Myosin V transports secretory vesicles via a Rab GTPase cascade and interaction with the exocyst complex

Developmental Cell

Volumn 21, Issue 6, 2011, Pages 1156-1170

  Jin, Yui ^a   Sultana, Azmiri ^b   Gandhi, Pallavi ^c   Franklin, Edward ^b   Hamamoto, Susan ^d   Khan, Amir R ^b   Munson, Mary ^c   Schekman, Randy ^d   Weisman, Lois S ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b TRINITY COLLEGE DUBLIN   (Ireland)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXOCYST; FUNGAL PROTEIN; MYOSIN II; MYOSIN V; PROTEIN SEC15; PROTEIN SEC4; PROTEIN YPT31; PROTEIN YPT32; RAB PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL VACUOLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN STRUCTURE; YEAST;

AMINO ACID SUBSTITUTION; BINDING SITES; EXOCYTOSIS; MEMBRANE FUSION; MODELS, MOLECULAR; MOLECULAR MOTOR PROTEINS; MUTAGENESIS, SITE-DIRECTED; MYOSIN HEAVY CHAINS; MYOSIN TYPE V; PROTEIN INTERACTION DOMAINS AND MOTIFS; RAB GTP-BINDING PROTEINS; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SECRETORY VESICLES; SIGNAL TRANSDUCTION; VESICULAR TRANSPORT PROTEINS;

EID: 83455229807     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2011.10.009     Document Type: Article

References (82)

1. Adamo J.E., Rossi G., Brennwald P. The Rho GTPase Rho3 has a direct role in exocytosis that is distinct from its role in actin polarity. Mol. Biol. Cell 1999, 10:4121-4133.
2. Beronja S., Laprise P., Papoulas O., Pellikka M., Sisson J., Tepass U. Essential function of Drosophila Sec6 in apical exocytosis of epithelial photoreceptor cells. J. Cell Biol. 2005, 169:635-646.
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. Calero M., Chen C.Z., Zhu W., Winand N., Havas K.A., Gilbert P.M., Burd C.G., Collins R.N. Dual prenylation is required for Rab protein localization and function. Mol. Biol. Cell 2003, 14:1852-1867.
6. Catlett N.L., Duex J.E., Tang F., Weisman L.S. Two distinct regions in a yeast myosin-V tail domain are required for the movement of different cargoes. J. Cell Biol. 2000, 150:513-526.
7. Cavanaugh L.F., Chen X., Richardson B.C., Ungar D., Pelczer I., Rizo J., Hughson F.M. Structural analysis of conserved oligomeric Golgi complex subunit 2. J. Biol. Chem. 2007, 282:23418-23426.
8. Collins R.N., Brennwald P., Garrett M., Lauring A., Novick P. Interactions of nucleotide release factor Dss4p with Sec4p in the post-Golgi secretory pathway of yeast. J. Biol. Chem. 1997, 272:18281-18289.
9. Croteau N.J., Furgason M.L., Devos D., Munson M. Conservation of helical bundle structure between the exocyst subunits. PLoS ONE 2009, 4:e4443.
10. Dong G., Hutagalung A.H., Fu C., Novick P., Reinisch K.M. The structures of exocyst subunit Exo70p and the Exo84p C-terminal domains reveal a common motif. Nat. Struct. Mol. Biol. 2005, 12:1094-1100.
11. Estrada P., Kim J., Coleman J., Walker L., Dunn B., Takizawa P., Novick P., Ferro-Novick S. Myo4p and She3p are required for cortical ER inheritance in Saccharomyces cerevisiae. J. Cell Biol. 2003, 163:1255-1266.
12. Evans L.L., Lee A.J., Bridgman P.C., Mooseker M.S. Vesicle-associated brain myosin-V can be activated to catalyze actin-based transport. J. Cell Sci. 1998, 111:2055-2066.
13. Fagarasanu A., Mast F.D., Knoblach B., Jin Y., Brunner M.J., Logan M.R., Glover J.N., Eitzen G.A., Aitchison J.D., Weisman L.S., Rachubinski R.A. Myosin-driven peroxisome partitioning in S. cerevisiae. J. Cell Biol. 2009, 186:541-554.
14. Fielding A.B., Schonteich E., Matheson J., Wilson G., Yu X., Hickson G.R., Srivastava S., Baldwin S.A., Prekeris R., Gould G.W. Rab11-FIP3 and FIP4 interact with Arf6 and the exocyst to control membrane traffic in cytokinesis. EMBO J. 2005, 24:3389-3399.
15. Fukuda M., Kuroda T.S., Mikoshiba K. Slac2-a/melanophilin, the missing link between Rab27 and myosin Va: implications of a tripartite protein complex for melanosome transport. J. Biol. Chem. 2002, 277:12432-12436.
16. 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.
17. 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.
18. Grosshans B.L., Andreeva A., Gangar A., Niessen S., Yates J.R., Brennwald P., Novick P. The yeast lgl family member Sro7p is an effector of the secretory Rab GTPase Sec4p. J. Cell Biol. 2006, 172:55-66.
19. 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.
20. Hamburger Z.A., Hamburger A.E., West A.P., Weis W.I. Crystal structure of the S.cerevisiae exocyst component Exo70p. J. Mol. Biol. 2006, 356:9-21.
21. Harsay E., Bretscher A. Parallel secretory pathways to the cell surface in yeast. J. Cell Biol. 1995, 131:297-310.
22. He B., Xi F., Zhang J., TerBush D., Zhang X., Guo W. Exo70p mediates the secretion of specific exocytic vesicles at early stages of the cell cycle for polarized cell growth. J. Cell Biol. 2007, 176:771-777.
23. Heuck A., Fetka I., Brewer D.N., Hüls D., Munson M., Jansen R.P., Niessing D. The structure of the Myo4p globular tail and its function in ASH1 mRNA localization. J. Cell Biol. 2010, 189:497-510.
24. Hill K.L., Catlett N.L., Weisman L.S. Actin and myosin function in directed vacuole movement during cell division in Saccharomyces cerevisiae. J. Cell Biol. 1996, 135:1535-1549.
25. Hoepfner D., van den Berg M., Philippsen P., Tabak H.F., Hettema E.H. A role for Vps1p, actin, and the Myo2p motor in peroxisome abundance and inheritance in Saccharomyces cerevisiae. J. Cell Biol. 2001, 155:979-990.
26. Hume A.N., Collinson L.M., Hopkins C.R., Strom M., Barral D.C., Bossi G., Griffiths G.M., Seabra M.C. The leaden gene product is required with Rab27a to recruit myosin Va to melanosomes in melanocytes. Traffic 2002, 3:193-202.
27. 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.
28. 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.
29. Jafar-Nejad H., Andrews H.K., Acar M., Bayat V., Wirtz-Peitz F., Mehta S.Q., Knoblich J.A., Bellen H.J. Sec15, a component of the exocyst, promotes notch signaling during the asymmetric division of Drosophila sensory organ precursors. Dev. Cell 2005, 9:351-363.
30. Jedd G., Mulholland J., Segev N. Two new Ypt GTPases are required for exit from the yeast trans-Golgi compartment. J. Cell Biol. 1997, 137:563-580.
31. Johnston G.C., Prendergast J.A., Singer R.A. The Saccharomyces cerevisiae MYO2 gene encodes an essential myosin for vectorial transport of vesicles. J. Cell Biol. 1991, 113:539-551.
32. Kaiser C., Michaelis S., Mitchell A. Methods in Yeast Genetics 1994, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
33. Kerppola T.K. Bimolecular fluorescence complementation (BiFC) analysis as a probe of protein interactions in living cells. Annu Rev Biophys 2008, 37:465-487.
34. Lambert C., Léonard N., De Bolle X., Depiereux E. ESyPred3D: Prediction of proteins 3D structures. Bioinformatics 2002, 18:1250-1256.
35. Langevin J., Morgan M.J., Sibarita J.B., Aresta S., Murthy M., Schwarz T., Camonis J., Bellaïche Y. Drosophila exocyst components Sec5, Sec6, and Sec15 regulate DE-Cadherin trafficking from recycling endosomes to the plasma membrane. Dev. Cell 2005, 9:365-376.
36. Lehman K., Rossi G., Adamo J.E., Brennwald P. Yeast homologues of tomosyn and lethal giant larvae function in exocytosis and are associated with the plasma membrane SNARE, Sec9. J. Cell Biol. 1999, 146:125-140.
37. Li B.X., Satoh A.K., Ready D.F. Myosin V, Rab11, and dRip11 direct apical secretion and cellular morphogenesis in developing Drosophila photoreceptors. J. Cell Biol. 2007, 177:659-669.
38. 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.
39. 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.
40. 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.
41. Medkova M., France Y.E., Coleman J., Novick P. The rab exchange factor Sec2p reversibly associates with the exocyst. Mol. Biol. Cell 2006, 17:2757-2769.
42. Mizuno-Yamasaki E., Medkova M., Coleman J., Novick P. Phosphatidylinositol 4-phosphate controls both membrane recruitment and a regulatory switch of the Rab GEF Sec2p. Dev. Cell 2010, 18:828-840.
43. Moore B.A., Robinson H.H., Xu Z. The crystal structure of mouse Exo70 reveals unique features of the mammalian exocyst. J. Mol. Biol. 2007, 371:410-421.
44. Munson M., Novick P. The exocyst defrocked, a framework of rods revealed. Nat. Struct. Mol. Biol. 2006, 13:577-581.
45. Nagashima K., Torii S., Yi Z., Igarashi M., Okamoto K., Takeuchi T., Izumi T. Melanophilin directly links Rab27a and myosin Va through its distinct coiled-coil regions. FEBS Lett. 2002, 517:233-238.
46. Olivares A.O., Chang W., Mooseker M.S., Hackney D.D., De La Cruz E.M. The tail domain of myosin Va modulates actin binding to one head. J. Biol. Chem. 2006, 281:31326-31336.
47. Ortiz D., Medkova M., Walch-Solimena C., Novick P. Ypt32 recruits the Sec4p guanine nucleotide exchange factor, Sec2p, to secretory vesicles; evidence for a Rab cascade in yeast. J. Cell Biol. 2002, 157:1005-1015.
48. Pashkova N., Jin Y., Ramaswamy S., Weisman L.S. Structural basis for myosin V discrimination between distinct cargoes. EMBO J. 2006, 25:693-700.
49. Pérez-Victoria F.J., Abascal-Palacios G., Tascón I., Kajava A., Magadán J.G., Pioro E.P., Bonifacino J.S., Hierro A. Structural basis for the wobbler mouse neurodegenerative disorder caused by mutation in the Vps54 subunit of the GARP complex. Proc. Natl. Acad. Sci. USA 2010, 107:12860-12865.
50. Prekeris R., Terrian D.M. Brain myosin V is a synaptic vesicle-associated motor protein: evidence for a Ca2+-dependent interaction with the synaptobrevin-synaptophysin complex. J. Cell Biol. 1997, 137:1589-1601.
51. Reck-Peterson S.L., Novick P.J., Mooseker M.S. The tail of a yeast class V myosin, myo2p, functions as a localization domain. Mol. Biol. Cell 1999, 10:1001-1017.
52. Ren Y., Yip C.K., Tripathi A., Huie D., Jeffrey P.D., Walz T., Hughson F.M. A structure-based mechanism for vesicle capture by the multisubunit tethering complex Dsl1. Cell 2009, 139:1119-1129.
53. Richardson B.C., Smith R.D., Ungar D., Nakamura A., Jeffrey P.D., Lupashin V.V., Hughson F.M. Structural basis for a human glycosylation disorder caused by mutation of the COG4 gene. Proc. Natl. Acad. Sci. USA 2009, 106:13329-13334.
54. Robinson N.G., Guo L., Imai J., Toh-E A., Matsui Y., Tamanoi F. Rho3 of Saccharomyces cerevisiae, which regulates the actin cytoskeleton and exocytosis, is a GTPase which interacts with Myo2 and Exo70. Mol. Cell. Biol. 1999, 19:3580-3587.
55. Rodriguez O.C., Cheney R.E. Human myosin-Vc is a novel class V myosin expressed in epithelial cells. J. Cell Sci. 2002, 115:991-1004.
56. 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.
57. Roland J.T., Lapierre L.A., Goldenring J.R. Alternative splicing in class V myosins determines association with Rab10. J. Biol. Chem. 2009, 284:1213-1223.
58. Roland J.T., Bryant D.M., Datta A., Itzen A., Mostov K.E., Goldenring J.R. Rab GTPase-Myo5B complexes control membrane recycling and epithelial polarization. Proc. Natl. Acad. Sci. USA 2011, 108:2789-2794.
59. Rossi G., Brennwald P. Yeast homologues of lethal giant larvae and type V myosin cooperate in the regulation of Rab-dependent vesicle clustering and polarized exocytosis. Mol. Biol. Cell 2011, 22:842-857.
60. 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.
61. 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.
62. 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.
63. Segev N., Mulholland J., Botstein D. The yeast GTP-binding YPT1 protein and a mammalian counterpart are associated with the secretion machinery. Cell 1988, 52:915-924.
64. Sivaram M.V., Furgason M.L., Brewer D.N., Munson M. The structure of the exocyst subunit Sec6p defines a conserved architecture with diverse roles. Nat. Struct. Mol. Biol. 2006, 13:555-556.
65. Strom M., Hume A.N., Tarafder A.K., Barkagianni E., Seabra M.C. A family of Rab27-binding proteins. Melanophilin links Rab27a and myosin Va function in melanosome transport. J. Biol. Chem. 2002, 277:25423-25430.
66. Tabb J.S., Molyneaux B.J., Cohen D.L., Kuznetsov S.A., Langford G.M. Transport of ER vesicles on actin filaments in neurons by myosin V. J. Cell Sci. 1998, 111:3221-3234.
67. Takagishi Y., Oda S., Hayasaka S., Dekker-Ohno K., Shikata T., Inouye M., Yamamura H. The dilute-lethal (dl) gene attacks a Ca2+ store in the dendritic spine of Purkinje cells in mice. Neurosci. Lett. 1996, 215:169-172.
68. TerBush D.R., Maurice T., Roth D., Novick P. The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J. 1996, 15:6483-6494.
69. 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.
70. Tripathi A., Ren Y., Jeffrey P.D., Hughson F.M. Structural characterization of Tip20p and Dsl1p, subunits of the Dsl1p vesicle tethering complex. Nat. Struct. Mol. Biol. 2009, 16:114-123.
71. Vasan N., Hutagalung A., Novick P., Reinisch K.M. Structure of a C-terminal fragment of its Vps53 subunit suggests similarity of Golgi-associated retrograde protein (GARP) complex to a family of tethering complexes. Proc. Natl. Acad. Sci. USA 2010, 107:14176-14181.
72. Wagner W., Bielli P., Wacha S., Ragnini-Wilson A. Mlc1p promotes septum closure during cytokinesis via the IQ motifs of the vesicle motor Myo2p. EMBO J. 2002, 21:6397-6408.
73. 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.
74. Walch-Solimena C., Collins R.N., Novick P.J. Sec2p mediates nucleotide exchange on Sec4p and is involved in polarized delivery of post-Golgi vesicles. J. Cell Biol. 1997, 137:1495-1509.
75. Walworth N.C., Goud B., Kabcenell A.K., Novick P.J. Mutational analysis of SEC4 suggests a cyclical mechanism for the regulation of vesicular traffic. EMBO J. 1989, 8:1685-1693.
76. 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.
77. Wu X., Bowers B., Wei Q., Kocher B., Hammer J.A. Myosin V associates with melanosomes in mouse melanocytes: evidence that myosin V is an organelle motor. J. Cell Sci. 1997, 110:847-859.
78. 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.
79. 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.
80. Wuestehube L.J., Duden R., Eun A., Hamamoto S., Korn P., Ram R., Schekman R. New mutants of Saccharomyces cerevisiae affected in the transport of proteins from the endoplasmic reticulum to the Golgi complex. Genetics 1996, 142:393-406.
81. Zhang X.M., Ellis S., Sriratana A., Mitchell C.A., Rowe T. Sec15 is an effector for the Rab11 GTPase in mammalian cells. J. Biol. Chem. 2004, 279:43027-43034.
82. Zhang X., Wang P., Gangar A., Zhang J., Brennwald P., TerBush D., Guo W. Lethal giant larvae proteins interact with the exocyst complex and are involved in polarized exocytosis. J. Cell Biol. 2005, 170:273-283.