Meiotic cells monitor the status of the interhomolog recombination complex

Genes and Development

Volumn 11, Issue 1, 1997, Pages 106-118

  Xu, Liuzhong ^a,b   Weiner, Beth M ^a   Kleckner, Nancy ^a  

^a HARVARD UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Checkpoint; double stranded breaks; meiosis; pachytene arrest; recombination; synaptonemal complex

Indexed keywords

DNA; PROTEIN KINASE; RECA PROTEIN;

ARTICLE; CONTROLLED STUDY; DNA STRAND BREAKAGE; GENETIC RECOMBINATION; MEIOSIS; MUTATION; NONHUMAN; PACHYTENE; PRIORITY JOURNAL; SYNAPTONEMAL COMPLEX; YEAST;

EID: 0031027869     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.11.1.106     Document Type: Article

References (56)

1. Alani, E., R. Padmore, and N. Kleckner. 1990. Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell 61: 419-436.
2. Baker, S.M., A.W. Plug, R.A. Prolla, C.E. Bronner, A.C. Harris, X. Yao, D.-M. Christie, C. Monell, N. Arnheim, A. Bradley, T. Ashley, and R.M. Liskay. 1996. Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nature Genet. 13: 336-342.
3. Bishop, D.K. 1994. RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell 79: 1081-1092.
4. Bishop, D.K., D. Park, L. Xu, and N. Kleckner. 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.
5. Cao, L., E. Alani, and N. Kleckner. 1990. A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61: 1089-1101.
6. Carpenter, A.T.C. 1994. Chiasma function. Cell 77: 957-962.
7. Christianson, T.W., R.S. Sikorski, M. Dante, J.H. Shero, and P. Hieter. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene 110: 119-122.
8. Church, G.M. and W. Gilbert. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. 81: 1991-1995.
9. de Massy, B., F. Baudat, and A. Nicolas. 1994. Initiation of recombination in Saccharomyces cerevisiae haploid meiosis. Proc. Natl. Acad. Sci. 91: 11929-11933.
10. de Massy, B., V. Rocco, and A. Nicolas. 1995. The nucleotide mapping of DNA double-strand breaks at the CYS3 initiation site of meiotic recombination in Saccharomyces cerevisiae. EMBO J. 14: 4589-4598.
11. Edelmann, W., P.E. Cohen, M. Kane, K. Lau, B. Morrow, S. Bennett, A. Umar, T. Kunkel, G. Cattoretti, R. Chaganti, et al. 1996. Meiotic pachytene arrest in MLH1-deficient mice. Cell 85: 1125-1134.
12. Engebrecht, J., J. Hirsch, and G.S. Roeder. 1990. Meiotic gene conversion and crossing over: Their relationship to each other and to chromosome synapsis and segregation. Cell 62: 927-937.
13. Feinberg, A.P. and B. Vogelstein. 1984. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 137: 266-267.
14. Hartwell, L.H. and T.A. Weinert. 1989. Checkpoints: Controls that ensure the order of cell cycle events. Science 246: 629-634.
15. Johzuka, K. and H. Ogawa. 1995. Interaction of Mre11 and Rad50: two proteins required for DNA repair and meiosis-specific double-strand break formation in Saccharomyces cerevisiae. Genetics 139: 1521-1532.
16. Kadyk, L.C. and L.H. Hartwell. 1992. Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics 132: 387-402.
17. Keeney, S. and N. Kleckner. 1995. Covalent protein-DNA complexes at the 5′ strand termini of meiosis-specific double strand breaks in yeast. Proc. Natl. Acad. Sci. 92: 11274-11278.
18. Klapholz, S., C.S. Waddell, and R.E. Esposito, 1985. The role of the SPO11 gene in meiotic recombination in yeast. Genetics 110: 187-216.
19. Kleckner, N. 1996. Meiosis: How could it work? Proc. Natl. Acad. Sci. 93: 8167-8174.
20. Kleckner, N., R. Padmore, and D.K. Bishop. 1991. Meiotic chromosome metabolism: One view. Cold Spring Harbor Symp. Quant. Biol 56: 729-743.
21. Leatherwood, J., A. Lopez-Girona, and P. Russell. 1996. Interaction of Cdc2 and Cdc18 with a fission yeast ORC2-like protein. Nature 379: 360-363.
22. Leem, S.-H. and H. Ogawa. 1992. The MRE4 gene encodes a novel protein kinase homologue required for meiotic recombination in Saccharomyces cerevisiae. Nucleic Acids Res. 20: 449-457.
23. Liu, J., T.-c. Wu, and M. Lichten. 1995. The location and structure of double-strand DNA breaks induced during meiosis: Evidence for a covalently linked DNA-protein intermediate. EMBO J. 14: 4599-4608.
24. Loidl, J., K. Nairz, and F. Klein. 1991. Meiotic chromosome synapsis in a haploid yeast. Chromosoma 100: 221-228.
25. Lydall, D. and T. Weinert. 1995. Yeast checkpoint genes in DNA damage processing: Implication for repair and arrest. Science 270: 1488-1491.
26. Lydall, D., Y. Nikolsky, D.K. Bishop, and T. Weinert. 1996. A meiotic recombination checkpoint controlled by mitotic DNA damage checkpoint genes. Nature 383: 840-843.
27. Malone, R.E., S. Bullard, M. Hermiston, R. Rieger, M. Cool, and A. Galbraith. 1991. Isolation of mutants defective in early steps of meiotic recombination in the yeast Saccharomyces cerevisiae. Genetics 128: 79-88.
28. Navas, T.A., Z. Zhou, and S.J. Elledge. 1995. DNA polymerase ∈ links the DNA replication machinery to the S phase checkpoint. Cell 80: 29-39.
29. Padmore, R., L. Cao, and N. Kleckner. 1991. Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell 66: 1239-1256.
30. Raymond, W.R. and N. Kleckner. 1993. Rad50 protein of S. cerevisiae exhibits ATP-dependent DNA binding. Nucleic Acids Res. 21:3851-3856.
31. Reed, S.I. 1980. The selection of S. cerevisiae mutants defective in the start event of cell division. Genetics 95: 561-577.
32. Resnick, M.A. 1987. Investigating the genetic control of biochemical events in meiotic recombination. In Meiosis (ed. P. Moens), pp. 157-210. Academic Press, New York, NY.
33. Rockmill, B. and G.S. Roeder. 1990. Meiosis in asynaptic yeast. Genetics 126: 563-574.
34. _. 1991. A meiosis-specific protein kinase homolog required for chromosome synapsis and recombination. Genes & Dev. 5: 2392-2404.
35. Rockmill, B., J. Engebrecht, H. Scherthan, J. Loidl, and G.S. Roeder. 1995a. The yeast MER2 gene is required for chromosome synapsis and the initiation of meiotic recombination. Genetics 141: 49-59.
36. Rockmill, B., M. Sym, H. Scherthan, and G.S. Roeder 1995b. Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes & Dev. 9: 2684-2695.
37. Roeder, G.S. 1990. Chromosome synapsis and genetic recombination: Their roles in meiotic chromosome segregation. Trends Genet. 6: 385-389.
38. Roeder, G.S. 1995. Sex and the single cell: Meiosis in yeast. Proc. Natl. Acad. Sci. 92: 10450-10456.
39. Rose, D. and C. Holm. 1993. Meiosis-specific arrest revealed in DNA topoisomerase II mutants. Mol. Cell. Biol. 13: 219-242.
40. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular cloning: A laboratory manual. 2nd edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
41. Schwacha, A. 1996. "Isolation and characterization of branched meiotic recombination intermediates from both wild-type and mutant strains of the yeast Saccharomyces cerevisiae." Ph.D. thesis, Harvard University, Cambridge, MA.
42. Schwacha, A. and N. Kleckner. 1994. Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell 76: 51-63.
43. _. 1995. Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83: 783-791.
44. Sherman, F., G. Fink, and J. Hicks. 1986. Methods in yeast genetics: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
45. Shinohara, A., H. Ogawa, and T. Ogawa. 1992. Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69: 457-470.
46. Shuster, E.O. and B. Byers. 1989. Pachytene arrest and other meiotic effects of the start mutations in Saccharomyces cerevisiae. Genetics 123: 29-43.
47. Storlazzi, A., L. Xu. L. Cao, and N. Kleckner. 1995. Crossover and noncrossover recombination during meiosis: Timing and pathway relationships. Proc. Natl Acad. Sci. 92: 8512-8516.
48. Storlazzi, A., L. Xu, A. Schwacha, and N. Kleckner. 1996. Synaptonemal complex component Zip1 plays a role in meiotic recombination independent of SC polymerization along the chromosomes. Proc. Natl. Acad. Sci. 93: 9043-9048.
49. Sym, M. and G.S. Roeder. 1994. Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell 79: 283-292.
50. Sym, M., J. Engebrecht, and G.S. Roeder. 1993. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72: 365-378.
51. Thorne, L.W. and B. Byers. 1993. Stage-specific effects of X-irradiation on yeast meiosis. Genetics 134: 29-42.
52. Weber, L. and B. Byers. 1992. A RAD9-dependent checkpoint blocks meiosis of cdc13 yeast cells. Genetics 131: 55-63.
53. Williamson, D.H., L.J. Johnson, D.J. Fennell, and G. Simchen. 1983. The timing of the S phase and other nuclear events in yeast meiosis. Exp. Cell Res. 145: 209-217.
54. Xu, L. and N. Kleckner. 1995. Sequence non-specific doublestrand breaks and interhomolog interactions prior to doublestrand break formation at a meiotic recombination hot spot in yeast. EMBO J. 14: 5115-5128.
55. Xu, L., M. Ajimura, R. Padmore, C. Klein, and N. Kleckner. 1995. NDT80, a meiosis-specific gene required for exit from pachytene in Saccharomyces cerevisiae. Mol. Cell. Biol. 15: 6572-6581.
56. Yamamoto, A., Guacci, V. and Koshland, D. 1996. PDS1p, an inhibitor of anaphase in budding yeast, plays a critical role in APC and checkpoint pathway(s). J. Cell Biol. 133: 99-110.