A large complex mediated by Moc1, Moc2 and Cpc2 regulates sexual differentiation in fission yeast

FEBS Journal

Volumn 276, Issue 18, 2009, Pages 5076-5093

  Paul, Swapan Kumar ^a   Oowatari, Yasuo ^a   Kawamukai, Makoto ^a  

^a SHIMANE UNIVERSITY   (Japan)

Author keywords

Fission yeast; Moc protein; Schizosaccharomyces pombe; Sexual differentiation; Translation

Indexed keywords

CPC2 PROTEIN; FUNGAL PROTEIN; MOC1 PROTEIN; MOC2 PROTEIN; MOC3 PROTEIN; MOC4 PROTEIN; RIBOSOME PROTEIN; RIBOSOME PROTEIN RP132 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR STE11; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; GENE OVEREXPRESSION; IMMUNOPRECIPITATION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; SEX DIFFERENTIATION; TRANSLATION REGULATION; TWO HYBRID SYSTEM; YEAST;

CELL CYCLE PROTEINS; DEAD-BOX RNA HELICASES; RECEPTORS, CELL SURFACE; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; TRANSCRIPTION FACTORS; TWO-HYBRID SYSTEM TECHNIQUES;

SCHIZOSACCHAROMYCES POMBE; SCHIZOSACCHAROMYCETACEAE;

EID: 69449086465     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07204.x     Document Type: Article

References (50)

1. Yamamoto M, Imai Y Watanabe Y (1997) Mating and sporulation in Schizosaccharomyces pombe. In The Molecular and Cellular Biology of the Yeast Saccharomyces (Pringle JT, Broach JR Jones EW eds pp. 1037 1106. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. Matsuo T, Otsubo Y, Urano J, Tamanoi F Yamamoto M (2007) Loss of the TOR kinase Tor2 mimics nitrogen starvation and activates the sexual development pathway in fission yeast. Mol Cell Biol 27, 3154 3164.
3. Ozoe F, Kurokawa R, Kobayashi Y, Jeong HT, Tanaka K, Sen K, Nakagawa T, Matsuda H Kawamukai M (2002) The 14-3-3 proteins Rad24 and Rad25 negatively regulate Byr2 by affecting its localization in Schizosaccharomyces pombe. Mol Cell Biol 22, 7105 7119.
4. Yamamoto TG, Chikashige Y, Ozoe F, Kawamukai M Hiraoka Y (2004) Activation of the pheromone-responsive MAP kinase drives haploid cells to undergo ectopic meiosis with normal telomere clustering and sister chromatid segregation in fission yeast. J Cell Sci 117, 3875 3886.
5. Kawamukai M, Ferguson K, Wigler M Young D (1991) Genetic and biochemical analysis of the adenylyl cyclase of Schizosaccharomyces pombe. Cell Regul 2, 155 164.
6. Hoffman CS (2005) Glucose sensing via the protein kinase A pathway in Schizosaccharomyces pombe. Biochem Soc Trans 33, 257 260.
7. Kawamukai M, Gerst J, Field J, Riggs M, Rodgers L, Wigler M Young D (1992) Genetic and biochemical analysis of the adenylyl cyclase-associated protein, cap, in Schizosaccharomyces pombe. Mol Biol Cell 3, 167 180.
8. Zhou GL, Yamamoto T, Ozoe F, Yano D, Tanaka K, Matsuda H Kawamukai M (2000) Identification of a 14-3-3 protein from Lentinus edodes that interacts with CAP (adenylyl cyclase-associated protein), and conservation of this interaction in fission yeast. Biosci Biotechnol Biochem 64, 149 159.
9. Maeda T, Watanabe Y, Kunitomo H Yamamoto M (1994) Cloning of the pka1 gene encoding the catalytic subunit of the cAMP-dependent protein kinase in Schizosaccharomyces pombe. J Biol Chem 269, 9632 9637.
10. Higuchi T, Watanabe Y Yamamoto M (2002) Protein kinase A regulates sexual development and gluconeogenesis through phosphorylation of the Zn finger transcriptional activator Rst2p in fission yeast. Mol Cell Biol 22, 1 11.
11. Kitamura K, Katayama S, Dhut S, Sato M, Watanabe Y, Yamamoto M Toda T (2001) Phosphorylation of Mei2 and Ste11 by Pat1 kinase inhibits sexual differentiation via ubiquitin proteolysis and 14-3-3 protein in fission yeast. Dev Cell 1, 389 399.
12. Qin J, Kang W, Leung B McLeod M (2003) Ste11p, a high-mobility-group box DNA-binding protein, undergoes pheromone- and nutrient-regulated nuclear-cytoplasmic shuttling. Mol Cell Biol 23, 3253 3264.
13. Oowatari Y, Toma K, Ozoe F Kawamukai M (2009) Identification of sam4 as a rad24 allele in Schizosaccharomyces pombe. Biosci Biotechnol Biochem 73, 1591 1598.
14. Kawamukai M (1999) Isolation of a novel gene, moc2, encoding a putative RNA helicase as a suppressor of sterile strains in Schizosaccharomyces pombe. Biochim Biophys Acta 1446, 93 101.
15. Goldar MM, Jeong HT, Tanaka K, Matsuda H Kawamukai M (2005) Moc3, a novel Zn finger type protein involved in sexual development, ascus formation, and stress response of Schizosaccharomyces pombe. Curr Genet 48, 345 355.
16. +. EMBO J 15, 6629 6640.
17. Yakura M, Ishikura Y, Adachi Y Kawamukai M (2006) Involvement of Moc1 in sexual development and survival of Schizosaccharomyces pombe. Biosci Biotechnol Biochem 70, 1740 1749.
18. Shimanuki M, Chung SY, Chikashige Y, Kawasaki Y, Uehara L, Tsutsumi C, Hatanaka M, Hiraoka Y, Nagao K Yanagida M (2007) Two-step, extensive alterations in the transcriptome from G0 arrest to cell division in Schizosaccharomyces pombe. Gene Cell 12, 677 692.
19. Jang YJ, Won M, Chung KS, Kim DU, Hoe KL, Park C Yoo HS (1997) A novel protein, Psp1, essential for cell cycle progression of Schizosaccharomyces pombe is phosphorylated by Cdc2-Cdc13 upon entry into G0-like stationary phase of cell growth. J Biol Chem 272, 19993 20002.
20. Goldar MM, Nishie T, Ishikura Y, Fukuda T, Takegawa K Kawamukai M (2005) Functional conservation between fission yeast moc1/sds23 and its two orthologs, budding yeast SDS23 and SDS24, and phenotypic differences in their disruptants. Biosci Biotechnol Biochem 69, 1422 1426.
21. Forbes KC, Humphrey T Enoch T (1998) Suppressors of cdc25p overexpression identify two pathways that influence the G2/M checkpoint in fission yeast. Genetics 150, 1361 1375.
22. Grallert B, Kearsey SE, Lenhard M, Carlson CR, Nurse P, Boye E Labib K (2000) A fission yeast general translation factor reveals links between protein synthesis and cell cycle controls. J Cell Sci 113, 1447 1458.
23. Liu HY, Nefsky BS Walworth NC (2002) The Ded1 DEAD box helicase interacts with Chk1 and Cdc2. J Biol Chem 277, 2637 2643.
24. + encoding a zinc-finger protein functions in the mating pheromone recognition pathway. Mol Biol Cell 6, 1185 1195.
25. Beltraminelli N, Murone M Simanis V (1999) The S. pombe zfs1 gene is required to prevent septation if mitotic progression is inhibited. J Cell Sci 112, 3103 3114.
26. Cuthbertson BJ, Liao Y, Birnbaumer L Blackshear PJ (2008) Characterization of zfs1 as an mRNA-binding and -destabilizing protein in Schizosaccharomyces pombe. J Biol Chem 283, 2586 2594.
27. Paul SK, Goldar MM, Yakura M, Oowatari Y Kawamukai M (2009) Glutamyl tRNA synthetases and glutamic acid induce sexual differentiation of Schizosaccharomyces pombe. Biosci Biotechnol Biochem 73, 1339 1347.
28. Nijtmans LG, Henderson NS Holt IJ (2002) Blue Native electrophoresis to study mitochondrial and other protein complexes. Methods 26, 327 334.
29. Shor B, Calaycay J, Rushbrook J McLeod M (2003) Cpc2/RACK1 is a ribosome-associated protein that promotes efficient translation in Schizosaccharomyces pombe. J Biol Chem 278, 49119 49128.
30. Hanyu Y, Imai KK, Kawasaki Y, Nakamura T, Nakaseko Y, Nagao K, Kokubu A, Ebe M, Fujisawa A, Hayashi T et al. (2009) Schizosaccharomyces pombe cell division cycle under limited glucose requires Ssp1 kinase, the putative CaMKK, and Sds23, a PP2A-related phosphatase inhibitor. Gene Cell 14, 539 554.
31. Jeong HT, Oowatari Y, Abe M, Tanaka K, Matsuda H Kawamukai M (2004) Interaction between a negative regulator (Msa2/Nrd1) and a positive regulator (Cpc2) of sexual differentiation in Schizosaccharomyces pombe. Biosci Biotechnol Biochem 68, 1621 1626.
32. Jeong HT, Ozoe F, Tanaka K, Nakagawa T, Matsuda H Kawamukai M (2004) A novel gene, msa1, inhibits sexual differentiation in Schizosaccharomyces pombe. Genetics 167, 77 91.
33. Katayama S, Ozoe F, Kurokawa R, Tanaka K, Nakagawa T, Matsuda H Kawamukai M (1996) Genetic analysis of the sam mutations, which induce sexual development with no requirement for nutritional starvation in fission yeast. Biosci Biotechnol Biochem 60, 994 999.
34. Won M, Park SK, Hoe KL, Jang YJ, Chung KS, Kim DU, Kim HB Yoo HS (2001) Rkp1/Cpc2, a fission yeast RACK1 homolog, is involved in actin cytoskeleton organization through protein kinase C, Pck2, signaling. Biochem Biophys Res Commun 282, 10 15.
35. McLeod M, Shor B, Caporaso A, Wang W, Chen H Hu L (2000) Cpc2, a fission yeast homologue of mammalian RACK1 protein, interacts with Ran1 (Pat1) kinase to regulate cell cycle progression and meiotic development. Mol Cell Biol 20, 4016 4027.
36. Sheth U Parker R (2006) Targeting of aberrant mRNAs to cytoplasmic processing bodies. Cell 125, 1095 1109.
37. Beckham C, Hilliker A, Cziko AM, Noueiry A, Ramaswami M Parker R (2008) The DEAD-box RNA helicase Ded1p affects and accumulates in Saccharomyces cerevisiae P-bodies. Mol Biol Cell 19, 984 993.
38. Linder P (2003) Yeast RNA helicases of the DEAD-box family involved in translation initiation. Biol Cell 95, 157 167.
39. Wang J, Yuan S Jiang S (2006) The ribosomal protein L32-2 (RPL32-2) of S. pombe exhibits a novel extraribosomal function by acting as a potential transcriptional regulator. FEBS Lett 580, 1827 1832.
40. Alfa C, Fantes P, Hyams J, McLeod M Warbrick E (1993) Experiments with Fission Yeast. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
41. Prentice HL (1992) High efficiency transformation of Schizosaccharomyces pombe by electroporation. Nucleic Acids Res 20, 621.
42. Sambrook J, Fritsch EF Maniatis T (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
43. Chien CT, Bartel PL, Sternglanz R Fields S (1991) The two-hybrid system: a method to identify and clone genes for proteins that interact with a protein of interest. Proc Natl Acad Sci USA 88, 9578 9582.
44. Ito H, Fukuda Y, Murata K Kimura A (1983) Transformation of intact yeast cells treated with alkali cations. J Bacteriol 153, 163 168.
45. Krawchuk MD Wahls WP (1999) High-efficiency gene targeting in Schizosaccharomyces pombe using a modular, PCR-based approach with long tracts of flanking homology. Yeast 15, 1419 1427.
46. Matsuo Y, Matsuura Y, Tanaka K, Matsuda H Kawamukai M (2004) Chr4, a Schizosaccharomyces pombe homologue of the Saccharomyces cerevisiae Chs4p/Skt5p protein, is related to septum formation and is required for the proper localization of Chs2. Yeast 21, 1005 1019.
47. Matsuo Y, Asakawa K, Toda T Katayama S (2006) A rapid method for protein extraction from fission yeast. Biosci Biotechnol Biochem 70, 1992 1994.
48. Yakura M, Ozoe F, Ishida H, Nakagawa T, Tanaka K, Matsuda H Kawamukai M (2006) zds1, a novel gene encoding an ortholog of Zds1 and Zds2, controls sexual differentiation, cell wall integrity and cell morphology in fission yeast. Genetics 172, 811 825.
49. Tanabe K, Ito N, Wakuri T, Ozoe F, Umeda M, Katayama S, Tanaka K, Matsuda H Kawamukai M (2003) Sla1, a Schizosaccharomyces pombe homolog of the human La protein, induces ectopic meiosis when its C terminus is truncated. Eukaryot Cell 2, 1274 1287.
50. Tanabe K, Tanaka K, Matsuda H Kawamukai M (2004) Truncated Sla1 induces haploid meiosis through the Pat1-Mei2 system in fission yeast. Biosci Biotechnol Biochem 68, 266 270.