Tracking individual secretory vesicles during exocytosis reveals an ordered and regulated process

Journal of Cell Biology

Volumn 210, Issue 2, 2015, Pages 181-189

  Donovan, Kirk W ^a   Bretscher, Anthony ^a  

^a School of Integrative Plant Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXOCYST; FUNGAL PROTEIN; GUANOSINE TRIPHOSPHATE; MYOSIN V; PROTEIN MYO2P; PROTEIN SEC2P; UNCLASSIFIED DRUG; MYO2 PROTEIN, S CEREVISIAE; MYOSIN HEAVY CHAIN; RAB PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SEC4 PROTEIN, S CEREVISIAE;

ARTICLE; DISSOCIATION; EXOCYTOSIS; HYDROLYSIS; MEMBRANE FUSION; MOLECULAR IMAGING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; SECRETORY VESICLE; WILD TYPE; YEAST CELL; FLUORESCENCE MICROSCOPY; METABOLISM; SACCHAROMYCES CEREVISIAE; SECRETORY PATHWAY;

MEMBRANE FUSION; MICROSCOPY, FLUORESCENCE; MYOSIN HEAVY CHAINS; MYOSIN TYPE V; RAB GTP-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SECRETORY PATHWAY; SECRETORY VESICLES;

EID: 84957667091     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201501118     Document Type: Article

References (43)

1. Boyd, C., T. Hughes, M. Pypaert, and P. Novick. 2004. Vesicles carry most exocyst subunits to exocytic sites marked by the remaining two subunits, Sec3p and Exo70p. J. Cell Biol. 167:889-901. http://dx.doi.org/10.1083/jcb.200408124.
2. Brennwald, P., and G. Rossi. 2007. Spatial regulation of exocytosis and cell polarity: yeast as a model for animal cells. FEBS Lett. 581:2119-2124. http://dx.doi.org/10.1016/j.febslet.2007.03.04 3.
3. Carr, C.M., E. Grote, M. Munson, F.M. Hughson, and P.J. Novick. 1999. Sec1p binds to SNARE complexes and concentrates at sites of secretion. J. Cell Biol. 146:333-344. http://dx.doi.org/10.1083/jcb.146.2.333.
4. D'Adamo, P., A. Menegon, C. Lo Nigro, M. Grasso, M. Gulisano, F. Tamanini, T. Bienvenu, A.K. Gedeon, B. Oostra, S.-K. Wu, et al. 1998. Mutations in GDI1 are responsible for X-linked non-specific mental retardation. Nat. Genet. 19:134-139. http://dx.doi.org/10.1038/487.
5. Donovan, K.W., and A. Bretscher. 2012. Myosin-V is activated by binding secretory cargo and released in coordination with Rab/exocyst function. Dev. Cell. 23:769-781. http://dx.doi.org/10.1016/j.devcel.2012.09.001.
6. Donovan, K.W., and A. Bretscher. 2015. Head-to-tail regulation is critical for the in vivo function of myosin V. J. Cell Biol. 209:359-365. http://dx.doi.org/10.1083/jcb.201411010.
7. Evangelista, M., D. Pruyne, D.C. Amberg, C. Boone, and A. Bretscher. 2002. Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat. Cell Biol. 4:32-41. (Corrected and republished in Nat. Cell Biol. 2002. 4:260-269) http://dx.doi.org/10.1038/ncb718.
8. Gao, X.-D., S. Albert, S.E. Tcheperegine, C.G. Burd, D. Gallwitz, and E. Bi. 2003. The GAP activity of Msb3p and Msb4p for the Rab GTPase Sec4p is required for efficient exocytosis and actin organization. J. Cell Biol. 162:635-646. http://dx.doi.org/10.1083/jcb.200302038.
9. Gietz, R.D., R.H. Schiestl, A.R. Willems, and R.A. Woods. 1995. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast. 11:355-360. http://dx.doi.org/10.1002/yea.320110408.
10. Grosshans, B.L., A. Andreeva, A. Gangar, S. Niessen, J.R. Yates III, P. Brennwald, and P. Novick. 2006. The yeast lgl family member Sro7p is an effector of the secretory Rab GTPase Sec4p. J. Cell Biol. 172:55-66. http://dx.doi.org/10.1083/jcb.200510016.
11. Guo, W., D. Roth, C. Walch-Solimena, and P. Novick. 1999. The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J. 18:1071-1080. http://dx.doi.org/10.1093/emboj/18.4.1071.
12. Guo, W., F. Tamanoi, and P. Novick. 2001. Spatial regulation of the exocyst complex by Rho1 GTPase. Nat. Cell Biol. 3:353-360. http://dx.doi.org/10.1038/35070029.
13. Hsu, S.-C., C.D. Hazuka, R. Roth, D.L. Foletti, J. Heuser, and R.H. Scheller. 1998. Subunit composition, protein interactions, and structures of the mammalian brain sec6/8 complex and septin filaments. Neuron. 20:1111-1122. http://dx.doi.org/10.1016/S0896-6273(00)80493-6.
14. Jin, Y., A. Sultana, P. Gandhi, E. Franklin, S. Hamamoto, A.R. Khan, M. Munson, R. Schekman, and L.S. Weisman. 2011. Myosin V transports secretory vesicles via a Rab GTPase cascade and interaction with the exocyst complex. Dev. Cell. 21:1156-1170. http://dx.doi.org/10.1016/j.devcel.2011.10.009.
15. 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. http://dx.doi.org/10.1083/jcb.113.3.539.
16. Lamping, E., K. Tanabe, M. Niimi, Y. Uehara, B.C. Monk, and R.D. Cannon. 2005. Characterization of the Saccharomyces cerevisiae sec6-4 mutation and tools to create S. cerevisiae strains containing the sec6-4 allele. Gene. 361:57-66. http://dx.doi.org/10.1016/j.gene.2005.07.014.
17. Lehman, K., G. Rossi, J.E. Adamo, and P. Brennwald. 1999. Yeast homologues of tomosyn and lethal giant larvae function in exocytosis and are associated with the plasma membrane SNARE, Sec9. J. Cell Biol. 146:125-140. http://dx.doi.org/10.1083/jcb.146.1.125.
18. 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. http://dx.doi.org/10.1083/jcb.125.4.825.
19. Liu, H.P., and A. Bretscher. 1989. Disruption of the single tropomyosin gene in yeast results in the disappearance of actin cables from the cytoskeleton. Cell. 57:233-242. http://dx.doi.org/10.1016/0092-8674(89)90961-6.
20. Longtine, M.S., A. McKenzie III, D.J. Demarini, N.G. Shah, A. Wach, A. Brachat, P. Philippsen, and J.R. Pringle. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast. 14:953-961. http://dx.doi.org/10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U.
21. Luo, G., J. Zhang, and W. Guo. 2014. The role of Sec3p in secretory vesicle targeting and exocyst complex assembly. Mol. Biol. Cell. 25:3813-3822. http://dx.doi.org/10.1091/mbc. E14-04-0907.
22. Mizuno-Yamasaki, E., M. Medkova, J. Coleman, and P. Novick. 2010. Phosphatidylinositol 4-phosphate controls both membrane recruitment and a regulatory switch of the Rab GEF Sec2p. Dev. Cell. 18:828-840. http://dx.doi.org/10.1016/j.devcel.2010.03.016.
23. Morgera, F., M.R. Sallah, M.L. Dubuke, P. Gandhi, D.N. Brewer, C.M. Carr, and M. Munson. 2012. Regulation of exocytosis by the exocyst subunit Sec6 and the SM protein Sec1. Mol. Biol. Cell. 23:337-346. http://dx.doi.org/10.1091/mbc. E11-08-0670.
24. Novick, P., and R. Schekman. 1983. Export of major cell surface proteins is blocked in yeast secretory mutants. J. Cell Biol. 96:541-547. http://dx.doi.org/10.1083/jcb.96.2.541.
25. Novick, P., C. Field, and R. Schekman. 1980. Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell. 21:205-215. http://dx.doi.org/10.1016/0092-8674(80)90128-2.
26. Ortiz, D., M. Medkova, C. Walch-Solimena, and P. Novick. 2002. Ypt32 recruits the Sec4p guanine nucleotide exchange factor, Sec2p, to secretory vesicles; evidence for a Rab cascade in yeast. J. Cell Biol. 157:1005-1016. http://dx.doi.org/10.1083/jcb.200201003.
27. Rivera-Molina, F., and D. Toomre. 2013. Live-cell imaging of exocyst links its spatiotemporal dynamics to various stages of vesicle fusion. J. Cell Biol. 201:673-680. http://dx.doi.org/10.1083/jcb.201212103.
28. Robinson, N.G., L. Guo, J. Imai, A. Toh-E, Y. Matsui, and F. Tamanoi. 1999. Rho3 of Saccharomyces cerevisiae, which regulates the actin cytoskeleton and exocytosis, is a GTPase which interacts with Myo2 and Exo70. Mol. Cell. Biol. 19:3580-3587.
29. Rossi, G., and P. Brennwald. 2011. 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. 22:842-857. http://dx.doi.org/10.1091/mbc. E10-07-0570.
30. Salminen, A., and P.J. Novick. 1987. A ras-like protein is required for a post-Golgi event in yeast secretion. Cell. 49:527-538. http://dx.doi.org/10.1016/0092-8674(87)90455-7.
31. Santiago-Tirado, F.H., A. Legesse-Miller, D. Schott, and A. Bretscher. 2011. PI4P and Rab inputs collaborate in myosin-V-dependent transport ofsecretory compartments in yeast. Dev. Cell. 20:47-59. http://dx.doi.org/10.1016/j.devcel.2010.11.006.
32. Schott, D., J. Ho, D. Pruyne, and A. Bretscher. 1999. The COOH-terminal domain of Myo2p, a yeast myosin V, has a direct role in secretory vesicle targeting. J. Cell Biol. 147:791-808. http://dx.doi.org/10.1083/jcb.147.4.791.
33. Schott, D.H., R.N. Collins, and A. Bretscher. 2002. Secretory vesicle transport velocity in living cells depends on the myosin-V lever arm length. J. Cell Biol. 156:35-40. http://dx.doi.org/10.1083/jcb.200110086.
34. Scott, B.L., J.S. Van Komen, H. Irshad, S. Liu, K.A. Wilson, and J.A. McNew. 2004. Sec1p directly stimulates SNARE-mediated membrane fusion in vitro. J. Cell Biol. 167:75-85. http://dx.doi.org/10.1083/jcb.200405018.
35. Sherman, F. 2002. Getting started with yeast. Methods Enzymol. 350:3-41.
36. Sivaram, M.V.S., J.A. Saporita, M.L.M. Furgason, A.J. Boettcher, and M. Munson. 2005. Dimerization of the exocyst protein Sec6p and its interaction with the t-SNARE Sec9p. Biochemistry. 44:6302-6311.http://dx.doi.org/10.1021/bi048008z
37. Stalder, D., E. Mizuno-Yamasaki, M. Ghassemian, and P.J. Novick. 2013. Phosphorylation of the Rab exchange factor Sec2p directs a switch in regulatory binding partners. Proc. Natl. Acad. Sci. USA. 110:19995-20002. http://dx.doi.org/10.1073/pnas.1320029110.
38. TerBush, D.R., and P. Novick. 1995. Sec6, Sec8, and Sec15 are components of a multisubunit complex which localizes to small bud tips in Saccharomyces cerevisiae. J. Cell Biol. 130:299-312. http://dx.doi.org/10.1083/jcb.130.2.299.
39. Togneri, J., Y.-S. Cheng, M. Munson, F.M. Hughson, and C.M. Carr. 2006. Specific SNARE complex binding mode of the Sec1/Munc-18 protein, Sec1p. Proc. Natl. Acad. Sci. USA. 103:17730-17735. http://dx.doi.org/10.1073/pnas.0605448103.
40. Walch-Solimena, C., R.N. Collins, and P.J. Novick. 1997. Sec2p mediates nucleotide exchange on Sec4p and is involved in polarized delivery of post-Golgi vesicles. J. Cell Biol. 137:1495-1509. http://dx.doi.org/10.1083/jcb.137.7.1495.
41. Walworth, N.C., P. Brennwald, A.K. Kabcenell, M. Garrett, and P. Novick. 1992. 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. 12:2017-2028.
42. Zhang, X., E. Bi, P. Novick, L. Du, K.G. Kozminski, J.H. Lipschutz, and W. Guo. 2001. Cdc42 interacts with the exocyst and regulates polarized secretion. J. Biol. Chem. 276:46745-46750. http://dx.doi.org/10.1074/jbc. M107464200.
43. Zhao, C., J. Takita, Y. Tanaka, M. Setou, T. Nakagawa, S. Takeda, H.W. Yang, S. Terada, T. Nakata, Y. Takei, et al. 2001. Charcot-Marie-Tooth disease type 2A caused by mutation in a microtubule motor KIF1Bbeta. Cell. 105:587-597. http://dx.doi.org/10.1016/S0092-8674(01)00363-4.