RAD6 promotes homologous recombination repair by activating the autophagy-mediated degradation of heterochromatin protein HP1

Molecular and Cellular Biology

Volumn 35, Issue 2, 2015, Pages 406-416

  Chen, Su ^a   Wang, Chen ^a   Sun, Luxi ^b,c   Wang, Da Liang ^c   Chen, Lu ^a   Huang, Zhuan ^a   Yang, Qi ^a   Gao, Jie ^a   Yang, Xi Bin ^a   Chang, Jian Feng ^a   Chen, Ping ^a   Lan, Li ^b   Mao, Zhiyong ^a   Sun, Fang Lin ^a  

^a TONGJI UNIVERSITY   (China)

^b UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^c Tsinghua University   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; HETEROCHROMATIN PROTEIN 1; HETEROCHROMATIN PROTEIN 1 ALPHA; PROTEIN P53; RAD6 PROTEIN; UBIQUITIN CONJUGATING ENZYME E2; UNCLASSIFIED DRUG; HETEROCHROMATIN; HETEROCHROMATIN-SPECIFIC NONHISTONE CHROMOSOMAL PROTEIN HP-1; NONHISTONE PROTEIN; UBE2A PROTEIN, HUMAN; UBE2B PROTEIN, HUMAN; UBIQUITIN CONJUGATING ENZYME;

ANIMAL CELL; ARTICLE; AUTOPHAGY; BIOINFORMATICS; CARCINOGENESIS; CATALYSIS; CHROMATIN STRUCTURE; DNA DAMAGE; DNA REPAIR; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; LUNG CANCER; NONHUMAN; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN INTERACTION; RECOMBINATION REPAIR; SURVIVAL RATE; UBIQUITINATION; ULTRAVIOLET RADIATION; X IRRADIATION; CELL LINE; GENETICS; HETEROCHROMATIN; METABOLISM;

AUTOPHAGY; CELL LINE; CHROMOSOMAL PROTEINS, NON-HISTONE; HETEROCHROMATIN; HUMANS; RECOMBINATIONAL DNA REPAIR; UBIQUITIN-CONJUGATING ENZYMES;

EID: 84919698910     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01044-14     Document Type: Article

References (60)

1. Haber JE. 2000. Partners and pathways repairing a double-strand break. Trends Genet 16:259-264. http://dx.doi.org/10.1016/S0168-9525(00)02022-9.
2. Mao Z, Bozzella M, Seluanov A, Gorbunova V. 2008. DNA repair by nonhomologous end joining and homologous recombination during cell cycle in human cells. Cell Cycle 7:2902-2906. http://dx.doi.org/10.4161/cc.7.18.6679.
3. Mao Z, Hine C, Tian X, Van Meter M, Au M, Vaidya A, Seluanov A, Gorbunova V. 2011. SIRT6 promotes DNA repair under stress by activating PARP1. Science 332:1443-1446. http://dx.doi.org/10.1126/science.1202723.
4. Lieber MR. 2008. The mechanism of human nonhomologous DNA end joining. J Biol Chem 283:1-5. http://dx.doi.org/10.1074/jbc.R700039200.
5. Thompson LH, Schild D. 2001. Homologous recombinational repair of DNAensures mammalian chromosome stability. Mutat Res 477:131-153. http://dx.doi.org/10.1016/S0027-5107(01)00115-4.
6. Bennett EJ, Harper JW. 2008. DNA damage: ubiquitin marks the spot. Nat Struct Mol Biol 15:20-22. http://dx.doi.org/10.1038/nsmb0108-20.
7. Bergink S, Jentsch S. 2009. Principles of ubiquitin and SUMO modifications in DNA repair. Nature 458:461-467. http://dx.doi.org/10.1038/nature07963.
8. Panier S, Durocher D. 2009. Regulatory ubiquitylation in response to DNA double-strand breaks. DNA Repair 8:436-443. http://dx.doi.org/10.1016/j.dnarep.2009.01.013.
9. Chau V, Tobias JW, Bachmair A, Marriott D, Ecker DJ, Gonda DK, Varshavsky A. 1989. A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 243:1576-1583. http://dx.doi.org/10.1126/science.2538923.
10. Kirkin V, McEwan DG, Novak I, Dikic I. 2009. A role for ubiquitin in selective autophagy. Mol Cell 34:259-269. http://dx.doi.org/10.1016/j.molcel.2009.04.026.
11. Kraft C, Peter M, Hofmann K. 2010. Selective autophagy: ubiquitinmediated recognition and beyond. Nat Cell Biol 12:836-841. http://dx.doi.org/10.1038/ncb0910-836.
12. Ulrich HD, Walden H. 2010. Ubiquitin signalling in DNA replication and repair. Nat Rev Mol Cell Biol 11:479-489. http://dx.doi.org/10.1038/nrm2921.
13. Weissman AM. 2001. Themes and variations on ubiquitylation. Nat Rev Mol Cell Biol 2:169-178. http://dx.doi.org/10.1038/35056563.
14. Game JC, Chernikova SB. 2009. The role of RAD6 in recombinational repair, checkpoints and meiosis via histone modification. DNA Repair 8:470-482. http://dx.doi.org/10.1016/j.dnarep.2009.01.007.
15. Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S. 2002. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419:135-141. http://dx.doi.org/10.1038/nature00991.
16. Torres-Ramos CA, Yoder BL, Burgers PM, Prakash S, Prakash L. 1996. Requirement of proliferating cell nuclear antigen in RAD6-dependent postreplicational DNA repair. Proc Natl Acad Sci U S A 93:9676-9681. http://dx.doi.org/10.1073/pnas.93.18.9676.
17. Dohmen RJ, Madura K, Bartel B, Varshavsky A. 1991. The N-end rule is mediated by the UBC2(RAD6) ubiquitin-conjugating enzyme. Proc Natl Acad Sci U S A 88:7351-7355. http://dx.doi.org/10.1073/pnas.88.16.7351.
18. Sancar G, Sancar C, Brügger B, Ha N, Sachsenheimer T, Gin E, Wdowik S, Lohmann I, Wieland F, Höfer T, Diernfellner A, Brunner M. 2011. A global circadian repressor controls antiphasic expression of metabolic genes in Neurospora. Mol Cell 44:687-697. http://dx.doi.org/10.1016/j.molcel.2011.10.019.
19. Sung P, Berleth E, Pickart C, Prakash S, Prakash L. 1991. Yeast RAD6 encoded ubiquitin conjugating enzyme mediates protein degradation dependent on the N-end-recognizing E3 enzyme. EMBO J 10:2187-2193.
20. Watkins JF, Sung P, Prakash S, Prakash L. 1993. The extremely conserved amino terminus of RAD6 ubiquitin-conjugating enzyme is essential for amino-end rule-dependent protein degradation. Genes Dev 7:250-261. http://dx.doi.org/10.1101/gad.7.2.250.
21. Chen S, Wang DL, Liu Y, Zhao L, Sun FL. 2012. RAD6 regulates the dosage of p53 by a combination of transcriptional and posttranscriptional mechanisms. Mol Cell Biol 32:576-587. http://dx.doi.org/10.1128/MCB.05966-11.
22. Chen S, Wei HM, Lv WW, Wang DL, Sun FL. 2011. E2 ligase dRad6 regulates DMP53 turnover in Drosophila. J Biol Chem 286:9020-9030. http://dx.doi.org/10.1074/jbc.M110.190314.
23. Liu C, Wang D, Wu J, Keller J, Ma T, Yu X. 2013. RNF168 forms a functional complex with RAD6 during the DNA damage response. J Cell Sci 126:2042-2051. http://dx.doi.org/10.1242/jcs.122945.
24. Akey CW, Luger K. 2003. Histone chaperones and nucleosome assembly. Curr Opin Struct Biol 13:6-14. http://dx.doi.org/10.1016/S0959-440X(03)00002-2.
25. Eitoku M, Sato L, Senda T, Horikoshi M. 2008. Histone chaperones: 30 years from isolation to elucidation of the mechanisms of nucleosome assembly and disassembly. Cell Mol Life Sci 65:414-444. http://dx.doi.org/10.1007/s00018-007-7305-6.
26. Palomera-Sanchez Z, Zurita M. 2011. Open, repair and close again: chromatin dynamics and the response to UV-induced DNA damage. DNA Repair 10:119-125. http://dx.doi.org/10.1016/j.dnarep.2010.10.010.
27. De Lucia F, Ni JQ, Vaillant C, Sun FL. 2005. HP1 modulates the transcription of cell-cycle regulators in Drosophila melanogaster. Nucleic Acids Res 33:2852-2858. http://dx.doi.org/10.1093/nar/gki584.
28. Eissenberg JC, Elgin SC. 2000. The HP1 protein family: getting a grip on chromatin. Curr Opin Genet Dev 10:204-210. http://dx.doi.org/10.1016/S0959-437X(00)00058-7.
29. Eissenberg JC, Elgin SC. 2014. HP1a: a structural chromosomal protein regulating transcription. Trends Genet 30:103-110. http://dx.doi.org/10.1016/j.tig.2014.01.002.
30. Lomberk G, Wallrath L, Urrutia R. 2006. The heterochromatin protein 1 family. Genome Biol 7:228. http://dx.doi.org/10.1186/gb-2006-7-7-228.
31. Smallwood A, Estève PO, Pradhan S, Carey M. 2007. Functional cooperation between HP1 and DNMT1 mediates gene silencing. Genes Dev 21:1169-1178. http://dx.doi.org/10.1101/gad.1536807.
32. Zeng W, Ball AR, Jr, Yokomori K. 2010. HP1: heterochromatin binding proteins working the genome. Epigenetics 5:287-292. http://dx.doi.org/10.4161/epi.5.4.11683.
33. Ayoub N, Jeyasekharan AD, Bernal JA, Venkitaraman AR. 2008. HP1-beta mobilization promotes chromatin changes that initiate the DNA damage response. Nature 453:682-686. http://dx.doi.org/10.1038/nature06875.
34. Ayoub N, Jeyasekharan AD, Venkitaraman AR. 2009. Mobilization and recruitment of HP1: a bimodal response to DNA breakage. Cell Cycle 8:2945-2950. http://dx.doi.org/10.4161/cc.8.18.9486.
35. Dinant C, Luijsterburg MS. 2009. The emerging role of HP1 in the DNA damage response. Mol Cell Biol 29:6335-6340. http://dx.doi.org/10.1128/MCB.01048-09.
36. Luijsterburg MS, Dinant C, Lans H, Stap J, Wiernasz E, Lagerwerf S, Warmerdam DO, Lindh M, Brink MC, Dobrucki JW, Aten JA, Fousteri MI, Jansen G, Dantuma NP, Vermeulen W, Mullenders LH, Houtsmuller AB, Verschure PJ, van Driel R. 2009. Heterochromatin protein 1 is recruited to various types of DNA damage. J Cell Biol 185:577-586. http://dx.doi.org/10.1083/jcb.200810035.
37. Chiolo I, Minoda A, Colmenares SU, Polyzos A, Costes SV, Karpen GH. 2011. Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 144:732-744. http://dx.doi.org/10.1016/j.cell.2011.02.012.
38. Liu LP, Ni JQ, Shi YD, Oakeley EJ, Sun FL. 2005. Sex-specific role of Drosophila melanogaster HP1 in regulating chromatin structure and gene transcription. Nat Genet 37:1361-1366. http://dx.doi.org/10.1038/ng1662.
39. Ni JQ, Liu LP, Hess D, Rietdorf J, Sun FL. 2006. Drosophila ribosomal proteins are associated with linker histone H1 and suppress gene transcription. Genes Dev 20:1959-1973. http://dx.doi.org/10.1101/gad.390106.
40. Lan L, Nakajima S, Wei L, Sun L, Hsieh CL, Sobol RW, Bruchez M, Van Houten B, Yasui A, Levine AS. 2014. Novel method for site-specific induction of oxidative DNA damage reveals differences in recruitment of repair proteins to heterochromatin and euchromatin. Nucleic Acids Res 42:2330-2345. http://dx.doi.org/10.1093/nar/gkt1233.
41. Peng JC, Karpen GH. 2009. Heterochromatic genome stability requires regulators of histone H3 K9 methylation. PLoS Genet. 5:e1000435. http://dx.doi.org/10.1371/journal.pgen.1000435.
42. Kwon SH, Workman JL. 2011. The changing faces of HP1: from heterochromatin formation and gene silencing to euchromatic gene expression: HP1 acts as a positive regulator of transcription. Bioessays 33:280-289. http://dx.doi.org/10.1002/bies.201000138.
43. Wallrath LL, Elgin SC. 2012. Enforcing silencing: dynamic HP1 complexes in Neurospora. Nat Struct Mol Biol 19:465-467. http://dx.doi.org/10.1038/nsmb.2291.
44. Mizushima N. 2007. Autophagy: process and function. Genes Dev 21:2861-2873. http://dx.doi.org/10.1101/gad.1599207.
45. Tanida I, Ueno T, Kominami E. 2004. LC3 conjugating system in mammalian autophagy. Int J Biochem Cell Biol 36:2503-2518. http://dx.doi.org/10.1016/j.biocel.2004.05.009.
46. Bjørkøy G, Lamark T, Brech A, Outzen H, Perander M, Overvatn A, Stenmark H, Johansen T. 2005. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 171:603-614. http://dx.doi.org/10.1083/jcb.200507002.
47. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Overvatn A, Bjørkøy G, Johansen T. 2007. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282:24131-24135. http://dx.doi.org/10.1074/jbc.M702824200.
48. Chapman JR, Taylor MR, Boulton SJ. 2012. Playing the end game: DNA double-strand break repair pathway choice. Mol Cell 47:497-510. http://dx.doi.org/10.1016/j.molcel.2012.07.029.
49. Mao Z, Bozzella M, Seluanov A, Gorbunova V. 2008. Comparison of nonhomologous end joining and homologous recombination in human cells. DNA Repair 7:1765-1771. http://dx.doi.org/10.1016/j.dnarep.2008.06.018.
50. Kim J, Guermah M, McGinty RK, Lee JS, Tang Z, Milne TA, Shilatifard A, Muir TW, Roeder RG. 2009. RAD6-mediated transcription-coupled H2B ubiquitylation directly stimulates H3K4 methylation in human cells. Cell 137:459-471. http://dx.doi.org/10.1016/j.cell.2009.02.027.
51. Lee JS, Shukla A, Schneider J, Swanson SK, Washburn MP, Florens L, Bhaumik SR, Shilatifard A. 2007. Histone crosstalk between H2B monoubiquitination and H3 methylation mediated by COMPASS. Cell 131:1084-1096. http://dx.doi.org/10.1016/j.cell.2007.09.046.
52. Robzyk K, Recht J, Osley MA. 2000. Rad6-dependent ubiquitination of histone H2B in yeast. Science 287:501-504. http://dx.doi.org/10.1126/science.287.5452.501.
53. Lachner M, O'Sullivan RJ, Jenuwein T. 2003. An epigenetic road map for histone lysine methylation. J Cell Sci 116:2117-2124. http://dx.doi.org/10.1242/jcs.00493.
54. Ciapponi L, Cenci G, Ducau J, Flores C, Johnson-Schlitz D, Gorski MM, Engels WR, Gatti M. 2004. The Drosophila Mre11/Rad50 complex is required to prevent both telomeric fusion and chromosome breakage. Curr Biol 14:1360-1366. http://dx.doi.org/10.1016/j.cub.2004.07.019.
55. Gao G, Walser JC, Beaucher ML, Morciano P, Wesolowska N, Chen J, Rong YS. 2010. HipHop interacts with HOAP and HP1 to protect Drosophila telomeres in a sequence-independent manner. EMBO J 29:819-829. http://dx.doi.org/10.1038/emboj.2009.394.
56. Figueiredo ML, Philip P, Stenberg P, Larsson J. 2012. HP1a recruitment to promoters is independent of H3K9 methylation in Drosophila melanogaster. PLoS Genet 8:e1003061. http://dx.doi.org/10.1371/journal.pgen.1003061.
57. Horáková AH, Bártová E, Galiová G, Uhlírová R, Matula P, Kozubek S. 2010. SUV39h-independent association of HP1 beta with fibrillarinpositive nucleolar regions. Chromosoma 119:227-241. http://dx.doi.org/10.1007/s00412-009-0252-2.
58. Haddad DM, Vilain S, Vos M, Esposito G, Matta S, Kalscheuer VM, Craessaerts K, Leyssen M, Nascimento RM, Vianna-Morgante AM, De Strooper B, Van Esch H, Morais VA, Verstreken P. 2013. Mutations in the intellectual disability gene Ube2a cause neuronal dysfunction and impair parkin-dependent mitophagy. Mol Cell 50:831-843. http://dx.doi.org/10.1016/j.molcel.2013.04.012.
59. Huen MS, Grant R, Manke I, Minn K, Yu X, Yaffe MB, Chen J. 2007. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131:901-914. http://dx.doi.org/10.1016/j.cell.2007.09.041.
60. Kim H, Chen J, Yu X. 2007. Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 316:1202-1205. http://dx.doi.org/10.1126/science.1139621.