Phosphorylation of Exo1 modulates homologous recombination repair of DNA double-strand breaks

Nucleic Acids Research

Volumn 38, Issue 6, 2010, Pages 1821-1831

  Bolderson, Emma ^a   Tomimatsu, Nozomi ^b   Richard, Derek J ^a   Boucher, Didier ^a   Kumar, Rakesh ^c   Pandita, Tej K ^c   Burma, Sandeep ^b   Khanna, Kum Kum ^a  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; DOUBLE STRANDED DNA; EXONUCLEASE; EXONUCLEASE 1; PROTEIN RPA; RAD51 PROTEIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; EXO1 PROTEIN, HUMAN; EXODEOXYRIBONUCLEASE; H2AFX PROTEIN, HUMAN; HISTONE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROTEIN SERINE THREONINE KINASE; RAD51 PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ARTICLE; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; GENETIC STABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IONIZING RADIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; CELL LINE; CHROMOSOME ABERRATION; DOUBLE STRANDED DNA BREAK; GENE SILENCING; GENETIC RECOMBINATION; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

CELL CYCLE PROTEINS; CELL LINE; CHROMOSOME ABERRATIONS; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; EXODEOXYRIBONUCLEASES; GENE KNOCKDOWN TECHNIQUES; HISTONES; HUMANS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RAD51 RECOMBINASE; RADIATION, IONIZING; RECOMBINATION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

EID: 77951251067     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp1164     Document Type: Article

References (41)

1. Mimitou, E.P. and Symington, L.S. (2009) Nucleases and helicases take center stage in homologous recombination. Trends Biochem. Sci., 34, 264-272.
2. Shiotani, B. and Zou, L. (2009) Single-stranded DNA orchestrates an ATM-to-ATR switch at DNA breaks. Mol. Cell, 33, 547-558.
3. Sartori, A.A., Lukas, C., Coates, J., Mistrik, M., Fu, S., Bartek, J., Baer, R., Lukas, J. and Jackson, S.P. (2007) Human CtIP promotes DNA end resection. Nature, 450, 509-514.
4. Bernstein, K.A. and Rothstein, R. (2009) At loose ends: resecting a double-strand break. Cell, 137, 807-810.
5. Szankasi, P. and Smith, G.R. (1992) A DNA exonuclease induced during meiosis of Schizosaccharomyces pombe. J. Biol. Chem., 267, 3014-3023.
6. Lee Bi, B.I., Nguyen, L.H., Barsky, D., Fernandes, M. and Wilson, D.M. III (2002) Molecular interactions of human Exo1 with DNA. Nucleic Acids Res., 30, 942-949.
7. Qiu, J., Qian, Y., Chen, V., Guan, M.X. and Shen, B. (1999) Human exonuclease 1 functionally complements its yeast homologues in DNA recombination, RNA primer removal, and mutation avoidance. J. Biol. Chem., 274, 17893-17900.
8. Lee, S.D. and Alani, E. (2006) Analysis of interactions between mismatch repair initiation factors and the replication processivity factor PCNA. J. Mol. Biol., 355, 175-184.
9. Fiorentini, P., Huang, K.N., Tishkoff, D.X., Kolodner, R.D. and Symington, L.S. (1997) Exonuclease I of Saccharomyces cerevisiae functions in mitotic recombination in vivo and in vitro. Mol. Cell Biol., 17, 2764-2773.
10. Kirkpatrick, D.T., Ferguson, J.R., Petes, T.D. and Symington, L.S. (2000) Decreased meiotic intergenic recombination and increased meiosis I nondisjunction in exo1 mutants of Saccharomyces cerevisiae. Genetics, 156, 1549-1557.
11. Tsubouchi, H. and Ogawa, H. (2000) Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerevisiae. Mol. Biol. Cell, 11, 2221-2233.
12. Wei, K., Clark, A.B., Wong, E., Kane, M.F., Mazur, D.J., Parris, T., Kolas, N.K., Russell, R., Hou, H. Jr, Kneitz, B. et al. (2003) Inactivation of Exonuclease 1 in mice results in DNA mismatch repair defects, increased cancer susceptibility, and male and female sterility. Genes Dev., 17, 603-614.
13. Sun, X., Zheng, L. and Shen, B. (2002) Functional alterations of human exonuclease 1 mutants identified in atypical hereditary nonpolyposis colorectal cancer syndrome. Cancer Res., 62, 6026-6030.
14. Wu, Y., Berends, M.J., Post, J.G., Mensink, R.G., Verlind, E., van der Sluis, T., Kempinga, C., Sijmons, R.H., van der Zee, A.G., Hollema, H. et al. (2001) Germline mutations of EXO1 gene in patients with hereditary nonpolyposis colorectal cancer (HNPCC) and atypical HNPCC forms. Gastroenterology, 120, 1580-1587.
15. Schaetzlein, S., Kodandaramireddy, N.R., Ju, Z., Lechel, A., Stepczynska, A., Lilli, D.R., Clark, A.B., Rudolph, C., Kuhnel, F., Wei, K. et al. (2007) Exonuclease-1 deletion impairs DNA damage signaling and prolongs lifespan of telomere-dysfunctional mice. Cell, 130, 863-877.
16. Bolderson, E., Richard, D.J., Edelmann, W. and Khanna, K.K. (2009) Involvement of Exo1b in DNA damage-induced apoptosis. Nucleic Acids Res., 37, 3452-3463.
17. Tomimatsu, N., Mukherjee, B. and Burma, S. (2009) Distinct roles of ATR and DNA-PKcs in triggering DNA damage responses in ATM-deficient cells. EMBO Rep., 10, 629-635.
18. Richard, D.J., Bolderson, E., Cubeddu, L., Wadsworth, R.I., Savage, K., Sharma, G.G., Nicolette, M.L., Tsvetanov, S., McIlwraith, M.J., Pandita, R.K. et al. (2008) Single-stranded DNA-binding protein hSSB1 is critical for genomic stability. Nature, 453, 677-681.
19. Uematsu, N., Weterings, E., Yano, K., Morotomi-Yano, K., Jakob, B., Taucher-Scholz, G., Mari, P.O., van Gent, D.C., Chen, B.P. and Chen, D.J. (2007) Autophosphorylation of DNA-PKCS regulates its dynamics at DNA double-strand breaks. J. Cell Biol., 177, 219-229.
20. Khanna, K.K., Keating, K.E., Kozlov, S., Scott, S., Gatei, M., Hobson, K., Taya, Y., Gabrielli, B., Chan, D., Lees-Miller, S.P. et al. (1998) ATM associates with and phosphorylates p53: mapping the region of interaction. Nat. Genet., 20, 398-400.
21. Young, D.B., Jonnalagadda, J., Gatei, M., Jans, D.A., Meyn, S. and Khanna, K.K. (2005) Identification of domains of ataxia-telangiectasia mutated required for nuclear localization and chromatin association. J. Biol. Chem., 280, 27587-27594.
22. Li, Y., Bolderson, E., Kumar, R., Muniandy, P.A., Xue, Y., Richard, D., Seidman, M., Pandita, T.K., Khanna, K.K. and Wang, W. (2009) hSSB1 and hSSB2 form similar multi-protein complexes that participate in DNA damage response. J. Biol. Chem., 284, 23525-23531.
23. Gupta, A., Sharma, G.G., Young, C.S., Agarwal, M., Smith, E.R., Paull, T.T., Lucchesi, J.C., Khanna, K.K., Ludwig, T. and Pandita, T.K. (2005) Involvement of human MOF in ATM function. Mol. Cell Biol., 25, 5292-5305.
24. Gravel, S., Chapman, J.R., Magill, C. and Jackson, S.P. (2008) DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev., 22, 2767-2772.
25. Rogakou, E.P., Pilch, D.R., Orr, A.H., Ivanova, V.S. and Bonner, W.M. (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem., 273, 5858-5868.
26. Chen, H.T., Bhandoola, A., Difilippantonio, M.J., Zhu, J., Brown, M.J., Tai, X., Rogakou, E.P., Brotz, T.M., Bonner, W.M., Ried, T. et al. (2000) Response to RAG-mediated VDJ cleavage by NBS1 and gamma-H2AX. Science, 290, 1962-1965.
27. Peterson, C.L. (2001) Chromatin: mysteries solved? Biochem. Cell Biol., 79, 219-225.
28. Litman, R., Peng, M., Jin, Z., Zhang, F., Zhang, J., Powell, S., Andreassen, P.R. and Cantor, S.B. (2005) BACH1 is critical for homologous recombination and appears to be the Fanconi anemia gene product FANCJ. Cancer Cell, 8, 255-265.
29. Pierce, A.J., Johnson, R.D., Thompson, L.H. and Jasin, M. (1999) XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev., 13, 2633-2638.
30. Zhou, B.B. and Elledge, S.J. (2000) The DNA damage response: putting checkpoints in perspective. Nature, 408, 433-439.
31. Mimitou, E.P. and Symington, L.S. (2008) Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature, 455, 770-774.
32. Zhu, Z., Chung, W.H., Shim, E.Y., Lee, S.E. and Ira, G. (2008) Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell, 134, 981-994.
33. Bakkenist, C.J. and Kastan, M.B. (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature, 421, 499-506.
34. Buis, J., Wu, Y., Deng, Y., Leddon, J., Westfield, G., Eckersdorff, M., Sekiguchi, J.M., Chang, S. and Ferguson, D.O. (2008) Mre11 nuclease activity has essential roles in DNA repair and genomic stability distinct from ATM activation. Cell, 135, 85-96.
35. Morin, I., Ngo, H.P., Greenall, A., Zubko, M.K., Morrice, N. and Lydall, D. (2008) Checkpoint-dependent phosphorylation of Exo1 modulates the DNA damage response. EMBO J., 27, 2400-2410.
36. Matsuoka, S., Ballif, B.A., Smogorzewska, A., McDonald, E.R. III, Hurov, K.E., Luo, J., Bakalarski, C.E., Zhao, Z., Solimini, N., Lerenthal, Y. et al. (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science, 316, 1160-1166.
37. van der Horst, A. and Khanna, K.K. (2009) The peptidyl-prolyl isomerase Pin1 regulates cytokinesis through Cep55. Cancer Res., 69, 6651-6659.
38. Nimonkar, A.V., Ozsoy, A.Z., Genschel, J., Modrich, P. and Kowalczykowski, S.C. (2008) Human exonuclease 1 and BLM helicase interact to resect DNA and initiate DNA repair. Proc. Natl Acad. Sci. USA, 105, 16906-16911.
39. El-Shemerly, M., Hess, D., Pyakurel, A.K., Moselhy, S. and Ferrari, S. (2008) ATR-dependent pathways control hEXO1 stability in response to stalled forks. Nucleic Acids Res., 36, 511-519.
40. Di Virgilio, M., Ying, C.Y. and Gautier, J. (2009) PIKK-dependent phosphorylation of Mre11 induces MRN complex inactivation by disassembly from chromatin. DNA Repair, 8, 1311-1320.
41. Beucher, A., Birraux, J., Tchouandong, L., Barton, O., Shibata, A., Conrad, S., Goodarzi, A.A., Krempler, A., Jeggo, P.A. and Lobrich, M. (2009) ATM and Artemis promote homologous recombination of radiation-induced DNA double-strand breaks in G2. EMBO J., 28, 3413-3427.