Yeast ime2 functions early in meiosis upstream of cell cycle-regulated sbf and mbf targets

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Brush, George S ^a,b   Najor, Nicole A ^a,c   Dombkowski, Alan A ^a   Cukovic, Daniela ^a   Sawarynski, Kara E ^a,d,e  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KARMANOS CANCER INSTITUTE   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d WILLIAM BEAUMONT HOSPITAL   (United States)

^e OAKLAND UNIVERSITY WILLIAM BEAUMONT SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; IME2 PROTEIN; MBF PROTEIN; PROTEIN KINASE; SBF PROTEIN; SIC1 PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; CLN1 PROTEIN, S CEREVISIAE; CLN2 PROTEIN, S CEREVISIAE; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE INHIBITOR; CYCLINE; IME2 PROTEIN, S CEREVISIAE; PROTEIN SERINE THREONINE KINASE; REPRESSOR PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SIC1 PROTEIN, S CEREVISIAE; SIGNAL PEPTIDE; WHI5 PROTEIN, S CEREVISIAE;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE REGULATION; CONTROLLED STUDY; ENZYME ACTIVITY; FUNGAL CELL; FUNGAL GENE; GENE EXPRESSION; IME2 GENE; MEIOSIS; NONHUMAN; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; WILD TYPE; BIOLOGICAL MODEL; CATALYSIS; CELL CYCLE; DNA MICROARRAY; DNA REPLICATION; GENE EXPRESSION PROFILING; GENETIC EPISTASIS; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PLOIDY; PROTEIN MOTIF; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

AMINO ACID MOTIFS; CATALYSIS; CDC2 PROTEIN KINASE; CELL CYCLE; CYCLIN-DEPENDENT KINASE INHIBITOR PROTEINS; CYCLIN-DEPENDENT KINASES; CYCLINS; DNA REPLICATION; EPISTASIS, GENETIC; GENE EXPRESSION PROFILING; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEIOSIS; MODELS, BIOLOGICAL; MODELS, GENETIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORYLATION; PLOIDIES; PROTEIN-SERINE-THREONINE KINASES; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84857662333     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031575     Document Type: Article

References (63)

1. Schwob E, Nasmyth K, (1993) CLB5 and CLB6, a new pair of B cyclins involved in DNA replication in Saccharomyces cerevisiae. Genes Dev 7: 1160-1175.
2. Schwob E, Böhm T, Mendenhall MD, Nasmyth K, (1994) The B-type cyclin kinase inhibitor p40SIC1 controls the G1 to S transition in S. cerevisiae. Cell 79: 233-244.
3. Dirick L, Goetsch L, Ammerer G, Byers B, (1998) Regulation of meiotic S phase by Ime2 and a Clb5,6-associated kinase in Saccharomyces cerevisiae. Science 281: 1854-1857.
4. Stuart D, Wittenberg C, (1998) CLB5 and CLB6 are required for premeiotic DNA replication and activation of the meiotic S/M checkpoint. Genes Dev 12: 2698-2710.
5. Sawarynski KE, Najor NA, Kepsel AC, Brush GS, (2009) Sic1-induced DNA rereplication during meiosis. Proc Natl Acad Sci USA 106: 232-237.
6. Dahmann C, Diffley JFX, Nasmyth KA, (1995) S-phase-promoting cyclin-dependent kinases prevent re-replication by inhibiting the transition of replication origins to a pre-replicative state. Current Biol 5: 1257-1269.
7. Remus D, Diffley JF, (2009) Eukaryotic DNA replication control: lock and load, then fire. Curr Opin Cell Biol 21: 771-777.
8. Sclafani RA, (2000) Cdc7p-Dbf4p becomes famous in the cell cycle. J Cell Sci 113: 2111-2117.
9. Valentin G, Schwob E, Seta FD, (2006) Dual role of the Cdc7-regulatory protein Dbf4 during yeast meiosis. J Biol Chem 281: 2828-2834.
10. Wan L, Zhang C, Shokat KM, Hollingsworth NM, (2006) Chemical inactivation of Cdc7 kinase in budding yeast results in a reversible arrest that allows efficient cell synchronization prior to meiotic recombination. Genetics 174: 1767-1774.
11. Tyers M, Tokiwa G, Futcher B, (1993) Comparison of the Saccharomyces cerevisiae G1 cyclins: Cln3 may be an upstream activator of Cln1, Cln2 and other cyclins. EMBO J 12: 1955-1968.
12. Dirick L, Böhm T, Nasmyth K, (1995) Roles and regulation of Cln-Cdc28 kinases at the start of the cell cycle of Saccharomyces cerevisiae. EMBO J 14: 4803-4813.
13. Stuart D, Wittenberg C, (1995) CLN3, not positive feedback, determines the timing of CLN2 transcription in cycling cells. Genes Dev 9: 2780-2794.
14. Costanzo M, Nishikawa JL, Tang X, Millman JS, Schub O, et al. (2004) CDK activity antagonizes Whi5, an inhibitor of G1/S transcription in yeast. Cell 117: 899-913.
15. de Bruin RAM, McDonald WH, Kalashnikova TI, Yates J 3rd, Wittenberg C, (2004) Cln3 activates G1-specific transcription via phosphorylation of the SBF bound repressor Whi5. Cell 117: 887-898.
16. Andrews BJ, Herskowitz I, (1989) Identification of a DNA binding factor involved in cell-cycle control of the yeast HO gene. Cell 57: 21-29.
17. Nasmyth K, Dirick L, (1991) The role of SWI4 and SWI6 in the activity of G1 cyclins in yeast. Cell 66: 995-1013.
18. Ogas J, Andrews BJ, Herskowitz I, (1991) Transcriptional activation of CLN1, CLN2, and a putative new G1 cyclin (HCS26) by SWI4, a positive regulator of G1-specific transcription. Cell 66: 1015-1026.
19. Koch C, Moll T, Neuberg M, Ahorn H, Nasmyth K, (1993) A role for the transcription factors Mbp1 and Swi4 in progression from G1 to S phase. Science 261: 1551-1557.
20. de Bruin RAM, Kalashnikova TI, Chahwan C, McDonald WH, Wohlschlegel J, et al. (2006) Constraining G1-specific transcription to late G1 phase: the MBF-associated corepressor Nrm1 acts via negative feedback. Mol Cell 23: 483-496.
21. Lowndes NF, Johnson AL, Breeden L, Johnston LH, (1992) SWI6 protein is required for transcription of the periodically expressed DNA synthesis genes in budding yeast. Nature 357: 505-508.
22. Ferrezuelo F, Colomina N, Futcher B, Aldea M, (2010) The transcriptional network activated by Cln3 cyclin at the G1-to-S transition of the yeast cell cycle. Genome Biol 11: R67.
23. Schneider BL, Yang QH, Futcher AB, (1996) Linkage of replication to start by the Cdk inhibitor Sic1. Science 272: 560-562.
24. Tyers M, (1996) The cyclin-dependent kinase inhibitor p40SIC1 imposes the requirement for Cln G1 cyclin function at Start. Proc Natl Acad Sci USA 93: 7772-7776.
25. Feldman RMR, Correll CC, Kaplan KB, Deshaies RJ, (1997) A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p. Cell 91: 221-230.
26. Skowyra D, Craig KL, Tyers M, Elledge SJ, Harper JW, (1997) F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91: 209-219.
27. Verma R, Annan RS, Huddleston MJ, Carr SA, Reynard G, et al. (1997) Phosphorylation of Sic1p by G1 Cdk required for its degradation and entry into S phase. Science 278: 455-460.
28. Colomina N, Garí E, Gallego C, Herrero E, Aldea M, (1999) G1 cyclins block the Ime1 pathway to make mitosis and meiosis incompatible in budding yeast. EMBO J 18: 320-329.
29. Benjamin KR, Zhang C, Shokat KM, Herskowitz I, (2003) Control of landmark events in meiosis by the CDK Cdc28 and the meiosis-specific kinase Ime2. Genes Dev 17: 1524-1539.
30. Mitchell AP, Driscoll SE, Smith HE, (1990) Positive control of sporulation-specific genes by the IME1 and IME2 products in Saccharomyces cerevisiae. Mol Cell Biol 10: 2104-2110.
31. Foiani M, Nadjar-Boger E, Capone R, Sagee S, Hashimshoni T, et al. (1996) A meiosis-specific protein kinase, Ime2, is required for the correct timing of DNA replication and for spore formation in yeast meiosis. Mol Gen Genet 253: 278-288.
32. Pak J, Segall J, (2002) Regulation of the premiddle and middle phases of expression of the NDT80 gene during sporulation of Saccharomyces cerevisiae. Mol Cell Biol 22: 6417-6429.
33. Ahmed NT, Bungard D, Shin ME, Moore M, Winter E, (2009) The Ime2 protein kinase enhances the disassociation of the Sum1 repressor from middle meiotic promoters. Mol Cell Biol 29: 4352-4362.
34. Sopko R, Raithatha S, Stuart D, (2002) Phosphorylation and maximal activity of Saccharomyces cerevisiae meiosis-specific transcription factor Ndt80 is dependent on Ime2. Mol Cell Biol 22: 7024-7040.
35. Nash P, Tang X, Orlicky S, Chen Q, Gertler FB, et al. (2001) Multisite phosphorylation of a CDK inhibitor sets a threshold for the onset of DNA replication. Nature 414: 514-521.
36. Sedgwick C, Rawluk M, Decesare J, Raithatha SA, Wohlschlegel J, et al. (2006) Saccharomyces cerevisiae Ime2 phosphorylates Sic1 at multiple PXS/T sites but is insufficient to trigger Sic1 degradation. Biochem J 399: 151-160.
37. Sawarynski KE, Kaplun A, Tzivion G, Brush GS, (2007) Distinct activities of the related protein kinases Cdk1 and Ime2. Biochim Biophys Acta 1773: 450-456.
38. Holt LJ, Hutti JE, Cantley LC, Morgan DO, (2007) Evolution of Ime2 phosphorylation sites on Cdk1 substrates provides a mechanism to limit the effects of the phosphatase Cdc14 in meiosis. Molec Cell 25: 689-702.
39. Moore M, Shin ME, Bruning A, Schindler K, Vershon A, et al. (2007) Arg-Pro-X-Ser/Thr is a consensus phosphoacceptor sequence for the meiosis-specific Ime2 protein kinase in Saccharomyces cerevisiae. Biochemistry 46: 271-278.
40. Boorsma A, Foat BC, Vis D, Klis F, Bussemaker HJ, (2005) T-profiler: scoring the activity of predefined groups of genes using gene expression data. Nucleic Acids Res 33: W592-W595.
41. Chu S, DeRisi J, Eisen M, Mulholland J, Botstein D, et al. (1998) The transcriptional program of sporulation in budding yeast. Science 282: 699-705.
42. Kane SM, Roth R, (1974) Carbohydrate metabolism during ascospore development in yeast. J Bacteriol 118: 8-14.
43. Mitchell AP, (1994) Control of meiotic gene expression in Saccharomyces cerevisiae. Microbiol Rev 58: 56-70.
44. Guttmann-Raviv N, Martin S, Kassir Y, (2002) Ime2, a meiosis-specific kinase in yeast, is required for destabilization of its transcriptional activator, Ime1. Mol Cell Biol 22: 2047-2056.
45. Mallory MJ, Cooper KF, Strich R, (2007) Meiosis-specific destruction of the Ume6p repressor by the Cdc20-directed APC/C. Mol Cell 27: 951-961.
46. Foat BC, Houshmandi SS, Olivas WM, Bussemaker HJ, (2005) Profiling condition-specific, genome-wide regulation of mRNA stability in yeast. Proc Natl Acad Sci U S A 102: 17675-17680.
47. Bussemaker HJ, Li H, Siggia ED, (2001) Regulatory element detection using correlation with expression. Nat Genet 27: 167-171.
48. Mendes ND, Casimiro AC, Santos PM, Sá-Correia I, Oliveira AL, et al. (2006) MUSA: a parameter free algorithm for the identification of biologically significant motifs. Bioinformatics 22: 2996-3002.
49. Hong EL, Balakrishnan R, Dong Q, Christie KR, Park J, et al. (2008) Gene Ontology annotations at SGD: new data sources and annotation methods. Nucleic Acids Res 36: D577-D581.
50. Day A, Markwardt J, Delaguila R, Zhang J, Purnapatre K, et al. (2004) Cell size and Cln-Cdc28 complexes mediate entry into meiosis by modulating cell growth. Cell Cycle 3: 1433-1439.
51. Foiani M, Liberi G, Lucchini G, Plevani P, (1995) Cell cycle-dependent phosphorylation and dephosphorylation of the yeast DNA polymerase alpha-primase B subunit. Mol Cell Biol 15: 883-891.
52. Ferrezuelo F, Aldea M, Futcher B, (2009) Bck2 is a phase-independent activator of cell cycle-regulated genes in yeast. Cell Cycle 8: 239-252.
53. Raithatha SA, Stuart DT, (2005) Meiosis-specific regulation of the Saccharomyces cerevisiae S-phase cyclin CLB5 is dependent on MluI cell cycle box (MCB) elements in its promoter but is independent of MCB-binding factor activity. Genetics 169: 1329-1342.
54. Leem SH, Chung CN, Sunwoo Y, Araki H, (1998) Meiotic role of SWI6 in Saccharomyces cerevisiae. Nucleic Acids Res 26: 3154-3158.
55. 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.
56. Clifford DM, Marinco SM, Brush GS, (2004) The meiosis-specific protein kinase Ime2 directs phosphorylation of replication protein A. J Biol Chem 279: 6163-6170.
57. Winzeler EA, Shoemaker DD, Astromoff A, Liang H, Anderson K, et al. (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906.
58. Tong AHY, Evangelista M, Parsons AB, Xu H, Bader GD, et al. (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2364-2368.
59. Padmore R, Cao L, Kleckner N, (1991) Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell 66: 1239-1256.
60. Kushnirov VV, (2000) Rapid and reliable protein extraction from yeast. Yeast 16: 857-860.
61. Schmitt ME, Brown TA, Trumpower BL, (1990) A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res 18: 3091-3092.
62. Monteiro PT, Mendes ND, Teixeira MC, d'Orey S, Tenreiro S, et al. (2008) YEASTRACT-DISCOVERER: new tools to improve the analysis of transcriptional regulatory associations in Saccharomyces cerevisiae. Nucleic Acids Res 36: D132-D136.
63. Spellman PT, Sherlock G, Zhang MQ, Iyer VR, Anders K, et al. (1998) Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell 9: 3273-3297.