The exocyst subunit Sec6 interacts with assembled exocytic SNARE complexes

Journal of Biological Chemistry

Volumn 290, Issue 47, 2015, Pages 28245-28256

  Dubuke, Michelle L ^a   Maniatis, Stephanie ^a   Shaffer, Scott A ^a   Munson, Mary ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; ENZYME ACTIVITY; MASS SPECTROMETRY; PROTEINS; YEAST;

EUKARYOTIC CELLS; EXTRACELLULAR ENVIRONMENTS; GROWTH DEFECTS; INTRACELLULAR COMPARTMENTS; INTRACELLULAR TRAFFICKING; MASS SPECTROMETRY ANALYSIS; PROTEIN COMPLEXES; VESICLE FUSION;

BINS;

SNARE PROTEIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNAPTOSOMAL ASSOCIATED PROTEIN 25 SUBUNIT SEC6; UNCLASSIFIED DRUG; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN; SEC6 PROTEIN, S CEREVISIAE; VESICULAR TRANSPORT PROTEIN;

ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; EXOCYTOSIS; FUNGAL GENE; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; SEC9 GENE; BINDING SITE; METABOLISM; SIZE EXCLUSION CHROMATOGRAPHY;

BINDING SITES; CHROMATOGRAPHY, GEL; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SNARE PROTEINS; VESICULAR TRANSPORT PROTEINS;

EID: 84945314264     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.673806     Document Type: Article

References (77)

1. Jahn, R., and Scheller, R. H. (2006) SNAREs: engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7, 631-643
2. Yu, I.-M., and Hughson, F. M. (2010) Tethering factors as organizers of intracellular vesicular traffic. Annu. Rev. Cell Dev. Biol. 26, 137-156
3. Heider, M. R., and Munson, M. (2012) Exorcising the exocyst complex. Traffic 13, 898-907
4. Rossetto, O., Schiavo, G., Montecucco, C., Poulain, B., Deloye, F., Lozzi, L., and Shone, C. C. (1994) SNARE motif and neurotoxins. Nature 372, 415-416
5. Söllner, T., Whiteheart, S. W., Brunner, M., Erdjument-Bromage, H., Geromanos, S., Tempst, P., and Rothman, J. E. (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318-324
6. Brennwald, P., Kearns, B., Champion, K., Keränen, S., Bankaitis, V., and Novick, P. (1994) Sec9 is a SNAP-25-like component of a yeast SNARE complex that may be the effector of Sec4 function in exocytosis. Cell 79, 245-258
7. Aalto, M. K., Ronne, H., and Keränen, S. (1993) Yeast syntaxins Sso1p and Sso2p belong to a family of related membrane proteins that function in vesicular transport. EMBO J. 12, 4095-4104
8. Gerst, J. E., Rodgers, L., Riggs, M., and Wigler, M. (1992) SNC1, a yeast homolog of the synaptic vesicle-associated membrane protein/synaptobrevin gene family: genetic interactions with the RAS and CAP genes. Proc. Natl. Acad. Sci. U.S.A. 89, 4338-4342
9. Weber, T., Zemelman, B. V., McNew, J. A., Westermann, B., Gmachl, M., Parlati, F., Söllner, T. H., and Rothman, J. E. (1998) SNAREpins: minimal machinery for membrane fusion. Cell 92, 759-772
10. Rice, L. M., Brennwald, P., and Brünger, A. T. (1997) Formation of a yeast SNARE complex is accompanied by significant structural changes. FEBS Lett. 415, 49-55
11. Nicholson, K. L., Munson, M., Miller, R. B., Filip, T. J., Fairman, R., and Hughson, F. M. (1998) Regulation of SNARE complex assembly by an N-terminal domain of the t-SNARE Sso1p. Nat. Struct. Biol. 5, 793-802
12. Fasshauer, D., Bruns, D., Shen, B., Jahn, R., and Brünger, A. T. (1997) A structural change occurs upon binding of syntaxin to SNAP-25. J. Biol. Chem. 272, 4582-4590
13. Söllner, T., Bennett, M. K., Whiteheart, S. W., Scheller, R. H., and Rothman, J. E. (1993) A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75, 409-418
14. Hayashi, T., McMahon, H., Yamasaki, S., Binz, T., Hata, Y., Südhof, T. C., and Niemann, H. (1994) Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly. EMBO J. 13, 5051-5061
15. McNew, J. A., Parlati, F., Fukuda, R., Johnston, R. J., Paz, K., Paumet, F., Söllner, T. H., and Rothman, J. E. (2000) Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature 407, 153-159
16. Izawa, R., Onoue, T., Furukawa, N., and Mima, J. (2012) Distinct contributions of vacuolar Qabc- and R-SNARE proteins to membrane fusion specificity. J. Biol. Chem. 287, 3445-3453
17. Yang, B., Gonzalez, L., Jr., Prekeris, R., Steegmaier, M., Advani, R. J., and Scheller, R. H. (1999) SNARE interactions are not selective: implications for membrane fusion specificity. J. Biol. Chem. 274, 5649-5653
18. Fasshauer, D., Antonin, W., Margittai, M., Pabst, S., and Jahn, R. (1999) Mixed and non-cognate SNARE complexes: characterization of assembly and biophysical properties. J. Biol. Chem. 274, 15440-15446
19. Hohenstein, A. C., and Roche, P. A. (2001) SNAP-29 is a promiscuous syntaxin-binding SNARE. Biochem. Biophys. Res. Commun. 285, 167-171
20. Weimbs, T., Low, S. H., Chapin, S. J., Mostov, K. E., Bucher, P., and Hofmann, K. (1997) A conserved domain is present in different families of vesicular fusion proteins: a new superfamily. Proc. Natl. Acad. Sci. U.S.A. 94, 3046-3051
21. Dietrich, L. E., Boeddinghaus, C., LaGrassa, T. J., and Ungermann, C. (2003) Control of eukaryotic membrane fusion by N-terminal domains of SNARE proteins. Biochim. Biophys. Acta 1641, 111-119
22. Munson, M., Chen, X., Cocina, A. E., Schultz, S. M., and Hughson, F. M. (2000) Interactions within the yeast t-SNARE Sso1p that control SNARE complex assembly. Nat. Struct. Biol. 7, 894-902
23. Medine, C. N., Rickman, C., Chamberlain, L. H., and Duncan, R. R. (2007) Munc18-1 prevents the formation of ectopic SNARE complexes in living cells. J. Cell Sci. 120, 4407-4415
24. Zhang, X., Bi, E., Novick, P., Du, L., Kozminski, K. G., Lipschutz, J. H., and Guo, W. (2001) Cdc42 interacts with the exocyst and regulates polarized secretion. J. Biol. Chem. 276, 46745-46750
25. Zhang, X., Orlando, K., He, B., Xi, F., Zhang, J., Zajac, A., and Guo, W. (2008) Membrane association and functional regulation of Sec3 by phospholipids and Cdc42. J. Cell Biol. 180, 145-158
26. Adamo, J. E., Rossi, G., and Brennwald, P. (1999) The Rho GTPase Rho3 has a direct role in exocytosis that is distinct from its role in actin polarity. Mol. Biol. Cell 10, 4121-4133
27. He, B., Xi, F., Zhang, X., Zhang, J., and Guo, W. (2007) Exo70 interacts with phospholipids and mediates the targeting of the exocyst to the plasma membrane. EMBO J. 26, 4053-4065
28. Yamashita, M., Kurokawa, K., Sato, Y., Yamagata, A., Mimura, H., Yoshikawa, A., Sato, K., Nakano, A., and Fukai, S. (2010) Structural basis for the Rho- and phosphoinositide-dependent localization of the exocyst subunit Sec3. Nat. Struct. Mol. Biol. 17, 180-186
29. Baek, K., Knödler, A., Lee, S. H., Zhang, X., Orlando, K., Zhang, J., Foskett, T. J., Guo, W., and Dominguez, R. (2010) Structure-function study of the N-terminal domain of exocyst subunit Sec3. J. Biol. Chem. 285, 10424-10433
30. Guo, W., Roth, D., Walch-Solimena, C., and Novick, P. (1999) The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J. 18, 1071-1080
31. Wu, H., Turner, C., Gardner, J., Temple, B., and Brennwald, P. (2010) The Exo70 subunit of the exocyst is an effector for both Cdc42 and Rho3 function in polarized exocytosis. Mol. Biol. Cell. 21, 430-442
32. Brunet, S., and Sacher, M. (2014) Are all multisubunit tethering complexes bona fide tethers? Traffic 15, 1282-1287
33. Novick, P., Field, C., and Schekman, R. (1980) Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell 21, 205-215
34. Grote, E., Carr, C. M., and Novick, P. J. (2000) Ordering the final events in yeast exocytosis. J. Cell Biol. 151, 439-452
35. Farré, J.-C., and Subramani, S. (2011) Rallying the exocyst as an autophagy scaffold. Cell 144, 172-174
36. Bodemann, B. O., Orvedahl, A., Cheng, T., Ram, R. R., Ou, Y.-H., Formstecher, E., Maiti, M., Hazelett, C. C., Wauson, E. M., Balakireva, M., Camonis, J. H., Yeaman, C., Levine, B., and White, M. A. (2011) RalB and the exocyst mediate the cellular starvation response by direct activation of autophagosome assembly. Cell 144, 253-267
37. Nichols, C. D., and Casanova, J. E. (2010) Salmonella-directed recruitment of new membrane to invasion foci via the host exocyst complex. Curr. Biol. 20, 1316-1320
38. Sivaram, M. V., Furgason, M. L., Brewer, D. N., and Munson, M. (2006) The structure of the exocyst subunit Sec6p defines a conserved architecture with diverse roles. Nat. Struct. Mol. Biol. 13, 555-556
39. Wu, S., Mehta, S. Q., Pichaud, F., Bellen, H. J., and Quiocho, F. A. (2005) Sec15 interacts with Rab11 via a novel domain and affects Rab11 localization in vivo. Nat. Struct. Mol. Biol. 12, 879-885
40. Dong, G., Hutagalung, A. H., Fu, C., Novick, P., and Reinisch, K. M. (2005) The structures of exocyst subunit Exo70p and the Exo84p C-terminal domains reveal a common motif. Nat. Struct. Mol. Biol. 12, 1094-1100
41. Hamburger, Z. A., Hamburger, A. E., West, A. P., Jr., and Weis, W. I. (2006) Crystal structure of the S. cerevisiae exocyst component Exo70p. J. Mol. Biol. 356, 9-21
42. Moore, B. A., Robinson, H. H., and Xu, Z. (2007) The crystal structure of mouse Exo70 reveals unique features of the mammalian exocyst. J. Mol. Biol. 371, 410-421
43. Croteau, N. J., Furgason, M. L., Devos, D., and Munson, M. (2009) Conservation of helical bundle structure between the exocyst subunits. PLoS ONE 4, e4443
44. Collins, K. M., Thorngren, N. L., Fratti, R. A., and Wickner, W. T. (2005) Sec17p and HOPS, in distinct SNARE complexes, mediate SNARE complex disruption or assembly for fusion. EMBO J. 24, 1775-1786
45. Shestakova, A., Suvorova, E., Pavliv, O., Khaidakova, G., and Lupashin, V. (2007) Interaction of the conserved oligomeric Golgi complex with t- SNARE Syntaxin5a/Sed5 enhances intra-Golgi SNARE complex stability. J. Cell Biol. 179, 1179-1192
46. Sivaram, M. V., Saporita, J. A., Furgason, M. L., Boettcher, A. J., and Munson, M. (2005) Dimerization of the exocyst protein Sec6p and its interaction with the t-SNARE Sec9p. Biochemistry 44, 6302-6311
47. Diefenbacher, M., Thorsteinsdottir, H., and Spang, A. (2011) The Dsl1 tethering complex actively participates in soluble NSF (N-ethylmaleimide- sensitive factor) attachment protein receptor (SNARE) complex assembly at the endoplasmic reticulum in Saccharomyces cerevisiae. J. Biol. Chem. 286, 25027-25038
48. Arasaki, K., Takagi, D., Furuno, A., Sohda, M., Misumi, Y., Wakana, Y., Inoue, H., and Tagaya, M. (2013) A new role for RINT-1 in SNARE complex assembly at the trans-Golgi network in coordination with the COG complex. Mol. Biol. Cell 24, 2907-2917
49. Conibear, E., Cleck, J. N., and Stevens, T. H. (2003) Vps51p mediates the association of the GARP (Vps52/53/54) complex with the late Golgi t- SNARE Tlg1p. Mol. Biol. Cell 14, 1610-1623
50. Pérez-Victoria, F. J., and Bonifacino, J. S. (2009) Dual roles of the mammalian GARP complex in tethering and SNARE complex assembly at the trans-Golgi network. Mol. Cell. Biol. 29, 5251-5263
51. Balderhaar, H. J. K., Lachmann, J., Yavavli, E., Bröcker, C., Lürick, A., and Ungermann, C. (2013) The CORVET complex promotes tethering and fusion of Rab5/Vps21-positive membranes. Proc. Natl. Acad. Sci. U.S.A. 10.1073/pnas.1221785110
52. Lürick, A., Kuhlee, A., Bröcker, C., Kümmel, D., Raunser, S., and Ungermann, C. (2015) The HABC domain of the snare vam3 interacts with the hops tethering complex to facilitate vacuole fusion. J. Biol. Chem. 290, 5405-5413
53. Lobingier, B. T., and Merz, A. J. (2012) Sec1/Munc18 protein Vps33 binds to SNARE domains and the quaternary SNARE complex. Mol. Biol. Cell. 10.1091/mbc.E12-05-0343
54. Krämer, L., and Ungermann, C. (2011) HOPS drives vacuole fusion by binding the vacuolar SNARE complex and the Vam7 PX domain via two distinct sites. Mol. Biol. Cell 22, 2601-2611
55. Starai, V. J., Hickey, C. M., and Wickner, W. (2008) HOPS proofreads the trans-SNARE complex for yeast vacuole fusion. Mol. Biol. Cell 19, 2500-2508
56. Xu, H., Jun, Y., Thompson, J., Yates, J. R., and Wickner, W. T. (2010)HOPS prevents the disassembly of trans-SNARE complexes by Sec17p/Sec18p during membrane fusion. EMBO J. 29, 1948-1960
57. Uversky, V. N. (2013) Unusual biophysics of intrinsically disordered proteins. Biochim. Biophys. Acta 1834, 932-951
58. Uversky, V. N. (2013) A decade and a half of protein intrinsic disorder: biology still waits for physics. Protein Sci. 10.1002/pro.2261
59. Uversky, V. N. (2002) Natively unfolded proteins: a point where biology waits for physics. Protein Sci. 11, 739-756
60. Wright, P. E., and Dyson, H. J. (2015) Intrinsically disordered proteins in cellular signalling and regulation. Nat. Rev. Mol. Cell Biol. 16, 18-29
61. ROSEN, H. (1957) A modified ninhydrin colorimetric analysis for amino acids. Arch. Biochem. Biophys. 67, 10-15
62. Olsen, J. V., Schwartz, J. C., Griep-Raming, J., Nielsen, M. L., Damoc, E., Denisov, E., Lange, O., Remes, P., Taylor, D., Splendore, M., Wouters, E. R., Senko, M., Makarov, A., Mann, M., and Horning, S. (2009) A dual pressure linear ion trap Orbitrap instrument with very high sequencing speed. Mol. Cell. Proteomics 8, 2759-2769
63. Panchaud, A., Singh, P., Shaffer, S. A., and Goodlett, D. R. (2010) xComb: A cross-linked peptide database approach to protein-protein interaction analysis. J. Proteome Res. 9, 2508-2515
64. Radulovic, D., Jelveh, S., Ryu, S., Hamilton, T. G., Foss, E., Mao, Y., and Emili, A. (2004) Informatics platform for global proteomic profiling and biomarker discovery using liquid chromatography-tandem mass spectrometry. Mol. Cell. Proteomics 3, 984-997
65. Brachmann, C. B., Davies, A., Cost, G. J., Caputo, E., Li, J., Hieter, P., and Boeke, J. D. (1998) Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132
66. Gietz, R. D., and Woods, R. A. (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 350, 87-96
67. Sikorski, R. S., and Hieter, P. (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27
68. McLellan, T. (1982) Electrophoresis buffers for polyacrylamide gels at various pH. Anal. Biochem. 126, 94-99
69. Wong, C., Sridhara, S., Bardwell, J. C., and Jakob, U. (2000) Heating greatly speeds Coomassie Blue staining and destaining. BioTechniques 28, 426-428, 430, 432
70. Shen, D., Yuan, H., Hutagalung, A., Verma, A., Kümmel, D., Wu, X., Reinisch, K., McNew, J. A., and Novick, P. (2013) The synaptobrevin homologue Snc2p recruits the exocyst to secretory vesicles by binding to Sec6p. J. Cell Biol. 202, 509-526
71. Wang, L., Merz, A. J., Collins, K. M., and Wickner, W. (2003) Hierarchy of protein assembly at the vertex ring domain for yeast vacuole docking and fusion. J. Cell Biol. 160, 365-374
72. Collins, K. M., and Wickner, W. T. (2007) Trans-SNARE complex assembly and yeast vacuole membrane fusion. Proc. Natl. Acad. Sci. U.S.A. 104, 8755-8760
73. Wiederkehr, A., de Craene, J.-O., Ferro-Novick, S., and Novick, P. (2004) Functional specialization within a vesicle tethering complex: bypass of a subset of exocyst deletion mutants by Sec1p or Sec4p. J. Cell Biol. 167, 875-887
74. Morgera, F., Sallah, M. R., Dubuke, M. L., Gandhi, P., Brewer, D. N., Carr, C. M., and Munson, M. (2012) Regulation of exocytosis by the exocyst subunit Sec6 and the SM protein Sec1. Mol. Biol. Cell. 23, 337-346
75. Laufman, O., Kedan, A., Hong, W., and Lev, S. (2009) Direct interaction between the COG complex and the SM protein, Sly1, is required for Golgi SNARE pairing. EMBO J. 28, 2006-2017
76. Laufman, O., Hong, W., and Lev, S. (2013) The COG complex interacts with multiple Golgi SNAREs and enhances fusogenic assembly of SNARE complexes. J. Cell Sci. 126, 1506-1516
77. Rost, B., Sander, C., and Langridge, R. (2004) SOPM: a self-optimized method for protein secondary structure prediction. Proteins 10.1110/ ps.03503304/full