Jumonji domain-containing protein 2B silencing induces DNA damage response via STAT3 pathway in colorectal cancer

British Journal of Cancer

Volumn 110, Issue 4, 2014, Pages 1014-1026

  Chen, L ^a   Fu, L ^a   Kong, X ^a   Xu, J ^a   Wang, Z ^a   Ma, X ^a   Akiyama, Y ^b   Chen, Y ^a   Fang, J ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; APOPTOSIS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL AGING; CELL CYCLE CHECKPOINTS; CELL HYPOXIA; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; COLORECTAL NEOPLASMS; DISEASE PROGRESSION; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HISTONES; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM TRANSPLANTATION; PHOSPHORYLATION; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTIONAL ACTIVATION;

EID: 84894358412     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2013.808     Document Type: Article

References (56)

1. Agger K, Cloos PA, Rudkjaer L, Williams K, Andersen G, Christensen J, Helin K (2009) The H3K27me3 demethylase JMJD3 contributes to the activation of the INK4A-ARF locus in response to oncogene-And stress-induced senescence. Genes Dev 23: 1171-1176.
2. Ahh JY, Schwarz JK, Piwnica-Worms H, Canman CE (2000) Threonine 68 phosphorylation by ataxia telangiectasia mutated is required for efficient activation of Chk2 in response to ionizing radiation. Cancer Res 60: 5934-5936.
3. Alas S, Bonavida B (2003) Inhibition of constitutive STAT3 activity sensitizes resistant non-Hodgkin's lymphoma and multiple myeloma to chemotherapeutic drug-mediated apoptosis. Clin Cancer Res 9: 316-326.
4. Bard JD, Gelebart P, Amin HM, Young LC, Ma Y, Lai R (2009) Signal transducer and activator of transcription 3 is a transcriptional factor regulating the gene expression of SALL4. FASEB J 23: 1405-1414.
5. Beyer S, Kristensen MM, Jensen KS, Johansen JV, Staller P (2008) The histone demethylases JMJD1A and JMJD2B are transcriptional targets of hypoxia-inducible factor HIF. J Biol Chem 283: 36542-36552.
6. Bindra RS, Gibson SL, Meng A, Westermark U, Jasin M, Pierce AJ, Bristow RG, Classon MK, Glazer PM (2005) Hypoxia-induced down-regulation of BRCA1 expression by E2Fs. Cancer Res 65: 11597-11604.
7. Bindra RS, Glazer PM (2007a) Co-repression of mismatch repair gene expression by hypoxia in cancer cells: Role of the Myc/Max network. Cancer Lett 252: 93-103.
8. Bindra RS, Glazer PM (2007b) Repression of RAD51 gene expression by E2F4/p130 complexes in hypoxia. Oncogene 26: 2048-2057.
9. Boengler K, Hilfiker-Kleiner D, Heusch G, Schulz R (2010) Inhibition of permeability transition pore opening by mitochondrial STAT3 and its role in myocardial ischemia/reperfusion. Basic Res Cardiol 105: 771-785.
10. Bonner JA, Yang ES, Trummell HQ, Nowsheen S, Willey CD, Raisch KP (2011) Inhibition of STAT-3 results in greater cetuximab sensitivity in head and neck squamous cell carcinoma. Radiother Oncol 99: 339-343.
11. Chan N, Koritzinsky M, Zhao H, Bindra R, Glazer PM, Powell S, Belmaaza A, Wouters B, Bristow RG (2008) Chronic hypoxia decreases synthesis of homologous recombination proteins to offset chemoresistance and radioresistance. Cancer Res 68: 605-614.
12. Chicas A, Kapoor A, Wang X, Aksoy O, Evertts AG, Zhang MQ, Garcia BA, Bernstein E, Lowe SW (2012) H3K4 demethylation by Jarid1a and Jarid1b contributes to retinoblastoma-mediated gene silencing during cellular senescence. Proc Natl Acad Sci USA 109: 8971-8976.
13. Collado M, Serrano M (2011) Senescence in tumours: Evidence from mice and humans. Nat Rev Cancer 10: 51-57.
14. d'Adda di Fagagna F (2008) Living on a break: Cellular senescence as a DNA-damage response. Nat Rev Cancer 8: 512-522.
15. Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, Luise C, Schurra C, Garre' M, Nuciforo PG, Bensimon A, Maestro R, Pelicci PG, d'Adda di Fagagna F (2006) Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 444: 638-642.
16. Dixit D, Sharma V, Ghosh S, Koul N, Mishra PK, Sen E (2009) Manumycin inhibits STAT3, telomerase activity, and growth of glioma cells by elevating intracellular reactive oxygen species generation. Eree Radic Biol Med 47: 364-374.
17. Draviam VM, Xie S, Sorger PK (2004) Chromosome segregation and genomic stability. Curr Opin Genet Dev 14: 120-125.
18. Du W, Hong J, Wang YC, Zhang YJ, Wang P, Su WY, Lin YW, Lu R, Zou WP, Xiong H, Fang JY (2012) Inhibiton of JAK2/STAT3 signalling induces colorectal cancer cell apoptosis via mitochondrial pathway. J Cell Mol Med 16: 1878-1888.
19. Fodor BD, Kubicek S, Yonezawa M, O'Sullivan RJ, Sengupta R, Perez-Burgos L, Opravil S, Mechtler K, Schotta G, Jenuwein T (2006) Jmjd2b antagonizes H3K9 trimethylation at pericentric heterochromatin in mammalian cells. Genes Dev 20: 1557-1562.
20. Fu L, Chen L, Yang J, Ye T, Chen Y, Fang J (2012) HIF-1a-induced histone demethylase JMJD2B contributes to the malignant phenotype of colorectal cancer cells via an epigenetic mechanism. Carcinogenesis 33: 1664-1673.
21. Harper JW, Elledge SJ (2007) The DNA damage response: Ten years after. Mol Cell 28: 739-745.
22. He J, Kallin EM, Tsukada Y, Zhang Y (2008) The H3K36 demethylase Jhdm1b/Kdm2b regulates cell proliferation and senescence through p15(Ink4b). Nat Struct Mol Biol 15: 1169-1175.
23. Itahana K, Campisi J, Dimri GP (2007) Methods to detect biomarkers of cellular senescence: The senescence-Associated beta-galactosidase assay. Methods Mol Biol 371: 21-31.
24. Kawazu M, Saso K, Tong KI, McQuire T, Goto K, Son DO, Wakeham A, Miyagishi M, Mak TW, Okada H (2011) Histone demethylase JMJD2B functions as a co-factor of estrogen receptor in breast cancer proliferation and mammary gland development. PLoS One 6: E17830.
25. Kim JG, Yi JM, Park SJ, Kim JS, Son TG, Yang K, Yoo MA, Heo K (2012) Histone demethylase JMJD2B-mediated cell proliferation regulated by hypoxia and radiation in gastric cancer cells. Biochim Biophys Acta 1819: 1200-1207.
26. Kulesza DW, Carré T, Chouaib S, Kaminska B (2013) Silencing of the transcription factor STAT3 sensitizes lung cancer cells to DNA damaging drugs, but not to TNFa-And NK cytotoxicity. Exp Cell Res 19: 506-516.
27. Li W, Zhao L, Zang W, Liu Z, Chen L, Liu T, Xu D, Jia J (2011) Histone demethylase JMJD2B is required for tumor cell proliferation and survival and is overexpressed in gastric cancer. Biochem Biophys Res Commun 416: 372-378.
28. Lord CJ, Ashworth A (2012) The DNA damage response and cancer therapy. Nature 481: 287-294.
29. Mallette FA, Mattiroli F, Cui G, Young LC, Hendzel MJ, Mer G, Sixma TK, Richard S (2012) RNF8-And RNF168-dependent degradation of KDM4A/JMJD2A triggers 53BP1 recruitment to DNA damage sites. EMBO J 31: 1865-1878.
30. Mallette FA, Richard S (2012) JMJD2A promotes cellular transformation by blocking cellular senescence through transcriptional repression of the tumor suppressor CHD5. Cell Rep 2: 1233-1243.
31. Negoro S, Kunisada K, Fujio Y, Funamoto M, Darville MI, Eizirik DL, Osugi T, Izumi M, Oshima Y, Nakaoka Y, Hirota H, Kishimoto T, Yamauchi-Takihara K (2001) Activation of signal transducer and activator of transcription 3 protects cardiomyocytes from hypoxia/reoxygenationinduced oxidative stress through the upregulation of manganese superoxide dismutase. Circulation 104: 979-981.
32. Palomera-Sanchez Z, Bucio-Mendez A, Valadez-Graham V, Reynaud E, Zurita M (2010) Drosophila p53 is required to increase the levels of the dKDM4B demethylase after UV-induced DNA damage to demethylate histone H3 lysine 9. J Biol Chem 285: 31370-31379.
33. Pires IM, Bencokova Z, Milani M, Folkes LK, Li JL, Stratford MR, Harris AL, Hammond EM (2010) Effects of acute versus chronic hypoxia on DNA damage response and genomic instability. Cancer Res 70: 925-935.
34. Pollard PJ, Loenarz C, Mole DR, McDonough MA, Gleadle JM, Schofield CJ, Ratcliffe PJ (2008) Regulation of Jumonji-domain-containing histone demethylases by hypoxia-inducible factor (HIF)-1alpha. Biochem J 416: 387-394.
35. Rodríguez-Jiménez FJ, Moreno-Manzano V, Lucas-Dominguez R, Sánchez-Puelles JM (2008) Hypoxia causes downregulation of mismatch repair system and genomic instability in stem cells. Stem Cells 26: 2052-2062.
36. 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.
37. Shi Y (2007) Histone lysine demethylases: Emerging roles in development, physiology and disease. Nat Rev Genet 8: 829-833.
38. Slee RB, Steiner CM, Herbert BS, Vance GH, Hickey RJ, Schwarz T, Christan S, Radovich M, Schneider BP, Schindelhauer D, Grimes BR (2012) Cancer-Associated alteration of pericentromeric heterochromatin may contribute to chromosome instability. Oncogene 31: 3244-3253.
39. Sullivan R, Graham CH (2009) Hypoxia prevents etoposide-induced DNA damage in cancer cells through a mechanism involving hypoxia-inducible factor 1. Mol Cancer Ther 8: 1702-1713.
40. Tierney BJ, McCann GA, Cohn DE, Eisenhauer E, Sudhakar M, Kuppusamy P, Hideg K, Selvendiran K (2012) HO-3867, a STAT3 inhibitor induces apoptosis by inactivation of STAT3 activity in BRCA1-mutated ovarian cancer cells. Cancer Biol Ther 13: 766-775.
41. Toyokawa G, Cho HS, Lwai Y, Yoshimatsu M, Takawa M, Hayami S, Maejima K, Shimizu N, Tanaka H, Tsunoda T, Field HI, Kelly JD, Neal DE, Ponder BA, Maehara Y, Nakamura Y, Hamamoto R (2011) The histone demethylase JMJD2B plays an essential role in human carcinogenesis through positive regulation of cyclin-dependent kinase 6. Cancer Prev Res (Phila) 4: 2051-2061.
42. Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol 552: 335-344.
43. Tzatsos A, Paskaleva P, Lymperi S, Contino G, Stoykova S, Chen Z, Wong KK, Bardeesy N (2011) Lysine-specific demethylase 2B (KDM2B)-let-7-enhancer of zester homolog 2 (EZH2) pathway regulates cell cycle progression and senescence in primary cells. J Biol Chem 286: 33061-33069.
44. Vilenchik MM, Knudson AG (2003) Endogenous DNA double-strand breaks: Production, fidelity of repair, and induction of cancer. Proc Natl Acad Sci USA 100: 12871-12876.
45. Watson JA, Watson CJ, McCann A, Baugh J (2010) Epigentics, the epicenter of the hypoxic response. Epigenetics 5: 293-296.
46. Wegrzyn J, Potla R, Chwae YJ, Sepuri NB, Zhang Q, Koeck T, Derecka M, Szczepanek K, Szelag M, Gornicka A, Moh A, Moghaddas S, Chen Q, Bobbili S, Cichy J, Dulak J, Baker DP, Wolfman A, Stuehr D, Hassan MO, Fu XY, Avadhani N, Drake JI, Fawcett P, Lesnefsky EJ, Larner AC (2009) Function of mitochondrial Stat3 in cellular respiration. Science 323: 793-797.
47. Wen L, Chen Y, Zeng LL, Zhao F, Li R, Liu Y, Zhang C (2012) Triptolide induces cell-cycle arrest and apoptosis of human multiple myeloma cells in vitro via altering expression of histone demethylase LSD1 and JMJD2B. Acta Pharmacol Sin 33: 109-119.
48. Xiong H, Zhang ZG, Tian XQ, Sun DF, Liang QC, Zhang YJ, Lu R, Chen YX, Fang JY (2008) Inhibition of JAK1,2/STAT3 signaling induces apoptosis, cell cycle arrest, and reduces tumor cell invasion in colorectal cancer cells. Neoplasia 10: 287-297.
49. Yamawaki Y, Kimura H, Hosoi T, Ozawa K (2010) MyD88 plays a key role in LPS-induced Stat3 activation in the hypothalamus. Am J Physiol Regul Integr Comp Physiol 298: R403-R410.
50. Yang J, Jubb AM, Pike L, Buffa FM, Turley H, Baban D, Leek R, Gatter KC, Ragoussis J, Harris AL (2010) The histone demethylase JMJD2B is regulated by estrogen receptor alpha and hypoxia, and is a key mediator of estrogen induced growth. Cancer Res 70: 6456-6466.
51. Young LC, McDonald DW, Hendzel MJ (2013) Kdm4b histone demethylase is a DNA damage response protein and confers a survival advantage following g-irradiation. J Biol Chem 288: 21376-21388.
52. Yuan J, Narayanan L, Rockwell S, Glazer PM (2000) Diminished DNA repair and elevated mutagenesis in mammalian cells exposed to hypoxia and low pH. Cancer Res 60: 4372-4376.
53. Zeng J, Ge Z, Wang L, Li Q, Wang N, Björkholm M, Jia J, Xu D (2010) The histone demethylase RBP2 is overexpressed in gastric cancer and its inhibition triggers senescence of cancer cells. Gastroenterology 138: 981-992.
54. Zhao H, Piwnica-Worms H (2001) ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol Cell Biol 21: 4129-4139.
55. Zheng H, Chen L, Pledger WJ, Fang J, Chen J (2013) p53 promotes repair of heterochromatin DNA by regulating JMJD2b and SUV39H1 expression. Oncogene; e-pub ahead of print 4 February 2013; doi:10.1038/onc.2013.6.
56. Zhu S, Li Y, Zhao L, Hou P, Shangguan C, Yao R, Zhang W, Zhang Y, Tan J, Huang B, Lu J (2012) TSA-induced JMJD2B downregulation is associated with cyclin B1-dependent survivin degradation and apoptosis in LNCap cells. J Cell Biochem 113: 2375-2382.