14-3-3 checkpoint regulatory proteins interact specifically with DNA repair protein human exonuclease 1 (hEXO1) via a semi-conserved motif

DNA Repair

Volumn 11, Issue 3, 2012, Pages 267-277

  Andersen, Sofie Dabros ^a   Keijzers, Guido ^g   Rampakakis, Emmanouil ^b   Engels, Kim ^c   Luhn, Patricia ^d   El Shemerly, Mahmoud ^c   Nielsen, Finn Cilius ^e   Du, Yuhong ^d   May, Alfred ^f   Bohr, Vilhelm A ^f   Ferrari, Stefano ^c   Zannis Hadjopoulos, Maria ^b   Fu, Haian ^d   Rasmussen, Lene Juel ^g  

^a ROSKILDE UNIVERSITY   (Denmark)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e Mental Health Center Glostrup   (Denmark)

^f NATIONAL INSTITUTE ON AGING   (United States)

^g UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

14 3 3; Cell cycle control; DNA damage; DNA repair; HEXO1; Protein phosphorylation

Indexed keywords

AMINO ACID; DOUBLE STRANDED DNA; EXONUCLEASE; PROTEIN 14 3 3; REGULATOR PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE CHECKPOINT; CELL NUCLEUS; CELLULAR DISTRIBUTION; DNA REPAIR; DNA REPLICATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; UBIQUITINATION;

14-3-3 PROTEINS; ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CELL CYCLE CHECKPOINTS; CELL NUCLEUS; DNA REPAIR; DNA REPAIR ENZYMES; DNA REPLICATION; EXODEOXYRIBONUCLEASES; HEK293 CELLS; HELA CELLS; HUMANS; MICE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; NIH 3T3 CELLS; PHOSPHORYLATION; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; RECOMBINANT PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84856560000     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2011.11.007     Document Type: Article

References (57)

1. Liberti S.E., Andersen S.D., Wang J., May A., Miron S., Perderiset M., Keijzers G., Nielsen F.C., Charbonnier J.B., Bohr V.A., Rasmussen L.J. Bi-directional routing of DNA mismatch repair protein human exonuclease 1 to replication foci and DNA double strand breaks. DNA Repair (Amst.) 2011, 10:73-86.
2. Nielsen F., Jäger A., Lützen A., Bundgaard J., Rasmussen L. Characterization of human exonuclease 1 in complex with mismatch repair proteins, subcellular localization and association with PCNA. Oncogene 2004, 23:1457-1468.
3. Qiu J., Qian Y., Chen V., Guan M.X., Shen B. Human exonuclease 1 functionally complements its yeast homologues in DNA recombination, RNA primer removal, and mutation avoidance. J. Biol. Chem. 1999, 274:17893-17900.
4. Genschel J., Bazemore L., Modrich P. Human exonuclease I is required for 5' and 3' mismatch repair. J. Biol. Chem. 2002, 277:13302-13311.
5. Gravel S., Chapman J., Magill C., Jackson S. DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev. 2008, 22:2767-2772.
6. Eid W., Steger M., El-Shemerly M., Ferretti L.P., Pena-Diaz J., Konig C., Valtorta E., Sartori A.A., Ferrari S. DNA end resection by CtIP and exonuclease 1 prevents genomic instability. EMBO Rep. 2010, 11:962-968.
7. Bolderson E., Tomimatsu N., Richard D.J., Boucher D., Kumar R., Pandita T.K., Burma S., Khanna K.K. Phosphorylation of Exo1 modulates homologous recombination repair of DNA double-strand breaks. Nucl. Acids Res. 2010.
8. Bardwell P.D., Woo C.J., Wei K., Li Z., Martin A., Sack S.Z., Parris T., Edelmann W., Scharff M.D. Altered somatic hypermutation and reduced class-switch recombination in exonuclease 1-mutant mice. Nat. Immunol. 2004, 5:224-229.
9. Bolderson E., Richard D., Edelmann W., Khanna K. Involvement of Exo1b in DNA damage-induced apoptosis. Nucl. Acids Res. 2009, 37:3452-3463.
10. Dherin C., Gueneau E., Francin M., Nunez M., Miron S., Liberti S., Rasmussen L., Zinn-Justin S., Gilquin B., Charbonnier J., Boiteux S. Characterization of a highly conserved binding site of Mlh1 required for exonuclease I-dependent mismatch repair. Mol. Cell Biol. 2009, 29:907-918.
11. Maringele L., Lydall D. EXO1-dependent single-stranded DNA at telomeres activates subsets of DNA damage and spindle checkpoint pathways in budding yeast yku70Delta mutants. Genes Dev. 2002, 16:1919-1933.
12. Schaetzlein S., Kodandaramireddy N., Ju Z., Lechel A., Stepczynska A., Lilli D., Clark A., Rudolph C., Kuhnel F., Wei K., Schlegelberger B., Schirmacher P., Kunkel T., Greenberg R., Edelmann W., Rudolph K. Exonuclease-1 deletion impairs DNA damage signaling and prolongs lifespan of telomere-dysfunctional mice. Cell 2007, 130:863-877.
13. Tinline-Purvis H., Savory A.P., Cullen J.K., Dave A., Moss J., Bridge W.L., Marguerat S., Bahler J., Ragoussis J., Mott R., Walker C.A., Humphrey T.C. Failed gene conversion leads to extensive end processing and chromosomal rearrangements in fission yeast. EMBO J. 2009, 28:3400-3412.
14. Tran P.T., Fey J.P., Erdeniz N., Gellon L., Boiteux S., Liskay R.M. A mutation in EXO1 defines separable roles in DNA mismatch repair and post-replication repair. DNA Repair (Amst.) 2007, 6:1572-1583.
15. Vallur A.C., Maizels N. Distinct activities of exonuclease 1 and flap endonuclease 1 at telomeric g4 DNA. PLoS ONE 2010, 5:e8908.
16. Lee B., D.r.Wilson The RAD2 domain of human exonuclease 1 exhibits 5' to 3' exonuclease and flap structure-specific endonuclease activities. J. Biol. Chem. 1999, 274:37763-37769.
17. Orans J., McSweeney E.A., Iyer R.R., Hast M.A., Hellinga H.W., Modrich P., Beese L.S. Structures of human exonuclease 1 DNA complexes suggest a unified mechanism for nuclease family. Cell 2011, 145:212-223.
18. Genschel J., Modrich P. Mechanism of 5'-directed excision in human mismatch repair. Mol. Cell 2003, 12:1077-1086.
19. Zhang Y., Yuan F., Presnell S., Tian K., Gao Y., Tomkinson A., Gu L., Li G. Reconstitution of 5'-directed human mismatch repair in a purified system. Cell 2005, 122:693-705.
20. El-Shemerly M., Janscak P., Hess D., Jiricny J., Ferrari S. Degradation of human exonuclease 1b upon DNA synthesis inhibition. Cancer Res. 2005, 65:3604-3609.
21. Doherty K.M., Sharma S., Uzdilla L.A., Wilson T.M., Cui S., Vindigni A., Brosh R.M. RECQ1 helicase interacts with human mismatch repair factors that regulate genetic recombination. J. Biol. Chem. 2005, 280:28085-28094.
22. Sharma S., Sommers J., Driscoll H., Uzdilla L., Wilson T., Brosh R.J. The exonucleolytic and endonucleolytic cleavage activities of human exonuclease 1 are stimulated by an interaction with the carboxyl-terminal region of the Werner syndrome protein. J. Biol. Chem. 2003, 278:23487-23496.
23. Zhu Z., Chung W., Shim E., Lee S., Ira G. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 2008, 134:981-994.
24. Mimitou E., Symington L. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 2008, 455:770-774.
25. Nicolette M.L., Lee K., Guo Z., Rani M., Chow J.M., Lee S.E., Paull T.T. Mre11-Rad50-Xrs2 and Sae2 promote 5' strand resection of DNA double-strand breaks. Nat. Struct. Mol. Biol. 2010, 17:1478-1485.
26. Nimonkar A., Ozsoy A., Genschel J., Modrich P., Kowalczykowski S. Human exonuclease 1 and BLM helicase interact to resect DNA and initiate DNA repair. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:16906-16911.
27. Nimonkar A.V., Genschel J., Kinoshita E., Polaczek P., Campbell J.L., Wyman C., Modrich P., Kowalczykowski S.C. BLM-DNA2-RPA-MRN and EXO1-BLM-RPA-MRN constitute two DNA end resection machineries for human DNA break repair. Genes Dev. 2011, 25:350-362.
28. Muslin A., Tanner J., Allen P., Shaw A. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell 1996, 84:889-897.
29. Yaffe M., Rittinger K., Volinia S., Caron P., Aitken A., Leffers H., Gamblin S., Smerdon S., Cantley L. The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 1997, 91:961-971.
30. Rittinger K., Budman J., Xu J., Volinia S., Cantley L.C., Smerdon S.J., Gamblin S.J., Yaffe M.B. Structural analysis of 14-3-3 phosphopeptide complexes identifies a dual role for the nuclear export signal of 14-3-3 in ligand binding. Mol. Cell 1999, 4:153-166.
31. Gardino A.K., Smerdon S.J., Yaffe M.B. Structural determinants of 14-3-3 binding specificities and regulation of subcellular localization of 14-3-3-ligand complexes: a comparison of the X-ray crystal structures of all human 14-3-3 isoforms. Semin. Cancer Biol. 2006, 16:173-182.
32. El-Shemerly M., Hess D., Pyakurel A., Moselhy S., Ferrari S. ATR-dependent pathways control hEXO1 stability in response to stalled forks. Nucl. Acids Res. 2008, 36:511-519.
33. Engels K., Giannattasio M., Muzi-Falconi M., Lopes M., Ferrari S. 14-3-3 Proteins regulate exonuclease 1-dependent processing of stalled replication forks. PLoS Genet. 2011, 7:e1001367.
34. Guerrette S., Wilson T., Gradia S., Fishel R. Interactions of human hMSH2 with hMSH3 and hMSH2 with hMSH6: examination of mutations found in hereditary nonpolyposis colorectal cancer. Mol. Cell Biol. 1998, 18:6616-6623.
35. Du Y., Masters S.C., Khuri F.R., Fu H. Monitoring 14-3-3 protein interactions with a homogeneous fluorescence polarization assay. J. Biomol. Screen 2006, 11:269-276.
36. Knudsen N., Nielsen F., Vinther L., Bertelsen R., Holten-Andersen S., Liberti S., Hofstra R., Kooi K., Rasmussen L. Nuclear localization of human DNA mismatch repair protein exonuclease 1 (hEXO1). Nucl. Acids Res. 2007, 35:2609-2619.
37. Fu H., Coburn J., Collier R.J. The eukaryotic host factor that activates exoenzyme S of Pseudomonas aeruginosa is a member of the 14-3-3 protein family. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:2320-2324.
38. Pearson C.E., Frappier L., Zannis-Hadjopoulos M. Plasmids bearing mammalian DNA-replication origin-enriched (ors) fragments initiate semiconservative replication in a cell-free system. Biochim. Biophys. Acta 1991, 1090:156-166.
39. Gyuris J., Golemis E., Chertkov H., Brent R. Cdi1, a human G1 and S phase protein phosphatase that associates with Cdk2. Cell 1993, 75:791-803.
40. Zhang L., Wang H., Liu D., Liddington R., Fu H. Raf-1 kinase and exoenzyme S interact with 14-3-3zeta through a common site involving lysine 49. J. Biol. Chem. 1997, 272:13717-13724.
41. Luhn P., Wang H., Marcus A.I., Fu H. Identification of FAKTS as a novel 14-3-3-associated nuclear protein. Proteins 2007, 67:479-489.
42. Fu H., Subramanian R.R., Masters S.C. 14-3-3 proteins: structure, function, and regulation. Annu. Rev. Pharmacol. Toxicol. 2000, 40:617-647.
43. Wang H., Zhang L., Liddington R., Fu H. Mutations in the hydrophobic surface of an amphipathic groove of 14-3-3zeta disrupt its interaction with Raf-1 kinase. J. Biol. Chem. 1998, 273:16297-16304.
44. Chaudhri M., Scarabel M., Aitken A. Mammalian and yeast 14-3-3 isoforms form distinct patterns of dimers in vivo. Biochem. Biophys. Res. Commun. 2003, 300:679-685.
45. Aitken A., Baxter H., Dubois T., Clokie S., Mackie S., Mitchell K., Peden A., Zemlickova E. Specificity of 14-3-3 isoform dimer interactions and phosphorylation. Biochem. Soc. Trans. 2002, 30:351-360.
46. Alvarez D., Novac O., Callejo M., Ruiz M.T., Price G.B., Zannis-Hadjopoulos M. 14-3-3sigma is a cruciform DNA binding protein and associates in vivo with origins of DNA replication. J. Cell. Biochem. 2002, 87:194-207.
47. Novac O., Alvarez D., Pearson C.E., Price G.B., Zannis-Hadjopoulos M. The human cruciform-binding protein, CBP, is involved in DNA replication and associates in vivo with mammalian replication origins. J. Biol. Chem. 2002, 277:11174-11183.
48. Zannis-Hadjopoulos M., Yahyaoui W., Callejo M. 14-3-3 cruciform-binding proteins as regulators of eukaryotic DNA replication. Trends Biochem. Sci. 2008, 33:44-50.
49. Cotta-Ramusino C., Fachinetti D., Lucca C., Doksani Y., Lopes M., Sogo J., Foiani M. Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Mol. Cell 2005, 17:153-159.
50. Wilker E., Grant R., Artim S., Yaffe M. A structural basis for 14-3-3sigma functional specificity. J. Biol. Chem. 2005, 280:18891-18898.
51. Waterman M., Stavridi E., Waterman J., Halazonetis T. ATM-dependent activation of p53 involves dephosphorylation and association with 14-3-3 proteins. Nat. Genet. 1998, 19:175-178.
52. Morin I., Ngo H., Greenall A., Zubko M., Morrice N., Lydall D. Checkpoint-dependent phosphorylation of Exo1 modulates the DNA damage response. EMBO J. 2008, 27:2400-2410.
53. Segurado M., Diffley J. Separate roles for the DNA damage checkpoint protein kinases in stabilizing DNA replication forks. Genes Dev. 2008, 22:1816-1827.
54. Usui T., Petrini J. The Saccharomyces cerevisiae 14-3-3 proteins Bmh1 and Bmh2 directly influence the DNA damage-dependent functions of Rad53. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:2797-2802.
55. Branzei D., Foiani M. The checkpoint response to replication stress. DNA Repair (Amst.) 2009, 8:1038-1046.
56. Jiang K., Pereira E., Maxfield M., Russell B., Goudelock D., Sanchez Y. Regulation of Chk1 includes chromatin association and 14-3-3 binding following phosphorylation on Ser-345. J. Biol. Chem. 2003, 278:25207-25217.
57. Porter G., Khuri F., Fu H. Dynamic 14-3-3/client protein interactions integrate survival and apoptotic pathways. Semin. Cancer Biol. 2006, 16:193-202.