The interplay between the lysine demethylase KDM1A and DNA methyltransferases in cancer cells is cell cycle dependent

Oncotarget

Volumn 7, Issue 37, 2016, Pages 58939-58952

  Brenner, Carmen ^a   Luciani, Judith ^a   Bizet, Martin ^a   Ndlovu, Matladi ^a   Josseaux, Eleonore ^a   Dedeurwaerder, Sarah ^a   Calonne, Emilie ^a   Putmans, Pascale ^a   Cartron, Pierre Francois ^b,c,d   Defrance, Matthieu ^a   Fuks, François ^a   Deplus, Rachel ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b Team 12   (France)

^c UNIVERSITÉ DE NANTES   (France)

^d UMR INSERM U892 CNRS 6299   (France)

Author keywords

Cancer; Cell cycle; DNA methylation; Histone demethylation; KDM1A

Indexed keywords

DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3B; HISTONE DEMETHYLASE; PROTEIN KDM1A; UNCLASSIFIED DRUG; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE 5) METHYLTRANSFERASE 1; DNMT1 PROTEIN, HUMAN; HISTONE; KDM1A PROTEIN, HUMAN; LYSINE; PROTEIN BINDING;

ARTICLE; CANCER CELL; CANCER CELL LINE; CELL CYCLE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA EXTRACTION; DNA METHYLATION; ENZYME BINDING; ENZYME LOCALIZATION; HETEROCHROMATIN; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; PROTEIN DEPLETION; PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA PURIFICATION; UPREGULATION; WESTERN BLOTTING; ANIMAL; CARCINOGENESIS; GENETICS; HELA CELL LINE; METABOLISM; MOUSE; NEOPLASM; NIH 3T3 CELL LINE; S PHASE CELL CYCLE CHECKPOINT;

ANIMALS; CARCINOGENESIS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1; DNA (CYTOSINE-5-)-METHYLTRANSFERASES; DNA METHYLATION; HELA CELLS; HISTONE DEMETHYLASES; HISTONES; HUMANS; LYSINE; MICE; NEOPLASMS; NIH 3T3 CELLS; PROTEIN BINDING; S PHASE CELL CYCLE CHECKPOINTS;

EID: 84991381413     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.10624     Document Type: Article

References (79)

1. Robertson KD. DNA methylation and human disease. Nat Rev Genet. 2005; 6:597-610
2. Ting AH, McGarvey KM, Baylin SB. The cancer epigenome-components and functional correlates. Genes Dev. 2006; 20:3215-31
3. Jones PA, Baylin SB. The epigenomics of cancer. Cell. 2007; 128:683-92
4. Rhee I, Bachman KE, Park BH, Jair KW, Yen RWC, Schuebel KE, Cui H, Feinberg AP, Lengauer C, Kinzler KW, Baylin SB, Vogelstein B. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature. 2002; 416:552-6
5. Mutze K, Langer R, Schumacher F, Becker K, Ott K, Novotny A, Hapfelmeier A, Höfler H, Keller G. DNA methyltransferase 1 as a predictive biomarker and potential therapeutic target for chemotherapy in gastric cancer. Eur J Cancer. 2011; 47:1817-25
6. Rajendran G, Shanmuganandam K, Bendre A, Muzumdar D, Mujumdar D, Goel A, Shiras A. Epigenetic regulation of DNA methyltransferases: DNMT1 and DNMT3B in gliomas. J Neurooncol. 2011; 104:483-94
7. Brenner C, Fuks F. DNA methyltransferases: facts, clues, mysteries. Curr Top Microbiol Immunol. 2006; 301:45-66
8. Leonhardt H, Page AW, Weier HU, Bestor TH. A targeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell. 1992; 71:865-73
9. Okano M, Bell DW, Haber DA, Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell. 1999; 99:247-57
10. Fatemi M, Hermann A, Gowher H, Jeltsch A. Dnmt3a and Dnmt1 functionally cooperate during de novo methylation of DNA. Eur J Biochem. 2002; 269:4981-4
11. Dedeurwaerder S, Desmedt C, Calonne E, Singhal SK, Haibe-Kains B, Defrance M, Michiels S, Volkmar M, Deplus R, Luciani J, Lallemand F, Larsimont D, Toussaint J, et al. DNA methylation profiling reveals a predominant immune component in breast cancers. EMBO Mol Med. 2011; 3:726-41
12. Revill K, Wang T, Lachenmayer A, Kojima K, Harrington A, Li J, Hoshida Y, Llovet JM, Powers S. Genome-wide methylation analysis and epigenetic unmasking identify tumor suppressor genes in hepatocellular carcinoma. Gastroenterology. 2013; 145:1424-35.e1-25
13. Lao VV, Grady WM. Epigenetics and colorectal cancer. Nat Rev Gastroenterol Hepatol. 2011; 8:686-700
14. Baylin SB. DNA methylation and gene silencing in cancer. Nat Clin Pract Oncol. 2005; 2 Suppl 1:S4-11
15. Gore SD. Combination therapy with DNA methyltransferase inhibitors in hematologic malignancies. Nat Clin Pr Oncol. 2005;2:S30-5
16. Griffiths EA, Gore SD. DNA methyltransferase and histone deacetylase inhibitors in the treatment of myelodysplastic syndromes. Semin Hematol. 2008; 45:23-30
17. Vendetti FP, Rudin CM. Epigenetic therapy in non-small-cell lung cancer: targeting DNA methyltransferases and histone deacetylases. Expert Opin Biol Ther. 2013; 13:1273-85
18. Epsztejn-Litman S, Feldman N, Abu-Remaileh M, Shufaro Y, Gerson A, Ueda J, Deplus R, Fuks F, Shinkai Y, Cedar H BY. De novo DNA methylation promoted by G9a prevents reprogramming of embryonically silenced genes. Nat Struct Mol Biol. 2008; 15:1176-83
19. Fuks F, Hurd PJ, Deplus R, Kouzarides T. The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Res. 2003; 31:2305-12
20. Wang J, Hevi S, Kurash JK, Lei H, Gay F, Bajko J, Su H, Sun W, Chang H, Xu G, Gaudet F, Li E, Chen T. The lysine demethylase LSD1 (KDM1) is required for maintenance of global DNA methylation. Nat Genet. 2009; 41:125-9
21. Nicholson TB, Chen T. LSD1 demethylates histone and non-histone proteins. Epigenetics. 2009; 4:129-32
22. Wang Y, Zhang H, Chen Y, Sun Y, Yang F, Yu W, Liang J, Sun L, Yang X, Shi L, Li R, Li Y, Zhang Y, et al. LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell. 2009; 138:660-72
23. Shi YJ, Matson C, Lan F, Iwase S, Baba T, Shi Y. Regulation of LSD1 Histone Demethylase Activity by Its Associated Factors. Mol Cell. 2005; 19:857-64
24. Pollock JA, Larrea MD, Jasper JS, McDonnell DP, McCafferty DG. Lysine-specific histone demethylase 1 inhibitors control breast cancer proliferation in ERα-dependent and-independent manners. ACS Chem Biol. 2012; 7:1221-31
25. Cai C, He HH, Chen S, Coleman I, Wang H, Fang Z, Chen S, Nelson PS, Liu XS, Brown M, Balk SP. Androgen receptor gene expression in prostate cancer is directly suppressed by the androgen receptor through recruitment of lysine-specific demethylase 1. Cancer Cell. 2011; 20:457-71
26. Cho HS, Suzuki T, Dohmae N, Hayami S, Unoki M, Yoshimatsu M, Toyokawa G, Takawa M, Chen T, Kurash JK, Field HI, Ponder BAJ, Nakamura Y, et al. Demethylation of RB regulator MYPT1 by histone demethylase LSD1 promotes cell cycle progression in cancer cells. Cancer Res. 2011; 71:655-60
27. Hayami S, Kelly JD, Cho HS, Yoshimatsu M, Unoki M, Tsunoda T, Field HI, Neal DE, Yamaue H, Ponder BAJ, Nakamura Y, Hamamoto R. Overexpression of LSD1 contributes to human carcinogenesis through chromatin regulation in various cancers. Int J Cancer. 2011; 128:574-86
28. Schulte JH, Lim S, Schramm A, Friedrichs N, Koster J, Versteeg R, Ora I, Pajtler K, Klein-Hitpass L, Kuhfittig-Kulle S, Metzger E, Schule R, Eggert A, et al. Lysinespecific demethylase 1 is strongly expressed in poorly differentiated neuroblastoma: implications for therapy. Cancer Res. 2009; 69:2065-71
29. Tochio N, Umehara T, Koshiba S, Inoue M, Yabuki T, Aoki M, Seki E, Watanabe S, Tomo Y, Hanada M, Ikari M, Sato M, Terada T, et al. Solution structure of the SWIRM domain of human histone demethylase LSD1. Structure. 2006; 14:457-68
30. Amente S, Milazzo G, Sorrentino MC, Ambrosio S, Di Palo G, Lania L, Perini G, Majello B. Lysine-specific demethylase (LSD1/KDM1A) and MYCN cooperatively repress tumor suppressor genes in neuroblastoma. Oncotarget. 2015; 6:14572-83. doi: 10.18632/oncotarget.3990
31. Estève PO, Chang Y, Samaranayake M, Upadhyay AK, Horton JR, Feehery GR, Cheng X, Pradhan S. A methylation and phosphorylation switch between an adjacent lysine and serine determines human DNMT1 stability. Nat Struct Mol Biol. 2011; 18:42-8
32. Tost J. DNA methylation: an introduction to the biology and the disease-associated changes of a promising biomarker. Mol Biotechnol. 2010; 44:71-81
33. Yang AS, Estécio MRH, Doshi K, Kondo Y, Tajara EH, Issa JPJ. A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements. Nucleic Acids Res. 2004; 32:e38
34. Hsiung DT, Marsit CJ, Houseman EA, Eddy K, Furniss CS, McClean MD, Kelsey KT. Global DNA methylation level in whole blood as a biomarker in head and neck squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev. 2007; 16:108-14
35. Wilhelm CS, Kelsey KT, Butler R, Plaza S, Gagne L, Zens MS, Andrew AS, Morris S, Nelson HH, Schned AR, Karagas MR, Marsit CJ. Implications of LINE1 methylation for bladder cancer risk in women. Clin Cancer Res. 2010; 16:1682-9
36. Choi SH, Worswick S, Byun HM, Shear T, Soussa JC, Wolff EM, Douer D, Garcia-Manero G, Liang G, Yang AS. Changes in DNA methylation of tandem DNA repeats are different from interspersed repeats in cancer. Int J Cancer. 2009; 125:723-9
37. Bibikova M, Le J, Barnes B, Saedinia-Melnyk S, Zhou L, Shen R, Gunderson KL. Genome-wide DNA methylation profiling using Infinium® assay. Epigenomics. 2009; 1: 177-200
38. Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA, Shi Y. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell. 2004; 119:941-53
39. Ding D, Liu X, Guo SW. Overexpression of lysine-specific demethylase 1 in ovarian endometriomas and its inhibition reduces cellular proliferation, cell cycle progression, and invasiveness. Fertil Steril. 2014; 101:740-9
40. Wang J, Lu F, Ren Q, Sun H, Xu Z, Lan R, Liu Y, Ward D, Quan J, Ye T, Zhang H. Novel Histone Demethylase LSD1 Inhibitors Selectively Target Cancer Cells with Pluripotent Stem Cell Properties. Cancer Res. NIH Public Access; 2011; 71:7238-49
41. Hervouet E, Nadaradjane A, Gueguen M, Vallette FM, Cartron PF. Kinetics of DNA methylation inheritance by the Dnmt1-including complexes during the cell cycle. Cell Div. 2012; 7:5
42. Schneider K, Fuchs C, Dobay A, Rottach A, Qin W, Wolf P, Álvarez-Castro JM, Nalaskowski MM, Kremmer E, Schmid V, Leonhardt H, Schermelleh L. Dissection of cell cycle-dependent dynamics of Dnmt1 by FRAP and diffusion-coupled modeling. Nucleic Acids Res. 2013; 41:4860-76
43. O'Keefe RT, Henderson SC, Spector DL. Dynamic organization of DNA replication in mammalian cell nuclei: spatially and temporally defined replication of chromosomespecific alpha-satellite DNA sequences. J Cell Biol. 1992; 116:1095-110
44. Rountree MR, Bachman KE, Baylin SB. DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat Genet. 2000; 25:269-77
45. Bachman KE, Rountree MR, Baylin SB. Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. J Biol Chem. 2001; 276:32282-7
46. Probst A V, Dunleavy E, Almouzni G. Epigenetic inheritance during the cell cycle. Nat Rev Mol Cell Biol. 2009; 10:192-206
47. Zhang J, Gao Q, Li P, Liu X, Jia Y, Wu W, Li J, Dong S, Koseki H, Wong J. S phase-dependent interaction with DNMT1 dictates the role of UHRF1 but not UHRF2 in DNA methylation maintenance. Cell Res. 2011; 21:1723-39
48. Deplus R, Blanchon L, Rajavelu A, Boukaba A, Defrance M, Luciani J, Rothé F, Dedeurwaerder S, Denis H, Brinkman AB, Simmer F, Müller F, Bertin B, et al. Regulation of DNA methylation patterns by CK2-mediated phosphorylation of Dnmt3a. Cell Rep. 2014; 8:743-53
49. Schönenberger F, Deutzmann A, Ferrando-May E, Merhof D. Discrimination of cell cycle phases in PCNAimmunolabeled cells. BMC Bioinformatics. 2015;16:180
50. Singh MM, Manton CA, Bhat KP, Tsai WW, Aldape K, Barton MC, Chandra J. Inhibition of LSD1 sensitizes glioblastoma cells to histone deacetylase inhibitors. Neuro Oncol. 2011; 13:894-903
51. Hashimoto H, Vertino PM, Cheng X. Molecular coupling of DNA methylation and histone methylation. Epigenomics. 2010; 2:657-69
52. Lehnertz B, Ueda Y, Derijck AAHA, Braunschweig U, Perez-Burgos L, Kubicek S, Chen T, Li E, Jenuwein T, Peters AHFM. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol. 2003; 13:1192-200
53. Smallwood A, Estève PO, Pradhan S, Carey M. Functional cooperation between HP1 and DNMT1 mediates gene silencing. Genes Dev. 2007; 21:1169-78
54. Keil KP, Vezina CM. DNA methylation as a dynamic regulator of development and disease processes: spotlight on the prostate. Epigenomics. 2015; 7:413-25
55. Dedeurwaerder S, Fuks F. DNA methylation markers for breast cancer prognosis: Unmasking the immune component. Oncoimmunology. 2012; 1:962-4
56. Lee EJ, Rath P, Liu J, Ryu D, Pei L, Noonepalle SK, Shull AY, Feng Q, Litofsky NS, Miller DC, Anthony DC, Kirk MD, Laterra J, et al. Identification of Global DNA Methylation Signatures in Glioblastoma-Derived Cancer Stem Cells. J Genet Genomics. 2015; 42:355-71
57. Miremadi A, Oestergaard MZ, Pharoah PDP, Caldas C. Cancer genetics of epigenetic genes. Hum Mol Genet. 2007; 16 Spec No:R28-49
58. Kahl P, Gullotti L, Heukamp LC, Wolf S, Friedrichs N, Vorreuther R, Solleder G, Bastian PJ, Ellinger J, Metzger E, Schüle R, Buettner R. Androgen receptor coactivators lysine-specific histone demethylase 1 and four and a half LIM domain protein 2 predict risk of prostate cancer recurrence. Cancer Res. 2006; 66:11341-7
59. Lv T, Yuan D, Miao X, Lv Y, Zhan P, Shen X, Song Y. Overexpression of LSD1 promotes proliferation, migration and invasion in non-small cell lung cancer. PLoS One. 2012; 7
60. Altun G, Loring JF, Laurent LC. DNA methylation in embryonic stem cells. J Cell Biochem. 2010; 109:1-6
61. Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, Cope L, Mohammad HP, Chen W, Daniel VC, Yu W, Berman DM, Jenuwein T, Pruitt K, et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet. 2007; 39:237-42
62. Bibikova M, Chudin E, Wu B, Zhou L, Garcia EW, Liu Y, Shin S, Plaia TW, Auerbach JM, Arking DE, Gonzalez R, Crook J, Davidson B, et al. Human embryonic stem cells have a unique epigenetic signature. Genome Res. 2006; 16:1075-83
63. Fuks F, Burgers WA, Godin N, Kasai M, Kouzarides T. Dnmt3a binds deacetylases and is recruited by a sequencespecific repressor to silence transcription. EMBO J. 2001; 20:2536-44
64. Fuks F. DNA methylation and histone modifications: teaming up to silence genes. Curr Opin Genet Dev. 2005; 15:490-5
65. Burgers WA, Fuks F, Kouzarides T. DNA methyltransferases get connected to chromatin. Trends Genet. 2002; 18:275-7
66. Milutinovic S, Brown SE, Zhuang Q, Szyf M. DNA methyltransferase 1 knock down induces gene expression by a mechanism independent of DNA methylation and histone deacetylation. J Biol Chem. 2004; 279:27915-27
67. Haney SL, Hlady RA, Opavska J, Klinkebiel D, Pirruccello SJ, Dutta S, Datta K, Simpson MA, Wu L, Opavsky R. Methylation-independent repression of Dnmt3b contributes to oncogenic activity of Dnmt3a in mouse MYC-induced T-cell lymphomagenesis. Oncogene.2015; 34:5436-46
68. Huang Y, Stewart TM, Wu Y, Baylin SB, Marton LJ, Perkins B, Jones RJ, Woster PM, Casero RA. Novel oligoamine analogues inhibit lysine-specific demethylase 1 and induce reexpression of epigenetically silenced genes. Clin Cancer Res. 2009; 15:7217-28
69. Schenk T, Chen WC, Göllner S, Howell L, Jin L, Hebestreit K, Klein HU, Popescu AC, Burnett A, Mills K, Casero RA, Marton L, Woster P, et al. Inhibition of the LSD1 (KDM1A) demethylase reactivates the all-transretinoic acid differentiation pathway in acute myeloid leukemia. Nat Med. 2012; 18:605-11
70. Harris WJ, Huang X, Lynch JT, Spencer GJ, Hitchin JR, Li Y, Ciceri F, Blaser JG, Greystoke BF, Jordan AM, Miller CJ, Ogilvie DJ, Somervaille TCP. The histone demethylase KDM1A sustains the oncogenic potential of MLL-AF9 leukemia stem cells. Cancer Cell. 2012; 21:473-87
71. Fahy J, Jeltsch A, Arimondo PB. DNA methyltransferase inhibitors in cancer: a chemical and therapeutic patent overview and selected clinical studies. Expert Opin Ther Pat. Informa UK, Ltd. London; 2012; 22:1427-42
72. Katan-Khaykovich Y, Struhl K. Heterochromatin formation involves changes in histone modifications over multiple cell generations. EMBO J. 2005; 24:2138-49
73. Holmes A, Roseaulin L, Schurra C, Waxin H, Lambert S, Zaratiegui M, Martienssen RA, Arcangioli B. Lsd1 and lsd2 control programmed replication fork pauses and imprinting in fission yeast. Cell Rep. 2012; 2:1513-20
74. Chen T, Hevi S, Gay F, Tsujimoto N, He T, Zhang B, Ueda Y, Li E. Complete inactivation of DNMT1 leads to mitotic catastrophe in human cancer cells. Nat Genet. 2007; 39:391-6
75. Seward DJ, Cubberley G, Kim S, Schonewald M, Zhang L, Tripet B, Bentley DL. Demethylation of trimethylated histone H3 Lys4 in vivo by JARID1 JmjC proteins. Nat Struct Mol Biol. Nature Publishing Group; 2007; 14:240-2
76. Fuks F, Burgers WA, Brehm A, Hughes-Davies L, Kouzarides T. DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nat Genet. 2000; 24:88-91
77. Denis H, Deplus R, Putmans P, Yamada M, Métivier RFF. Functional connection between deimination and deacetylation of histones. Mol Cell Biol. 2009; 29:4982-93
78. Price ME, Cotton AM, Lam LL, Farré P, Emberly E, Brown CJ, Robinson WP, Kobor MS. Additional annotation enhances potential for biologically-relevant analysis of the Illumina Infinium HumanMethylation450 BeadChip array. Epigenetics Chromatin. 2013; 6:4
79. Hervouet E, Hulin P, Vallette FM, Cartron P-F. Proximity ligation in situ assay for monitoring the global DNA methylation in cells. BMC Biotechnol. 2011; 11:31