Dual Control of Yen1 Nuclease Activity and Cellular Localization by Cdk and Cdc14 Prevents Genome Instability

Molecular Cell

Volumn 54, Issue 1, 2014, Pages 94-106

  Blanco, Miguel G ^a   Matos, Joao ^a,b   West, Stephen C ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE; NUCLEASE; PHOSPHOPROTEIN PHOSPHATASE CDC14; UNCLASSIFIED DRUG; YEN1 NUCLEASE;

ANAPHASE; ARTICLE; CATALYSIS; CELL CYCLE S PHASE; CELL STRESS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA REPAIR; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; ENZYME REGULATION; GENETIC RECOMBINATION; GENOMIC INSTABILITY; GENOTOXICITY; HETEROZYGOSITY LOSS; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PHOSPHORYLATION AND DEPHOSPHORYLATION; PROTEIN DNA BINDING;

ACTIVE TRANSPORT, CELL NUCLEUS; ANAPHASE; CDC2 PROTEIN KINASE; CELL CYCLE PROTEINS; CELL NUCLEUS; CYCLIN-DEPENDENT KINASES; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, FUNGAL; GENOMIC INSTABILITY; HOLLIDAY JUNCTION RESOLVASES; LOSS OF HETEROZYGOSITY; MUTATION; PHOSPHORYLATION; PROTEIN TYROSINE PHOSPHATASES; S PHASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84898034120     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.02.011     Document Type: Article

References (49)

1. Bardin A.J., Amon A. Men and sin: what's the difference?. Nat. Rev. Mol. Cell Biol. 2001, 2:815-826.
2. Bishop A.C., Ubersax J.A., Petsch D.T., Matheos D.P., Gray N.S., Blethrow J., Shimizu E., Tsien J.Z., Schultz P.G., Rose M.D., et al. A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 2000, 407:395-401.
3. Blanco M.G., Matos J., Rass U., Ip S.C.Y., West S.C. Functional overlap between the structure-specific nucleases Yen1 and Mus81-Mms4 for DNA-damage repair in S.cerevisiae. DNA Repair (Amst.) 2010, 9:394-402.
4. Bloom J., Cristea I.M., Procko A.L., Lubkov V., Chait B.T., Snyder M., Cross F.R. Global analysis of Cdc14 phosphatase reveals diverse roles in mitotic processes. J.Biol. Chem. 2011, 286:5434-5445.
5. Boddy M.N., Gaillard P.H.L., McDonald W.H., Shanahan P., Yates J.R., Russell P. Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 2001, 107:537-548.
6. Branzei D., Foiani M. Regulation of DNA repair throughout the cell cycle. Nat. Rev. Mol. Cell Biol. 2008, 9:297-308.
7. Bremmer S.C., Hall H., Martinez J.S., Eissler C.L., Hinrichsen T.H., Rossie S., Parker L.L., Hall M.C., Charbonneau H. Cdc14 phosphatases preferentially dephosphorylate a subset of cyclin-dependent kinase (Cdk) sites containing phosphoserine. J.Biol. Chem. 2012, 287:1662-1669.
8. Bzymek M., Thayer N.H., Oh S.D., Kleckner N., Hunter N. Double Holliday junctions are intermediates of DNA break repair. Nature 2010, 464:937-941.
9. Castor D., Nair N., Déclais A.C., Lachaud C., Toth R., Macartney T.J., Lilley D.M.J., Arthur J.S., Rouse J. Cooperative control of holliday junction resolution and DNA repair by the SLX1 and MUS81-EME1 nucleases. Mol. Cell 2013, 52:221-233.
10. Cejka P., Plank J.L., Bachrati C.Z., Hickson I.D., Kowalczykowski S.C. Rmi1 stimulates decatenation of double Holliday junctions during dissolution by Sgs1-Top3. Nat. Struct. Mol. Biol. 2010, 17:1377-1382.
11. Chen X.B., Melchionna R., Denis C.M., Gaillard P.H.L., Blasina A., Van de Weyer I., Boddy M.N., Russell P., Vialard J., McGowan C.H. Human Mus81-associated endonuclease cleaves Holliday junctions invitro. Mol. Cell 2001, 8:1117-1127.
12. Dayani Y., Simchen G., Lichten M. Meiotic recombination intermediates are resolved with minimal crossover formation during return-to-growth, an analogue of the mitotic cell cycle. PLoS Genet. 2011, 7:e1002083.
13. Dehé P.-M., Coulon S., Scaglione S., Shanahan P., Takedachi A., Wohlschlegel J.A., Yates J.R., Llorente B., Russell P., Gaillard P.-H. Regulation of Mus81-Eme1 Holliday junction resolvase in response to DNA damage. Nat. Struct. Mol. Biol. 2013, 20:598-603.
14. Ehmsen K.T., Heyer W.D. Saccharomyces cerevisiae Mus81-Mms4 is a catalytic, DNA structure-selective endonuclease. Nucleic Acids Res. 2008, 36:2182-2195.
15. El-Shemerly M., Janscak P., Hess D., Jiricny J., Ferrari S.R. Degradation of human exonuclease 1b upon DNA synthesis inhibition. Cancer Res. 2005, 65:3604-3609.
16. El-Shemerly M., Hess D., Pyakurel A.K., Moselhy S., Ferrari S.R. ATR-dependent pathways control hEXO1 stability in response to stalled forks. Nucleic Acids Res. 2008, 36:511-519.
17. Fabre F., Chan A., Heyer W.D., Gangloff S. Alternate pathways involving Sgs1/Top3, Mus81/ Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication. Proc. Natl. Acad. Sci. USA 2002, 99:16887-16892.
18. Gallo-Fernández M., Saugar I., Ortiz-Bazán M.A., Vázquez M.V., Tercero J.A. Cell cycle-dependent regulation of the nuclease activity of Mus81-Eme1/Mms4. Nucleic Acids Res. 2012, 40:8325-8335.
19. Garner E., Kim Y., Lach F.P., Kottemann M.C., Smogorzewska A. Human GEN1 and the SLX4-associated nucleases MUS81 and SLX1 are essential for the resolution of replication-induced Holliday junctions. Cell Rep 2013, 5:207-215.
20. Guo Z., Qian L.M., Liu R., Dai H.F., Zhou M., Zheng L., Shen B. Nucleolar localization and dynamic roles of flap endonuclease 1 in ribosomal DNA replication and damage repair. Mol. Cell. Biol. 2008, 28:4310-4319.
21. Guo Z., Kanjanapangka J., Liu N., Liu S., Liu C., Wu Z., Wang Y., Loh T., Kowolik C., Jamsen J., et al. Sequential posttranslational modifications program FEN1 degradation during cell-cycle progression. Mol. Cell 2012, 47:444-456.
22. Henneke G., Friedrich-Heineken E., Hübscher U. Flap endonuclease 1: a novel tumour suppresser protein. Trends Biochem. Sci. 2003, 28:384-390.
23. Ho C.K., Mazón G., Lam A.F., Symington L.S. Mus81 and Yen1 promote reciprocal exchange during mitotic recombination to maintain genome integrity in budding yeast. Mol. Cell 2010, 40:988-1000.
24. Holliday R. A mechanism for gene conversion in fungi. Genet. Res. 1964, 5:282-304.
25. Interthal H., Heyer W.D. MUS81 encodes a novel helix-hairpin-helix protein involved in the response to UV- and methylation-induced DNA damage in Saccharomyces cerevisiae. Mol. Gen. Genet. 2000, 263:812-827.
26. Ip S.C.Y., Rass U., Blanco M.G., Flynn H.R., Skehel J.M., West S.C. Identification of Holliday junction resolvases from humans and yeast. Nature 2008, 456:357-361.
27. Ira G., Malkova A., Liberi G., Foiani M., Haber J.E. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 2003, 115:401-411.
28. Kaffman A., Rank N.M., O'Neill E.M., Huang L.S., O'Shea E.K. The receptor Msn5 exports the phosphorylated transcription factor Pho4 out of the nucleus. Nature 1998, 396:482-486.
29. Kaliraman V., Mullen J.R., Fricke W.M., Bastin-Shanower S.A., Brill S.J. Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes Dev. 2001, 15:2730-2740.
30. Kosugi S., Hasebe M., Tomita M., Yanagawa H. Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc. Natl. Acad. Sci. USA 2009, 106:10171-10176.
31. Lieber M.R. The FEN-1 family of structure-specific nucleases ineukaryotic DNA replication, recombination and repair. Bioessays 1997, 19:233-240.
32. Loog M., Morgan D.O. Cyclin specificity in the phosphorylation of cyclin-dependent kinase substrates. Nature 2005, 434:104-108.
33. Luo G.B., Santoro I.M., McDaniel L.D., Nishijima I., Mills M., Youssoufian H., Vogel H., Schultz R.A., Bradley A. Cancer predisposition caused by elevated mitotic recombination in Bloom mice. Nat. Genet. 2000, 26:424-429.
34. Matos J., Blanco M.G., Maslen S.L., Skehel J.M., West S.C. Regulatory control of the resolution of DNA recombination intermediates during meiosis and mitosis. Cell 2011, 147:158-172.
35. Matos J., Blanco M.G., West S.C. Cell-cycle kinases coordinate the resolution of recombination intermediates with chromosome segregation. Cell Rep. 2013, 4:76-86.
36. Morin I., Ngo H.P., Greenall A., Zubko M.K., Morrice N., Lydall D. Checkpoint-dependent phosphorylation of Exo1 modulates the DNA damage response. EMBO J. 2008, 27:2400-2410.
37. Rass U., Compton S.A., Matos J., Singleton M.R., Ip S.C.Y., Blanco M.G., Griffith J.D., West S.C. Mechanism of Holliday junction resolution by the human GEN1 protein. Genes Dev. 2010, 24:1559-1569.
38. Schwartz E.K., Wright W.D., Ehmsen K.T., Evans J.E., Stahlberg H., Heyer W.D. Mus81-Mms4 functions as a single heterodimer to cleave nicked intermediates in recombinational DNA repair. Mol. Cell. Biol. 2012, 32:3065-3080.
39. Shou W., Seol J.H., Shevchenko A., Baskerville C., Moazed D., Chen Z.W.S., Jang J., Shevchenko A., Charbonneau H., Deshaies R.J. Exit from mitosis is triggered by Tem1-dependent release of the protein phosphatase Cdc14 from nucleolar RENT complex. Cell 1999, 97:233-244.
40. Shou W., Sakamoto K.M., Keener J., Morimoto K.W., Traverso E.E., Azzam R., Hoppe G.J., Feldman R.M., DeModena J., Moazed D., et al. Net1 stimulates RNA polymerase I transcription and regulates nucleolar structure independently of controlling mitotic exit. Mol. Cell 2001, 8:45-55.
41. Stegmeier F., Amon A. Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. Annu. Rev. Genet. 2004, 38:203-232.
42. Szakal B., Branzei D. Premature Cdk1/Cdc5/Mus81 pathway activation induces aberrant replication and deleterious crossover. EMBO J. 2013, 32:1155-1167.
43. Ubersax J.A., Woodbury E.L., Quang P.N., Paraz M., Blethrow J.D., Shah K., Shokat K.M., Morgan D.O. Targets of the cyclin-dependent kinase Cdk1. Nature 2003, 425:859-864.
44. Visintin R., Craig K., Hwang E.S., Prinz S., Tyers M.D., Amon A. The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk-dependent phosphorylation. Mol. Cell 1998, 2:709-718.
45. Visintin R., Hwang E.S., Amon A. Cfi1 prevents premature exit from mitosis by anchoring Cdc14 phosphatase in the nucleolus. Nature 1999, 398:818-823.
46. Wechsler T., Newman S., West S.C. Aberrant chromosome morphology in human cells defective for Holliday junction resolution. Nature 2011, 471:642-646.
47. West S.C. Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell Biol. 2003, 4:435-445.
48. Wu L., Hickson I.D. The Bloom's syndrome helicase suppressescrossing over during homologous recombination. Nature 2003, 426:870-874.
49. Wyatt H.D.M., Sarbajna S., Matos J., West S.C. Coordinated actions of SLX1-SLX4 and MUS81-EME1 for Holliday junction resolution in human cells. Mol. Cell 2013, 52:234-247.