The Myosin Passenger Protein Smy1 Controls Actin Cable Structure and Dynamics by Acting as a Formin Damper

Developmental Cell

Volumn 21, Issue 2, 2011, Pages 217-230

  Chesarone Cataldo, Melissa ^a   Guérin, Christophe ^b   Yu, Jerry H ^c   Wedlich Soldner, Roland ^c   Blanchoin, Laurent ^b   Goode, Bruce L ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b CNRS   (France)

^c MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; MYOSIN; MYOSIN V; PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SMY 1 PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; GENE OVEREXPRESSION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE;

ACTINS; CYTOSKELETAL PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; MICROFILAMENT PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; MYOSIN TYPE V; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 79961235785     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2011.07.004     Document Type: Article

References (60)

1. Amberg D.C. Three-dimensional imaging of the yeast actin cytoskeleton through the budding cell cycle. Mol. Biol. Cell 1998, 9:3259-3262.
2. Beningo K.A., Lillie S.H., Brown S.S. The yeast kinesin-related protein Smy1p exerts its effects on the class V myosin Myo2p via a physical interaction. Mol. Biol. Cell 2000, 11:691-702.
3. Brown E.J., Schlöndorff J.S., Becker D.J., Tsukaguchi H., Tonna S.J., Uscinski A.L., Higgs H.N., Henderson J.M., Pollak M.R. Mutations in the formin gene INF2 cause focal segmental glomerulosclerosis. Nat. Genet. 2010, 42:72-76.
4. Buttery S.M., Yoshida S., Pellman D. Yeast formins Bni1 and Bnr1 utilize different modes of cortical interaction during the assembly of actin cables. Mol. Biol. Cell 2007, 18:1826-1838.
5. Cardoso C.M., Groth-Pedersen L., Høyer-Hansen M., Kirkegaard T., Corcelle E., Andersen J.S., Jäättelä M., Nylandsted J. Depletion of kinesin 5B affects lysosomal distribution and stability and induces peri-nuclear accumulation of autophagosomes in cancer cells. PLoS ONE 2009, 4:e4424.
6. Chesarone M.A., Goode B.L. Actin nucleation and elongation factors: mechanisms and interplay. Curr. Opin. Cell Biol. 2009, 21:28-37.
7. Chesarone M., Gould C.J., Moseley J.B., Goode B.L. Displacement of formins from growing barbed ends by bud14 is critical for actin cable architecture and function. Dev. Cell 2009, 16:292-302.
8. Chesarone M.A., DuPage A.G., Goode B.L. Unleashing formins to remodel the actin and microtubule cytoskeletons. Nat. Rev. Mol. Cell Biol. 2010, 11:62-74.
9. Chhabra E.S., Higgs H.N. The many faces of actin: matching assembly factors with cellular structures. Nat. Cell Biol. 2007, 9:1110-1121.
10. Evangelista M., Pruyne D., Amberg D.C., Boone C., Bretscher A. Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat. Cell Biol. 2002, 4:32-41.
11. Favaro P.M., de Souza Medina S., Traina F., Bassères D.S., Costa F.F., Saad S.T. Human leukocyte formin: a novel protein expressed in lymphoid malignancies and associated with Akt. Biochem. Biophys. Res. Commun. 2003, 311:365-371.
12. Ghaemmaghami S., Huh W.K., Bower K., Howson R.W., Belle A., Dephoure N., O'Shea E.K., Weissman J.S. Global analysis of protein expression in yeast. Nature 2003, 425:737-741.
13. Goode B.L., Eck M.J. Mechanism and function of formins in the control of actin assembly. Annu. Rev. Biochem. 2007, 76:593-627.
14. Gupta V., Palmer K.J., Spence P., Hudson A., Stephens D.J. Kinesin-1 (uKHC/KIF5B) is required for bidirectional motility of ER exit sites and efficient ER-to-Golgi transport. Traffic 2008, 9:1850-1866.
15. Higgs H.N., Pollard T.D. Regulation of actin polymerization by Arp2/3 complex and WASp/Scar proteins. J. Biol. Chem. 1999, 274:32531-32534.
16. Hodges A.R., Bookwalter C.S., Krementsova E.B., Trybus K.M. A nonprocessive class V myosin drives cargo processively when a kinesin- related protein is a passenger. Curr. Biol. 2009, 19:2121-2125.
17. Huang J.D., Brady S.T., Richards B.W., Stenolen D., Resau J.H., Copeland N.G., Jenkins N.A. Direct interaction of microtubule- and actin-based transport motors. Nature 1999, 397:267-270.
18. Huckaba T.M., Lipkin T., Pon L.A. Roles of type II myosin and a tropomyosin isoform in retrograde actin flow in budding yeast. J. Cell Biol. 2006, 175:957-969.
19. Imamura H., Tanaka K., Hihara T., Umikawa M., Kamei T., Takahashi K., Sasaki T., Takai Y. Bni1p and Bnr1p: downstream targets of the Rho family small G-proteins which interact with profilin and regulate actin cytoskeleton in Saccharomyces cerevisiae. EMBO J. 1997, 16:2745-2755.
20. Jaulin F., Xue X., Rodriguez-Boulan E., Kreitzer G. Polarization-dependent selective transport to the apical membrane by KIF5B in MDCK cells. Dev. Cell 2007, 13:511-522.
21. Kaiser D.A., Vinson V.K., Murphy D.B., Pollard T.D. Profilin is predominantly associated with monomeric actin in Acanthamoeba. J. Cell Sci. 1999, 112:3779-3790.
22. Kamasaki T., Arai R., Osumi M., Mabuchi I. Directionality of F-actin cables changes during the fission yeast cell cycle. Nat. Cell Biol. 2005, 7:916-917.
23. Karpova T.S., McNally J.G., Moltz S.L., Cooper J.A. Assembly and function of the actin cytoskeleton of yeast: relationships between cables and patches. J. Cell Biol. 1998, 142:1501-1517.
24. Kikyo M., Tanaka K., Kamei T., Ozaki K., Fujiwara T., Inoue E., Takita Y., Ohya Y., Takai Y. An FH domain-containing Bnr1p is a multifunctional protein interacting with a variety of cytoskeletal proteins in Saccharomyces cerevisiae. Oncogene 1999, 18:7046-7054.
25. Kovar D.R., Pollard T.D. Insertional assembly of actin filament barbed ends in association with formins produces piconewton forces. Proc. Natl. Acad. Sci. USA 2004, 101:14725-14730.
26. Kovar D.R., Pollard T.D. Progressing actin: Formin as a processive elongation machine. Nat. Cell Biol. 2004, 6:1158-1159.
27. Kovar D.R., Kuhn J.R., Tichy A.L., Pollard T.D. The fission yeast cytokinesis formin Cdc12p is a barbed end actin filament capping protein gated by profilin. J. Cell Biol. 2003, 161:875-887.
28. Kovar D.R., Harris E.S., Mahaffy R., Higgs H.N., Pollard T.D. Control of the assembly of ATP- and ADP-actin by formins and profilin. Cell 2006, 124:423-435.
29. Lawrence C.J., Malmberg R.L., Muszynski M.G., Dawe R.K. Maximum likelihood methods reveal conservation of function among closely related kinesin families. J. Mol. Evol. 2002, 54:42-53.
30. Li F., Higgs H.N. The mouse Formin mDia1 is a potent actin nucleation factor regulated by autoinhibition. Curr. Biol. 2003, 13:1335-1340.
31. Lillie S.H., Brown S.S. Suppression of a myosin defect by a kinesin-related gene. Nature 1992, 356:358-361.
32. Lillie S.H., Brown S.S. 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. 1994, 125:825-842.
33. Lillie S.H., Brown S.S. Smy1p, a kinesin-related protein that does not require microtubules. J. Cell Biol. 1998, 140:873-883.
34. Moseley J.B., Goode B.L. Differential activities and regulation of Saccharomyces cerevisiae formin proteins Bni1 and Bnr1 by Bud6. J. Biol. Chem. 2005, 280:28023-28033.
35. Moseley J.B., Sagot I., Manning A.L., Xu Y., Eck M.J., Pellman D., Goode B.L. A conserved mechanism for Bni1- and mDia1-induced actin assembly and dual regulation of Bni1 by Bud6 and profilin. Mol. Biol. Cell 2004, 15:896-907.
36. Moseley J.B., Maiti S., Goode B.L. Formin proteins: purification and measurement of effects on actin assembly. Methods Enzymol. 2006, 406:215-234.
37. Okada K., Ravi H., Smith E.M., Goode B.L. Aip1 and cofilin promote rapid turnover of yeast actin patches and cables: a coordinated mechanism for severing and capping filaments. Mol. Biol. Cell 2006, 17:2855-2868.
38. Pollard T.D., Weeds A.G. The rate constant for ATP hydrolysis by polymerized actin. FEBS Lett. 1984, 170:94-98.
39. Pring M., Evangelista M., Boone C., Yang C., Zigmond S.H. Mechanism of formin-induced nucleation of actin filaments. Biochemistry 2003, 42:486-496.
40. Pruyne D.W., Schott D.H., Bretscher A. Tropomyosin-containing actin cables direct the Myo2p-dependent polarized delivery of secretory vesicles in budding yeast. J. Cell Biol. 1998, 143:1931-1945.
41. Pruyne D., Evangelista M., Yang C., Bi E., Zigmond S., Bretscher A., Boone C. Role of formins in actin assembly: nucleation and barbed-end association. Science 2002, 297:612-615.
42. Pruyne D., Gao L., Bi E., Bretscher A. Stable and dynamic axes of polarity use distinct formin isoforms in budding yeast. Mol. Biol. Cell 2004, 15:4971-4989.
43. Romero S., Le Clainche C., Didry D., Egile C., Pantaloni D., Carlier M.F. Formin is a processive motor that requires profilin to accelerate actin assembly and associated ATP hydrolysis. Cell 2004, 119:419-429.
44. Rose R., Weyand M., Lammers M., Ishizaki T., Ahmadian M.R., Wittinghofer A. Structural and mechanistic insights into the interaction between Rho and mammalian Dia. Nature 2005, 435:513-518.
45. Sagot I., Klee S.K., Pellman D. Yeast formins regulate cell polarity by controlling the assembly of actin cables. Nat. Cell Biol. 2002, 4:42-50.
46. Sagot I., Rodal A.A., Moseley J., Goode B.L., Pellman D. An actin nucleation mechanism mediated by Bni1 and profilin. Nat. Cell Biol. 2002, 4:626-631.
47. Schmidt M.R., Maritzen T., Kukhtina V., Higman V.A., Doglio L., Barak N.N., Strauss H., Oschkinat H., Dotti C.G., Haucke V. Regulation of endosomal membrane traffic by a Gadkin/AP-1/kinesin KIF5 complex. Proc. Natl. Acad. Sci. USA 2009, 106:15344-15349.
48. Schott D., Ho J., Pruyne D., Bretscher A. The COOH-terminal domain of Myo2p, a yeast myosin V, has a direct role in secretory vesicle targeting. J. Cell Biol. 1999, 147:791-808.
49. Schott D.H., Collins R.N., Bretscher A. Secretory vesicle transport velocity in living cells depends on the myosin-V lever arm length. J. Cell Biol. 2002, 156:35-39.
50. Seth A., Otomo C., Rosen M.K. Autoinhibition regulates cellular localization and actin assembly activity of the diaphanous-related formins FRLalpha and mDia1. J. Cell Biol. 2006, 174:701-713.
51. Spudich J.A., Watt S. The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin. J. Biol. Chem. 1971, 246:4866-4871.
52. Tanaka Y., Kanai Y., Okada Y., Nonaka S., Takeda S., Harada A., Hirokawa N. Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 1998, 93:1147-1158.
53. Vallen E.A., Caviston J., Bi E. Roles of Hof1p, Bni1p, Bnr1p, and myo1p in cytokinesis in Saccharomyces cerevisiae. Mol. Biol. Cell 2000, 11:593-611.
54. Vavylonis D., Kovar D.R., O'Shaughnessy B., Pollard T.D. Model of formin-associated actin filament elongation. Mol. Cell 2006, 21:455-466.
55. Vinson V.K., De La Cruz E.M., Higgs H.N., Pollard T.D. Interactions of Acanthamoeba profilin with actin and nucleotides bound to actin. Biochemistry 1998, 37:10871-10880.
56. Watanabe N., Kato T., Fujita A., Ishizaki T., Narumiya S. Cooperation between mDia1 and ROCK in Rho-induced actin reorganization. Nat. Cell Biol. 1999, 1:136-143.
57. Yang H.C., Pon L.A. Actin cable dynamics in budding yeast. Proc. Natl. Acad. Sci. USA 2002, 99:751-756.
58. Yonetani A., Lustig R.J., Moseley J.B., Takeda T., Goode B.L., Chang F. Regulation and targeting of the fission yeast formin cdc12p in cytokinesis. Mol. Biol. Cell 2008, 19:2208-2219.
59. Yu J.H., Crevenna A.H., Bettenbühl M., Freisinger T., Wedlich-Söldner R. Cortical actin dynamics driven by formins and myosin V. J. Cell Sci. 2011, 124:1533-1541.
60. Zhu X.L., Liang L., Ding Y.Q. Overexpression of FMNL2 is closely related to metastasis of colorectal cancer. Int. J. Colorectal Dis. 2008, 23:1041-1047.