Mus81/Mms4 Endonuclease and Sgs1 Helicase Collaborate to Ensure Proper Recombination Intermediate Metabolism during Meiosis

Molecular Cell

Volumn 31, Issue 3, 2008, Pages 313-323

  Jessop, Lea ^a   Lichten, Michael ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

DNA

Indexed keywords

ENDONUCLEASE; HELICASE; PROTEIN MMS4; PROTEIN MUS81; PROTEIN SGS1;

ARTICLE; ENZYME ANALYSIS; GENE EXPRESSION; GENE INDUCTION; GENETIC RECOMBINATION; MEIOSIS; METABOLISM; NONHUMAN; PROTEIN EXPRESSION; YEAST;

CELL NUCLEUS; DNA, CRUCIFORM; DNA-BINDING PROTEINS; ENDONUCLEASES; GENE EXPRESSION REGULATION, FUNGAL; MEIOSIS; MODELS, BIOLOGICAL; MUTATION; PACHYTENE STAGE; PROMOTER REGIONS (GENETICS); RECOMBINATION, GENETIC; RECQ HELICASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANS-ACTIVATORS;

SACCHAROMYCETALES;

EID: 48349141924     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2008.05.021     Document Type: Article

References (50)

1. Allers T., and Lichten M. A method for preparing genomic DNA that restrains branch migration of Holliday junctions. Nucleic Acids Res. 28 (2000) e6
2. Allers T., and Lichten M. Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106 (2001) 47-57
3. Allers T., and Lichten M. Intermediates of yeast meiotic recombination contain heteroduplex DNA. Mol. Cell 8 (2001) 225-231
4. Argueso J.L., Wanat J., Gemici Z., and Alani E. Competing crossover pathways act during meiosis in Saccharomyces cerevisiae. Genetics 168 (2004) 1805-1816
5. Bastin-Shanower S.A., Fricke W.M., Mullen J.R., and Brill S.J. The mechanism of Mus81-Mms4 cleavage site selection distinguishes it from the homologous endonuclease Rad1-Rad10. Mol. Cell. Biol. 23 (2003) 3487-3496
6. Benjamin K.R., Zhang C., Shokat K.M., and Herskowitz I. Control of landmark events in meiosis by the CDK Cdc28 and the meiosis-specific kinase Ime2. Genes Dev. 17 (2003) 1524-1539
7. Boddy M.N., Gaillard P.H., McDonald W.H., Shanahan P., Yates III J.R., and Russell P. Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107 (2001) 537-548
8. Chang M., Bellaoui M., Zhang C., Desai R., Morozov P., Delgado-Cruzata L., Rothstein R., Freyer G.A., Boone C., and Brown G.W. RMI1/NCE4, a suppressor of genome instability, encodes a member of the RecQ helicase/Topo III complex. EMBO J. 24 (2005) 2024-2033
9. Chu S., and Herskowitz I. Gametogenesis in yeast is regulated by a transcriptional cascade dependent on Ndt80. Mol. Cell 1 (1998) 685-696
10. Clyne R.K., Katis V.L., Jessop L., Benjamin K.R., Herskowitz I., Lichten M., and Nasmyth K. Polo-like kinase Cdc5 promotes chiasmata formation and cosegregation of sister centromeres at meiosis I. Nat. Cell Biol. 5 (2003) 480-485
11. Cromie G.A., and Smith G.R. Branching out: meiotic recombination and its regulation. Trends Cell Biol. 17 (2007) 448-455
12. Cromie G.A., Hyppa R.W., Taylor A.F., Zakharyevich K., Hunter N., and Smith G.R. Single Holliday junctions are intermediates of meiotic recombination. Cell 127 (2006) 1167-1178
13. de los Santos T., Loidl J., Larkin B., and Hollingsworth N.M. A role for MMS4 in the processing of recombination intermediates during meiosis in Saccharomyces cerevisiae. Genetics 159 (2001) 1511-1525
14. de los Santos T., Hunter N., Lee C., Larkin B., Loidl J., and Hollingsworth N.M. The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics 164 (2003) 81-94
15. Fabre F., Chan A., Heyer W.D., and 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 99 (2002) 16887-16892
16. Foiani M., Marini F., Gamba D., Lucchini G., and Plevani P. The B subunit of the DNA polymerase alpha-primase complex in Saccharomyces cerevisiae executes an essential function at the initial stage of DNA replication. Mol. Cell. Biol. 14 (1994) 923-933
17. Gangloff S., McDonald J.P., Bendixen C., Arthur L., and Rothstein R. The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol. Cell. Biol. 14 (1994) 8391-8398
18. Gaskell L.J., Osman F., Gilbert R.J., and Whitby M.C. Mus81 cleavage of Holliday junctions: a failsafe for processing meiotic recombination intermediates?. EMBO J. 26 (2007) 1891-1901
19. Gelbart M.E., Rechsteiner T., Richmond T.J., and Tsukiyama T. Interactions of Isw2 chromatin remodeling complex with nucleosomal arrays: analyses using recombinant yeast histones and immobilized templates. Mol. Cell. Biol. 21 (2001) 2098-2106
20. Goldstein A.L., and McCusker J.H. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15 (1999) 1541-1553
21. Goyon C., and Lichten M. Timing of molecular events in meiosis in Saccharomyces cerevisiae: stable heteroduplex DNA is formed late in meiotic prophase. Mol. Cell. Biol. 13 (1993) 373-382
22. Ii M., Ii T., and Brill S.J. Mus81 functions in the quality control of replication forks at the rDNA and is involved in the maintenance of rDNA repeat number in Saccharomyces cerevisiae. Mutat. Res. 625 (2007) 1-19
23. Jessop L., Allers T., and Lichten M. Infrequent co-conversion of markers flanking a meiotic recombination initiation site in Saccharomyces cerevisiae. Genetics 169 (2005) 1353-1367
24. Jessop L., Rockmill B., Roeder G.S., and Lichten M. Meiotic chromosome synapsis-promoting proteins antagonize the anti-crossover activity of Sgs1. PLoS Genet. 2 (2006) e155 10.1371/journal.pgen.0020155
25. Kaliraman V., Mullen J.R., Fricke W.M., Bastin-Shanower S.A., and Brill S.J. Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes Dev. 15 (2001) 2730-2740
26. Kane S.M., and Roth R. Carbohydrate metabolism during ascospore development in yeast. J. Bacteriol. 118 (1974) 8-14
27. 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
28. Lee B.H., and Amon A. Role of Polo-like kinase CDC5 in programming meiosis I chromosome segregation. Science 300 (2003) 482-486
29. Longtine M.S., McKenzie III A., Demarini D.J., Shah N.G., Wach A., Brachat A., Philippsen P., and Pringle J.R. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14 (1998) 953-961
30. Lynn A., Soucek R., and Börner G. ZMM proteins during meiosis: Crossover artists at work. Chromosome Res. 15 (2007) 591-605
31. Mankouri H.W., and Hickson I.D. The RecQ helicase-topoisomerase III-Rmi1 complex: a DNA structure-specific 'dissolvasome'?. Trends Biochem. Sci. 32 (2007) 538-546
32. McMahill M.S., Sham C.W., and Bishop D.K. Synthesis-dependent strand annealing in meiosis. PLoS Biol. 5 (2007) e299 10.1371/journal.pbio.0050299
33. Mullen J.R., Kaliraman V., and Brill S.J. Bipartite structure of the SGS1 DNA helicase in Saccharomyces cerevisiae. Genetics 154 (2000) 1101-1114
34. Mullen J.R., Kaliraman V., Ibrahim S.S., and Brill S.J. Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 157 (2001) 103-118
35. Mullen J.R., Nallaseth F.S., Lan Y.Q., Slagle C.E., and Brill S.J. Yeast Rmi1/Nce4 controls genome stability as a subunit of the Sgs1-Top3 complex. Mol. Cell. Biol. 25 (2005) 4476-4487
36. Nasmyth K., Adolf G., Lydall D., and Seddon A. The identification of a second cell cycle control on the HO promoter in yeast: cell cycle regulation of SWI5 nuclear entry. Cell 62 (1990) 631-647
37. Oh S.D., Lao J.P., Hwang P.Y., Taylor A.F., Smith G.R., and Hunter N. BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules. Cell 130 (2007) 259-272
38. Oh S.D., Lao J.P., Taylor A.F., Smith G.R., and Hunter N. RecQ helicase, Sgs1, and XPF-family endonuclease, Mus81-Mms4, resolve aberrant joint molecules during meiotic recombination. Mol. Cell 31 (2008) 324-336 this issue
39. Rockmill B., Fung J.C., Branda S.S., and Roeder G.S. The Sgs1 helicase regulates chromosome synapsis and meiotic crossing over. Curr. Biol. 13 (2003) 1954-1962
40. Roeder G.S., and Bailis J.M. The pachytene checkpoint. Trends Genet. 16 (2000) 395-403
41. Schwacha A., and Kleckner N. Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell 76 (1994) 51-63
42. Schwacha A., and Kleckner N. Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83 (1995) 783-791
43. Smith G.R., Boddy M.N., Shanahan P., and Russell P. Fission yeast Mus81·Eme1 Holliday junction resolvase is required for meiotic crossing over but not for gene conversion. Genetics 165 (2003) 2289-2293
44. Smith C.E., Llorente B., and Symington L.S. Template switching during break-induced replication. Nature 447 (2007) 102-105
45. St Onge R.P., Mani R., Oh J., Proctor M., Fung E., Davis R.W., Nislow C., Roth F.P., and Giaever G. Systematic pathway analysis using high-resolution fitness profiling of combinatorial gene deletions. Nat. Genet. 39 (2007) 199-206
46. Watt P.M., Hickson I.D., Borts R.H., and Louis E.J. SGS1, a homologue of the Bloom's and Werner's syndrome genes, is required for maintenance of genome stability in Saccharomyces cerevisiae. Genetics 144 (1996) 935-945
47. White M.A., Dominska M., and Petes T.D. Transcription factors are required for the meiotic recombination hotspot at the HIS4 locus in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 90 (1993) 6621-6625
48. Wu L., Bachrati C.Z., Ou J., Xu C., Yin J., Chang M., Wang W., Li L., Brown G.W., and Hickson I.D. BLAP75/RMI1 promotes the BLM-dependent dissolution of homologous recombination intermediates. Proc. Natl. Acad. Sci. USA 103 (2006) 4068-4073
49. Xu L., Ajimura M., Padmore R., Klein C., and Kleckner N. NDT80, a meiosis-specific gene required for exit from pachytene in Saccharomyces cerevisiae. Mol. Cell. Biol. 15 (1995) 6572-6581
50. Yin J., Sobeck A., Xu C., Meetei A.R., Hoatlin M., Li L., and Wang W. BLAP75, an essential component of Bloom's syndrome protein complexes that maintain genome integrity. EMBO J. 24 (2005) 1465-1476