SET8 promotes epithelial-mesenchymal transition and confers TWIST dual transcriptional activities

EMBO Journal

Volumn 31, Issue 1, 2012, Pages 110-123

  Yang, Fen ^a,b   Sun, Luyang ^a   Li, Qian ^a   Han, Xiao ^a   Lei, Liandi ^a   Zhang, Hua ^b   Shang, Yongfeng ^a,c  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b China Astronaut Research and Training Center   (China)

^c TIANJIN MEDICAL UNIVERSITY   (China)

Author keywords

breast cancer; EMT; metastasis; SET8; TWIST

Indexed keywords

NERVE CELL ADHESION MOLECULE; PROTEIN; SET8 PROTEIN; TRANSCRIPTION FACTOR TWIST; UNCLASSIFIED DRUG; UVOMORULIN;

ARTICLE; BREAST CANCER; CANCER CELL; CANCER INVASION; CONTROLLED STUDY; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; METASTASIS; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

BREAST NEOPLASMS; CADHERINS; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HISTONE-LYSINE N-METHYLTRANSFERASE; HUMANS; NEOPLASM INVASIVENESS; NUCLEAR PROTEINS; TRANSCRIPTION, GENETIC; TWIST TRANSCRIPTION FACTOR;

EID: 84855340668     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.364     Document Type: Article

References (63)

1. Abbas T, Shibata E, Park J, Jha S, Karnani N, Dutta A (2010) CRL4(Cdt2) regulates cell proliferation and histone gene expression by targeting PR-Set7/Set8 for degradation. Mol Cell 40: 9-21
2. Acevedo VD, Gangula RD, Freeman KW, Li R, Zhang Y, Wang F, Ayala GE, Peterson LE, Ittmann M, Spencer DM (2007) Inducible FGFR-1 activation leads to irreversible prostate adenocarcinoma and an epithelial-to-mesenchymal transition. Cancer Cell 12: 559-571 (Pubitemid 350199071)
3. Alexander NR, Tran NL, Rekapally H, Summers CE, Glackin C, Heimark RL (2006) N-cadherin gene expression in prostate carcinoma is modulated by integrin-dependent nuclear transloca-tion of Twist1. Cancer Res 66: 3365-3369
4. Ansieau S, Bastid J, Doreau A, Morel AP, Bouchet BP, Thomas C, Fauvet F, Puisieux I, Doglioni C, Piccinin S, Maestro R, Voeltzel T, Selmi A, Valsesia-Wittmann S, Caron de Fromentel C, Puisieux A (2008) Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence. Cancer Cell 14: 79-89 (Pubitemid 351890463)
5. Castanon I, Von Stetina S, Kass J, Baylies MK (2001) Dimerization partners determine the activity of the Twist bHLH protein during Drosophila mesoderm development. Development 128: 3145-3159 (Pubitemid 32825758)
6. Centore RC, Havens CG, Manning AL, Li JM, Flynn RL, Tse A, Jin J, Dyson NJ, Walter JC, Zou L (2010) CRL4(Cdt2)-mediated destruction of the histone methyltransferase Set8 prevents premature chromatin compaction in S phase. Mol Cell 40: 22-33
7. Cheng GZ, Chan J, Wang Q, Zhang W, Sun CD, Wang LH (2007) Twist transcriptionally up-regulates AKT2 in breast cancer cells leading to increased migration, invasion, and resistance to pacli-taxel. Cancer Res 67: 1979-1987 (Pubitemid 46424214)
8. Cheng GZ, Zhang WZ, Sun M, Wang Q, Coppola D, Mansour M, Xu LM, Costanzo C, Cheng JQ, Wang LH (2008) Twist is transcrip-tionally induced by activation of STAT3 and mediates STAT3 oncogenic function. J Biol Chem 283: 14665-14673
9. Chi P, Allis CD, Wang GG (2010) Covalent histone modifications- miswritten, misinterpreted and mis-erased in human cancers. Nat Rev Cancer 10: 457-469
10. Congdon LM, Houston SI, Veerappan CS, Spektor TM, Rice JC (2010) PR-Set7-mediated monomethylation of histone H4 lysine 20 at specific genomic regions induces transcriptional repression. J Cell Biochem 11 0 : 609-619
11. Dalton TP, Bittel D, Andrews GK (1997) Reversible activation of mouse metal response element-binding transcription factor 1 DNA binding involves zinc interaction with the zinc finger domain. Mol Cell Biol 17: 2781-2789 (Pubitemid 27175161)
12. Fang J, Feng Q, Ketel CS, Wang H, Cao R, Xia L, Erdjument-Bromage H, Tempst P, Simon JA, Zhang Y (2002) Purification and functional characterization of SET8, a nucleosomal histone H4-lysine 20-specific methyltransferase. Curr Biol 12: 1086-1099 (Pubitemid 34766930)
13. Fu J, Qin L, He T, Qin J, Hong J, Wong J, Liao L, Xu J (2011) The TWIST/Mi2/NuRD protein complex and its essential role in cancer metastasis. Cell Res 21: 275-289
14. Hasselblatt M, Mertsch S, Koos B, Riesmeier B, Stegemann H, Jeibmann A, Tomm M, Schmitz N, Wrede B, Wolff JE, Zheng W, Paulus W (2009) TWIST-1 is overexpressed in neoplastic choroid plexus epithelial cells and promotes proliferation and invasion. Cancer Res 69: 2219-2223
15. Horikawa T, Yang J, Kondo S, Yoshizaki T, Joab I, Furukawa M, Pagano JS (2007) Twist and epithelial-mesenchymal transition are induced by the EBV oncoprotein latent membrane protein 1 and are associated with metastatic nasopharyngeal carcinoma. Cancer Res 67: 1970-1978 (Pubitemid 46424213)
16. Houston SI, McManus KJ, Adams MM, Sims JK, Carpenter PB, Hendzel MJ, Rice JC (2008) Catalytic function of the PR-Set7 histone H4 lysine 20 monomethyltransferase is essential for mitotic entry and genomic stability. J Biol Chem 283: 19478-19488
17. Jorgensen S, Elvers I, Trelle MB, Menzel T, Eskildsen M, Jensen ON, Helleday T, Helin K, Sorensen CS (2007) The histone methyl-transferase SET8 is required for S-phase progression. J Cell Biol 179: 1337-1345
18. Joyce JA, Pollard JW (2009) Microenvironmental regulation of metastasis. Nat Rev Cancer 9: 239-252
19. Kalakonda N, Fischle W, Boccuni P, Gurvich N, Hoya-Arias R, Zhao X, Miyata Y, Macgrogan D, Zhang J, Sims JK, Rice JC, Nimer SD (2008) Histone H4 lysine 20 monomethylation promotes tran-scriptional repression by L3MBTL1. Oncogene 27: 4293-4304 (Pubitemid 352009998)
20. Klein CA (2009) Parallel progression of primary tumours and metastases. Nat Rev Cancer 9: 302-312
21. Krivtsov AV, Armstrong SA (2007) MLL translocations, histone modifications and leukaemia stem-cell development. Nat Rev Cancer 7: 823-833 (Pubitemid 350006257)
22. Kudo-Saito C, Shirako H, Takeuchi T, Kawakami Y (2009) Cancer metastasis is accelerated through immunosuppression during Snail-induced EMT of cancer cells. Cancer Cell 15: 195-206
23. Kwok WK, Ling MT, Lee TW, Lau TC, Zhou C, Zhang X, Chua CW, Chan KW, Chan FL, Glackin C, Wong YC, Wang X (2005) Up-regulation of TWIST in prostate cancer and its implication as a therapeutic target. Cancer Res 65: 5153-5162 (Pubitemid 40827324)
24. Li R, Zhang H, Yu W, Chen Y, Gui B, Liang J, Wang Y, Sun L, Yang X, Zhang Y, Shi L, Li Y, Shang Y (2009) ZIP: a novel transcription repressor, represses EGFR oncogene and suppresses breast carcinogenesis. EMBO J 28: 2763-2776
25. Li Y, Sun L, Zhang Y, Wang D, Wang F, Liang J, Gui B, Shang Y (2011a) The histone modifications governing TFF1 transcription mediated by estrogen receptor. J Biol Chem 286: 13925-13936
26. Li Z, Nie F, Wang S, Li L (2011b) Histone H4 Lys 20 monomethyla-tion by histone methylase SET8 mediates Wnt target gene activation. Proc Natl Acad Sci USA 108: 3116-3123
27. Lu C, Han HD, Mangala LS, Ali-Fehmi R, Newton CS, Ozbun L, Armaiz-Pena GN, Hu W, Stone RL, Munkarah A, Ravoori MK, Shahzad MM, Lee JW, Mora E, Langley RR, Carroll AR, Matsuo K, Spannuth WA, Schmandt R, Jennings NB et al (2010) Regulation of tumor angiogenesis by EZH2. Cancer Cell 18: 185-197
28. Mani SA, Yang J, Brooks M, Schwaninger G, Zhou A, Miura N, Kutok JL, Hartwell K, Richardson AL, Weinberg RA (2007) Mesenchyme Forkhead 1 (FOXC2) plays a key role in metastasis and is associated with aggressive basal-like breast cancers. Proc Natl Acad Sci USA 104: 10069-10074 (Pubitemid 47175264)
29. Minucci S, Pelicci PG (2006) Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer 6: 38-51 (Pubitemid 43054973)
30. Mironchik Y, Winnard Jr PT, Vesuna F, Kato Y, Wildes F, Pathak AP, Kominsky S, Artemov D, Bhujwalla Z, Van Diest P, Burger H, Glackin C, Raman V (2005) Twist overexpression induces in vivo angiogenesis and correlates with chromosomal instability in breast cancer. Cancer Res 65: 10801-10809 (Pubitemid 41715228)
31. Morin RD, Johnson NA, Severson TM, Mungall AJ, An J, Goya R, Paul JE, Boyle M, Woolcock BW, Kuchenbauer F, Yap D, Humphries RK, Griffith OL, Shah S, Zhu H, Kimbara M, Shashkin P, Charlot JF, Tcherpakov M, Corbett R et al (2010) Somatic mutations altering EZH2 (Tyr641) in follicular and diffuse large B-cell lymphomas of germinal-center origin. Nat Genet 42: 181-185
32. Nguyen DX, Bos PD, Massague J (2009) Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer 9: 274-284
33. Nicoloso MS, Spizzo R, Shimizu M, Rossi S, Calin GA (2009) MicroRNAs-the micro steering wheel of tumour metastases. Nat Rev Cancer 9: 293-302
34. Nishioka K, Rice JC, Sarma K, Erdjument-Bromage H, Werner J, Wang Y, Chuikov S, Valenzuela P, Tempst P, Steward R, Lis JT, Allis CD, Reinberg D (2002) PR-Set7 is a nucleosome-specific methyltransferase that modifies lysine 20 of histone H4 and is associated with silent chromatin. Mol Cell 9: 1201-1213 (Pubitemid 34722300)
35. Oda H, Okamoto I, Murphy N, Chu J, Price SM, Shen MM, Torres-Padilla ME, Heard E, Reinberg D (2009) Monomethylation of histone H4-lysine 20 is involved in chromosome structure and stability and is essential for mouse development. Mol Cell Biol 29: 2278-2295
36. Oft M, Heider KH, Beug H (1998) TGFbeta signaling is necessary for carcinoma cell invasiveness and metastasis. Curr Biol 8: 1243-1252 (Pubitemid 28540052)
37. Pan D, Fujimoto M, Lopes A, Wang YX (2009) Twist-1 is a PPARdelta-inducible, negative-feedback regulator of PGC-1alpha in brown fat metabolism. Cell 137: 73-86
38. Polyak K, Weinberg RA (2009) Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 9: 265-273
39. Psaila B, Lyden D (2009) The metastatic niche: adapting the foreign soil. Nat Rev Cancer 9: 285-293
40. Radisky DC, Bissell MJ (2007) NF-kappaB links oestrogen receptor signalling and EMT. Nat Cell Biol 9: 361-363 (Pubitemid 46511067)
41. Rayasam GV, Wendling O, Angrand PO, Mark M, Niederreither K, Song L, Lerouge T, Hager GL, Chambon P, Losson R (2003) NSD1 is essential for early post-implantation development and has a catalytically active SET domain. EMBO J 22: 3153-3163 (Pubitemid 36758635)
42. Richter GH, Plehm S, Fasan A, Rossler S, Unland R, Bennani-Baiti IM, Hotfilder M, Lowel D, von Luettichau I, Mossbrugger I, Quintanilla-Martinez L, Kovar H, Staege MS, Muller-Tidow C, Burdach S (2009) EZH2 is a mediator of EWS/FLI1 driven tumor growth and metastasis blocking endothelial and neuro-ectoder-mal differentiation. Proc Natl Acad Sci USA 106: 5324-5329
43. Schotta G, Lachner M, Sarma K, Ebert A, Sengupta R, Reuter G, Reinberg D, Jenuwein T (2004) A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev 18: 1251-1262 (Pubitemid 38720593)
44. Shi L, Sun L, Li Q, Liang J, Yu W, Yi X, Yang X, Li Y, Han X, Zhang Y, Xuan C, Yao Z, Shang Y (2011) Histone demethylase JMJD2B coordinates H3K4/H3K9 methylation and promotes hormonally responsive breast carcinogenesis. Proc Natl Acad Sci USA 108: 7541-7546
45. Shi X, Kachirskaia I, Yamaguchi H, West LE, Wen H, Wang EW, Dutta S, Appella E, Gozani O (2007) Modulation of p53 function by SET8-mediated methylation at lysine 382. Mol Cell 27: 636-646 (Pubitemid 47238634)
46. Shiota M, Izumi H, Onitsuka T, Miyamoto N, Kashiwagi E, Kidani A, Yokomizo A, Naito S, Kohno K (2008) Twist promotes tumor cell growth through YB-1 expression. Cancer Res 68: 98-105 (Pubitemid 351380110)
47. Smirnova IV, Bittel DC, Ravindra R, Jiang H, Andrews GK (2000) Zinc and cadmium can promote rapid nuclear translocation of metal response element-binding transcription factor-1. J Biol Chem 275: 9377-9384 (Pubitemid 30185162)
48. Subramanian K, Jia D, Kapoor-Vazirani P, Powell DR, Collins RE, Sharma D, Peng J, Cheng X, Vertino PM (2008) Regulation of estrogen receptor alpha by the SET7 lysine methyltransferase. Mol Cell 30: 336-347 (Pubitemid 351615317)
49. Talasz H, Lindner HH, Sarg B, Helliger W (2005) Histone H4-lysine 20 monomethylation is increased in promoter and coding regions of active genes and correlates with hyperacetylation. J Biol Chem 280: 38814-38822 (Pubitemid 43853784)
50. Tardat M, Brustel J, Kirsh O, Lefevbre C, Callanan M, Sardet C, Julien E (2010) The histone H4 Lys 20 methyltransferase PR-Set7 regulates replication origins in mammalian cells. Nat Cell Biol 12: 1086-1093
51. Tardat M, Murr R, Herceg Z, Sardet C, Julien E (2007) PR-Set7-dependent lysine methylation ensures genome replication and stability through S phase. J Cell Biol 179: 1413-1426
52. Taube JH, Herschkowitz JI, Komurov K, Zhou AY, Gupta S, Yang J, Hartwell K, Onder TT, Gupta PB, Evans KW, Hollier BG, Ram PT, Lander ES, Rosen JM, Weinberg RA, Mani SA (2010) Core epithelial-to-mesenchymal transition interactome gene-expression signature is associated with claudin-low and metaplastic breast cancer subtypes. Proc Natl Acad Sci USA 107 : 15449-15454
53. Trojer P, Li G, Sims III RJ, Vaquero A, Kalakonda N, Boccuni P, Lee D, Erdjument-Bromage H, Tempst P, Nimer SD, Wang YH, Reinberg D (2007) L3MBTL1, a histone-methylation-dependent chromatin lock. Cell 129: 915-928 (Pubitemid 46802701)
54. Wakabayashi K, Okamura M, Tsutsumi S, Nishikawa NS, Tanaka T, Sakakibara I, Kitakami J, Ihara S, Hashimoto Y, Hamakubo T, Kodama T, Aburatani H, Sakai J (2009) The peroxisome proliferator-activated receptor gamma/retinoid X receptor alpha heterodimer targets the histone modification enzyme PR-Set7/Setd8 gene and regulates adipogenesis through a positive feedback loop. Mol Cell Biol 29: 3544-3555
55. Wang GG, Song J, Wang Z, Dormann HL, Casadio F, Li H, Luo JL, Patel DJ, Allis CD (2009a) Haematopoietic malignancies caused by dysregulation of a chromatin-binding PHD finger. Nature 459: 847-851
56. 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, Li Q, Yi X, Shang Y (2009b) LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell 138: 660-672
57. Wu H, Chen Y, Liang J, Shi B, Wu G, Zhang Y, Wang D, Li R, Yi X, Zhang H, Sun L, Shang Y (2005) Hypomethylation-linked activation of PAX2 mediates tamoxifen-stimulated endometrial carci-nogenesis. Nature 438: 981-987 (Pubitemid 43093965)
58. Wu S, Wang W, Kong X, Congdon LM, Yokomori K, Kirschner MW, Rice JC (2010) Dynamic regulation of the PR-Set7 histone methyl-transferase is required for normal cell cycle progression. Genes Dev 24: 2531-2542
59. Yamane K, Tateishi K, Klose RJ, Fang J, Fabrizio LA, Erdjument-Bromage H, Taylor-Papadimitriou J, Tempst P, Zhang Y (2007) PLU-1 is an H3K4 demethylase involved in transcriptional repression and breast cancer cell proliferation. Mol Cell 25: 801-812 (Pubitemid 46436533)
60. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA (2004) Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117: 927-939 (Pubitemid 38798858)
61. Yang MH, Wu MZ, Chiou SH, Chen PM, Chang SY, Liu CJ, Teng SC, Wu KJ (2008) Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat Cell Biol 10 : 295-305
62. Zhang H, Sun L, Liang J, Yu W, Zhang Y, Wang Y, Chen Y, Li R, Sun X, Shang Y (2006) The catalytic subunit of the proteasome is engaged in the entire process of estrogen receptor-regulated transcription. EMBO J 25: 4223-4233 (Pubitemid 44435220)
63. Zhang H, Yi X, Sun X, Yin N, Shi B, Wu H, Wang D, Wu G, Shang Y (2004) Differential gene regulation by the SRC family of coacti-vators. Genes Dev 18: 1753-1765 (Pubitemid 38938190)