Novel response to microtubule perturbation in meiosis

Molecular and Cellular Biology

Volumn 25, Issue 11, 2005, Pages 4767-4781

  Hochwagen, Andreas ^a   Wrobel, Gunnar ^b   Cartron, Marie ^b   Demougin, Philippe ^b   Niederhauser Wiederkehr, Christa ^b   Boselli, Monica G ^a   Primig, Michael ^b   Amon, Angelika ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BENOMYL;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; DEPOLYMERIZATION; GENE EXPRESSION; LOW TEMPERATURE; MEIOSIS; METAPHASE; MICROTUBULE; MITOSIS; MITOSIS INHIBITION; NONHUMAN; PRIORITY JOURNAL; SPINDLE CELL; SPOROGENESIS;

BENOMYL; CELL CYCLE; CHROMOSOME PAIRING; COLD; CYCLIN-DEPENDENT KINASES; CYCLINS; FUNGICIDES, INDUSTRIAL; GENE EXPRESSION; GENE EXPRESSION PROFILING; MEIOSIS; MICROTUBULES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCETALES;

EID: 18944381109     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.11.4767-4781.2005     Document Type: Article

References (73)

1. Allen, J. W., J. B. Gibson, P. A. Poorman, L. C. Backer, and M. J. Moses. 1988. Synaptonemal complex damage induced by clastogenic and anti-mitotic chemicals: implications for non-disjunction and aneuploidy. Mutat. Res. 201:313-324.
2. Amon, A., M. Tyers, B. Futcher, and K. Nasmyth. 1993. Mechanisms that help the yeast cell cycle clock tick: G2 cyclins transcriptionally activate G2 cyclins and repress G1 cyclins. Cell 74:993-1007.
3. Bailis, J. M., and G. S. Roeder. 2000. Pachytene exit controlled by reversal of Mek1-dependent phosphorylation. Cell 101:211-221.
4. Bascom-Slack, C. A., and D. S. Dawson. 1997. The yeast motor protein, Kar3p, is essential for meiosis I. J. Cell Biol. 139:459-467.
5. Buonomo, S. B., K. P. Rabitsch, J. Fuchs, S. Gruber, M. Sullivan, F. Uhlmann, M. Petronczki, A. Toth, and K. Nasmyth. 2003. Division of the nucleolus and its release of CDC14 during anaphase of meiosis I depends on separase, SPO12, and SLK19. Dev. Cell 4:727-739.
6. 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.
7. Chu, S., J. DeRisi, M. Eisen, J. Mulholland, D. Botstein, P. O. Brown, and I. Herskowitz. 1998. The transcriptional program of sporulation in budding yeast. Science 282:699-705.
8. Chu, S., and I. Herskowitz. 1998. Gametogenesis in yeast is regulated by a transcriptional cascade dependent on Ndt80. Mol. Cell 1:685-696.
9. Cleveland, D. W., M. A. Lopala, P. Sherline, and M. W. Kirschner. 1981. Unpolymerized tubulin modulates the level of tubulin mRNAs. Cell 25:537-546.
10. Davis, L., M. Barbera, A. McDonnell, K. McIntyre, R. Sternglanz, Q. Jin, J. Loidl, and J. Engebrecht. 2001. The Saccharomyces cerevisiae MUM2 gene interacts with the DNA replication machinery and is required for meiotic levels of double strand breaks. Genetics 157:1179-1189.
11. Downing, K. H. 2000. Structural basis for the interaction of tubulin with proteins and drugs that affect microtubule dynamics. Annu. Rev. Cell Dev. Biol. 16:89-111.
12. Edgar, R., M. Domrachev, and A. E. Lash. 2002. Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30:207-210.
13. Giaever, G., A. M. Chu, L. Ni, C. Connelly, L. Riles, S. Veronneau, S. Dow, A. Lucau-Danila, K. Anderson, B. Andre, A. P. Arkin, A. Astromoff, M. El-Bakkoury, K. Bangham, R. Benito, S. Brachat, S. Campanaro, M. Curtiss, K. Davis, A. Deutschbauer, K. D. Entian, P. Flaherty, F. Foury, D. J. Garfinkel, M. Gerstein, D. Gotte, U. Guldener, J. H. Hegemann, S. Hempel, Z. Herman, D. F. Jaramillo, D. E. Kelly, S. L. Kelly, P. Kotter, D. LaBonte, D. C. Lamb, N. Lan, H. Liang, H. Liao, L. Liu, C. Luo, M. Lussier, R. Mao, P. Menard, S. L. Ooi, J. L. Revuelta, C. J. Roberts, M. Rose, P. Ross-Macdonald, B. Scherens, G. Schimmack, B. Shafer, D. D. Shoemaker, S. Sookhai-Mahadeo, R. K. Storms, J. N. Strathern, G. Valle, M. Voet, G. Volckaert, C. Y. Wang, T. R. Ward, J. Wilhelmy, E. A. Winzeler, Y. Yang, G. Yen, E. Youngman, K. Yu, H. Bussey, J. D. Boeke, M. Snyder, P. Philippsen, R. W. Davis, and M. Johnston. 2002. Functional profiling of the Saccharomyces cerevisiae genome. Nature 418:387-391.
14. Gupta, M. L., Jr., C. J. Bode, C. A. Dougherty, R. T. Marquez, and R. H. Himes. 2001. Mutagenesis of beta-tubulin cysteine residues in Saccharomyces cerevisiae: mutation of cysteine 354 results in cold-stable microtubules. Cell Motil. Cytoskeleton 49:67-77.
15. Guttmann-Raviv, N., S. Martin, and Y. Kassir. 2002. Ime2, a meiosis-specific kinase in yeast, is required for destabilization of its transcriptional activator, Ime1. Mol. Cell. Biol. 22:2047-2056.
16. Harris, M. A., J. Clark, A. Ireland, J. Lomax, M. Ashburner, R. Foulger, K. Eilbeck, S. Lewis, B. Marshall, C. Mungall, J. Richter, G. M. Rubin, J. A. Blake, C. Bult, M. Dolan, H. Drabkin, J. T. Eppig, D. P. Hill, L. Ni, M. Ringwald, R. Balakrishnan, J. M. Cherry, K. R. Christie, M. C. Costanzo, S. S. Dwight, S. Engel, D. G. Fisk, J. E. Hirschman, E. L. Hong, R. S. Nash, A. Sethuraman, C. L. Theesfeld, D. Botstein, K. Dolinski, B. Feierbach, T. Berardini, S. Mundodi, S. Y. Rhee, R. Apweiler, D. Barrell, E. Camon, E. Dimmer, V. Lee, R. Chisholm, P. Gaudet, W. Kibbe, R. Kishore, E. M. Schwarz, P. Sternberg, M. Gwinn, L. Hannick, J. Wortman, M. Berriman, V. Wood, N. de la Cruz, P. Tonellato, P. Jaiswal, T. Seigfried, and R. White. 2004. The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res. 32:D258-D261.
17. Hepworth, S. R., H. Friesen, and J. Segall. 1998. NDT80 and the meiotic recombination checkpoint regulate expression of middle sporulation-specific genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 18:5750-5761.
18. Honigberg, S. M., and K. Purnapatre. 2003. Signal pathway integration in the switch from the mitotic cell cycle to meiosis in yeast. J. Cell Sci. 116:2137-2147.
19. Hosack, D. A., G. Dennis, Jr., B. T. Sherman, H. C. Lane, and R. A. Lempicki. 2003. Identifying biological themes within lists of genes with EASE. Genome Biol. 4:R70.
20. Huber, W., A. von Heydebreck, H. Sultmann, A. Poustka, and M. Vingron. 2002. Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics 18(Suppl. 1):S96-S104.
21. Hwang, L. H., L. F. Lau, D. L. Smith, C. A. Mistrot, K. G. Hardwick, E. S. Hwang, A. Amon, and A. W. Murray. 1998. Budding yeast Cdc20: a target of the spindle checkpoint. Science 279:1041-1044.
22. Irizarry, R. A., B. M. Bolstad, F. Collin, L. M. Cope, B. Hobbs, and T. P. Speed. 2003. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31:e15.
23. Jacobs, C. W., A. E. Adams, P. J. Szaniszlo, and J. R. Pringle. 1988. Functions of microtubules in the Saccharomyces cerevisiae cell cycle. J. Cell Biol. 107:1409-1426.
24. Kaczanowski, A., J. Gaertig, and J. Kubiak. 1985. Effect of the antitubulin drug nocodazole on meiosis and postmeiotic development in Tetrahymena thermophila. Induction of achiasmatic meiosis. Exp. Cell Res. 158:244-256.
25. Kane, S. M., and R. Roth. 1974. Carbohydrate metabolism during ascospore development in yeast. J. Bacteriol. 118:8-14.
26. Kassir, Y., N. Adir, E. Boger-Nadjar, N. G. Raviv, I. Rubin-Bejerano, S. Sagee, and G. Shenhar. 2003. Transcriptional regulation of meiosis in budding yeast. Int. Rev. Cytol. 224:111-171.
27. Kaufman, L., and P. J. Rousseeuw. 1987. Clustering by means of mediods, p. 405-416. In Y. Dodge (ed.), Statistical data analysis based on the L1-norm and related methods. North-Holland/Elsevier, Amsterdam, The Netherlands.
28. Klein, F., P. Mahr, M. Galova, S. B. C. Buonomo, C. Michaelis, K. Nairz, and K. Nasmyth. 1999. A central role for cohesins in sister chromatid cohesion, formation of axial elements and recombination during yeast meiosis. Cell 98:91-103.
29. Kohrer, K., and H. Domdey. 1991. Preparation of high molecular weight RNA. Methods Enzymol. 194:398-405.
30. Lee, B. H., and A. Amon. 2003. Role of Polo-like kinase CDC5 in programming meiosis I chromosome segregation. Science 300:482-486.
31. Leisch, F. 2002. Sweave: dynamic generation of statistical reports using literate data analysis, p. 575-580. In W. Hardle and B. Ronz (ed.), Compstat 2002-proceedings in computational statistics. Physika Verlag, Heidelberg, Germany.
32. Leu, J. Y., and G. S. Roeder. 1999. The pachytene checkpoint in S. cerevisiae depends on Swc 1-mediated phosphorylation of the cyclin-dependent kinase Cdc28. Mol. Cell 4:805-814.
33. Lew, D. J., and D. J. Burke. 2003. The spindle assembly and spindle position checkpoints. Annu. Rev. Genet. 37:251-282.
34. Loidl, J. 1988. The effect of colchicine on synaptonemal complex formation in Allium ursinum. Exp. Cell Res. 178:93-97.
35. Longtine, M. S., A. McKenzie III, D. J. Demarini, N. G. Shah, A. Wach, A. Brachat, P. Philippsen, and J. R. Pringle. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953-961.
36. Machin, N. A., J. M. Lee, and G. Barnes. 1995. Microtubule stability in budding yeast: characterization and dosage suppression of a benomyl-dependent tubulin mutant. Mol. Biol. Cell 6:1241-1259.
37. Marston, A. L., B. H. Lee, and A. Amon. 2003. The Cdc14 phosphatase and the FEAR network control meiotic spindle disassembly and chromosome segregation. Dev. Cell 4:711-726.
38. Marston, A. L., W. H. Tham, H. Shah, and A. Amon. 2004. A genome-wide screen identifies genes required for centromcric cohesion. Science 303:1367-1370.
39. Michaelis, C., R. Ciosk, and K. Nasmyth. 1997. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91:35-45.
40. Mikhailov, A., and C. L. Rieder. 2002. Cell cycle: stressed out of mitosis. Curr. Biol. 12:R331-R333.
41. Miyake, T., J. Reese, C. M. Loch, D. T. Auble, and R. Li. 2004. Genome-wide analysis of ARS (autonomously replicating sequence) binding factor 1 (Abf1p)-mediated transcriptional regulation in Saccharomyces cerevisiae. J. Biol. Chem. 279:34865-34872.
42. Morgan, D. O. 1997. Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu. Rev. Cell Dev Biol. 13:261-291.
43. Nairz, K., and F. Klein. 1997. mrel1S-a yeast mutation that blocks double-strand-break processing and permits nonhomologous synapsis in meiosis. Genes Dev. 11:2272-2290.
44. Primig, M., C. Wiederkehr, R. Basavaraj, C. Sarrauste de Menthiere, L. Hermida, R. Koch, U. Schlecht, H. G. Dickinson, M. Fellous, J. A. Grootegoed, R. S. Hawley, B. Jegou, B. Maro, A. Nicolas, T. Orr-Weaver, T. Schedl, A. Villeneuve, D. J. Wolgemuth, M. Yamamoto, D. Zickler, N. Lamb, and R. E. Esposito. 2003. GermOnline, a new cross-species community annotation database on germ-line development and gametogenesis. Nat. Genet. 35:291-292.
45. Primig, M., R. M. Williams, E. A. Winzeler, G. G. Tevzadze, A. R. Conway, S. Y. Hwang, R. W. Davis, and R. E. Esposito. 2000. The core meiotic transcriptome in budding yeasts. Nat. Genet. 26:415-423.
46. Prinz, S., F. Klein, H. Auer, D. Schweizer, and M. Primig. 1995. A DNA binding factor (UBF) interacts with a positive regulatory element in the promoters of genes expressed during meiosis and vegetative growth in yeast. Nucleic Acids Res. 23:3449-3456.
47. Rabitsch, K. P., M. Petronczki, J. P. Javerzat, S. Genier, B. Chwalla, A. Schleiffer, T. U. Tanaka, and K. Nasmyth. 2003. Kinetochore recruitment of two nucleolar proteins is required for homolog segregation in meiosis I. Dev. Cell 4:535-548.
48. Rieder, C. L., and R. Cole. 2000. Microtubule disassembly delays the G2-M transition in vertebrates. Curr. Biol. 10:1067-1070.
49. Roeder, G. S. 1997. Meiotic chromosomes: it takes two to tango. Genes Dev. 11:2600-2621.
50. Roeder, G. S., and J. M. Bailis. 2000. The pachytene checkpoint. Trends Genet. 16:395-403.
51. Saunders, W., D. Hornack, V. Lengyel, and C. Deng. 1997. The Saccharomyces cerevisiae kinesin-related motor Kar3p acts at preanaphase spindle poles to limit the number and length of cytoplasmic microtubules. J. Cell Biol. 137:417-431.
52. Schlecht, U., P. Demougin, R. Koch, L. Hermida, C. Wiederkehr, P. Descombes, C. Pineau, B. Jegou, and M. Primig. 2004. Expression profiling of mammalian male meiosis and gametogenesis identifies novel candidate genes for roles in the regulation of fertility. Mol. Biol. Cell 15:1031-1043.
53. Schlecht, U., and M. Primig. 2003. Mining meiosis and gametogenesis with DNA microarrays. Reproduction 125:447-456.
54. Shanks, R. M., C. Bascom-Slack, and D. S. Dawson. 2004. Analysis of the kar3 meiotic arrest in Saccharomyces cerevisiae. Cell Cycle 3:363-371.
55. Shanks, R. M., R. J. Kamieniecki, and D. S. Dawson. 2001. The Kar3-interacting protein Cik1p plays a critical role in passage through meiosis I in Saccharomyces cerevisiae. Genetics 159:939-951.
56. Shepard, J., E. R. Boothroyd, and H. Stern. 1974. The effect of colchicine on synapsis and chiasma formation in microsporocytes of Lilium. Chromosoma 44:423-437.
57. Shonn, M. A., R. McCarroll, and A. W. Murray. 2000. Requirement of the spindle checkpoint for proper chromosome segregation in budding yeast meiosis. Science 289:300-303.
58. Shonn, M. A., A. L. Murray, and A. W. Murray. 2003. Spindle checkpoint component Mad2 contributes to biorientation of homologous chromosomes. Curr. Biol. 13:1979-1984.
59. Sora, S., P. Melchioretto, P. Primignani, and M. L. Agostoni Carbone. 1988. Caffeine interactions with methyl methanesulphonate, hycanthone, benlate, and cadmium chloride in chromosomal meiotic segregation of Saccharomyces cerevisiae. Mutat. Res. 201:9-16.
60. Sym, M., J. A. Engebrecht, and G. S. Roeder. 1993. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72:365-378.
61. Tepperberg, J. H., M. J. Moses, and J. Nath. 1997. Colchicine effects on meiosis in the male mouse. I. Meiotic prophase: synaptic arrest, univalents, loss of damaged spermatocytes and a possible checkpoint at pachytene. Chromosoma 106:183-192.
62. Tepperberg, J. H., M. J. Moses, and J. Nath. 1999. Colchicine effects on meiosis in the male mouse. II. Inhibition of synapsis and induction of non-disjunction. Mutat. Res. 429:93-105.
63. Thomas, J. H., N. F. Neff, and D. Botstein. 1985. Isolation and characterization of mutations in the beta-tubulin gene of Saccharomyces cerevisiae. Genetics 111:715-734.
64. Tung, K. S., E. J. Hong, and G. S. Roeder. 2000. The pachytene checkpoint prevents accumulation and phosphorylation of the meiosis-specific transcription factor Ndt80. Proc. Natl. Acad. Sci. USA 97:12187-12192.
65. Visintin, R., K. Craig, E. S. Hwang, S. Prinz, M. Tyers, and A. Amon. 1998. The phosphatase Cdc14 triggers mitotic exit by reversal of Cdk-dependent phosphorylation. Mol. Cell 2:709-718.
66. Visinlin, R., E. S. Hwang, and A. Amon. 1999. Cfi1 prevents premature exit from mitosis by anchoring Cdc14 phosphatase in the nucleolus. Nature 398:818-823.
67. Wiederkehr, C., K. Basavaraj, C. Sarrauste de Menthiere, L. Hermida, R. Koch, U. Schlecht, A. Amon, S. Brachat, M. Breitenbach, P. Briza, S. Caburet, M. Cherry, R. Davis, A. Deutschbauer, H. G. Dickinson, T. Dumitrescu, M. Fellous, A. Goldman, J. A. Grootegoed, R. Hawley, R. Ishii, B. Jegou, R. J. Kaufman, F. Klein, N. Lamb, B. Maro, K. Nasmyth, A. Nicolas, T. Orr-Weaver, P. Philippsen, C. Pineau, K. P. Rabitsch, V. Reinke, H. Roest, W. Saunders, M. Schroder, T. Schedl, M. Siep, A. Villeneuve, D. J. Wolgemuth, M. Yamamoto, D. Zickler, R. E. Esposito, and M. Primig. 2004. GermOnline, a cross-species community knowledgebase on germ cell differentiation. Nucleic Acids Res. 32:D560-D567.
68. Wiederkehr, C., R. Basavaraj, C. Sarrauste de Menthiere, R. Koch, U. Schlecht, L. Hermida, B. Masdoua, K. Ishii, V. Cassen, M. Yamamoto, C. Lane, M. Cherry, N. Lamb, and M. Primig. 2004. Database model and specification of GermOnline Release 2.0, a cross-species community annotation knowledgebase on germ cell differentiation. Bioinformatics 20:808-811.
69. Williams, R. M., M. Primig, B. K. Washburn, E. A. Winzeler, M. Bellis, C. Sarrauste de Menthiere, R. W. Davis, and R. E. Esposito. 2002. The Ume6 regulon coordinates metabolic and meiotic gene expression in yeast. Proc. Natl. Acad. Sci. USA 99:13431-13436.
70. Xu, L., B. M. Weiner, and N. Kleckner. 1997. Meiotic cells monitor the status of the interhomolog recombination complex. Genes Dev. 11:106-118.
71. Zickler, D., and N. Kleckner. 1998. The leptotene-zygotene transition of meiosis. Annu. Rev. Genet. 32:619-697.
72. Zickler, D., and N. Kleckner. 1999. Meiotic Chromosomes: integrating structure and function. Annu. Rev. Genet. 33:603-754.
73. Ziegelbauer, J., B. Shan, D. Yager, C. Larabell, B. Hoffmann, and R. Tjian. 2001. Transcription factor MIZ-1 is regulated via microtubule association. Mol. Cell 8:339-349.