ATM and SIRT6/SNF2H Mediate Transient H2AX Stabilization When DSBs Form by Blocking HUWE1 to Allow Efficient γH2AX Foci Formation

Cell Reports

Volumn 13, Issue 12, 2015, Pages 2728-2740

  Atsumi, Yuko ^a,b   Minakawa, Yusuke ^a,c   Ono, Masaya ^a   Dobashi, Sachiko ^a   Shinohe, Keitaro ^d   Shinohara, Akira ^e   Takeda, Shunichi ^f   Takagi, Masatoshi ^g   Takamatsu, Nobuhiko ^b   Nakagama, Hitoshi ^a   Teraoka, Hirobumi ^d   Yoshioka, Ken ichi ^a  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^b KITASATO UNIVERSITY   (Japan)

^c TOKYO UNIVERSITY OF SCIENCE   (Japan)

^d TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^e OSAKA UNIVERSITY   (Japan)

^f KYOTO UNIVERSITY   (Japan)

^g TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; CHROMATIN ASSEMBLY FACTOR 1; HISTONE H2AX; HUWE1 LIGASE; PROTEASOME; SIRTUIN 6; SNF2H PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; ATM PROTEIN, HUMAN; CHROMATIN; H2AFX PROTEIN, HUMAN; HISTONE; HUWE1 PROTEIN, HUMAN; SIRT6 PROTEIN, HUMAN; SIRTUIN; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CELL DAMAGE; CHROMATIN; DNA REPAIR; DOUBLE STRANDED DNA BREAK; HELA CELL LINE; HUMAN; HUMAN CELL; MEF CELL LINE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UBIQUITINATION; WI-38 CELL LINE; ANIMAL; ANTAGONISTS AND INHIBITORS; GENETICS; METABOLISM; MOUSE; PHOSPHORYLATION;

ANIMALS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CHROMATIN; DNA BREAKS, DOUBLE-STRANDED; HELA CELLS; HISTONES; HUMANS; MICE; PHOSPHORYLATION; SIRTUINS; UBIQUITIN-PROTEIN LIGASES;

EID: 84971530972     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.11.054     Document Type: Article

References (43)

1. Atsumi, Y., Fujimori, H., Fukuda, H., Inase, A., Shinohe, K., Yoshioka, Y., Shikanai, M., Ichijima, Y., Unno, J., Mizutani, S., et al. Onset of quiescence following p53 mediated down-regulation of H2AX in normal cells. PLoS ONE, 6, 2011, e23432.
2. Atsumi, Y., Inase, A., Osawa, T., Sugihara, E., Sakasai, R., Fujimori, H., Teraoka, H., Saya, H., Kanno, M., Tashiro, F., et al. The Arf/p53 protein module, which induces apoptosis, down-regulates histone H2AX to allow normal cells to survive in the presence of anti-cancer drugs. J. Biol. Chem. 288 (2013), 13269–13277.
3. Bassing, C.H., Alt, F.W., H2AX may function as an anchor to hold broken chromosomal DNA ends in close proximity. Cell Cycle 3 (2004), 149–153.
4. Bentley, M.L., Corn, J.E., Dong, K.C., Phung, Q., Cheung, T.K., Cochran, A.G., Recognition of UbcH5c and the nucleosome by the Bmi1/Ring1b ubiquitin ligase complex. EMBO J. 30 (2011), 3285–3297.
5. Bonner, W.M., West, M.H., Stedman, J.D., Two-dimensional gel analysis of histones in acid extracts of nuclei, cells, and tissues. Eur. J. Biochem. 109 (1980), 17–23.
6. Bonner, W.M., Redon, C.E., Dickey, J.S., Nakamura, A.J., Sedelnikova, O.A., Solier, S., Pommier, Y., GammaH2AX and cancer. Nat. Rev. Cancer 8 (2008), 957–967.
7. Chang, T.C., Wentzel, E.A., Kent, O.A., Ramachandran, K., Mullendore, M., Lee, K.H., Feldmann, G., Yamakuchi, M., Ferlito, M., Lowenstein, C.J., et al. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol. Cell 26 (2007), 745–752.
8. Doil, C., Mailand, N., Bekker-Jensen, S., Menard, P., Larsen, D.H., Pepperkok, R., Ellenberg, J., Panier, S., Durocher, D., Bartek, J., et al. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 136 (2009), 435–446.
9. Facchino, S., Abdouh, M., Chatoo, W., Bernier, G., BMI1 confers radioresistance to normal and cancerous neural stem cells through recruitment of the DNA damage response machinery. J. Neurosci. 30 (2010), 10096–10111.
10. Fernandez-Capetillo, O., Lee, A., Nussenzweig, M., Nussenzweig, A., H2AX: the histone guardian of the genome. DNA Repair (Amst.) 3 (2004), 959–967.
11. Fradet-Turcotte, A., Canny, M.D., Escribano-Díaz, C., Orthwein, A., Leung, C.C., Huang, H., Landry, M.C., Kitevski-LeBlanc, J., Noordermeer, S.M., Sicheri, F., Durocher, D., 53BP1 is a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark. Nature 499 (2013), 50–54.
12. Fukawa, T., Ono, M., Matsuo, T., Uehara, H., Miki, T., Nakamura, Y., Kanayama, H.O., Katagiri, T., DDX31 regulates the p53-HDM2 pathway and rRNA gene transcription through its interaction with NPM1 in renal cell carcinomas. Cancer Res. 72 (2012), 5867–5877.
13. Gatti, M., Pinato, S., Maspero, E., Soffientini, P., Polo, S., Penengo, L., A novel ubiquitin mark at the N-terminal tail of histone H2As targeted by RNF168 ubiquitin ligase. Cell Cycle 11 (2012), 2538–2544.
14. Gertler, A.A., Cohen, H.Y., SIRT6, a protein with many faces. Biogerontology 14 (2013), 629–639.
15. Ginjala, V., Nacerddine, K., Kulkarni, A., Oza, J., Hill, S.J., Yao, M., Citterio, E., van Lohuizen, M., Ganesan, S., BMI1 is recruited to DNA breaks and contributes to DNA damage-induced H2A ubiquitination and repair. Mol. Cell. Biol. 31 (2011), 1972–1982.
16. Ichijima, Y., Yoshioka, K., Yoshioka, Y., Shinohe, K., Fujimori, H., Unno, J., Takagi, M., Goto, H., Inagaki, M., Mizutani, S., Teraoka, H., DNA lesions induced by replication stress trigger mitotic aberration and tetraploidy development. PLoS ONE, 5, 2010, e8821.
17. Ismail, I.H., Andrin, C., McDonald, D., Hendzel, M.J., BMI1-mediated histone ubiquitylation promotes DNA double-strand break repair. J. Cell Biol. 191 (2010), 45–60.
18. Jia, G., Su, L., Singhal, S., Liu, X., Emerging roles of SIRT6 on telomere maintenance, DNA repair, metabolism and mammalian aging. Mol. Cell. Biochem. 364 (2012), 345–350.
19. Kaidi, A., Weinert, B.T., Choudhary, C., Jackson, S.P., Human SIRT6 promotes DNA end resection through CtIP deacetylation. Science 329 (2010), 1348–1353.
20. Kobayashi, A., Kang, M.I., Okawa, H., Ohtsuji, M., Zenke, Y., Chiba, T., Igarashi, K., Yamamoto, M., Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol. Cell. Biol. 24 (2004), 7130–7139.
21. Lal, A., Pan, Y., Navarro, F., Dykxhoorn, D.M., Moreau, L., Meire, E., Bentwich, Z., Lieberman, J., Chowdhury, D., miR-24-mediated downregulation of H2AX suppresses DNA repair in terminally differentiated blood cells. Nat. Struct. Mol. Biol. 16 (2009), 492–498.
22. Mao, Z., Hine, C., Tian, X., Van Meter, M., Au, M., Vaidya, A., Seluanov, A., Gorbunova, V., SIRT6 promotes DNA repair under stress by activating PARP1. Science 332 (2011), 1443–1446.
23. Martinez-Pastor, B., Mostoslavsky, R., Sirtuins, metabolism, and cancer. Front. Pharmacol., 3, 2012, 22.
24. Matsuoka, S., Ballif, B.A., Smogorzewska, A., McDonald, E.R. 3rd, Hurov, K.E., Luo, J., Bakalarski, C.E., Zhao, Z., Solimini, N., Lerenthal, Y., et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316 (2007), 1160–1166.
25. Mattiroli, F., Vissers, J.H., van Dijk, W.J., Ikpa, P., Citterio, E., Vermeulen, W., Marteijn, J.A., Sixma, T.K., RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell 150 (2012), 1182–1195.
26. McCord, R.A., Michishita, E., Hong, T., Berber, E., Boxer, L.D., Kusumoto, R., Guan, S., Shi, X., Gozani, O., Burlingame, A.L., et al. SIRT6 stabilizes DNA-dependent protein kinase at chromatin for DNA double-strand break repair. Aging (Albany, N.Y.) 1 (2009), 109–121.
27. Min, S., Jo, S., Lee, H.S., Chae, S., Lee, J.S., Ji, J.H., Cho, H., ATM-dependent chromatin remodeler Rsf-1 facilitates DNA damage checkpoints and homologous recombination repair. Cell Cycle 13 (2014), 666–677.
28. Ono, M., Shitashige, M., Honda, K., Isobe, T., Kuwabara, H., Matsuzuki, H., Hirohashi, S., Yamada, T., Label-free quantitative proteomics using large peptide data sets generated by nanoflow liquid chromatography and mass spectrometry. Mol. Cell. Proteomics 5 (2006), 1338–1347.
29. Osawa, T., Atsumi, Y., Sugihara, E., Saya, H., Kanno, M., Tashiro, F., Masutani, M., Yoshioka, K., Arf and p53 act as guardians of a quiescent cellular state by protecting against immortalization of cells with stable genomes. Biochem. Biophys. Res. Commun. 432 (2013), 34–39.
30. Pinder, J.B., Attwood, K.M., Dellaire, G., Reading, writing, and repair: the role of ubiquitin and the ubiquitin-like proteins in DNA damage signaling and repair. Front. Genet., 4, 2013, 45.
31. Raver-Shapira, N., Marciano, E., Meiri, E., Spector, Y., Rosenfeld, N., Moskovits, N., Bentwich, Z., Oren, M., Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol. Cell 26 (2007), 731–743.
32. Rogakou, E.P., Boon, C., Redon, C., Bonner, W.M., Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146 (1999), 905–916.
33. Sonoda, E., Zhao, G.Y., Kohzaki, M., Dhar, P.K., Kikuchi, K., Redon, C., Pilch, D.R., Bonner, W.M., Nakano, A., Watanabe, M., et al. Collaborative roles of gammaH2AX and the Rad51 paralog Xrcc3 in homologous recombinational repair. DNA Repair (Amst.) 6 (2007), 280–292.
34. Stucki, M., Jackson, S.P., gammaH2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair (Amst.) 5 (2006), 534–543.
35. Todaro, G.J., Green, H., Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell Biol. 17 (1963), 299–313.
36. Toiber, D., Erdel, F., Bouazoune, K., Silberman, D.M., Zhong, L., Mulligan, P., Sebastian, C., Cosentino, C., Martinez-Pastor, B., Giacosa, S., et al. SIRT6 recruits SNF2H to DNA break sites, preventing genomic instability through chromatin remodeling. Mol. Cell 51 (2013), 454–468.
37. van Attikum, H., Gasser, S.M., Crosstalk between histone modifications during the DNA damage response. Trends Cell Biol. 19 (2009), 207–217.
38. Wang, Y., Huang, J.W., Li, M., Cavenee, W.K., Mitchell, P.S., Zhou, X., Tewari, M., Furnari, F.B., Taniguchi, T., MicroRNA-138 modulates DNA damage response by repressing histone H2AX expression. Mol. Cancer Res. 9 (2011), 1100–1111.
39. Wu, C.Y., Kang, H.Y., Yang, W.L., Wu, J., Jeong, Y.S., Wang, J., Chan, C.H., Lee, S.W., Zhang, X., Lamothe, B., et al. Critical role of monoubiquitination of histone H2AX protein in histone H2AX phosphorylation and DNA damage response. J. Biol. Chem. 286 (2011), 30806–30815.
40. Xu, C., Xu, Y., Gursoy-Yuzugullu, O., Price, B.D., The histone variant macroH2A1.1 is recruited to DSBs through a mechanism involving PARP1. FEBS Lett. 586 (2012), 3920–3925.
41. Xu, Y., Ayrapetov, M.K., Xu, C., Gursoy-Yuzugullu, O., Hu, Y., Price, B.D., Histone H2A.Z controls a critical chromatin remodeling step required for DNA double-strand break repair. Mol. Cell 48 (2012), 723–733.
42. Yata, K., Lloyd, J., Maslen, S., Bleuyard, J.Y., Skehel, M., Smerdon, S.J., Esashi, F., Plk1 and CK2 act in concert to regulate Rad51 during DNA double strand break repair. Mol. Cell 45 (2012), 371–383.
43. Yoshioka, K., Yoshioka, Y., Hsieh, P., ATR kinase activation mediated by MutSalpha and MutLalpha in response to cytotoxic O6-methylguanine adducts. Mol. Cell 22 (2006), 501–510.