Pch2 acts through Xrs2 and Tel1/ATM to modulate interhomolog bias and checkpoint function during meiosis

PLoS Genetics

Volumn 7, Issue 11, 2011, Pages

  Ho, Hsuan Chung ^a   Burgess, Sean M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ATM PROTEIN; FUNGAL PROTEIN; HOP1 PROTEIN; MEC1 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; PCH2 PROTEIN; RAD17 PROTEIN; SINGLE STRANDED DNA; TEL1 PROTEIN; UNCLASSIFIED DRUG; XRS2 PROTEIN; ABC TRANSPORTER; ATM1 PROTEIN, S CEREVISIAE; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; HOP1 PROTEIN, S CEREVISIAE; NUCLEAR PROTEIN; PCH2 PROTEIN, S CEREVISIAE; PROTEIN SERINE THREONINE KINASE; RAD17 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL PEPTIDE; TEL1 PROTEIN, S CEREVISIAE; XRS2 PROTEIN, S CEREVISIAE;

AMINO TERMINAL SEQUENCE; ARTICLE; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; GENETIC RECOMBINATION; MEIOSIS; NONHUMAN; PHENOTYPE; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; YEAST; CHROMOSOME; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; CROSSING OVER; G2 PHASE CELL CYCLE CHECKPOINT; GENETICS; LONG TERMINAL REPEAT; METABOLISM; PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCETALES; SYNAPSIS;

ADENOSINE TRIPHOSPHATASES; ATP-BINDING CASSETTE TRANSPORTERS; CELL CYCLE PROTEINS; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; CHROMOSOMES, FUNGAL; CROSSING OVER, GENETIC; DNA BREAKS, DOUBLE-STRANDED; DNA-BINDING PROTEINS; G2 PHASE CELL CYCLE CHECKPOINTS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAP KINASE KINASE 1; MEIOSIS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TERMINAL REPEAT SEQUENCES;

EID: 81755163053     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002351     Document Type: Article

References (58)

1. Zickler D, Kleckner N, (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33: 603-754.
2. Keeney S, Giroux CN, Kleckner N, (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88: 375-384.
3. Bishop DK, Park D, Xu L, Kleckner N, (1992) DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell 69: 439-456.
4. Shinohara A, Ogawa H, Ogawa T, (1992) Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69: 457-470.
5. Kadyk LC, Hartwell LH, (1992) Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics 132: 387-402.
6. Bzymek M, Thayer NH, Oh SD, Kleckner N, Hunter N, (2011) Double Holliday junctions are intermediates of DNA break repair. Nature 464: 937-941.
7. Schwacha A, Kleckner N, (1997) Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell 90: 1123-1135.
8. Allers T, Lichten M, (2001) Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106: 47-57.
9. Hunter N, Kleckner N, (2001) The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination. Cell 106: 59-70.
10. Schwacha A, Kleckner N, (1995) Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83: 783-791.
11. Youds JL, Boulton SJ, (2011) The choice in meiosis - defining the factors that influence crossover or non-crossover formation. J Cell Sci 124: 501-513.
12. Carballo JA, Johnson AL, Sedgwick SG, Cha RS, (2008) Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination. Cell 132: 758-770.
13. Wu HY, Ho HC, Burgess SM, (2010) Mek1 kinase governs outcomes of meiotic recombination and the checkpoint response. Curr Biol 20: 1707-1716.
14. Niu H, Wan L, Baumgartner B, Schaefer D, Loidl J, et al. (2005) Partner choice during meiosis is regulated by Hop1-promoted dimerization of Mek1. Mol Biol Cell 16: 5804-5818.
15. Wan L, de los Santos T, Zhang C, Shokat K, Hollingsworth NM, (2004) Mek1 kinase activity functions downstream of RED1 in the regulation of meiotic double strand break repair in budding yeast. Mol Biol Cell 15: 11-23.
16. Kim KP, Weiner BM, Zhang L, Jordan A, Dekker J, et al. (2010) Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 143: 924-937.
17. Hochwagen A, Amon A, (2006) Checking your breaks: surveillance mechanisms of meiotic recombination. Curr Biol 16: R217-228.
18. Usui T, Ogawa H, Petrini JH, (2001) A DNA damage response pathway controlled by Tel1 and the Mre11 complex. Mol Cell 7: 1255-1266.
19. Lydall D, Nikolsky Y, Bishop DK, Weinert T, (1996) A meiotic recombination checkpoint controlled by mitotic checkpoint genes. Nature 383: 840-843.
20. Wu HY, Burgess SM, (2006) Two distinct surveillance mechanisms monitor meiotic chromosome metabolism in budding yeast. Curr Biol 16: 2473-2479.
21. Borner GV, Barot A, Kleckner N, (2008) Yeast Pch2 promotes domainal axis organization, timely recombination progression, and arrest of defective recombinosomes during meiosis. Proc Natl Acad Sci U S A 105: 3327-3332.
22. Joshi N, Barot A, Jamison C, Borner GV, (2009) Pch2 links chromosome axis remodeling at future crossover sites and crossover distribution during yeast meiosis. PLoS Genet 5: e1000557 doi:10.1371/journal.pgen.1000557.
23. Zanders S, Alani E, (2009) The pch2Delta mutation in baker's yeast alters meiotic crossover levels and confers a defect in crossover interference. PLoS Genet 5: e1000571 doi:10.1371/journal.pgen.1000571.
24. Zanders S, Sonntag Brown M, Chen C, Alani E, (2011) Pch2 Modulates Chromatid Partner Choice During Meiotic Double-Strand Break Repair in Saccharomyces cerevisiae. Genetics.
25. Roig I, Dowdle JA, Toth A, de Rooij DG, Jasin M, et al. (2010) Mouse TRIP13/PCH2 Is Required for Recombination and Normal Higher-Order Chromosome Structure during Meiosis. PLoS Genet 6: e1001062 doi.org/10.1371/journal.pgen.1001062.
26. Wojtasz L, Daniel K, Roig I, Bolcun-Filas E, Xu H, et al. (2009) Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase. PLoS Genet 5: e1000702 doi:10.1371/journal.pgen.1000702.
27. Li XC, Schimenti JC, (2007) Mouse pachytene checkpoint 2 (trip13) is required for completing meiotic recombination but not synapsis. PLoS Genet 3: e130 doi:10.1371/journal.pgen.0030130.
28. Bhalla N, Dernburg AF, (2005) A conserved checkpoint monitors meiotic chromosome synapsis in Caenorhabditis elegans. Science 310: 1683-1686.
29. Joyce EF, McKim KS, (2009) Drosophila PCH2 is required for a pachytene checkpoint that monitors double-strand-break-independent events leading to meiotic crossover formation. Genetics 181: 39-51.
30. Joyce EF, McKim KS, (2010) Chromosome Axis Defects Induce a Checkpoint-Mediated Delay and Interchromosomal Effect on Crossing Over during Drosophila Meiosis. PLoS Genet 6: e1001059 doi:10.1371/journal.pgen.1001059.
31. San-Segundo PA, Roeder GS, (1999) Pch2 links chromatin silencing to meiotic checkpoint control. Cell 97: 313-324.
32. Dong H, Roeder GS, (2000) Organization of the yeast Zip1 protein within the central region of the synaptonemal complex. J Cell Biol 148: 417-426.
33. Sym M, Engebrecht JA, Roeder GS, (1993) ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72: 365-378.
34. Lynn A, Soucek R, Borner GV, (2007) ZMM proteins during meiosis: crossover artists at work. Chromosome Res 15: 591-605.
35. Lao JP, Oh SD, Shinohara M, Shinohara A, Hunter N, (2008) Rad52 promotes postinvasion steps of meiotic double-strand-break repair. Mol Cell 29: 517-524.
36. Niu H, Li X, Job E, Park C, Moazed D, et al. (2007) Mek1 kinase is regulated to suppress double-strand break repair between sister chromatids during budding yeast meiosis. Mol Cell Biol 27: 5456-5467.
37. Grushcow JM, Holzen TM, Park KJ, Weinert T, Lichten M, et al. (1999) Saccharomyces cerevisiae checkpoint genes MEC1, RAD17 and RAD24 are required for normal meiotic recombination partner choice. Genetics 153: 607-620.
38. Borner GV, Kleckner N, Hunter N, (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117: 29-45.
39. Bishop DK, Zickler D, (2004) Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117: 9-15.
40. Nakada D, Matsumoto K, Sugimoto K, (2003) ATM-related Tel1 associates with double-strand breaks through an Xrs2-dependent mechanism. Genes Dev 17: 1957-1962.
41. Cartagena-Lirola H, Guerini I, Viscardi V, Lucchini G, Longhese MP, (2006) Budding Yeast Sae2 is an In Vivo Target of the Mec1 and Tel1 Checkpoint Kinases During Meiosis. Cell Cycle 5: 1549-1559.
42. Becker E, Meyer V, Madaoui H, Guerois R, (2006) Detection of a tandem BRCT in Nbs1 and Xrs2 with functional implications in the DNA damage response. Bioinformatics 22: 1289-1292.
43. Matsuzaki K, Shinohara A, Shinohara M, (2008) Forkhead-associated domain of yeast Xrs2, a homolog of human Nbs1, promotes nonhomologous end joining through interaction with a ligase IV partner protein, Lif1. Genetics 179: 213-225.
44. Shima H, Suzuki M, Shinohara M, (2005) Isolation and characterization of novel xrs2 mutations in Saccharomyces cerevisiae. Genetics 170: 71-85.
45. Hochwagen A, Tham WH, Brar GA, Amon A, (2005) The FK506 binding protein Fpr3 counteracts protein phosphatase 1 to maintain meiotic recombination checkpoint activity. Cell 122: 861-873.
46. Macqueen AJ, Hochwagen A, (2011) Checkpoint mechanisms: the puppet masters of meiotic prophase. Trends Cell Biol.
47. Joyce EF, McKim KS, (2011) Meiotic checkpoints and the interchromosomal effect on crossing over in Drosophila females. Fly (Austin) 5.
48. Williams RS, Dodson GE, Limbo O, Yamada Y, Williams JS, et al. (2009) Nbs1 flexibly tethers Ctp1 and Mre11-Rad50 to coordinate DNA double-strand break processing and repair. Cell 139: 87-99.
49. Lukas C, Melander F, Stucki M, Falck J, Bekker-Jensen S, et al. (2004) Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. EMBO J 23: 2674-2683.
50. Mukherjee S, LaFave MC, Sekelsky J, (2009) DNA damage responses in Drosophila nbs mutants with reduced or altered NBS function. DNA Repair (Amst) 8: 803-812.
51. Mitra N, Roeder GS, (2007) A novel nonnull ZIP1 allele triggers meiotic arrest with synapsed chromosomes in Saccharomyces cerevisiae. Genetics 176: 773-787.
52. Bhalla N, Dernburg AF, (2008) Prelude to a division. Annu Rev Cell Dev Biol 24: 397-424.
53. Vojtek AB, Hollenberg SM, Cooper JA, (1993) Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell 74: 205-214.
54. Goldstein AL, McCusker JH, (1999) Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541-1553.
55. Wach A, Brachat A, Pohlmann R, Philippsen P, (1994) New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10: 1793-1808.
56. Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
57. Yaffe MP, Schatz G, (1984) Two nuclear mutations that block mitochondrial protein import in yeast. Proc Natl Acad Sci U S A 81: 4819-4823.
58. Arora C, Kee K, Maleki S, Keeney S, (2004) Antiviral protein Ski8 is a direct partner of Spo11 in meiotic DNA break formation, independent of its cytoplasmic role in RNA metabolism. Mol Cell 13: 549-559.