Synaptonemal complex morphogenesis and sister-chromatid cohesion require Mek1-dependent phosphorylation of a meiotic chromosomal protein

Genes and Development

Volumn 12, Issue 22, 1998, Pages 3551-3563

  Bailis, Julie M ^a   Roeder, G Shirleen ^a,b  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chromosome cores; Lateral elements; Meiosis; Phosphorylation; Sister chromatid cohesion; Synaptonemal complex

Indexed keywords

ARTICLE; MEIOSIS; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; SISTER CHROMATID; SYNAPTOSOME;

SACCHAROMYCES CEREVISIAE;

EID: 0032533905     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.12.22.3551     Document Type: Article

References (52)

1. Bai, C. and S.J. Elledge. 1997. Gene identification using the yeast two-hybrid system. Methods Enzymol. 283: 141-156.
2. Bishop, D., 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.
3. Brunelli, J.P. and M.L. Pall. 1993. A series of yeast shuttle vectors for the expression of cDNAs and other DNA sequences. Yeast 9: 1299-1308.
4. Burns, N., B. Grimwade, P.B. Ross-Macdonald, E.-Y. Choi, K. Finberg, G.S. Roeder, and M. Snyder. 1994. Large-scale analysis of gene expression, protein localization and gene disruption in Saccharomyces cerevisiae. Genes & Dev. 8: 1087-1105.
5. Chua, P.R. and G.S. Roeder. 1998. Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93: 349-359.
6. Durfee T., K. Becherer, P.L. Chen, S.H. Yeh, Y. Yang, A.E. Kilburn, W.H. Lee, and S.J. Elledge. 1993. The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes & Dev. 7: 555-569.
7. Flaggs, G., A.W. Plug, K.M. Dunks , K.E. Mundt, J.C. Ford, M.R. Quiggle, E.M. Taylor, C.H. Westphal, T. Ashley, M. F. Hoekstra, and A.M. Carr. 1997. Atm-dependent interactions of a mammalian Chk1 homolog with meiotic chromosomes. Curr. Biol. 7: 977-986.
8. Friedman, D.B., N.M. Hollingsworth, and B. Byers. 1994. Insertional mutations in the yeast HOP1 gene: Evidence for multimeric assembly in meiosis. Genetics 136: 449-464.
9. Gasior, S.L., A.K. Wong, Y. Kora, A. Shinohara, and D.K. Bishop. 1998. Rad52 associates with RPA and functions with Rad55 and Rad57 to assemble meiotic recombination complexes. Genes & Dev. 12: 2208-2221.
10. Gietz, R.D., R.H. Schiestl, A.R. Willems, and R.A. Woods. 1995. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11: 355-360.
11. Guacci, V., D. Koshland, and A. Strunnikov. 1997. A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae. Cell 91: 47-57.
12. Guan, K. and J.E. Dixon. 1991. Eukaryotic proteins expressed in Escherichia coli: An improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal. Biochem. 192: 262-267.
13. Hofmann, K. and P. Bucher. 1995. The FHA domain: A putative nuclear signalling domain found in protein kinases and transcription factors. Trends Biochem. Sci. 20: 347-349.
14. Hollingsworth, N. and B. Byers. 1989. HOP1: A yeast meiotic pairing gene. Genetics 121: 445-462.
15. Hollingsworth, N.M. and A.D. Johnson. 1993. A conditional allele of the Saccharomyces cerevisiae HOP1 gene is suppressed by overexpression of two other meiosis-specific genes: RED1 and REC104. Genetics 133: 785-797.
16. Hollingsworth, N.M. and L. Ponte. 1997. Genetic interactions between HOP1, RED1 and MEK1 suggest that MEK1 regulates assembly of axial element components during meiosis in the yeast Saccharomyces cerevisiae. Genetics 147: 33-42.
17. Hollingsworth, N.M., L. Goetsch, and B. Byers. 1990. The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell 61: 73-84.
18. James, P., J. Halladay, and E.A. Craig. 1996. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144: 1425-1436.
19. Jans, D. 1995. The regulation of protein transport to the nucleus. Biochem. J. 311: 705-716.
20. Keegan, K.S., D.A. Holtzman, A.W. Plug, E.R. Christenson, E.E. Brainerd, G. Flaggs, N.J. Bentley, E.M. Taylor, M.S. Meyn, S.B. Moss, A.M. Carr, T. Ashley, and M.F. Hoekstra. 1996. The Atr and Atm protein kinases associate with different sites along meiotically pairing chromosomes. Genes & Dev. 10: 2423-2437.
21. Kironmai, K.M., K. Muniyappa, D.B. Friedman, N.M. Hollingsworth, and B. Byers. 1998. DNA-binding activities of Hop1 protein, a synaptonemal complex component from Saccharomyces cerevisiae. Mol. Cell Biol. 18: 1424-1435.
22. r synaptonemal complex proteins of the rat between early and mid-pachytene. Chromosoma 104: 154-163.
23. 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.
24. Loidl, J., F. Klein, and H. Scherthan. 1994. Homologous pairing is reduced but not abolished in asynaptic mutants of yeast. J. Cell Biol. 125: 1191-1200.
25. Michaelis, C., R. Ciosk, and K. Nasmyth. 1997. Cohesins: Chromosomal proteins that prevent premature separation of sister chromatids. Cell 91: 35-45.
26. Miyazaki, W.Y. and T.L. Orr-Weaver. 1994. Sister-chromatid cohesion in mitosis and meiosis. Annu. Rev. Genet. 28: 167-187.
27. Moens, P.B. and B. Spyropoulos. 1995. Immunocytology of chiasmata and chromosomal disjunction at mouse meiosis. Chromosoma 104: 175-182.
28. Molnar, M., J. Bahler, M. Sipiczki, and J. Kohli. 1995. The rec8 gene of Schizosaccharomyces pombe is involved in linear element formation, chromosome pairing, and sister-chromatid cohesion during meiosis. Genetics 141: 61-73.
29. Moreau, P.J.F., D. Zickler, and G. Leblon. 1985. One class of mutants with disturbed centromere cleavage and chromosome pairing in Sordaria macrospora. Mol. & Gen. Genet. 198: 189-197.
30. Nag, D.K., H. Scherthan, B. Rockmill, J. Bhargava, and G.S. Roeder. 1995. Heteroduplex DNA formation and homolog pairing in yeast meiotic mutants. Genetics 141: 75-86.
31. Page, B.D. and M. Snyder. 1992. CIK1: A developmentally regulated spindle pole body-associated protein important for microtubule functions in Saccharomyces cerevisiae. Genes & Dev. 6: 1414-1429.
32. Rockmill, B. and G.S. Roeder. 1990. Meiosis in asynaptic yeast. Genetics 126: 563-574.
33. _. 1991. A meiosis-specific protein kinase homolog required for chromosome synapsis and recombination. Genes & Dev. 5: 2392-2404.
34. _. 1994. The yeast med1 mutant undergoes both meiotic homolog nondisjunction and precocious separation of sister chromatids. Genetics 136: 65-74.
35. Roeder, G.S. 1997. Meiotic chromosomes: It takes two to tango. Genes & Dev. 11: 2600-2621.
36. Rothstein, R. 1991. Targeting, disruption, replacement and allele rescue: Integrative DNA transformation in yeast. Methods Enzymol. 194: 281-301.
37. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular cloning: A laboratory manual (ed. C. Nolan, N. Ford, N. Irwin and M. Ferguson). Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
38. Schneider, B.L., W. Seufert, B. Steiner, Q.H. Yang, and B. Futcher. 1995. Use of polymerase chain reaction epitope tagging in Saccharomyces cerevisiae. Yeast 11: 1265-1274.
39. Schwacha, A. and N. Kleckner. 1994. Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis. Cell 90: 1123-1135.
40. _. 1997. Interhomolog bias during meiotic recombination: Meiotic functions promote a highly differentiated interhomolog-only pathway. Cell 90: 1123-1135.
41. Sears. D.D., P. Hieter, and G. Simchen. 1994. An implanted recombination hot spot stimulates recombination and enhances sister chromatid cohesion of heterologous YACs during yeast meiosis. Genetics 138: 1055-1065.
42. Sherman, F., G.R. Fink, and J.B. Hicks. 1986. Methods in yeast genetics: A laboratory manual, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
43. Sikorski, R. and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
44. Smith, A.V. and G S. Roeder. 1997. The yeast Red1 protein localizes to the cores of meiotic chromosomes. J. Cell Biol. 136: 957-967.
45. Sun, Z., D.S. Fay, F. Marini, M. Foiani, and D.F. Stern. 1996. Spk1/Rad53 is regulated by Mec1-dependent protein phosphorylation in DNA replication and damage checkpoint pathways. Genes & Dev. 10: 395-406.
46. Sun, Z., J. Hsiao, D.S. Fay, and D.F. Stern. 1998. Rad53 FHA domain associated with phosphorylated Rad9 in response to the DNA damage checkpoint. Science 281: 272-274.
47. Sym, M. and G.S. Roeder. 1994. Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell 79: 283-292.
48. Sym, M., J. Engebrecht, and G.S. Roeder. 1993. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72: 365-378.
49. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc. Natl. Acad. Sci. 76: 4350-4354.
50. Tu, J., W. Song, and M. Carlson. 1996. Protein phosphatase type 1 interacts with proteins required for meiosis and other cellular processes in Saccharomyces cerevisiae. Mol. Cell. Biol. 16: 4199-4206.
51. Xu, L., B.M. Weiner, and N. Kleckner. 1997. Meiotic cells monitor the status of the interhomolog recombination complex. Genes & Dev. 11: 106-118.
52. Zhou, Z. and S.J. Elledge. 1993. DUN1 encodes a protein kinase that controls the DNA damage response in yeast. Cell 75: 1119-1127.