PAK-family kinases regulate cell and actin polarization throughout the cell cycle of Saccharomyces cerevisiae

Journal of Cell Biology

Volumn 147, Issue 4, 1999, Pages 845-856

  Holly, Stephen P ^a   Blumer, Kendall J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Actin; Cdc42; Cell cycle; p21 activated kinase; Polarity

Indexed keywords

ARTICLE; CELL CYCLE; CELL SURFACE; CYTOSKELETON; DEPOLYMERIZATION; ENZYME ACTIVATION; ENZYME REGULATION; MITOSIS; POLARIZATION; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

ACTINS; CDC42 GTP-BINDING PROTEIN; CELL CYCLE; CELL POLARITY; FUNGAL PROTEINS; GENOTYPE; KINETICS; MICROSCOPY, VIDEO; MITOSIS; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 0033571294     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.147.4.845     Document Type: Article

References (62)

1. Abo, A., J. Qu, M.S. Cammarano, C. Dan, A. Fritsch, V. Baud, B. Belisle, and A. Minden. 1998. PAK4, a novel effector for Cdc42Hs, is implicated in the reorganization of the actin cytoskeleton and in the formation of filopodia. EMBO (Eur. Mol. Biol. Organ.) J. 17:6527-6540.
2. Adams, A.E., D.I. Johnson, R.M. Longnecker, B.F. Sloat, and J.R. Pringle. 1990. CDC42 and CDC43, two additional genes involved in budding and the establishment of cell polarity in the yeast Saccharomyces cerevisiae. J. Cell Biol. 111:131-142.
3. Amatruda, J.F., D.J. Gattermeir, T.S. Karpova, and J.A. Cooper. 1992. Effects of null mutations and overexpression of capping protein on morphogenesis, actin distribution, and polarized secretion in yeast. J. Cell Biol. 119:1151-1162.
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. Barrai, Y., M. Parra, S. Bidlingmaier, and M. Snyder. 1999. Nim1-related kinases coordinate cell cycle progression with the organization of the peripheral cytoskeleton in yeast. Genes Dev. 13:176-187.
6. Benton, B.K., A. Tinkelenberg, I. Gonzalez, and F.R. Cross. 1997. Cla4p, a Saccharomyces cerevisiae Cdc42p-activated kinase involved in cytokinesis, is activated at mitosis. Mol Cell Biol. 17:5067-5076.
7. Bi, E., P. Maddox, D.J. Lew, E.D. Salmon, J.N. McMillan, E. Yeh, and J.R. Pringle. 1998. Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis. J. Cell Biol. 142:1301-1312.
8. Botstein, D., D. Amberg, J. Mulholland, T. Huffaker, A. Adams, D. Drubin, and T. Stearns. 1997. The yeast cytoskeleton. 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, Plainview, NY. 1-90.
9. Bretscher, A., B. Drees, E. Harsay, D. Schott, and T. Wang. 1994. What are the basic functions of microfilaments? Insights from studies in budding yeast. J. Cell Biol. 126:821-825.
10. Brown, J.L., M. Jaquenoud, M.P. Gulli, J. Chant, and M. Peter. 1997. Novel Cdc42-binding proteins Gic1 and Gic2 control cell polarity in yeast. Genes Dev. 11:2972-2982.
11. Carroll, C.W., R. Altman, D. Schieltz, J.R. Yates, and D. Kellogg. 1998. The septins are required for the mitosis-specific activation of the Gin4 kinase. J. Cell Biol. 143:709-717.
12. Chen, G.C., Y.J. Kim, and C.S.M. Chan. 1997. The Cdc42 GTPase-associated proteins Gic1 and Gic2 are required for polarized cell growth in Saccharomyces cerevisiae. Genes Dev. 11:2958-2971.
13. Chenevert, J., K. Corrado, A. Bender, J. Pringle, and I. Herskowitz. 1992. A yeast gene (BEM1) necessary for cell polarization whose product contains two SH3 domains. Nature. 356:77-79.
14. Cvrckova, F., C. De Virgilio, E. Manser, J.R. Pringle, and K. Nasmyth. 1995. Ste20-like protein kinases are required for normal localization of cell growth and for cytokinesis in budding yeast. Genes Dev. 9:1817-1830.
15. Daniels, R.H., P.S. Hall, and G.M. Bokoch. 1998. Membrane targeting of p21-activated kinase 1 (PAK1) induces neurite outgrowth from PC12 cells. EMBO (Eur. Mol. Biol. Organ.) J. 17:754-764.
16. Dohmen, R.J., P. Wu, and A. Varshavsky. 1994. Heat-inducible degron: a method for constructing temperature-sensitive mutants. Science. 263:1273-1276.
17. Doyle, T., and D. Botstein. 1996. Movement of yeast cortical actin cytoskeleton visualized in vivo. Proc. Natl. Acad. Sci. USA. 93:3886-3891.
18. Drubin, D.G., and W.J. Nelson. 1996. Origins of cell polarity. Cell. 84:335-344.
19. Eby, J.J., S.P. Holly, F. van Drogen, A.V. Grishin, M. Peter, D.G. Drubin, and K.J. Blumer. 1998. Actin cytoskeleton organization regulated by the PAK family of protein kinases. Curr. Biol. 8:967-970.
20. Epp, J.A., and J. Chant. 1997. An IQGAP-related protein controls actin-ring formation and cytokinesis in yeast. Curr. Biol. 7:921-929.
21. Field, C., and R. Schekman. 1980. Localized secretion of acid phosphatase reflects the pattern of cell surface growth in Saccharomyces cerevisiae. J. Cell Biol. 86:123-128.
22. Finger, F.P., and P. Novick. 1998. Spatial regulation of exocytosis: lessons from yeast. J. Cell Biol. 142:609-612.
23. Goodson, H.V., and J.A. Spudich. 1995. Identification and molecular characterization of a yeast myosin I. Cell Motil. Cytoskelet. 30:73-84.
24. Goodson, H.V., B.L. Anderson, H.M. Warrick, L.A. Pon, and J.A. Spudich. 1996. Synthetic lethality screen identifies a novel yeast myosin I gene (MYO5): myosin I proteins are required for polarization of the actin cytoskeleton. J. Cell Biol. 133:1277-1291.
25. Haarer, B.K., and J.R. Pringle. 1987. Immunofluorescence localization of the Saccharomyces cerevisiae CDC12 gene product to the vicinity of the 10-nm filaments in the mother-bud neck. Mol. Cell. Biol. 7:3678-3687.
26. Johnson, D.I. 1999. Cdc42: an essential rho-type GTPase controlling eukaryotic cell polarity. Microbiol. Mol. Biol. Rev. 63:54-105.
27. Johnson, D.I., and J.R. Pringle. 1990. Molecular characterization of CDC42, a Saccharomyces cerevisiae gene involved in the development of cell polarity. J. Cell Biol. 111:143-152.
28. Karpova, T.S., K. Tatchell, and J.A. Cooper. 1995. Actin filaments in yeast are unstable in the absence of capping protein or fimbrin. J. Cell Biol. 131:1483-1493.
29. Karpova, T.S., J.G. McNally, S.L. Moltz, and J.A. Cooper. 1998. Assembly and function of the actin cytoskeleton of yeast: relationships between cables and patches. J. Cell Biol. 142:1501-1517.
30. Keller, P., and K. Simons. 1997. Post-Golgi biosynthetic trafficking. J. Cell Sci. 110:3001-3009.
31. Kim, H.B., B.K. Haarer, and J.R. Pringle. 1991. Cellular morphogenesis in the Saccharomyces cerevisiae cell cycle: localization of the CDC3 gene product and the timing of events at the budding site. J. Cell Biol. 112:535-544.
32. Leberer, E., C. Wu, T. Leeuw, A. Fourest-Lieuvin, J.E. Segall, and D.Y. Thomas. 1997. Functional characterization of the Cdc42p binding domain of yeast Ste20p protein kinase. EMBO (Eur. Mol. Biol. Organ.) J. 16:83-97.
33. Leeuw, T., A. Fourest-Lieuvin, C. Wu, J. Chenevert, K. Clark, M. Whiteway, D.Y. Thomas, and E. Leberer. 1995. Pheromone response in yeast: association of Bemlp with proteins of the MAP kinase cascade and actin. Science. 270:1210-1213.
34. Lew, D.J., and S.I. Reed. 1993. Morphogenesis in the yeast cell cycle: regulation by Cdc28 and cyclins. J. Cell Biol. 120:1305-1320.
35. Lew, D.J., and S.I. Reed. 1995a. A cell cycle checkpoint monitors cell morphogenesis in budding yeast. J. Cell Biol. 129:739-749.
36. Lew, D.J., and S.I. Reed. 1995b. Cell cycle control of morphogenesis in budding yeast. Curr. Opin. Genet. Dev. 5:17-23.
37. Li, R. 1997. Beel, a yeast protein with homology to Wiscott-Aldrich syndrome protein, is critical for the assembly of the cortical actin cytoskeleton. J. Cell Biol. 136:649-658.
38. Li, R., Y. Zheng, and D.G. Drubin. 1995. Regulation of cortical actin cytoskeleton assembly during polarized cell growth in budding yeast. J. Cell Biol. 128: 599-615.
39. Longtine, M.S., H. Fares, and J.R. Pringle. 1998. Role of the yeast Gin4p protein kinase in septin assembly and the relationship between septin assembly and septin function. J. Cell Biol. 143:719-736.
40. Ma, L., R. Rohatgi, and M.W. Kirschner. 1998. The Arp2/3 complex mediates actin polymerization induced by the small GTP-binding protein Cdc42. Proc. Natl. Acad. Sci. USA. 95:15362-15367.
41. McMillan, J.N., R.A.L. Sia, and D.J. Lew. 1998. A morphogenesis checkpoint monitors the actin cytoskeleton in yeast. J. Cell Biol. 142:1487-1499.
42. Novick, P., and R. Schekman. 1979. Secretion and cell-surface growth are blocked in a temperature-sensitive mutant of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 76:1858-1862.
43. Novick, P., and D. Bolstein. 1985. Phenotypic analysis of temperature-sensitive yeast actin mutants. Cell. 40:405-416.
44. Peter, M., A.M. Neiman, H.O. Park, M. van Lohuizen, and I. Herskowitz. 1996. Functional analysis of the interaction between the small GTP binding protein Cdc42 and the Ste20 protein kinase in yeast. EMBO (Eur. Mol. Biol. Organ.) J. 15:7046-7059.
45. Pringle, J.R., A.E. Adams, D.G. Drubin, and B.K. Haarer. 1991. Immunofluorescence methods for yeast. Methods Enzymol. 194:565-602.
46. 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.
47. Rohatgi, R., L. Ma, H. Miki, M. Lopez, T. Kirchhausen, T. Takenawa, and M.W. Kirschner. 1999. The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell. 97:221-231.
48. Schmidt, A., J. Kunz, and M.N. Hall. 1996. TOR2 is required for organization of the actin cytoskeleton in yeast. Proc. Natl. Acad. Sci. USA. 93:13780-13785.
49. Sells, M.A., U.G. Knaus, S. Bagrodia, D.M. Ambrose, G.M. Bokoch, and J. Chernoff. 1997. Human p21-aclivaled kinase (Pak1) regulates actin organization in mammalian cells. Curr. Biol. 7:202-210.
50. Shannon, K.B., and R. Li. 1999. The multiple roles of Cyk1p in the assembly and function of the actomyosin ring in budding yeast. Mol. Biol. Cell. 10: 283-296.
51. Sherman, F. 1991. Getting started with yeast. Methods Enzymol. 194:3-21.
52. Srinivasa, S.P., L.S. Bernstein, K.J. Blumer, and M.E. Linder. 1998. Plasma membrane localization is required for RGS4 function in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 95:5584-5589.
53. Straight, A.F., W.F. Marshall, J.W. Sedat, and A.W. Murray. 1997. Mitosis in living budding yeast: anaphase A but no metaphase plate. Science. 277:574-578.
54. Tjandra, H., J. Compton, and D. Kellogg. 1998. Control of mitotic events by the Cdc42 GTPase, the Clb2 cyclin and a member of the PAK kinase family. Curr. Biol. 8:991-1000.
55. Waddle, J.A., T.S. Karpova, R.H. Waterston, and J.A. Cooper. 1996. Movement of cortical actin patches in yeast. J. Cell Biol. 132:861-870.
56. Weinert, T.A., and L.H. Hartwell. 1988. The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science. 241:317-322.
57. Weinert, T.A., and L.H. Hartwell. 1993. Cell cycle arrest of cdc mutants and specificity of the RAD9 checkpoint. Genetics. 134:63-80.
58. Weinert, T.A., G.L. Kiser, and L.H. Hartwell. 1994. Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev. 8:652-665.
59. Winter, D., A.V. Podtelejnikov, M. Mann, and R. Li. 1997. The complex containing actin-related proteins Arp2 and Arp3 is required for the motility and integrity of yeast actin patches. Curr. Biol. 7:519-529.
60. Wu, C., V. Lytvyn, D.Y. Thomas, and E. Leberer. 1997. The phosphorylation site for Ste20p-like protein kinases is essential for the function of myosin-I in yeast. J. Biol. Chem. 272:30623-30626.
61. Yaffe, M.P., and G. Schatz. 1984. Two nuclear mutations that block mitochondrial protein import in yeast. Proc. Natl. Acad. Sci. USA. 81:4819-4823.
62. Zhao, Z.S., E. Manser, X.Q. Chen, C. Chong, T. Leung, and L. Lim. 1998. A conserved negative regulatory region in alphaPAK: inhibition of PAK kinases reveals their morphological roles downstream of Cdc42 and Rac1. Mol. Cell. Biol. 18:2153-2163.