Sae2 Is an Endonuclease that Processes Hairpin DNA Cooperatively with the Mre11/Rad50/Xrs2 Complex

Molecular Cell

Volumn 28, Issue 4, 2007, Pages 638-651

  Lengsfeld, Bettina M ^a   Rattray, Alison J ^b   Bhaskara, Venugopal ^a   Ghirlando, Rodolfo ^c   Paull, Tanya T ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

DNA

Indexed keywords

DNA; DOUBLE STRANDED DNA; ENDONUCLEASE; MRE11 PROTEIN; RAD50 PROTEIN; SAE2 PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; XRS2 PROTEIN;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; DNA BINDING; DNA STRAND BREAKAGE; ENZYME ACTIVITY; MEIOSIS; MISSENSE MUTATION; NONHUMAN;

DNA, FUNGAL; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; ENDODEOXYRIBONUCLEASES; ENDONUCLEASES; EXODEOXYRIBONUCLEASES; MUTANT PROTEINS; NUCLEIC ACID CONFORMATION; PHENOTYPE; PROTEIN BINDING; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCETALES;

EID: 36248942617     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.11.001     Document Type: Article

References (36)

1. Alani E., Padmore R., and Kleckner N. Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell 61 (1990) 419-436
2. Baroni E., Viscardi V., Cartagena-Lirola H., Lucchini G., and Longhese M.P. The functions of budding yeast Sae2 in the DNA damage response require Mec1- and Tel1-dependent phosphorylation. Mol. Cell. Biol. 24 (2004) 4151-4165
3. Boulton S.J., and Jackson S.P. Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J. 17 (1998) 1819-1828
4. Bressan D.A., Olivares H.A., Nelms B.E., and Petrini J.H. Alteration of N-terminal phosphoesterase signature motifs inactivates saccharomyces cerevisiae mre11. Genetics 150 (1998) 591-600
5. Chen C., and Kolodner R.D. Gross chromosomal rearrangements in Saccharomyces cerevisiae replication and recombination defective mutants. Nat. Genet. 23 (1999) 81-85
6. Clerici M., Mantiero D., Lucchini G., and Longhese M.P. The Saccharomyces cerevisiae Sae2 protein promotes resection and bridging of double strand break ends. J. Biol. Chem. 280 (2005) 38631-38638
7. Connelly J.C., and Leach D.R. The sbcC and sbcD genes of Escherichia coli encode a nuclease involved in palindrome inviability and genetic recombination. Genes Cells 1 (1996) 285-291
8. Connelly J.C., Kirkham L.A., and Leach D.R. The SbcCD nuclease of Escherichia coli is a structural maintenance of chromosomes (SMC) family protein that cleaves hairpin DNA. Proc. Natl. Acad. Sci. USA 95 (1998) 7969-7974
9. Downs J.A., and Jackson S.P. Involvement of DNA end-binding protein Ku in Ty element retrotransposition. Mol. Cell. Biol. 19 (1999) 6260-6268
10. Furuse M., Nagase Y., Tsubouchi H., Murakami-Murofushi K., Shibata T., and Ohta K. Distinct roles of two separable in vitro activities of yeast Mre11 in mitotic and meiotic recombination. EMBO J. 17 (1998) 6412-6425
11. Gibson F.P., Leach D.R., and Lloyd R.G. Identification of sbcD mutations as cosuppressors of recBC that allow propagation of DNA palindromes in Escherichia coli K-12. J. Bacteriol. 174 (1992) 1222-1228
12. Ivanov E.L., Sugawara N., White C.I., Fabre F., and Haber J.E. Mutations in XRS2 and RAD50 delay but do not prevent mating-type switching in Saccharomyces cerevisiae. Mol. Cell. Biol. 14 (1994) 3414-3425
13. Keeney S., Giroux C.N., and Kleckner N. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88 (1997) 375-384
14. Krogh B.O., and Symington L.S. Recombination proteins in yeast. Annu. Rev. Genet. 38 (2004) 233-271
15. Lee K., and Lee S.E. Saccharomyces cerevisiae Sae2- and Tel1-dependent single strand DNA formation at DNA break promotes microhomology-mediated end joining. Genetics 176 (2007) 2003-2014
16. Lewis L.K., Storici F., Van Komen S., Calero S., Sung P., and Resnick M.A. Role of the nuclease activity of Saccharomyces cerevisiae Mre11 in repair of DNA double-strand breaks in mitotic cells. Genetics 166 (2004) 1701-1713
17. Lisby M., Barlow J.H., Burgess R.C., and Rothstein R. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118 (2004) 699-713
18. Lobachev K.S., Gordenin D.A., and Resnick M.A. The Mre11 complex is required for repair of hairpin-capped double-strand breaks and prevention of chromosome rearrangements. Cell 108 (2002) 183-193
19. McKee A.H., and Kleckner N. A general method for identifying recessive diploid-specific mutations in Saccharomyces cerevisiae, its application to the isolation of mutants blocked at intermediate stages of meiotic prophase and characterization of a new gene SAE2. Genetics 146 (1997) 797-816
20. Moore J.K., and Haber J.E. Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol. Cell. Biol. 16 (1996) 2164-2173
21. Moreau S., Ferguson J.R., and Symington L.S. The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol. Cell. Biol. 19 (1999) 556-566
22. Nairz K., and Klein F. mre11S-a yeast mutation that blocks double-strand-break processing and permits nonhomologous synapsis in meiosis. Genes Dev. 11 (1997) 2272-2290
23. Paull T.T., and Gellert M. The 3′ to 5′ exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol. Cell 1 (1998) 969-979
24. Paull T.T., and Gellert M. Nbs1 potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex. Genes Dev. 13 (1999) 1276-1288
25. Prinz S., Amon A., and Klein F. Isolation of COM1, a new gene required to complete meiotic double-strand break-induced recombination in Saccharomyces cerevisiae. Genetics 146 (1997) 781-795
26. Rattray A.J., McGill C.B., Shafer B.K., and Strathern J.N. Fidelity of mitotic double-strand-break repair in Saccharomyces cerevisiae: a role for SAE2/COM1. Genetics 158 (2001) 109-122
27. Rattray A.J., Shafer B.K., Neelam B., and Strathern J.N. A mechanism of palindromic gene amplification in Saccharomyces cerevisiae. Genes Dev. 19 (2005) 1390-1399
28. Sawyer S.L., and Malik H.S. Positive selection of yeast nonhomologous end-joining genes and a retrotransposon conflict hypothesis. Proc. Natl. Acad. Sci. USA 103 (2006) 17614-17619
29. Scholes D.T., Banerjee M., Bowen B., and Curcio M.J. Multiple regulators of Ty1 transposition in Saccharomyces cerevisiae have conserved roles in genome maintenance. Genetics 159 (2001) 1449-1465
30. Sharples G.J., and Leach D.R. Structural and functional similarities between the SbcCD proteins of Escherichia coli and the RAD50 and MRE11 (RAD32) recombination and repair proteins of yeast. Mol. Microbiol. 17 (1995) 1215-1217
31. Symington L.S. Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev. 66 (2002) 630-670
32. Trujillo K.M., Roh D.H., Chen L., Van Komen S., Tomkinson A., and Sung P. Yeast xrs2 binds DNA and helps target rad50 and mre11 to DNA ends. J. Biol. Chem. 278 (2003) 48957-48964
33. Trujillo K.M., and Sung P. DNA structure-specific nuclease activities in the Saccharomyces cerevisiae Rad50/Mre11 complex. J. Biol. Chem. 276 (2001) 35458-35464
34. Tsubouchi H., and Ogawa H. A novel mre11 mutation impairs processing of double-strand breaks of DNA during both mitosis and meiosis. Mol. Cell. Biol. 18 (1998) 260-268
35. Uetz P., Giot L., Cagney G., Mansfield T.A., Judson R.S., Knight J.R., Lockshon D., Narayan V., Srinivasan M., Pochart P., et al. A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403 (2000) 623-627
36. Yu J., Marshall K., Yamaguchi M., Haber J.E., and Weil C.F. Microhomology-dependent end joining and repair of transposon-induced DNA hairpins by host factors in Saccharomyces cerevisiae. Mol. Cell. Biol. 24 (2004) 1351-1364