medicine, University of Rome, Sapienza, Italy.

Carmen Maresca (C)

Oncogenomic and Epigenetic Unit, Regina Elena National Cancer Institute, Rome, Italy.

Caterina Catalanotto (C)

Department of Molecular Medicine, University of Rome, Sapienza, Italy.

Rachele Marino (R)

Department of Molecular Medicine, University of Rome, Sapienza, Italy.

Carlo Cogoni (C)

Department of Molecular Medicine, University of Rome, Sapienza, Italy.

Anna Reale (A)

Department of Experimental Medicine, University of Rome, Sapienza, Italy.

Michele Zampieri (M)

Department of Experimental Medicine, University of Rome, Sapienza, Italy.

Giuseppe Zardo (G)

Department of Experimental Medicine, University of Rome, Sapienza, Italy.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH