Myosin-V Is Activated by Binding Secretory Cargo and Released in Coordination with Rab/Exocyst Function

Developmental Cell

Volumn 23, Issue 4, 2012, Pages 769-781

  Donovan, Kirk W ^a   Bretscher, Anthony ^a  

^a School of Integrative Plant Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXOCYST; MYOSIN V; RAB PROTEIN; SECRETORY PROTEIN;

ARTICLE; CELL GROWTH; CELL MEMBRANE; EXOCYTOSIS; IN VIVO STUDY; MEMBRANE FUSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN HYDROLYSIS; PROTEIN SECRETION; SECRETORY VESICLE; YEAST;

ACTINS; BINDING SITES; CELL PROLIFERATION; EXOCYTOSIS; MUTATION; MYOSIN TYPE V; RAB GTP-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SECRETORY VESICLES;

EID: 84867667224     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.09.001     Document Type: Article

References (63)

1. Aalto M.K., Ronne H., Keränen S. Yeast syntaxins Sso1p and Sso2p belong to a family of related membrane proteins that function in vesicular transport. EMBO J. 1993, 12:4095-4104.
2. Akhmanova A., Hammer J.A. Linking molecular motors to membrane cargo. Curr. Opin. Cell Biol. 2010, 22:479-487.
3. Boyd C., Hughes T., Pypaert M., Novick P. Vesicles carry most exocyst subunits to exocytic sites marked by the remaining two subunits, Sec3p and Exo70p. J. Cell Biol. 2004, 167:889-901.
4. Brennwald P., Kearns B., Champion K., Keränen S., Bankaitis V., Novick P. Sec9 is a SNAP-25-like component of a yeast SNARE complex that may be the effector of Sec4 function in exocytosis. Cell 1994, 79:245-258.
5. Fagarasanu A., Fagarasanu M., Eitzen G.A., Aitchison J.D., Rachubinski R.A. The peroxisomal membrane protein Inp2p is the peroxisome-specific receptor for the myosin V motor Myo2p of Saccharomyces cerevisiae. Dev. Cell 2006, 10:587-600.
6. Ferro-Novick S., Novick P. The role of GTP-binding proteins in transport along the exocytic pathway. Annu. Rev. Cell Biol. 1993, 9:575-599.
7. Gangar A., Rossi G., Andreeva A., Hales R., Brennwald P. Structurally conserved interaction of Lgl family with SNAREs is critical to their cellular function. Curr. Biol. 2005, 15:1136-1142.
8. Gao X.D., Albert S., Tcheperegine S.E., Burd C.G., Gallwitz D., Bi E. The GAP activity of Msb3p and Msb4p for the Rab GTPase Sec4p is required for efficient exocytosis and actin organization. J. Cell Biol. 2003, 162:635-646.
9. 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.
10. Gietz R.D., Schiestl R.H., Willems A.R., Woods R.A. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 1995, 11:355-360.
11. Goode B.L., Drubin D.G., Barnes G. Functional cooperation between the microtubule and actin cytoskeletons. Curr. Opin. Cell Biol. 2000, 12:63-71.
12. Govindan B., Bowser R., Novick P. The role of Myo2, a yeast class V myosin, in vesicular transport. J. Cell Biol. 1995, 128:1055-1068.
13. Guo W., Roth D., Walch-Solimena C., Novick P. The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J. 1999, 18:1071-1080.
14. Hales C.M., Vaerman J.P., Goldenring J.R. Rab11 family interacting protein 2 associates with Myosin Vb and regulates plasma membrane recycling. J. Biol. Chem. 2002, 277:50415-50421.
15. Hammer J.A., Sellers J.R. Walking to work: roles for class V myosins as cargo transporters. Nat. Rev. Mol. Cell Biol. 2012, 13:13-26.
16. He B., Guo W. The exocyst complex in polarized exocytosis. Curr. Opin. Cell Biol. 2009, 21:537-542.
17. Hodges A.R., Krementsova E.B., Bookwalter C.S., Fagnant P.M., Sladewski T.E., Trybus K.M. Tropomyosin is essential for processive movement of a class V myosin from budding yeast. Curr. Biol. 2012, 22:1410-1416.
18. Ishikawa K., Catlett N.L., Novak J.L., Tang F., Nau J.J., Weisman L.S. Identification of an organelle-specific myosin V receptor. J. Cell Biol. 2003, 160:887-897.
19. Ishikura S., Klip A. Muscle cells engage Rab8A and myosin Vb in insulin-dependent GLUT4 translocation. Am. J. Physiol. Cell Physiol. 2008, 295:C1016-C1025.
20. Jin Y., Sultana A., Gandhi P., Franklin E., Hamamoto S., Khan A.R., Munson M., Schekman R., Weisman L.S. Myosin V transports secretory vesicles via a Rab GTPase cascade and interaction with the exocyst complex. Dev. Cell 2011, 21:1156-1170.
21. Joglekar A.P., Bouck D., Finley K., Liu X., Wan Y., Berman J., He X., Salmon E.D., Bloom K.S. Molecular architecture of the kinetochore-microtubule attachment site is conserved between point and regional centromeres. J. Cell Biol. 2008, 181:587-594.
22. Kaiser C.A., Schekman R. Distinct sets of SEC genes govern transport vesicle formation and fusion early in the secretory pathway. Cell 1990, 61:723-733.
23. Kaksonen M., Sun Y., Drubin D.G. A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 2003, 115:475-487.
24. Katz L., Hanson P.I., Heuser J.E., Brennwald P. Genetic and morphological analyses reveal a critical interaction between the C-termini of two SNARE proteins and a parallel four helical arrangement for the exocytic SNARE complex. EMBO J. 1998, 17:6200-6209.
25. Krementsov D.N., Krementsova E.B., Trybus K.M. Myosin V: regulation by calcium, calmodulin, and the tail domain. J. Cell Biol. 2004, 164:877-886.
26. Lapierre L.A., Kumar R., Hales C.M., Navarre J., Bhartur S.G., Burnette J.O., Provance D.W., Mercer J.A., Bähler M., Goldenring J.R. Myosin vb is associated with plasma membrane recycling systems. Mol. Biol. Cell 2001, 12:1843-1857.
27. Lawrimore J., Bloom K.S., Salmon E.D. Point centromeres contain more than a single centromere-specific Cse4 (CENP-A) nucleosome. J. Cell Biol. 2011, 195:573-582.
28. Li X.D., Mabuchi K., Ikebe R., Ikebe M. Ca2+-induced activation of ATPase activity of myosin Va is accompanied with a large conformational change. Biochem. Biophys. Res. Commun. 2004, 315:538-545.
29. Li X.D., Jung H.S., Wang Q., Ikebe R., Craig R., Ikebe M. The globular tail domain puts on the brake to stop the ATPase cycle of myosin Va. Proc. Natl. Acad. Sci. USA 2008, 105:1140-1145.
30. Lipatova Z., Tokarev A.A., Jin Y., Mulholland J., Weisman L.S., Segev N. Direct interaction between a myosin V motor and the Rab GTPases Ypt31/32 is required for polarized secretion. Mol. Biol. Cell 2008, 19:4177-4187.
31. Liu W., Santiago-Tirado F.H., Bretscher A. Yeast formin Bni1p has multiple localization regions that function in polarized growth and spindle orientation. Mol. Biol. Cell 2012, 23:412-422.
32. Liu J., Taylor D.W., Krementsova E.B., Trybus K.M., Taylor K.A. Three-dimensional structure of the myosin V inhibited state by cryoelectron tomography. Nature 2006, 442:208-211.
33. Mulholland J., Preuss D., Moon A., Wong A., Drubin D., Botstein D. Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane. J. Cell Biol. 1994, 125:381-391.
34. Müller T., Hess M.W., Schiefermeier N., Pfaller K., Ebner H.L., Heinz-Erian P., Ponstingl H., Partsch J., Röllinghoff B., Köhler H., et al. MYO5B mutations cause microvillus inclusion disease and disrupt epithelial cell polarity. Nat. Genet. 2008, 40:1163-1165.
35. Pastural E., Barrat F.J., Dufourcq-Lagelouse R., Certain S., Sanal O., Jabado N., Seger R., Griscelli C., Fischer A., de Saint Basile G. Griscelli disease maps to chromosome 15q21 and is associated with mutations in the myosin-Va gene. Nat. Genet. 1997, 16:289-292.
36. Prescianotto-Baschong C., Riezman H. Morphology of the yeast endocytic pathway. Mol. Biol. Cell 1998, 9:173-189.
37. Protopopov V., Govindan B., Novick P., Gerst J.E. Homologs of the synaptobrevin/VAMP family of synaptic vesicle proteins function on the late secretory pathway in S. cerevisiae. Cell 1993, 74:855-861.
38. Pruyne D., Legesse-Miller A., Gao L., Dong Y., Bretscher A. Mechanisms of polarized growth and organelle segregation in yeast. Annu. Rev. Cell Dev. Biol. 2004, 20:559-591.
39. 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.
40. Reck-Peterson S.L., Tyska M.J., Novick P.J., Mooseker M.S. The yeast class V myosins, Myo2p and Myo4p, are nonprocessive actin-based motors. J. Cell Biol. 2001, 153:1121-1126.
41. Rexach M.F., Schekman R.W. Distinct biochemical requirements for the budding, targeting, and fusion of ER-derived transport vesicles. J. Cell Biol. 1991, 114:219-229.
42. Roland J.T., Kenworthy A.K., Peranen J., Caplan S., Goldenring J.R. Myosin Vb interacts with Rab8a on a tubular network containing EHD1 and EHD3. Mol. Biol. Cell 2007, 18:2828-2837.
43. Rossanese O.W., Reinke C.A., Bevis B.J., Hammond A.T., Sears I.B., O'Connor J., Glick B.S. A role for actin, Cdc1p, and Myo2p in the inheritance of late Golgi elements in Saccharomyces cerevisiae. J. Cell Biol. 2001, 153:47-62.
44. Rossi G., Salminen A., Rice L.M., Brünger A.T., Brennwald P. Analysis of a yeast SNARE complex reveals remarkable similarity to the neuronal SNARE complex and a novel function for the C terminus of the SNAP-25 homolog, Sec9. J. Biol. Chem. 1997, 272:16610-16617.
45. Salminen A., Novick P.J. A ras-like protein is required for a post-Golgi event in yeast secretion. Cell 1987, 49:527-538.
46. Salmon E.D., Leslie R.J., Saxton W.M., Karow M.L., McIntosh J.R. Spindle microtubule dynamics in sea urchin embryos: analysis using a fluorescein-labeled tubulin and measurements of fluorescence redistribution after laser photobleaching. J. Cell Biol. 1984, 99:2165-2174.
47. Santiago-Tirado F.H., Legesse-Miller A., Schott D., Bretscher A. PI4P and Rab inputs collaborate in myosin-V-dependent transport of secretory compartments in yeast. Dev. Cell 2011, 20:47-59.
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. Sherman F. Getting started with yeast. Methods Enzymol. 2002, 350:3-41.
51. Tang F., Kauffman E.J., Novak J.L., Nau J.J., Catlett N.L., Weisman L.S. Regulated degradation of a class V myosin receptor directs movement of the yeast vacuole. Nature 2003, 422:87-92.
52. TerBush D.R., Novick P. Sec6, Sec8, and Sec15 are components of a multisubunit complex which localizes to small bud tips in Saccharomyces cerevisiae. J. Cell Biol. 1995, 130:299-312.
53. Thirumurugan K., Sakamoto T., Hammer J.A., Sellers J.R., Knight P.J. The cargo-binding domain regulates structure and activity of myosin 5. Nature 2006, 442:212-215.
54. Wagner W., Brenowitz S.D., Hammer J.A. Myosin-Va transports the endoplasmic reticulum into the dendritic spines of Purkinje neurons. Nat. Cell Biol. 2011, 13:40-48.
55. Walworth N.C., Brennwald P., Kabcenell A.K., Garrett M., Novick P. Hydrolysis of GTP by Sec4 protein plays an important role in vesicular transport and is stimulated by a GTPase-activating protein in Saccharomyces cerevisiae. Mol. Cell. Biol. 1992, 12:2017-2028.
56. Wang F., Thirumurugan K., Stafford W.F., Hammer J.A., Knight P.J., Sellers J.R. Regulated conformation of myosin V. J. Biol. Chem. 2004, 279:2333-2336.
57. Weber-Boyvat M., Aro N., Chernov K.G., Nyman T., Jäntti J. Sec1p and Mso1p C-terminal tails cooperate with the SNAREs and Sec4p in polarized exocytosis. Mol. Biol. Cell 2011, 22:230-244.
58. Weisman L.S. Organelles on the move: insights from yeast vacuole inheritance. Nat. Rev. Mol. Cell Biol. 2006, 7:243-252.
59. Wöllert T., Patel A., Lee Y.L., Provance D.W., Vought V.E., Cosgrove M.S., Mercer J.A., Langford G.M. Myosin5a tail associates directly with Rab3A-containing compartments in neurons. J. Biol. Chem. 2011, 286:14352-14361.
60. Wu J.-Q., Pollard T.D. Counting cytokinesis proteins globally and locally in fission yeast. Science 2005, 310:310-314.
61. Wu S., Mehta S.Q., Pichaud F., Bellen H.J., Quiocho F.A. Sec15 interacts with Rab11 via a novel domain and affects Rab11 localization in vivo. Nat. Struct. Mol. Biol. 2005, 12:879-885.
62. Wu X.S., Rao K., Zhang H., Wang F., Sellers J.R., Matesic L.E., Copeland N.G., Jenkins N.A., Hammer J.A. Identification of an organelle receptor for myosin-Va. Nat. Cell Biol. 2002, 4:271-278.
63. Yin H., Pruyne D., Huffaker T.C., Bretscher A. Myosin V orientates the mitotic spindle in yeast. Nature 2000, 406:1013-1015.