Functional homology of protein kinases required for sexual differentiation in Schizosaccharomyces pombe and Saccharomyces cerevisiae suggests a … (original) (raw)
1993, Molecular biology of …
Abstract
We present genetic evidence that three presumptive protein kinases of Schizosaccharomyces pombe, byr2, byrl, and spkl that are structurally related to protein kinases of Saccharomyces cerevisiae, STE11, STE7, and FUS3, respectively, are also functionally related. In some cases, introduction of the heterologous protein kinase into a mutant was sufficient for complementation. In other cases (as in a stellmutant of S. cerevisiae), expression of two S. pombe protein kinases (byr2 and byrl) was required to observe complementation, suggesting that byr2 and byrl act cooperatively. Complementation in S. pombe mutants is observed as restoration of sporulation and conjugation and in S. cerevisiae as restoration of conjugation, pheromone-induced cell cycle arrest, and pheromone-induced transcription of the FUSI gene. We also show that the S. pombe kinases bear a similar relationship to the mating pheromone receptor apparatus as do their S. cerevisiae counterparts. Our results indicate that pheromone-induced signal transduction employs a conserved set of kinases in these two evolutionarily distant yeasts despite an apparently significant difference in function of the heterotrimeric G proteins. We suggest that the STE11/byr2, STE7/byrl, and FUS3/spkl kinases comprise a signal transduction module that may be conserved in higher eukaryotes. Consistent with this hypothesis, we show that a mammalian mitogenactivated protein (MAP) kinase, ERK2, can partially replace spkl function in S. pombe. Laboratory collection AN40-5A MATa his4-519 ura3-52 leu2 trpl ste7A2 stellAl This study AN42-2A MATa his4-519 ura3-52 leu2 trpl fus3::URA3 kssl::URA3 This study AN37-4C-S MATa ura3-52 leu2 trpl ade2 metl HMLa HMRa barl-i Laboratory collection AN1015 MATa ura3-52 leu2 trpl ade2 metl HMLa HMRa barl-I fus3::URA3 This study AN1016 MATa his4-519 ura3-52 leu2 trpl stellAl FUSI::lacZ (LEU2) This study 5815-7-1 MATca ura3 his3 hopl-1
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References (72)
- Ballester, R., Michaeli, T., Ferguson, K., Xu, H.-P., McCormick, F., and Wigler, M. (1989). Genetic analysis of mammalian GAP expressed in yeast. Cell 59, 681-686.
- Boulton, T.G., Gregory, J.S., Jong, S.-M., Wang, L.-H., Ellis, L., and Cobb, M.H. (1990a). Evidence for insulin-dependent activation of S6 and microtubule-associated protein-2 kinases via a human insulin receptor/v-ros hybrid. J. Biol. Chem. 265, 2713-2719.
- Boulton, T.G., Nye, S.H., Robbins, D.J., Ip, N.Y., Radziejewska, E., Morgenbesser, S.D., DePinho, R.A., Panayotatos, N., Cobb, M.H., and Yancopoulos, G.D. (1991). ERKs: a family of protein-serine/thre- onine kinases that are activated and tyrosine phosphorylated in re- sponse to insulin and NGF. Cell 65, 663-675.
- Boulton, T.G., Yancopoulos, G.D., Gregory, J.S., Slaughter, C., Moomaw, C., Hsu, J., and Cobb, M.H. (1990b). An insulin-stimulated protein kinase similar to yeast kinases involved in cell cycle control. Science 249, 64-67.
- Burkholder, A.C., and Hartwell, L.H. (1985). The yeast a-factor rector: structural properties deduced from the sequence of the STE2 gene. Nucleic Acids Res. 13, 8463-8475.
- Chaleff, D.T., and Tatchell, K. (1985). Molecular cloning and char- acterization of the STE7 and STEll genes of Saccharomyces cerevisiae. Mol. Cell. Biol. 5, 1878-1886.
- Courchesne, W.E., Kunisawa, R., and Thomer, J. (1989). A putative protein kinase overcomes pheromone-induced arrest of cell cycling in S. cerevisiae. Cell 58, 1107-1119.
- Crews, C.M., and Erikson, R.L. (1992). Purification of a murine protein- tyrosine/threonine kinase that phosphorylates and activates the ERK- 1 gene product: relationship to the fission yeast byrl gene product. Proc. Natl. Acad. Sci. USA 89, 8205-8209.
- Cross, F. (1988). Conjugation in Saccharomyces cerevisiae. Ann. Rev. Cell Biol. 4, 429-457.
- Davey, J. (1991). Isolation and quantitation of M-factor, a diffusible mating factor from the fission yeast Schizosaccharomyces pombe. Yeast 7, 357-366.
- Davey, J. (1992). Mating pheromones of the fission yeast Schizosac- charomyces pombe: purification and structural characterization of M- factor and isolation and analysis of two genes encoding the phero- mone. EMBO J. 11, 951-960.
- Deshpande, A.K., and Kung, H.F. (1987). Insulin induction of Xenopus laevis oocyte maturation is inhibited by monoclonal antibody against p12 ras proteins. Mol. Cell. Biol. 7, 1285-1288.
- Devereux, J., Haeberli, P., and Smithies, 0. (1984). A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids. Res. 12, 387-395.
- Dietzel, C., and Kurjan, J. (1987). The yeast SCG1 gene: A Ga-like protein implicated in the a-and a-factor response pathway. Cell 50, 1001-1010.
- Egel, R., Nielsen, O., and Weilguny, D. (1990). Sexual differentiation in fission yeast. Trends Genet. 6, 369-373.
- Elion, E.A., Grisafi, P.L., and Fink, G.R. (1990). FUS3 encodes a cdc2+/ CDC28-related kinase required for the transition from mitosis into conjugation. Cell 60, 649-664.
- Elion, E.A., Brill, J., and Fink, G.R. (1991). FUS3 represses CLN1 and CLN2 and in concert with KSS1 promotes signal transduction. Proc. Natl. Acad. Sci. USA 88, 9392-9396.
- Evan, G.I., Lewis, G.K., Ramsey, G., and Bishop, J.M. (1985). Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5, 3610-3616.
- Feig, L.A., and Cooper, G.M. (1988). Inhibition of NIH 3T3 cell pro- liferation by a mutant ras protein with preferential affinity for GDP. Mol. Cell. Biol. 8, 3235-3243.
- Field, J., Nikawa, J.-I., Broek, D., MacDonald, B., Rodgers, L., Wilson, I.A., Lerner, R.A., and Wigler, M.W. (1988). Purification of a RAS- responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method. Mol. Cell. Biol. 8, 2159-2165.
- Fields, S., and Song, 0. (1989). A novel genetic system to detect pro- tein-protein interactions. Nature 340, 245-246.
- Friedmann, K.L., and Egel, R. (1978). Protein patterns during spor- ulation in fission yeast. Z. Naturforsch. 33c, 84-91.
- Fukui, Y., Kaziro, Y., and Yamamoto, M. (1986a). Mating pheromone- like diffusible factor released by Schizosaccharomyces pombe. EMBO J. 5, 1991-1993.
- Fukui, Y., Kozasa, T., Kaziro, Y., Takeda, T., and Yamamoto, M. (1986b). Role of a ras homolog in the life cycle of Schizosaccharomyces pombe. Cell 44, 329-336.
- Gartner, A., Nasmyth, K., and Ammerer, G. (1992). Signal transduction in Saccharomyces cerevisiae requires tyrosine and threonine phos- phorylation of FUS3 and KSS1. Genes Dev. 6, 1280-1292.
- Hagen, D.C., McCaffrey, G., and Sprague, G.F., Jr. (1986). Evidence the yeast STE3 gene encodes a receptor for the peptide pheromone a-factor: gene sequence and implications for the structure of the pre- sumed receptor. Proc. Natl. Acad. Sci. USA 83, 1418-1422.
- Hicks, J.B., and Herskowitz, I. (1976). Interconversion of yeast mating types I. Direct observation of the action of the homothallism (HO) gene. Genetics 83, 245-258.
- Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K., and Pease, L.R. (1989). Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59.
- Hoshi, M., Nishida, E., and Sakai, H. (1988). Activation of a Ca21_ inhibitable protein kinase that phosphorylates microtubule-associated protein 2 in vivo by growth factors, phorbol esters, and serum in quiescent cultured human fibroblasts. J. Biol. Chem. 263, 5396-5401.
- Ito, H., Fukuda, Y., Murata, K., and Kimura, A. (1983). Transformation of intact yeast cells treated with alkali. J. Bacteriol. 153, 163-168. Molecular Biology of the Cell
- Jahng, K.-Y., Ferguson, J., and Reed, S.I. (1988). Mutations in a gene encoding the a subunit of a Saccharomyces cerevisiae G protein indicate a role in mating pheromone signaling. Mol. Cell. Biol. 8, 2484-2493.
- Jones, S.J., and Prakash, L. (1990). Yeast Saccharomyces cerevisiae se- lectable markers in pUC18 polylinkers. Yeast 6, 363-366.
- Kelly, M., Burke, J., Smith, M., Klar, A., and Beach, D. (1988). Four mating-type genes control sexual differentiation in the fission yeast. EMBO J. 7, 1537-1547.
- Kitamura, K., and Shimoda, C. (1991). The Schizosaccharomyces pombe mam2 gene encodes a putative pheromone receptor which has a sig- nificant homology with the Saccharomyces cerevisiae Ste2 protein. EMBO J. 12, 3743-375 1.
- Korn, L.J., Siebel, C.N., McCormick, F., and Roth, R.A. (1987). Ras p21 as a potential mediator of insulin action in Xenopus oocytes. Science 236, 840-843.
- Kosako, H., Gotoh, Y., Matsuda, S., Ishikawa, M., and Nishida, E. (1992). Xenopus MAP kinase activator is a serine/threonine/tyrosine kinase activated by threonine phosphorylation. EMBO J. 11, 2903- 2908.
- Leupold, U. (1987). Sex appeal in fission yeast. Curr. Genet. 12, 543- 545. Leupold, U., Nielsen, O., and Egel, R. (1989). Pheromone induced meiosis in P-specific mutants of fission yeast. Current Genet. 15, 403- 405.
- Lund, P.M., Hasegawa, Y., Kitamura, K., Shimoda, C., Fukui, Y., and Yamamoto, M. (1987). Mapping of the rasl gene of Schizosaccharo- myces pombe. Mol. Gen. Genet. 209, 627-629.
- Marsh, L., Neiman, A.M., and Herkowitz, I. (1991). Signal transduction during pheromone response in yeast. Annu. Rev. Cell Biol. 7, 699- 728. McCaffrey, G., Clay, F., Kelsey, K., and Sprague, G.F., Jr. (1987). Identification and regulation of a gene required for cell fusion during mating of the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 7, 2680- 2690.
- McLeod, M., Stein, M., and Beach, D. (1987). The product of the mei3+ gene expressed under control of the mating-type locus induces meiosis and sporulation in fission yeast. EMBO J. 6, 729-736.
- Miyajima, I., Nakafuku, M., Nakayama, N., Brenner, C., Miyajima, A., Kaibuchi, K., Arai, K., Kaziro, Y., and Matsumoto, K. (1987). GPA1, a haploid-specific essential gene, encodes a yeast homolog of mam- malian G protein which may be involved in the mating factor-mediated signal transduction pathway. Cell 50, 1011-1019.
- Mortimer, R.K., and Hawthorne, D.C. (1969). Yeast genetics. In: The Yeasts, ed. A.H. Rose, and J.S. Harrison, New York: Academic, 385- 460. Nadin-Davis, S.A., and Nasim, A. (1988). A gene which encodes a predicted protein kinase can restore some functions of the ras gene in fission yeast. EMBO J. 7, 985-993.
- Nadin-Davis, S.A., and Nasim, A. (1990). Schizosaccharomyces pombe rasl and byrl are functionally related genes of the ste family that affect starvation-induced transcription of mating-type genes. Mol. Cell. Biol. 10, 549-560.
- Nadin-Davis, S.A., Nasim, A., and Beach, D. (1986). Involvement of ras in sexual differentiation but not in growth control in fission yeast. EMBO J. 5, 2963-2971.
- Nakayama, N., Miyajima, A., and Arai, K. (1985). Nucleotide se- quences of STE2 and STE3, cell type-specific sterile genes from Sac- charomyces cerevisiae. EMBO J. 4, 2643-2648.
- Needleman, S.B., and Wunsch, C.D. (1970). A general method ap- plicable to the search for similarities in the amino acid sequences of two proteins. J. Mol. Biol. 48, 443-453.
- Neiman, A.M., Chang, F., Komachi, K., and Herskowitz, I. (1990). CDC36 and CDC39 are negative elements in the signal transduction pathway of yeast. Cell Regul. 1, 391-401.
- Nielson, O., Davey, J., and Egel, R. (1992). The rasl function of Schizosaccharomyces pombe mediates pheromone-induced transcription. EMBO J. 11, 1391-1395.
- Obara, T., Nakafuku, M., Yamamoto, M., and Kaziro, Y. (1991). Iso- lation and characterization of a gene encoding a G-protein a subunit from Schizosaccharomyces pombe: Involvement in mating and sporu- lation pathways. Proc. Natl. Acad. Sci. USA 88, 5877-5881.
- Ray, L.B., and Sturgill, T.W. (1987). Rapid stimulation by insulin of a serine/threonine kinase in 3T3-L1 adipocytes that phosphorylates microtubule-associated protein 2 in vivo. Proc. Natl. Acad. Sci. USA 84, 1502-1506.
- Ray, L.B., and Sturgill, T.W. (1988). Insulin-stimulated microtubule- associated protein kinase is phosphorylated on tyrosine and threonine in vivo. Proc. Natl. Acad. Sci. USA 85, 3753-3757.
- Rhodes, N., Connell, L., and Errede, B. (1990). STEl1 is a protein kinase required for cell-type-specific transcription and signal trans- duction in yeast. Genes Dev. 4, 1862-1874.
- Rose, M.D., Winston, F., and Hieter, P. (1990). Methods in Yeast Genetics: A Laboratory Course Manual. Cold Spring Harbor NY: Cold Spring Harbor Press.
- Rothstein, R. (1983). One-step gene disruption in yeast. Methods En- zymol. 101, 202-209.
- Rubin, G.M. (1991). Signal transduction and the fate of the R7 pho- toreceptor in Drosophila. Trends Genet. 7, 372-377.
- Sanger, F., Nicklen, S., and Coulson, A.R. (1977). DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74, 5463- 5467.
- Shimoda, C., Uehira, M., Kishida, M., Fujioka, H., Iino, Y., Watanabe, Y., and Yamamoto, M. (1987). Cloning and analysis of transcription of the mei2 gene responsible for initiation of meiosis in the fission yeast Schizosaccharomyces pombe. J. Bacteriol. 169, 93-96.
- Smith, M.R., DeGudicibus, S.J., and Stacey, D.W. (1986). Requirement for c-ras proteins during viral oncogene transformation. Nature 320, 540-543.
- Stern, M., Jensen, R., and Herskowitz, I. (1984). Five SWI genes are required for expression of the HO gene in yeast. J. Mol. Biol. 178, 853-868.
- Stemnberg, P.W., and Horvitz, R.H. (1991). Signal transduction during C. elegans vulval induction. Trends Genet. 7, 366-371.
- Stevenson, B.J., Rhodes, N., Errede, B., and Sprague, G.F., Jr. (1992). Constitutive mutants of the protein kinase STEl1 activate the yeast pheromone response pathway in the absence of the G protein. Genes Dev. 6, 1293-1304.
- Stotz, A., and Linder, P. (1990). The ADE2 gene from Saccharomyces cerevisiae: sequence and new vectors. Gene 95, 91-98.
- Sugimoto, A., lino, Y., Maeda, T., Watanabe, Y., and Yamamoto, M. (1991). Schizosaccharomyces pombe stell+ encodes a transcription factor with an HMG motif that is a critical regulator of sexual development. Genes Dev. 5, 1990-1999.
- Teague, M.A., Chaleff, D.T., and Errede, B. (1986). Nucleotide se- quence of the yeast regulatory gene STE7 predicts a protein homol- ogous to protein kinases. Proc. Natl. Acad. Sci. USA 83, 7371-7375.
- Thomas, G. (1992). MAP kinase by any other name smells just as sweet. Cell 68, 3-6.
- Thomas, S.M., DeMarco, M., D'Arcangelo, G., Halegoua, S., and Brugge, J.S. (1992). Ras is essential for nerve growth factor-and phor- bol ester-induced tyrosine phosphorylation of MAP kinases. Cell 68, 1031-1040.
- Toda, T., Shimanuki, M., and Yanagida, M. (1991). Fission yeast genes that confer resistance to staurosporine encode an AP-1 -like transcrip- tion factor and a protein kinase related to the mammalian ERK1/ MAP2 and budding yeast FUS3 and KSS1 kinases. Genes Dev. 5, 60- 73. Trueheart, J., Boeke, J.D., and Fink, G.R. (1987). Two genes required for cell fusion during yeast conjugation: evidence for a pheromone- induced surface protein. Mol. Cell. Biol. 7, 2316-2328.
- Wang, Y., Xu, H.-P., Riggs, M., Rodgers, L., and Wigler, M. (1991). byr2, a Schizosaccharomyces pombe gene encoding a protein kinase capable of partial suppression of the rasl mutant phenotype. Mol. Cell. Biol. 11, 3554-3563.
- Whiteway, M., Hougan, L., Dignard, D., Thomas, D.Y., Bell, L., Saari, G.C., Grant, F.J., O'Hare, P., and MacKay, V.L. (1989). The STE4 and STE18 genes of yeast encode potential ,B and y subunits of the mating factor receptor-coupled G protein. Cell 56, 467-477.
- Wood, K.W., Samecki, C., Roberts, T.M., and Blenis, J. (1992). Ras mediates nerve growth factor receptor modulation of three signal- transducing protein kinases: MAP kinase, Raf-1, and RSK. Cell 68, 1041-1050.
- Xu, H.-P., Jung, V., Riggs, M., Rodgers, L., and Wigler, M. (1992). A gene encoding a protein with seven zinc finger domains acts on the sexual differentiation pathways of Schizosaccharomyces pombe. Mol. Biol. Cell 3, 721-734.
- Xu, H.-P., Wang, Y., Riggs, M., Rodgers, L., and Wigler, M. (1990). Biological activity of the mammalian RAP genes in Yeast. Cell Regul. 1, 763-769.