Fission yeast α-glucan synthase Mok1 requires the actin cytoskeleton to localize the sites of growth and plays an essential role in cell morphogenesis downstream of protein kinase C function

Journal of Cell Biology

Volumn 144, Issue 6, 1999, Pages 1173-1186

  Katayama, Satoshi ^a   Hirata, Dai ^a,c   Arellano, Manuel ^b   Pérez, Pilar ^b   Toda, Takashi ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b UNIVERSITY OF SALAMANCA   (Spain)

^c HIROSHIMA UNIVERSITY   (Japan)

Author keywords

Actin; Fission yeast; Morphogenesis; Protein kinase C; glucan synthase

Indexed keywords

ACTIN; GLUCAN SYNTHASE; PROTEIN KINASE C;

ACTIN FILAMENT; ARTICLE; ENZYME ACTIVITY; IMMUNOFLUORESCENCE; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN LOCALIZATION; YEAST;

SCHIZOSACCHAROMYCES POMBE;

EID: 0033594101     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.144.6.1173     Document Type: Article

References (51)

1. Amano, M., H. Mukai, Y. Ono, K. Chihara, T. Matsui, Y. Hamajima, K. Okawa, A. Iwamatsu, and K. Kaibuchi. 1996. Identification of a putative target for Rho as the serine-threonine kinase protein kinase N. Science. 271: 648-650.
2. Arellano, M., A. Durán, and P. Pérez. 1996. Rho1 GTPase activates the (1-3)β-D-glucan synthase and is involved in Schizosaccharomyces pombe morphogenesis. EMBO (Eur. Mol. Biol. Organ.) J. 15:4584-4591.
3. Arellano, M., A. Duran, and P. Pérez. 1997. Localisation of the Schizosaccharomyces pombe rho1p GTPase and its involvement in the organisation of the actin cytoskeleton. J. Cell Sci. 110:2547-2555.
4. Ayscough, K.R., J. Stryker, N. Pokala, M. Sanders, P. Crews, and D.G. Drubin. 1997. High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor latrunculin-A. J. Cell Biol. 137:399-416.
5. Bähler, J., J. Wu, M.S. Longtine, N.G. Shah, A. McKenzie III, A.B. Steever, A. Wach, P. Philippsen, and J.R. Pringle. 1998. Heterologous modules for efficient and versatile PCR-hased gene targeting in Schizosaccharomyces pombe. Yeast. 14:943-951.
6. Balasubramanian, M.K., D.M. Helfman, and S.M. Hemmingsen. 1992. A new tropomyosin essential for cytokinesis in the fission yeast S. pombe. Nature. 360:84-87.
7. - gene encodes a profilin essential for cytokinesis. J. Cell Biol. 125:1289-1301.
8. Cabib, E., T. Drgon, J. Drgonová, R.A. Ford, and R. Kollár. 1997. The yeast cell wall, a dynamic structure engaged in growth and morphogenesis. Biochem. Soc. Trans. 1:200-204.
9. Drgonová, J., T. Drgon, K. Tanaka, R. Kollár, G.-C. Chen, R.A. Ford, C.S.M. Chan, Y. Takai, and E. Cabib. 1996. Rho1p, a yeast protein at the interface between cell polarization and morphogenesis. Science. 272:277-279.
10. Drubin, D.G., and W.J. Nelson. 1996. Origins of cell polarity. Cell. 84:335-344.
11. Flynn, P., H. Mellor, R. Palmer, G. Panayotou, and P.J. Parker. 1998. Multiple interactions of PRK1 with RhoA. functional assignment of the HR1 motif. J. Biol. Chem. 273:2698-2705.
12. Furukawa, K., M. Tagaya, K. Tanizawa, and T. Fukui. 1993. Role of the conserved Lys-X-Gly-Gly sequence at the ADP-glucose-binding site in Escherichia coli glycogen synthase. J. Biol. Chem. 268:23837-23842.
13. Hall, A. 1998. Rho GTPases and the actin cytoskeleton. Science. 279:509-514.
14. Henrissat, B., and G. Davies. 1997. Structural and sequence-based classification ol glycoside hydrolases. Curr. Opin. Struct. Biol. 7:637-644.
15. Hochstenbach, F., F.M. Klis, H. van den Ende, E. van Donselaar, P.J. Peters, and R.D. Klausner. 1998. Identification of a putative alpha-glucan synthase essential for cell wall construction and morphogenesis in fission yeast. Proc. Natl. Acad. Sci. USA. 95:9161-9166.
16. Ishiguro, J. 1998. Genetic control of fission yeast cell wall synthesis: the genes involved in wall biogenesis and their interactions in Schizosaccharomyces pombe. Genes Genet. Syst. 73:181-191.
17. +, a Schizosaccharomyces pombe gene homolog of Saccharomyces cerevisiae FKS genes whose mutation confers hypersensitivity to cyclosporin A and papulocandin B. J. Bacteriol. 179:7653-7662.
18. Jochová, J., I. Rupes, and E. Streiblová. 1991. F-actin contractile rings in protoplasts of the yeast Schizosaccharomyes pombe. Cell Biol. Int. Rep. 15:607-610.
19. Kaiser, C.A., R.H. Gimeno, and D.A. Shaywitz. 1997. Protein secretion, membrane biogenesis, and endocytosis. In The Molecular and Cellular Biology of the Yeast Saccharomyces. Vol. 3. J.R. Pringle, J.R. Broach, and E.W. Jones, editors. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 91-227.
20. Kitayama, C., A. Sugimoto, and M. Yamamoto. 1997. Type II myosin heavy chain encoded by the myo2 gene composes the contractile ring during cytokinesis in Schizosaccharomyes pombe. J. Cell Biol. 137:1309-1319.
21. Kobori, H., T. Toda, H. Yaguchi, M. Toya, M. Yanagida, and M. Osumi. 1994. Fission yeast protein kinase C homologues are required for protoplast regeneration: a functional link between cell wall formation and cell shape control. J Cell Sci. 107:1131-1136.
22. Kopecká, M., G.H. Fleet, and H.J. Phaff. 1995. Ultrastructure of the cell wall of Schizosaccharomyces pombe following treatment with various glucanases. J. Struct. Biol. 114:140-152.
23. Kumar, A., C.E. Larsen, and J. Preiss. 1986. Biosynthesis of bacterial glycogen. primary structure of Escherichia coli ADP-glucose: alpha-1.4-glucan. 4-glucosyltransferase as deduced from the nucleotide sequence of the glgA gene. J. Biol. Chem. 261:16256-16259.
24. Kyte, J., and R.F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
25. Levin, D.E., and E. Bartrett-Heubusch. 1992. Mutants in the S. cerevisiae PKC1 gene display a cell cycle-specific osmotic stability defect. J. Cell Biol. 116: 1079-1088.
26. Manners, D.J., and M.T. Meyer. 1977. The molecular structure of some glucans from the cell wall of Schizosaccharomyces prombe. Carbohydr. Res. 57:189-203.
27. Marks, M., and J.S. Hyams. 1985. Localization of F-actin through the cell division cycle of Schizosaccharomyces pombe. Eur. J. Cell Biol. 39:27-32.
28. Marks, J., I.M. Hagan, and J.S. Hyams. 1986. Growth polarity and cytokinesis in fission yeast: the role of the cytoskeleton. J. Cell Sci. Suppl. 5:229-241.
29. Maundrell, K. 1990. nmt1 of fission yeast. J. Biol. Chem. 265:10857-10864.
30. Mitchison, J.M., and P. Nurse. 1985. Growth in cell length in the fission yeast Schizosaccharomyces pombe. J. Cell Sci. 75:357-376.
31. Moreno, S., A. Klar, and P. Nurse. 1991. Molecular genetic analyses of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194:773-782.
32. Mulholland, J., D. Preuss, A. Moon, A. Wong, D. Drubin, and D. Botstein. 1994. Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane. J. Cell Biol. 125:381-391.
33. Nakano, K., R, Arai, and I. Mabuchi. 1997. The small GTP-binding protein Rho1 is a multifunctional protein that regulates aetin localization, cell polarity, and septum formation in the fission yeast Schizosaccharomyces pombe. Genes Cells. 2:679-694.
34. Nonaka, H., K. Tanaka, H. Hirano, T. Fujiwara, H. Kohno, M. Umikawa, A. Mino, and Y. Takai, 1995. A downstream target of RHOI small GTP-binding protein is PKC1, a homolog of protein kinase C, which leads to activation of the MAP kinase cascade in Saccharomyces cerevisiae. EMBO (Eur. Mol. Biol. Organ.) J. 14:5931-5938.
35. Nurse. P. 1994. Fission yeast morphogenesis-posing the problems. Mol. Biol. Cell. 5:613-616.
36. Orlean, P. 1997. Biogenesis of yeast wall and surface components. In The Molecular and Cellular Biology of the Yeast Saccharomyces. Vol. 3. J.R. Pringle, J.R. Broach, and E.W. Jones, editors. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 229-362.
37. Pruyne, D.W., D.H. Schott, and A. Bretscher. 1998. Tropomyosin-containing actin cables direct the Myo2p-dependent polarized delivery of secretory vesicles in budding yeast. J. Cell Biol. 143:1931-1945.
38. Qadota, H., C.P. Python, S.B. Inoue, M. Arisawa, Y. Anraku, Y. Zheng, T. Watanabe, D.E. Levin, and Y. Ohya. 1996. Identification of yeast Rho1p GTP-ase as a regulatory subunit of 1.3-β-glucan synthetase. Science. 272:279-281.
39. Ridley, A.J. 1996. Rho: theme and variations. Curr. Biol. 6:1256-1264.
40. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, NY. 545 pp.
41. Sanger, F., S. Nicklen, and A.R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA. 74:5463-5467.
42. 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 (Eur. Mol. Biol. Organ.) J. 14:492-502.
43. Spector, I., N. Shochet, D. Blasberger, and Y. Karshaman. 1989. Latrunculins-novel marine macrilides that disrupt microfilament organization and affect cell growth: 1. comparison with cytochalasin D. Cell Motil. Cytoskeleton. 13: 127-144.
44. Tamaoki, T., and H. Nakano. 1990. Potent and specific inhibitors of protein kinase C of microbial origin. Biotechnol. 8:732-735.
45. Tanaka, K., and K. Takai. 1998. Control of reorganization of the actin cytoskeleton by Rho family GTP-binding proteins in yeast. Curr. Opin. Cell Biol. 10: 112-116.
46. Toda, T. 1997. Genetic approaches in yeast. In Protein kinase C. Molecular Biology Intelligence Unit. P.J. Parker, and L.V. Dekker, editors. R.G. Landes Company, Georgetown, TX. 189-203.
47. 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 (Eur. Mol. Biol. Organ.) J. 12:1987-1995.
48. + gene encodes a novel MAPK homologue which regulates cell integrity and functions coordinately with the PKC pathway. Mol. Cell. Biol. 16:6752-6764.
49. + 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.
50. van der Leij, F.R., R.G. Visser, A.S. Ponstein, E. Jacobsen, and W.J. Feenstra. 1991. Sequence of the structural gene for granule-bound starch synthase of potato (Solanum tuberosum L.) and evidence for a single point deletion in the amf allele. Mol. Gen. Genet. 228:240-248.
51. Watanabe, N., Y. Saito, P. Madaule, T. Ishizaki, K. Fujisawa, N. Morii, H. Mukai, Y. Ono, A. Kakizuka, and S. Narumiya. 1996. Protein kinase N (PKN) and PKN-related protein Rhophilin as targets of small GTPase Rho. Science. 271:645-648.