The fission yeast pmk1+ gene encodes a novel mitogen-activated protein kinase homolog which regulates cell integrity and functions coordinately with the protein kinase C pathway

Molecular and Cellular Biology

Volumn 16, Issue 12, 1996, Pages 6752-6764

  Toda, Takashi ^a,c   Dhut, Susheela ^a   Superti Furga, Giulio ^b   Gotoh, Yukiko ^c   Nishida, Eisuke ^c   Sugiura, Reiko ^d   Kuno, Takayoshi ^d  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c KYOTO UNIVERSITY   (Japan)

^d KOBE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; POTASSIUM; PROTEIN KINASE C; SODIUM;

AMINO ACID SEQUENCE; ARTICLE; CANDIDA; CELL SHAPE; CELL WALL; CYTOKINESIS; FUNGAL GENETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SACCHAROMYCES; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; YEAST;

ANURA; CANDIDA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES POMBE; SACCHAROMYCETALES; SCHIZOSACCHAROMYCES POMBE;

EID: 0029923979     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.16.12.6752     Document Type: Article

References (98)

1. Ammerer, G. 1994. Sex, stress and integrity: the importance of MAP kinase in yeast. Curr. Opin. Genet. Dev. 4:90-95.
2. Basi, G., E. Schmid, and K. Maundrell. 1993. TATA box mutations in the Schizosaccharomyces pombe nmt1 promoter affect transcriptional efficiency but not the transcription start point or thiamine repressibility. Gene 123: 131-136.
3. +, a cell cycle control gene of the fission yeast Schizosaccharomyces pombe. Mol. Cell. Biol. 6:3523-3530.
4. Boulton, T. G., S. H. Nye, D. J. Robbins, N. Y. Ip, E. Radziejewska, S. D. Morgenbesser, R. A. DePinho, N. Panayotatos, M. H. Cobb, and G. D. Yancopoulos. 1991. ERKs: a family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell 65:663-675.
5. Brewster, J. L., T. de Valoir, N. D. Dwyer, E. Winter, and M. C. Gustin. 1993. An osmosensing signal transduction pathway in yeast. Science 259:1760-1763.
6. Brown, J. L., H. Bussey, and R. C. Stewart. 1994. Yeast SKN7p functions in a eukaryotic two-component regulatory pathway. EMBO J. 13:5186-5194.
7. Cobb, M. H., and E. J. Goldsmith. 1995. How MAP kinases are regulated. J. Biol. Chem. 270:14843-14846.
8. Costigan, C., S. Gehrung, and M. Snyder. 1992. A synthetic lethal screen identifies SLK1, a novel protein kinase homolog implicated in yeast cell morphogenesis and cell growth. Mol. Cell. Biol. 12:1162-1178.
9. Costigan, C., D. Kolodrubetz, and M. Snyder. 1994. NHP6A and NHP6B, which encode HMG1-like proteins, are candidates for downstream components of the yeast SLT2 mitogen-activated protein kinase pathway. Mol. Cell. Biol. 14:2391-2403.
10. Courchesne, W. E., R. Kunisawa, and J. Thorner. 1989. A putative protein kinase overcomes pheromone-induced arrest of cell cycling in S. cerevisiae. Cell 58:1107-1119.
11. Davenport, K. R., M. Sohaskey, Y. Kamada, D. E. Levin, and M. C. Gustin. 1995. A second osmosensing signal transduction pathway in yeast. J. Biol. Chem. 270:30157-30161.
12. Degols, G., K. Shiozaki, and P. Russell. 1996. Activation of the Spc1 stress-activated protein kinase in Schizosaccharomyces pombe. Mol. Cell. Biol. 16:2870-2877.
13. +/ CDC28-related protein kinase required for the transition from mitosis and conjugation. Cell 60:649-664.
14. Errede, B., and D. E. Levin. 1993. A conserved kinase cascade for MAP kinase activation in yeast. Curr. Biol. 5:254-260.
15. Ferrando, A., S. J. Fron, G. Rios, G. R. Fink, and R. Serrano. 1995. Regulation of cation transport in Saccharomyces cerevisiae by the salt tolerance gene HAL3. Mol. Cell. Biol. 15:5470-5481.
16. + T cells. Science 271:1276-1278.
17. 1-arrest of the cell cycle in Saccharomyces cerevisiae. Curr. Genet. 18:395-400.
18. Galcheva-Gargova, Z., B. Derijard, I.-H. Wu, and R. Davis. 1994. An osmosensing signal transduction pathway in mammalian cells. Science 265:806-808.
19. +-ATPase. Mol. Cell. Biol. 15:4103-4114.
20. Gotoh, Y., N. Masuyama, A. Suzuki, N. Ueno, and E. Nishida. 1995. Involvement of the MAP kinase cascade in Xenopus mesoderm induction. EMBO J. 14:2491-2498.
21. Gotoh, Y., E. Nishida, M. Shimanuki, T. Toda, V. Imai, and M. Yamamoto. 1993. Schizosaccharomyces pombe Spk1 is a tyrosine-phosphorylated protein functionally related to Xenopus mitogen-activated protein kinase. Mol. Cell. Biol. 13:6427-6434.
22. Grimm, C., J. Kohli, J. Murray, and K. Maundrell. 1988. Genetic engineering of Schizosaccharomyces pombe: a system for gene disruption and replacement using the ura4 gene as a selectable marker. Mol. Gen. Genet. 215:81-86.
23. Gutz, H., H. Heslot, U. Leopold, and N. Loprieno. 1974. Schizosaccharomyces pombe, p. 395-446. In R. C. King (ed.), Handbook of genetics. Plenum Press, New York.
24. Han, J., J.-D. Lee, L. Bibbs, and R. J. Ulevitch. 1994. A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Science 265:808-811.
25. Hanks, S. K., A. M. Quinn, and T. Hunter. 1988. The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42-52.
26. Hattori, M., and T. Sakaki. 1986. Dideoxy sequencing method using denatured plasmid templates. Anal. Biochem. 152:232-238.
27. Herskowitz, I. 1995. MAP kinase pathway in yeast: for mating and more. Cell 80:187-197.
28. Inoue, S. B., H. Qadota, M. Arisawa, Y. Anraku, T. Watanabe, and Y. Ohya. Signaling toward yeast 1,2-β-glucan synthesis. Cell Struct. Funct., in press.
29. Irie, K., M. Takase, K. S. Lee, D. E. Levin, H. Araki, K. Matsumoto, and Y. Oshima. 1993. MKK1 and MKK2, which encode Saccharomyces cerevisiae mitogen-activated protein kinase-kinase homologs, function in the pathway mediated by protein kinase C. Mol. Cell. Biol. 13:3076-3083.
30. Ito, H., Y. Fukuda, K. Murata, and A. Kimura. 1983. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153:163-168.
31. Jonak, C., S. Kiegerrl, C. Lloyd, J. Chan, and H. Hirt. 1995. MKK2, a novel alfalfa MAP kinase, specifically complements the yeast MPK1 function. Mol. Gen. Genet. 248:686-694.
32. Kamada, Y., U. S. Jung, J. Piotrowski, and D. E. Levin. 1995. The protein kinase C-activated MAP kinase pathway of Saccharomyces cerevisiae mediates a novel aspect of the heat shock response. Genes Dev. 9:1559-1571.
33. Kamada, Y., H. Qadota, C. P. Python, Y. Anraku, Y. Ohya, and D. E. Levin. 1996. Activation of yeast protein kinase C by Rho1 GTPase. J. Biol. Chem. 271:9193-9196.
34. Kato, T., K. Okazaki, H. Murakami, S. Stettler, P. Fantes, and H. Okayama. 1996. Stress signal, mediated by a Hog1-like MAP kinase, controls sexual development in fission yeast. FEBS Lett. 378:207-212.
35. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head bacteriophage T4. Nature (London) 227:680-685.
36. Lee, K. S., L. K. Hines, and D. E. Levin. 1993. A pair of functionally redundant yeast genes (PPZ1 and PPZ2) encoding type I-related protein phosphatases function within the PKC1-mediated pathway. Mol. Cell. Biol. 13:5843-5853.
37. Lee, K. S., K. Irie, Y. Gotoh, Y. Watanabe, H. Araki, E. Nishida, K. Matsumoto, and D. E. Levin. 1993. A yeast mitogen-activated protein kinase homolog (Mpk1p) mediates signalling by protein kinase C. Mol. Cell. Biol. 13:3067-3075.
38. Lee, K. S., and D. E. Levin. 1992. Dominant mutations in a gene encoding a putative protein kinase (BCK1) bypass the requirement for a Saccharomyces cerevisiae protein kinase C homolog. Mol. Cell. Biol. 12:172-182.
39. +) is important for growth polarity in Schizosaccharomyces pombe. Proc. Natl. Acad. Sci. USA 87:8272-8276.
40. Levin, D. E., B. Bowers, C.-Y. Chen, Y. Kamada, and M. Watanabe. 1994. Dissecting the protein kinase C/MAP kinase signalling pathway of Saccharomyces cerevisiae. Cell. Mol. Biol. Res. 40:229-239.
41. Levin, D. E., and B. Errede. 1995. The proliferation of MAP kinase signalling pathways in yeast. Curr. Biol. 7:197-202.
42. Levin, D. E., F. O. Fields, R. Kunisawa, J. M. Bishop, and J. Thorner. 1990. A candidate protein kinase C gene, PKC1, is required for the S. cerevisiae cell cycle. Cell 62:213-224.
43. + T cells. Science 271:1272-1276.
44. Mandaule, P., R. Axel, and A. M. Myers. 1987. Characterization of two members of the rho gene family from the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 84:779-783.
45. Marshall, C. J. 1995. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80:179-185.
46. Martin, H., J. Arroyo, M. Sánchez, M. Molina, and C. Nombela. 1993. Activity of the yeast MAP kinase homologue Slt2 is critically required for cell integrity. Mol. Gen. Genet. 241:177-184.
47. + is required for alteration of growth polarity and actin localization in fission yeast. EMBO J. 14:3325-3338.
48. Mazur, P., N. Morin, W. Baginsky, M. El-Sherbeini, J. A. Clemas, J. B. Nielsen, and F. Foor. 1995. Differential expression and function of two homologous subunits of yeast 1,3-β-D-glucan synthase. Mol. Cell. Biol. 15: 5671-5681.
49. 2+ -independent protein kinase C from fission yeast. J. Biol. Chem. 268:7401-7406.
50. Millar, J. B. A., V. Buck, and M. G. Wilkinson. 1995. Pyp1 and Pyp2 PTPases dephosphorylate an osmosensing MAP kinase controlling cell size at division in fission yeast. Genes Dev. 9:2117-2130.
51. Mizoguchi, T., N. Hayashida, K. Yamaguchi-Shinozaki, H. Kamada, and K. Shinozaki. 1993. ATMPKs: a gene family of plant MAP kinases in Arabidopsis thaliana. FEBS Lett. 336:440-444.
52. Mizukami, T., W. I. Chang, I. Garkavtsev, N. Kaplan, D. Lombardi, T. Matsumoto, O. Niwa, A. Kounosu, M. Yanagida, T. G. Marr, and D. Beach. 1993. A 13kb resolution cosmid map of the 14 Mb fission yeast genome by nonrandom sequence-tagged site mapping. Cell 73:121-132.
53. Moreno, S., A. Klar, and P. Nurse. 1991. Molecular genetic analyses of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194:773-782.
54. Morishita, T., H. Mitsuzawa, M. Nakafuku, S. Nakamura, S. Haltori, and Y. Anraku. 1995. Requirement of Saccharomyces cerevisiae Ras for completion of mitosis. Science 270:1213-1215.
55. Navarro-García, F., M. Sánchez, J. Pla, and C. Nombela. 1995. Functional characterization of the MKC1 gene of Candida albicans, which encodes a mitogen-activated protein kinase homolog related to cell integrity. Mol. Cell. Biol. 15:2197-2206.
56. Nielsen, O. 1993. Signal transduction during mating and meiosis in S. pombe. Trends Cell Biol. 3:60-65.
57. Nieman, A. M., B. J. Stevenson, H.-P. Xu, G. F. Sprague, Jr., I. Herskowitz, M. Wigler, and S. Marcus. 1993. Functional homology of protein kinases required for sexual differentiation in Schizosaccharomyces pombe and Saccharomyces cerevisiae suggests a conserved signal transduction module in eukaryotic organisms. Mol. Biol. Cell 4:107-120.
58. Niman, H. L., R. A. Houghten, L. E. Walker, R. A. Reisfeld, I. A. Wilson, J. M. Holge, and R. A. Lerner. 1983. Generation of protein-reactive anti-bodies by short peptides is an event of high frequency: implications for the structural basis of immune recognition. Proc. Natl. Acad. Sci. USA 80:4949-4953.
59. Nishida, E., and Y. Gotoh. 1993. The MAP kinase cascade is essential for diverse signal transduction pathways. EMBO J. 18:128-131.
60. Nonaka, H., K. Tanaka, H. Hirano, T. Fujiwara, H. Kohno, M. Umikawa, A. Mino, and Y. Takai. 1995. A downstream target of RHO1 small GTP-binding protein is PKC1, a homolog of protein kinase C, which leads to activation of the MAP kinasc cascade in Saccharomyces cerevisiae. EMBO J. 14:5931-5938.
61. Nurse, P. 1990. Universal control mechanism regulating onset of M-phase. Nature (London) 344:503-508.
62. Paravicini, G., M. Cooper, L. Friedli, D. J. Smith, J.-L. Carpentier, L. S. Klig, and M. A. Payton. 1992. The osmotic integrity of the yeast cell requires a functional PKC1 gene product. Mol. Cell. Biol. 12:4896-4905.
63. Prabhala, G., G. H. Rosenberg, and N. F. Kaufer. 1992. Architectural features of pre-mRNA introns in the fission yeast Schizosaccharomyces pombe. Yeast 8:171-182.
64. Roemer, T., G. Paravicine, M. A. Payton, and H. Bussey. 1994. Characterization of the yeast (1-6)-β-glucan biosynthetic components, Kre6p and Skn1p, and genetic interactions between the PKC1 pathway and extracellular matrix assembly. J. Cell Biol. 127:567-579.
65. Rosenberg, A. H., B. N. Lade, D.-S. Chui, S.-W. Lin, J. J. Dunn, and F. W. Studier. 1987. Vectors for selective expression of cloned DNAs by T7 RNA polymerase. Gene 56:125-135.
66. Rothstein, R. J. 1983. One-step gene disruption in yeast. Methods Enzymol. 101:202-211.
67. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. 2nd ed. Cold Spring Harbor Laboratory. Cold Spring Harbor, N.Y.
68. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
69. Shimizu, J., K. Yoda, and M. Yamasaki. 1994. The hypo-osmolarity-sensitive phenotype of the Saccharomyces cerevisiae hpo2 mutant is due to a mutation in PKC1, which regulates expression of β-glucanase. Mol. Gen. Genet. 242: 641-648.
70. Shiozaki, K., and P. Russell. 1995. Cell-cycle control linked to extracellular environment by MAP kinase pathway in fission yeast. Nature (London) 378:739-743.
71. Shiozaki, K., and P. Russell. 1995. Counteractive roles of protein phosphatase 2C (PP2C) and a MAP kinase kinase homolog in the osmoregulation of fission yeast. EMBO J. 14:492-502.
72. Shiozaki, K., and P. Russell. 1996. Conjugation, meiosis, and the osmotic stress response are regulated by Spc1 kinase through Atf1 transcription factor in fission yeast. Genes Dev. 10:2276-2288.
73. Streiblová, E., and A. Wolf. 1963. Cell wall growth during the cell cycle of Schizosaccharomyces pombe. Z. Allg. Mikrobiol. 12:673-684.
74. Studier, F. W., and B. A. Moffatt. 1986. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189:113-130.
75. Sugiura, R., H. Shuntoh, T. Toda, M. Yanagida, and T. Kuno. Unpublished results.
76. ++ dependent protein kinase. Biochem. Biophys. Res. Commun. 135:397-402.
77. Toda, T., S. Dhut, J. Millar, R. Sugiura, and T. Kuno. Unpublished results.
78. Toda, T., and M. A. N. Hajibagheri. Unpublished results.
79. + is required for establishment of growth polarity and functionally interacts with protein kinase C and an osmosensing MAP-kinase pathway. J. Cell Sci. 109:2331-2342.
80. Toda, T., M. Shimanuki, and M. Yanagida. 1991. The fission yeast genes that confer resistance to staurosporine encode an AP-1-like factor and a protein kinase related to the mammalian ERK1/MAP2 and budding yeast FUS3 and KSS1 kinases. Genes Dev. 5:60-73.
81. Toda, T., M. Shimanuki, and M. Yanagida. 1993. Two novel protein kinase C-related genes of fission yeast are essential for cell viability and implicated in cell shape control. EMBO J. 12:1987-1995.
82. Toda, T., I. Uno, T. Ishikawa, S. Powers, T. Kataoka, D. Broek, S. Cameron, J. Broach, K. Matsumoto, and M. Wigler. 1985. In yeast. Ras proteins are controlling elements of adenylate cyclase. Cell 40:27-36.
83. Torres, L., H. Martin, M. R. Garcia-Saez, J. Arroyo, M. Molina, M. Sanchez, and C. Nombela. 1991. A protein kinase gene complements the lytic phenotype of Saccharomyces cerevisiae lyt2 mutants. Mol. Microbiol. 5:2845-2854.
84. 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. USA 76:4350-4354.
85. Treisman, R. 1996. Regulation of transcription by MAP kinase cascades. Curr. Opin. Cell Biol. 8:205-215.
86. Umbhauer, M., C. J. Marshall, C. S. Mason, R. W. Osl, and J. C. Smith. 1995. Mesoderm induction in Xenopus caused by activation of MAP kinase. Nature (London) 376:58-62.
87. Vieira, J., and J. Messing. 1982. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene 19:259-268.
88. Warbrick, E., and P. Fantes. 1991. The Wis1 protein kinase is a dose-dependent regulator of mitosis in Schizosaccharomyces pombe. EMBO J. 10:4291-4299.
89. Watanabe, Y., K. Irie, and K. Matsumoto. 1995. Yeast RLM1 encodes a serum response factor-like protein that may function downstream of the Mpk1 (Slt2) mitogen-activated protein kinase pathway. Mol. Cell. Biol. 15: 5740-5749.
90. White, M. A., C. Nicolette, A. Minden, A. Polverino, L. Van Aelst, M. Karin, and M. Wigler. 1995. Multiple Ras functions can contribute to mammalian cell transformation. Cell 80:533-541.
91. Wilkinson, M. G., M. Samuels, T. Takeda, W. M. Toonen, J.-C. Shieh, T. Toda, J. B. A. Millar, and N. Jones. 1996. The Atf1 transcription factor is a target for the Sty1 stress-activated MAP kinase pathway in fission yeast. Genes Dev. 10:2289-2301.
92. Wilson, I. A., H. L. Niman, R. A. Houghten, A. R. Cherenson, M. L. Connelly, and R. A. Lerner. 1984. The structure of an antigenic determinant in a protein. Cell 37:767-778.
93. Xia, Z., M. Dickens, J. Raingeaud, R. J. Davis, and M. E. Greenberg. 1995. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270:1326-1331.
94. Yashar, B., K, Irie, J. A. Printen, B. J. Stevenson, G. F. Sprague, Jr., K. Matsumoto, and B. Errede. 1995. Yeast MEK-dependent signal transduction: response thresholds and parameters affecting fidelity. Mol. Cell. Biol. 15:6545-6553.
95. Yoshida, S., E. Ikeda, I. Uno, and H. Mitsuzawa. 1992. Characterization of a staurosporine- and temperature-sensitive mutant, stt1, of Saccharomyces cerevisiae: STT1 is allelic to PKC1. Mol. Gen. Genet. 231:337-344.
96. Yoshida, S., Y. Ohya, A. Nakano, and Y. Anraku. 1994. Genetic interactions among genes involved in the STT4-PKC1 pathway of Saccharomyces cerevisiae. Mol. Gen. Genet. 242:631-640.
97. Yoshida, T., T. Toda, and M. Yanagida. 1994. A calcineurin-like gene ppb1 in fission yeast: mutant defects in cytokinesis, cell polarity, mating and spindle pole body positioning. J. Cell Sci. 107:1725-1735.
98. Zarzov, P., C. Mazioni, and C. Mann. 1996. The SLT2 (MPK1) MAP kinase is activated during periods of polarized cell growth in yeast. EMBO J. 15:83-91.