Kdm4b histone demethylase is a dna damage response protein and confers a survival advantage following γ-irradiation

Journal of Biological Chemistry

Volumn 288, Issue 29, 2013, Pages 21376-21388

  Young, Leah C ^a   McDonald, Darin W ^a   Hendzel, Michael J ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOTOXIC; DEMETHYLASE; DNA DAMAGE RESPONSE; DNA DAMAGES; DOUBLE STRAND BREAK REPAIR; OVER-EXPRESSION;

IRRADIATION; REPAIR;

DNA;

HISTONE DEMETHYLASE; HISTONE DEMETHYLASE KDM4B; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CATALYSIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; DNA DAMAGE; DNA DETERMINATION; DNA REPAIR; DOUBLE STRANDED DNA BREAK; EPIGENETICS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GAMMA RADIATION; GENE OVEREXPRESSION; HUMAN; IMMUNOFLUORESCENCE; IMMUNOFLUORESCENCE MICROSCOPY; IONIZING RADIATION; MEMBRANE PERMEABILITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN METABOLISM; PROTEIN MODIFICATION;

CHROMATIN REGULATION; CHROMATIN REMODELING; CHROMATIN STRUCTURE; DNA DAMAGE RESPONSE; DNA REPAIR; HETEROCHROMATIN; HISTONE METHYLATION;

ANIMALS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL LINE, TUMOR; CELL SURVIVAL; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; DNA-ACTIVATED PROTEIN KINASE; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GAMMA RAYS; GREEN FLUORESCENT PROTEINS; HISTONES; HUMANS; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; LASERS; LYSINE; METHYLATION; MICE; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS;

EID: 84880557003     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.491514     Document Type: Article

References (63)

1. Hanahan, D., and Weinberg, R. A. (2011) Hallmarks of cancer. The next generation. Cell 144, 646-674
2. Tzao, C., Tung, H. J., Jin, J. S., Sun, G. H., Hsu, H. S., Chen, B. H., Yu, C. P., and Lee, S. C. (2009) Prognostic significance of global histone modifications in resected squamous cell carcinoma of the esophagus. Mod. Pathol. 22, 252-260
3. I H., Ko, E., Kim, Y., Cho, E. Y., Han, J., Park, J., Kim, K., Kim, D. H., and Shim, Y. M. (2010) Association of global levels of histone modifications with recurrence-free survival in stage IIB and III esophageal squamous cell carcinomas. Cancer Epidemiol. Biomarkers Prev. 19, 566-573
4. Barlési, F., Giaccone, G., Gallegos-Ruiz, M. I., Loundou, A., Span, S. W., Lefesvre, P., Kruyt, F. A., and Rodriguez, J. A. (2007) Global histone modifications predict prognosis of resected non small-cell lung cancer. J. Clin. Oncol. 25, 4358-4364
5. Song, J. S., Kim, Y. S., Kim, D. K., Park, S. I., and Jang, S. J. (2012) Global histone modification pattern associated with recurrence and disease-free survival in non-small cell lung cancer patients. Pathol. Int. 62, 182-190
6. Manuyakorn, A., Paulus, R., Farrell, J., Dawson, N. A., Tze, S., Cheung-Lau, G., Hines, O. J., Reber, H., Seligson, D. B., Horvath, S., Kurdistani, S. K., Guha, C., and Dawson, D. W. (2010) Cellular histone modification patterns predict prognosis and treatment response in resectable pancreatic adenocarcinoma. results from RTOG 9704. J. Clin. Oncol. 28, 1358-1365
7. Wei, Y., Xia, W., Zhang, Z., Liu, J., Wang, H., Adsay, N. V., Albarracin, C., Yu, D., Abbruzzese, J. L., Mills, G. B., Bast, R. C., Jr., Hortobagyi, G. N., and Hung, M. C. (2008) Loss of trimethylation at lysine 27 of histone H3 is a predictor of poor outcome in breast, ovarian, and pancreatic cancers. Mol. Carcinog. 47, 701-706
8. Tamagawa, H., Oshima, T., Shiozawa, M., Morinaga, S., Nakamura, Y., Yoshihara, M., Sakuma, Y., Kameda, Y., Akaike, M., Masuda, M., Imada, T., and Miyagi, Y. (2012) The global histone modification pattern correlates with overall survival in metachronous liver metastasis of colorectal cancer. Oncol. Rep. 27, 637-642
9. Ellinger, J., Kahl, P., von der Gathen, J., Rogenhofer, S., Heukamp, L. C., Gütgemann, I., Walter, B., Hofstädter, F., Büttner, R., Müller, S. C., Bastian, P. J., and von Ruecker, A. (2010) Global levels of histone modifications predict prostate cancer recurrence. Prostate. 70, 61-69
10. Elsheikh, S. E., Green, A. R., Rakha, E. A., Powe, D. G., Ahmed, R. A., Collins, H. M., Soria, D., Garibaldi, J. M., Paish, C. E., Ammar, A. A., Grainge, M. J., Ball, G. R., Abdelghany, M. K., Martinez-Pomares, L., Heery, D. M., and Ellis, I. O. (2009) Global histone modifications in breast cancer correlate with tumor phenotypes, prognostic factors, and patient outcome. Cancer Res. 69, 3802-3809
11. Seligson, D. B., Horvath, S., McBrian, M. A., Mah, V., Yu, H., Tze, S., Wang, Q., Chia, D., Goodglick, L., and Kurdistani, S. K. (2009) Global levels of histone modifications predict prognosis in different cancers. Am. J. Pathol. 174, 1619-1628
12. Ellinger, J., Kahl, P., Mertens, C., Rogenhofer, S., Hauser, S., Hartmann, W., Bastian, P. J., Büttner, R., Müller, S. C., and von Ruecker A. (2010) Prognostic relevance of global histone H3 lysine 4 (H3K4) methylation in renal cell carcinoma. Int. J. Cancer 127, 2360-2366
13. He, C., Xu, J., Zhang, J., Xie, D., Ye, H., Xiao, Z., Cai, M., Xu, K., Zeng, Y., Li, H., and Wang, J. (2012) High expression of trimethylated histone H3 lysine 4 is associated with poor prognosis in hepatocellular carcinoma. Hum. Pathol. 43, 1425-1435
14. Park, Y. S., Jin, M. Y., Kim, Y. J., Yook, J. H., Kim, B. S., and Jang, S. J. (2008) The global histone modification pattern correlates with cancer recurrence and overall survival in gastric adenocarcinoma. Ann. Surg. Oncol. 15, 1968-1976
15. Chen, M. W., Hua, K. T., Kao, H. J., Chi, C. C., Wei, L. H., Johansson, G., Shiah, S. G., Chen, P. S., Jeng, Y. M., Cheng, T. Y., Lai, T. C., Chang, J. S., Jan, Y. H., Chien, M. H., Yang, C. J., Huang, M. S., Hsiao, M., and Kuo, M. L. (2010) H3K9 histone methyltransferase G9a promotes lung cancer invasion and metastasis by silencing the cell adhesion molecule Ep-CAM. Cancer Res. 70, 7830-7840
16. Peters, A. H., O'Carroll, D., Scherthan, H., Mechtler, K., Sauer, S., Schöfer, C., Weipoltshammer, K., Pagani, M., Lachner, M., Kohlmaier, A., Opravil, S., Doyle, M., Sibilia, M., and Jenuwein, T. (2001) Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107, 323-337
17. McManus, K. J., Biron, V. L., Heit, R., Underhill, D. A., and Hendzel, M. J. (2006) Dynamic changes in histone H3 lysine 9 methylations. Identification of a mitosis-specific function for dynamic methylation in chromosome congression and segregation. J. Biol. Chem. 281, 8888-8897
18. Heit, R., Rattner, J. B., Chan, G. K., and Hendzel, M. J. (2009) G2 histone methylation is required for the proper segregation of chromosomes. J. Cell Sci. 122, 2957-2968
19. Kondo, Y., Shen, L., Ahmed, S., Boumber, Y., Sekido, Y., Haddad, B. R., and Issa, J. P. (2008) Downregulation of histone H3 lysine 9 methyltransferase G9a induces centrosome disruption and chromosome instability in cancer cells. PLoS ONE 3, e2037
20. Tachibana, M., Sugimoto, K., Fukushima, T., and Shinkai, Y. (2001) Set domain-containing protein, G9a, is a novel lysine-preferring mammalian histone methyltransferase with hyperactivity and specific selectivity to lysines 9 and 27 of histone H3. J. Biol. Chem. 276, 25309-25317
21. Peters, A. H., Kubicek, S., Mechtler, K., O'Sullivan, R. J., Derijck, A. A., Perez-Burgos, L., Kohlmaier, A., Opravil, S., Tachibana, M., Shinkai, Y., Martens, J. H., and Jenuwein, T. (2003) Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol. Cell 12, 1577-1589
22. Robin, P., Fritsch, L., Philipot, O., Svinarchuk, F., and Ait-Si-Ali, S. (2007) Post-translational modifications of histones H3 and H4 associated with the histone methyltransferases Suv39h1 and G9a. Genome Biol. 8, R270
23. Rossetto, D., Truman, A. W., Kron, S. J., and Côté, J. (2010) Epigenetic modifications in double-strand break DNA damage signaling and repair. Clin. Cancer Res. 16, 4543-4552
24. Cann, K. L., and Dellaire, G. (2011) Heterochromatin and the DNA damage response. The need to relax. Biochem. Cell Biol. 89, 45-60
25. Casas-Delucchi, C. S., van Bemmel, J. G., Haase, S., Herce, H. D., Nowak, D., Meilinger, D., Stear, J. H., Leonhardt, H., and Cardoso, M. C. (2012) Histone hypoacetylation is required to maintain late replication timing of constitutive heterochromatin. Nucleic Acids Res. 40, 159-169
26. Murga, M., Jaco, I., Fan, Y., Soria, R., Martinez-Pastor, B., Cuadrado, M., Yang, S. M., Blasco, M. A., Skoultchi, A. I., and Fernandez-Capetillo, O. (2007) Global chromatin compaction limits the strength of theDNAdamage response. J. Cell Biol. 178, 1101-1108
27. Lavin, M. F. (2008) Ataxia-telangiectasia. From a rare disorder to a paradigm for cell signalling and cancer. Nat. Rev. Mol. Cell Biol. 9, 759-769
28. Goodarzi, A. A., Noon, A. T., Deckbar, D., Ziv, Y., Shiloh, Y., Löbrich, M., and Jeggo, P. A. (2008) ATM signaling facilitates repair of DNA doublestrand breaks associated with heterochromatin. Mol. Cell 31, 167-177
29. Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J. R., Cole, P. A., Casero, R. A., and Shi, Y. (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119, 941-953
30. Whetstine, J. R., Nottke, A., Lan, F., Huarte, M., Smolikov, S., Chen, Z., Spooner, E., Li, E., Zhang, G., Colaiacovo, M., and Shi, Y. (2006) Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell 125, 467-481
31. Chen, Z., Zang, J., Whetstine, J., Hong, X., Davrazou, F., Kutateladze, T. G., Simpson, M., Mao, Q., Pan, C. H., Dai, S., Hagman, J., Hansen, K., Shi, Y., and Zhang, G. (2006) Structural insights into histone demethylation by JMJD2 family members. Cell 125, 691-702
32. Young, L. C., and Hendzel, M. J. (2012) The oncogenic potential of Jumonji D2 (JMJD2/KDM4) histone demethylase overexpression. Biochem. Cell Biol. 10.1139/bcb-2012-0054
33. Kawazu, M., Saso, K., Tong, K. I., McQuire, T., Goto, K., Son, D. O., Wakeham, A., Miyagishi, M., Mak, T. W., and 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
34. Yang, J., Jubb, A. M., Pike, L., Buffa, F. M., Turley, H., Baban, D., Leek, R., Gatter, K. C., Ragoussis, J., and Harris, A. L. (2010) The histone demethylase JMJD2B is regulated by estrogen receptor α and hypoxia and is a key mediator of estrogen-induced growth. Cancer Res. 70, 6456-6466
35. Mallette, F. A., and Richard, S. (2012) JMJD2A promotes cellular transformation by blocking cellular senescence through transcriptional repression of the tumor suppressor CHD5. Cell Rep. 2, 1233-1243
36. Liu, G., Bollig-Fischer, A., Kreike, B., van de Vijver, M. J., Abrams, J., Ethier, S. P., and Yang, Z. Q. (2009) Genomic amplification and oncogenic properties of the GASC1 histone demethylase gene in breast cancer. Oncogene 28, 4491-4500
37. Fodor, B. D., Kubicek, S., Yonezawa, M., O'Sullivan, R. J., Sengupta, R., Perez-Burgos, L., Opravil, S., Mechtler, K., Schotta, G., and Jenuwein, T. (2006) Jmjd2b antagonizes H3K9 trimethylation at pericentric heterochromatin in mammalian cells. Genes Dev. 20, 1557-1562
38. Carpenter, A. E., Jones, T. R., Lamprecht, M. R., Clarke, C., Kang, I. H., Friman, O., Guertin, D. A., Chang, J. H., Lindquist, R. A., Moffat, J., Golland, P., and Sabatini, D. M. (2006) CellProfiler. image analysis software for identifying and quantifying cell phenotypes. Genome Biol. 7, R100
39. Jones, T. R., Kang, I. H., Wheeler, D. B., Lindquist, R. A., Papallo, A., Sabatini, D. M., Golland, P., and Carpenter, A. E. (2008) CellProfiler Analyst. Data exploration and analysis software for complex image-based screens. BMC Bioinformatics 9, 482
40. Kamentsky, L., Jones, T. R., Fraser, A., Bray, M. A., Logan, D. J., Madden, K. L., Ljosa, V., Rueden, C., Eliceiri, K. W., and Carpenter, A. E. (2011) Improved structure, function, and compatibility for CellProfiler. Modular high-throughput image analysis software. Bioinformatics 27, 1179-1180
41. Koike, M., and Koike, A. (2008) Accumulation of Ku80 proteins at DNA double-strand breaks in living cells. Exp. Cell Res. 314, 1061-1070
42. Sun, Y., Jiang, X., Xu, Y., Ayrapetov, M. K., Moreau, L. A., Whetstine, J. R., and Price, B. D. (2009) Histone H3 methylation links DNA damage detection to activation of the tumour suppressor Tip60. Nat. Cell Biol. 11, 1376-1382
43. Burma, S., Chen, B. P., Murphy, M., Kurimasa, A., and Chen, D. J. (2001) ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem. 276, 42462-42467
44. Hillringhaus, L., Yue, W. W., Rose, N. R., Ng, S. S., Gileadi, C., Loenarz, C., Bello, S. H., Bray, J. E., Schofield, C. J., and Oppermann, U. (2011) Structural and evolutionary basis for the dual substrate selectivity of human KDM4 histone demethylase family. J. Biol. Chem. 286, 41616-41625
45. Peng, J. C., and Karpen, G. H. (2009) Heterochromatic genome stability requires regulators of histone H3 K9 methylation. PLoS Genet 5, e1000435
46. Loh, Y. H., Zhang, W., Chen, X., George, J., and Ng, H. H. (2007) Jmjd1a and Jmjd2c histone H3 Lys 9 demethylases regulate self-renewal in embryonic stem cells. Genes Dev. 21, 2545-2557
47. Wang, J., Zhang, M., Zhang, Y., Kou, Z., Han, Z., Chen, D. Y., Sun, Q. Y., and Gao, S. (2010) The histone demethylase JMJD2C is stage-specifically expressed in preimplantation mouse embryos and is required for embryonic development. Biol Reprod. 82, 105-111
48. Rouleau, M., Patel, A., Hendzel, M. J., Kaufmann, S. H., and Poirier, G. G. (2010) PARP inhibition. PARP1 and beyond. Nat. Rev. Cancer 10, 293-301
49. Haince, J. F., McDonald, D., Rodrigue, A., Déry, U., Masson, J. Y., Hendzel, M. J., and Poirier, G. G. (2008) PARP1-dependent kinetics of recruitment of MRE11 and NBS1 proteins to multipleDNAdamage sites. J. Biol. Chem. 283, 1197-1208
50. Sousa, F. G., Matuo, R., Soares, D. G., Escargueil, A. E., Henriques, J. A., Larsen, A. K., and Saffi, J. (2012) PARPs and the DNA damage response. Carcinogenesis 33, 1433-1440
51. Boehler, C., Gauthier, L. R., Mortusewicz, O., Biard, D. S., Saliou, J. M., Bresson, A., Sanglier-Cianferani, S., Smith, S., Schreiber, V., Boussin, F., and Dantzer, F. (2011) Poly(ADP-ribose) polymerase 3 (PARP3), a newcomer in cellular response to DNA damage and mitotic progression. Proc. Natl. Acad. Sci. U.S.A. 108, 2783-2788
52. Mallette, F. A., Mattiroli, F., Cui, G., Young, L. C., Hendzel, M. J., Mer, G., Sixma, T. K., and Richard, S. (2012) RNF8- and RNF168-dependent degradation of KDM4A/JMJD2A triggers 53BP1 recruitment to DNA damage sites. EMBO J. 31, 1865-1878
53. Hong, Z., Jiang, J., Lan, L., Nakajima, S., Kanno, S., Koseki, H., and Yasui, A. (2008) A polycomb group protein, PHF1, is involved in the response to DNA double-strand breaks in human cell. Nucleic Acids Res. 36, 2939-2947
54. Mirzoeva, O. K., and Petrini, J. H. (2001)DNAdamage-dependent nuclear dynamics of the Mre11 complex. Mol. Cell. Biol. 21, 281-288
55. Kühne, M., Riballo, E., Rief, N., Rothkamm, K., Jeggo, P. A., and Löbrich, M. (2004) A double-strand break repair defect in ATM-deficient cells contributes to radiosensitivity. Cancer Res. 64, 500-508
56. Fnu, S., Williamson, E. A., De Haro, L. P., Brenneman, M., Wray, J., Shaheen, M., Radhakrishnan, K., Lee, S. H., Nickoloff, J. A., and Hromas, R. (2011) Methylation of histone H3 lysine 36 enhances DNA repair by nonhomologous end-joining. Proc. Natl. Acad. Sci. U.S.A. 108, 540-545
57. Yin, D. T., Wang, Q., Chen, L., Liu, M. Y., Han, C., Yan, Q., Shen, R., He, G., Duan, W., Li, J. J., Wani, A., and Gao, J. X. (2011) Germline stem cell gene PIWIL2 mediates DNA repair through relaxation of chromatin. PLoS ONE 6, e27154
58. Tjeertes, J. V., Miller, K. M., and Jackson, S. P. (2009) Screen for DNA damage-responsive histone modifications identifies H3K9Ac and H3K56Ac in human cells. EMBO J. 28, 1878-1889
59. Chiolo, I., Minoda, A., Colmenares, S. U., Polyzos, A., Costes, S. V., and Karpen, G. H. (2011) Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 144, 732-744
60. Zheng, H., Chen, L., Pledger, W. J., Fang, J., and Chen, J. (2013) p53 promotes repair of heterochromatin DNA by regulating JMJD2b and SUV39H1 expression. Oncogene 10.1038/onc.2013.6
61. Li, W., Zhao, L., Zang, W., Liu, Z., Chen, L., Liu, T., Xu, D., and 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
62. Kim, T. D., Shin, S., Berry, W. L., Oh, S., and Janknecht, R. (2012) The JMJD2A demethylase regulates apoptosis and proliferation in colon cancer cells. J. Cell. Biochem. 113, 1368-1376
63. Kim, T. D., Oh, S., Shin, S., and Janknecht, R. (2012) Regulation of tumor suppressor p53 and HCT116 cell physiology by histone demethylase JMJD2D/KDM4D. PLoS ONE 7, e34618