The Src homology domain 3 (SH3) of a yeast type I myosin, Myo5p, binds to verprolin and is required for targeting to sites of actin polarization

Journal of Cell Biology

Volumn 141, Issue 6, 1998, Pages 1357-1370

  Anderson, Blake L ^a   Boldogh, Istvan ^a   Evangelista, Marie ^b   Boone, Charles ^b   Greene, Lloyd A ^a   Pon, Liza A ^a,c  

^a College of Physicians and Surgeons ^*  (United States)

^b QUEEN S UNIVERSITY   (Canada)

^c Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; FUNGAL PROTEIN; MUTANT PROTEIN; MYO5P PROTEIN; MYOSIN; PROLINE; UNCLASSIFIED DRUG; VERPROLIN;

ARTICLE; CELL POLARITY; CONTROLLED STUDY; DELETION MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN POLYMORPHISM; PROTEIN TARGETING; SACCHAROMYCES CEREVISIAE; YEAST CELL;

ACTINS; CELL DIVISION; CYTOSKELETON; FUNGAL PROTEINS; MICROFILAMENT PROTEINS; MUTAGENESIS; MYOSIN TYPE I; MYOSINS; PROLINE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SRC HOMOLOGY DOMAINS; TEMPERATURE;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 0032526679     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.141.6.1357     Document Type: Article

References (77)

1. Adams, R.J., and T.D. Pollard. 1989. Binding of myosin I to membrane lipids. Nature. 340:565-568.
2. Adams, A.E., D. Botstein, and D.G. Drubin. 1991. Requirement of yeast fimbrin for actin organization and morphogenesis in vivo. Nature. 354:404-408.
3. Altschul, S.F., W. Gish, W. Miller, E.W. Myers, and D.J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
4. 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.
5. 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.
6. Baines, I.C., A. Corigliano-Murphy, and E.D. Korn. 1995. Quantification and localization of phosphorylated myosin I isoforms in Acanthamoeba castellani. J. Biol. Chem. 130:591-603.
7. Bar-Sagi, D., D. Rotin, A. Batzer, V. Mandiyan, and J. Schlessinger. 1993. SH3 domains direct cellular localization of signaling molecules. Cell. 74:83-91.
8. Bauer, F., M. Urdaci, M. Aigle, and M. Crouzet. 1993. Alteration of a yeast SH3 protein leads to conditional viability with defects in cytoskeletal and budding patterns. Mol. Cell Biol. 13:5070-5084.
9. Bement, W.M., J.A. Wirth, and M.S. Mooseker. 1994. Cloning and mRNA expression of human unconventional myosin 1C. A homologue of amoeboid myosins-I with a single IQ motif and an SH3 domain. J. Mol. Biol. 243:356-363.
10. Bender, L., H. Lo, H. Lee, V. Kokojan, J. Peterson, and A. Bender. 1996. Associations among PH and SH3-containing proteins and Rho-type GTPases in yeast. J. Cell Biol. 133:879-894.
11. Chenevert, J., K. Corrado, A. Bender, J. Pringle, and I. Herskowitz. 1992. A yeast gene (BEM1) necessary for cell polarization contains two SH3 domains. Nature. 356:77-79.
12. Cheney, R.E., and M.S. Mooseker, M.S. 1995. Unconventional myosins. Annu. Rev. Cell Dev. Biol. 11:633-675.
13. Chowdhury, S., K.W. Smith, and M.C. Gustin. 1992. Osmotic stress and the actin cytoskeleton: phenotype-specific suppression of an actin mutation. J. Cell Biol. 118:561-571.
14. de Mendez, I., M.C. Garrett, A.G. Adams, and T.L. Leto. 1994. Role of the p67-phox SH3 domains in assembly of the NADPH oxidase system. J. Biol. Chem. 269:16326-16332.
15. de Mendez., I., A.G. Adams, R.A. Sokolic, H.L. Malech, and T.L. Leto. 1996. Multiple SH3 domain interactions regulate NADPH oxidase assembly in whole cells. EMBO (Eur. Mol. Biol. Organ.) J. 15:1211-1220.
16. Doberstein, S.K., and T.D. Pollard. 1992. Localization and specificity of the phospholipid and actin binding sites on the tail of Acanthomoeba myosin IC. J. Cell Biol. 117:1241-1249.
17. Doberstein, S.K., I.C. Baines, G. Wiegand, E.D. Korn, and T.D. Pollard. 1993. Inhibition of contractile vacuole function in vivo by antibodies against myosin-1. Nature. 365:841-843.
18. Donnelly, S.F.H., M.J. Pocklington, D. Pallotta, and E. Orr. 1993. A proline-rich protein, verprolin, involved in cyloskeletal organization and cellular growth in the yeast Saccharomyces cerevisiae. Mol. Microbiol. 10:585-596.
19. Drubin, D.G., K.G. Miller, and D. Botstein. 1988. Yeast actin-binding proteins: evidence for a role in morphogenesis. J. Cell Biol. 107:2551-2561.
20. Drubin, D.G., J. Mulholland, Z. Zhu, and D. Botstein. 1990. Homology of a yeast actin-binding protein to signal transduction proteins and myosin-1. Nature, 343:288-290.
21. Drubin, D.G., H.D. Jones, and K.F. Wertman. 1993. Actin structure and function: roles in mitochondrial organization and morphogenesis in budding yeast and identification of the phalloidin-binding site. Mol. Biol. Cell. 4:1277-1294.
22. Durfee, T., K. Becherer, P.L. Chen, S.H. Yeh, Y. Yang, A.B. Kilburn, W.H. Lee, and S.J. Elledge. 1993. The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes Dev. 7:555-569.
23. Evan, G.I., G.K. Lewis, G. Ramsay, and J.M. Bishop. 1985. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5:3610-3616.
24. Evangelista, M., K. Blundell, M.S., Longtine, C.J. Chow, N. Adames, J.R. Pringle, M. Pete, and C. Bonne. 1997. Bni1p, a yeast formin linking Cdc42p and the actin cytoskeleton during polarized morphogenesis. Science. 276:118-122.
25. Footer, M., and A. Bretscher. 1994. Brush border myosin I microinjected into cultured cells is targeted to actin-containing surface structures. J. Cell Sci. 107:1623-1631.
26. Freeman, N.L., T. Lila, K.A. Mintzer, Z. Chen, A.J. Pahk, R. Ren, D.G. Drubin, and J. Field. 1996. A conserved proline-rich region of the Saccharomyces cerevisiae cyclase-associated protein binds SH3 domains and modulates cytoskeletal localization. Mol. Cell Biol. 16:548-556.
27. Fukui, Y., T.J. Lynch, H. Brzeska, and E.D. Korn. 1989. Myosin 1 is located at the leading edge of locomoting Dictyostelium amoebae. Nature. 341:328-331.
28. Geli, M.I., and H. Riezman. 1996. Role of type I myosins in receptor-mediated endocytosis in yeast. Science. 272:533-535.
29. Goodson, H.V., and J.A. Spudich. 1995. Identification and molecular characterization of a yeast myosin I. Cell Motil. Cytoskeleton. 30:73-84.
30. Goodson, H.V., B.L. Anderson, H.M. Warrick, L.A. Pon, and J.A. Spudich. 1996. Synthetic lethality screen identities a novel yeast myosin I gene (MYO5): myosin I proteins are required for organization of the actin cytoskeleton. J. Cell Biol. 133:1277-1291.
31. Guthrie, C., and G.R. Fink. 1991. Guide to Yeast Genetics and Molecular Biology. In Methods in Enzymology Vol. 194. J.N. Abelson and M.I. Simon, editors. Academic Press, Inc., San Diego, CA. 931 pp.
32. Gyuris, J., E. Golemis, H. Chertkov, and R. Brent. 1993. Cdi1, a human G1 and S phase protein phosphatase that associates with Cdk2. Cell. 75:791-803.
33. Haarer, B.K., S.H. Lillie, A.E. Adams, V. Magdolen, W. Bandlow, and S.S. Brown. 1990. Purification of profilin from Saccharomyces cerevisiae and analysis of profilin-deficient cells. J. Cell Biol. 110:105-114.
34. Johnston, G.C., J.A. Prendergast, and R.A. Singer. 1991. The Saccharomyces cerevisiae MYO2 gene encodes an essential myosin for vectorial transport of vesicles. J. Cell Biol. 113:539-551.
35. Jung, G., and J.A. Hammer. 1990. Generation and characterization of Dictyostelium cells deficient in a myosin I heavy chain isoform. J. Cell Biol. 110: 1955-1964.
36. Jung, G., and J.A. Hammer. 1994. The actin binding site in the tail domain of Dictyostelium myosin IC (myoC) resides within the glycine-and proline-rich sequence (tail homology region 2). FEBS (Fed. Eur. Biochem. Soc.) Lett. 342:197-202.
37. Jung, G., X. Wu, and J.A. Hammer. 1996. Dictyostelium mutants lacking multiple classic myosin I isoforms reveal combinations of shared and distinct functions. J. Cell Biol. 133:305-323.
38. Jung, G., Y. Fukui, B. Martin, and J.A. Hammer. 1993. Sequence, expression pattern, intracellular localization, and targeted disruption of the Dictyostelium myosin ID heavy chain isoform. J. Biol. Chem. 268:14981-14990.
39. Kilmartin, J.V., and A.E.M. Adams. 1984. Structural rearrangements of tubulin and actin during cell cycle of the yeast Saccharomyces. J. Cell Biol. 98:922-933.
40. Kühler, E., and H. Riezman. 1993. Actin and fimbrin are required for the internalization step of endocytosis in yeast. EMBO (Eur. Mol. Biol. Organ.) J. 12: 2855-2862.
41. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685
42. Lazzarino, D., I. Boldogh, M.G. Smith, J. Rosand, and L.A. Pon. 1994. Yeast mitochondria contain ATP-sensitive, reversible actin-binding activity. Mol. Biol. Cell. 5:807-818.
43. Lila, T., and D.G. Drubin. 1997. Evidence for physical and functional interactions among two Saccharomyces cerevisiae SH3 domain protein, adenylyl cyclase-associated protein and the actin cytoskeleton. Mol. Biol. Cell. 8:367-385.
44. Lillie, S.H., and S.S. Brown. 1994. Immunofluorescence localization of the unconventional myosin, Myo2p, and the putative kinesin-related protein, Smy1p, to the same regions of polarized growth in Saccharomyces cerevisiae. J. Cell Biol. 125:825-842.
45. Liu, H., and A. Bretscher. 1992. Characterization of TPM1 disrupted yeast cells indicates an involvement of tropomyosin in directed vesicular transport. J. Cell Biol. 118:285-299.
46. Longtine, M.S., A. McKenzie III, D.J. DeMarini, N.G. Shah, A. Wach, A. Brachat, P. Philippsen, and J. Pringle. 1998. Additional molecules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast. In press.
47. Lynch, T., J.P. Albanesi, E.D. Korn, E.A. Robinson, B. Bowers, and H. Fujisaki. 1986. ATPase activities and actin-binding properties of subfragments of Acanthamoeba myosin IA. J. Biol. Chem. 261:17156-17162.
48. Matsui, Y., R. Matsui, R. Akada, and A. Toh-e. 1996. Yeast src homology 3 domain binding proteins involved in bud formation. J. Cell Biol. 133:865-878.
49. McGoldrick, C.A., C. Gruver, and G.S. May. 1995. MyoA of Aspergillus nidulans encodes an essential myosin I required for secretion and polarized growth. J. Cell Biol. 128:577-587.
50. Merilainen, J., R. Palvuori, R. Sormunen, V.M. Wasenius, and V.P. Lehto. 1993. Binding of the alpha-fodrin SH3 domain to the leading lamellae of locomoting chicken fibroblasts. J. Cell Sci. 105:647-654.
51. Novak, K.D., and M.A. Titus. 1997. Myosin I overexpression impairs cell migration. J. Cell Biol. 136:633-647.
52. Novick, P., and D. Botstein. 1985. Phenotypic analysis of temperature sensitive yeast actin mutants. Cell. 40:405-416.
53. Novak, K.D., M.D. Peterson, M.C. Reedy, and M.A. Titus. 1995. Dictyostelium myosin 1 double mutants exhibit conditional defects in pinocytosis. J. Cell Biol. 131:1205-1221.
54. Novick, P., S. Ferro, and R. Schekman. 1981. Order of events in the yeast secretory pathway. Cell. 25:461-469.
55. Peterson, M.D., K.D. Novak, M.C. Reedy, J.L. Ruman, and M.A. Titus. 1995. Molecular genetic analysis of myoC, a Dictyostelium myosin I. J. Cell Sci. 108:1093-1103.
56. Phizicky, E.M., and S. Fields. 1995. Protein-protein interactions: methods for detection and analysis. Microbiol. Rev. 59:94-123.
57. Pleiman, C.M., W.M. Hertz, and J.C. Cambier. 1994. Activation of phosphatidylinositol-3′ kinase by Src-family kinase SH3 binding to the p85 subunit. Science. 263:1609-1612.
58. Pollard, T.D., and E.D. Korn. 1973. Acanthamoeba myosin. I. Isolation from Acanthamoeba castellanii of an enzyme similar to muscle myosin. J. Biol. Chem. 248:4682-4690.
59. Pollard, T.P., S.K. Doberstein, and H.G. Zot. 1991. Myosin-I. Annu. Rev. Physiol. 53:653-681.
60. Pringle, J.R., A.E. Adams, D.G. Drubin, and B.K. Haarer. 1991. Immunofluorescence methods for yeast. Methods Enzymol. 194:565-601.
61. Rodriguez, J.R., and B.M. Paterson. 1990. Yeast myosin heavy chain mutant: maintenance of the cell type specific budding pattern and the normal deposition of chitin and cell wall components requires an intact myosin heavy chain gene. Cell Motil. Cytoskeleton. 17:301-308.
62. Rosenfeld, S.S., and B. Rener. 1994. The GPQ-rich segment of Dictyostelium myosin IB contains an actin binding site. Biochemistry. 33:2322-2328.
63. Ruppert, C., R. Kroschewski, and M. Bähler. 1993. Identification, characterization and cloning of myr 1, a mammalian myosin-I. J. Cell Biol. 120:1393-1403.
64. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Second edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 545 pp.
65. Sellers, J.R., and H.V. Goodson. 1995. Motor proteins 2: myosins. Protein Profiles. 2:1323-1423.
66. Simon, V.R., T.C. Swayne, and L.A. Pon. 1995. Actin-dependent mitochondrial motility in mitotic yeast and cell-free systems: identification of a motor activity on the mitochondrial surface. J Cell Biol. 130:345-354.
67. Spector, I., N.R. Shochet, Y. Kashman, and A. Groweiss. 1983. Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells. Science. 219:493-495.
68. Stevens, B. 1977. Variation in number and volume of the mitochondria in yeast according to growth conditions. A study based on serial sectioning and computer graphics reconstruction. Biologie Celllulaire. 28:37-56.
69. Stoffler, H.E., C. Ruppert, J. Reinhard, and M. Bähler. 1995. A novel mammalian myosin I from rat with an SH3 domain localizes to Con A-inducible, F-actin-rich structures at cell-cell contacts. J. Cell Biol. 129:819-830.
70. Temesvari, L.A., J.M. Bush, M.D. Peterson, K.D. Novak, M.A. Titus, and J.A. Cardelli. 996. Examination of the endosomal and lysosomal pathways in Dictyostelium discoideum myosin I mutants. J. Cell Sci. 109:663-673.
71. Titus, M.A., D. Wessels, J.A. Spudich, and D. Soll. 1993. The unconventional myosin encoded by the myoA gene plays a role in Dictyostelium motility. Mol. Biol. Cell. 4:233-246.
72. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA. 76:4350-4354.
73. Vaduva, G., N.C. Martin, and A.K. Hopper. 1997. Actin-binding verprolin is a polarity development protein required for the morphogenesis and function of the yeast actin cytoskeleton. J. Cell Biol. 139:1821-1833.
74. Wach, A. 1996. PCR-synthesis of marker cassettes with long flanking homology regions for gene disruption in S. cerevisiae. Yeast. 12:259-265.
75. Wang, K., M. Knipfer, Q.Q. Huang, A. van Heerden, L.C. Hsu, G. Gutierrex, X.L. Quian, and H. Stedman. 1996. Human skeletal muscle nebulin sequence encodes a blueprint for thin filament architecture. Sequence motifs and affinity profiles of tandem repeats and terminal SH3. J. Biol. Chem. 271: 4304-4314.
76. Wu., H., and J.T. Parsons. 1993. Cortactin, an 80/85-kilodalton Pp60src substrate, is a filamentous actin-binding protein enriched in the cell cortex. J. Cell Biol. 120:1417-1426.
77. Xu, P., A.S. Zot, and H. Zot. 1995. Identification of Acan125 as a myosin-I-binding protein present with myosin 1 on cellular organelles in Acanthamoeba. Proc. Natl. Acad. Sci. USA. 270:25316-25319.