The N- and C-terminal domains of tomosyn play distinct roles in soluble N-ethylmaleimide-sensitive factor attachment protein receptor binding and fusion regulation

Journal of Biological Chemistry

Volumn 289, Issue 37, 2014, Pages 25571-25580

  Yu, Haijia ^a   Rathore, Shailendra S ^a   Gulbranson, Daniel R ^a   Shen, Jingshi ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINS; CELL MEMBRANES; PROTEINS; THERMONUCLEAR REACTIONS;

INHIBITORY FUNCTION; INSULIN SECRETION; MOLECULAR MECHANISM; N-AND C-TERMINAL DOMAINS; N-TERMINAL DOMAINS; NEUROTRANSMITTER RELEASE; SOLUBLE N-ETHYLMALEIMIDE-SENSITIVE FACTOR ATTACHMENT PROTEIN RECEPTOR; UNIQUE FEATURES;

FUSION REACTIONS;

MEMBRANE PROTEIN; N ETHYLMALEIMIDE; SNARE PROTEIN; SYNTAXIN; TOMOSYN; UNCLASSIFIED DRUG; GLUCOSE TRANSPORTER 4; NERVE PROTEIN; SLC2A4 PROTEIN, HUMAN; STXBP5 PROTEIN, RAT; SYNAPTOBREVIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; IN VITRO STUDY; MEMBRANE FUSION; MOLECULAR DYNAMICS; PROTEIN ASSEMBLY; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; REGULATORY MECHANISM; ANIMAL; CELL MEMBRANE; CHEMISTRY; EXOCYTOSIS; GENETICS; METABOLISM; PC12 CELL LINE; PROTEIN TERTIARY STRUCTURE; RAT; SYNAPTIC TRANSMISSION;

ANIMALS; CELL MEMBRANE; ETHYLMALEIMIDE; EXOCYTOSIS; GLUCOSE TRANSPORTER TYPE 4; MEMBRANE FUSION; NERVE TISSUE PROTEINS; PC12 CELLS; PROTEIN INTERACTION MAPS; PROTEIN STRUCTURE, TERTIARY; QA-SNARE PROTEINS; R-SNARE PROTEINS; RATS; SNARE PROTEINS; SYNAPTIC TRANSMISSION;

EID: 84907171839     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.591487     Document Type: Article

References (76)

1. Südhof, T. C., and Rothman, J. E. (2009) Membrane fusion: grappling with SNARE and SM proteins. Science 323, 474-477
2. Wickner, W., and Schekman, R. (2008) Membrane fusion. Nat. Struct. Mol. Biol. 15, 658-664
3. Rizo, J., and Südhof, T. C. (2012) The membrane fusion enigma: SNAREs, Sec1/Munc18 proteins, and their accomplices-guilty as charged? Annu. Rev. Cell Dev. Biol. 28, 279-308
4. Jahn, R., and Fasshauer, D. (2012) Molecular machines governing exocytosis of synaptic vesicles. Nature 490, 201-207
5. 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
6. Sutton, R. B., Fasshauer, D., Jahn, R., and Brunger, A. T. (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution. Nature 395, 347-353
7. Schwartz, M. L., and Merz, A. J. (2009) Capture and release of partially zipped trans-SNARE complexes on intact organelles. J. Cell Biol. 185, 535-549
8. Burgoyne, R. D., and Morgan, A. (2007) Membrane trafficking: three steps to fusion. Curr. Biol. 17, R255-R258
9. 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
10. Martens, S., and McMahon, H. T. (2008) Mechanisms of membrane fusion: disparate players and common principles. Nat. Rev. Mol. Cell Biol. 9, 543-556
11. Ohya, T., Miaczynska, M., Coskun, U., Lommer, B., Runge, A., Drechsel, D., Kalaidzidis, Y., and Zerial, M. (2009) Reconstitution of Rab- and SNARE-dependent membrane fusion by synthetic endosomes. Nature 459, 1091-1097
12. Katz, L., and Brennwald, P. (2000) Testing the 3Q:1R "rule": mutational analysis of the ionic "zero" layer in the yeast exocytic SNARE complex reveals no requirement for arginine. Mol. Biol. Cell 11, 3849-3858
13. Melia, T. J., Weber, T., McNew, J. A., Fisher, L. E., Johnston, R. J., Parlati, F., Mahal, L. K., Sollner, T. H., and Rothman, J. E. (2002) Regulation of membrane fusion by the membrane-proximal coil of the t-SNARE during zippering of SNAREpins. J. Cell Biol. 158, 929-940
14. Pobbati, A.V., Stein, A., and Fasshauer, D. (2006) N- to C-terminal SNARE complex assembly promotes rapid membrane fusion. Science 313, 673-676
15. 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
16. Gao, Y., Zorman, S., Gundersen, G., Xi, Z., Ma, L., Sirinakis, G., Rothman, J. E., and Zhang, Y. (2012) Single reconstituted neuronal SNARE complexes zipper in three distinct stages. Science 337, 1340-1343
17. Eliasson, L., Abdulkader, F., Braun, M., Galvanovskis, J., Hoppa, M. B., and Rorsman, P. (2008) Novel aspects of the molecular mechanisms controlling insulin secretion. J. Physiol. 586, 3313-3324
18. Rhodes, C. J. (2005) Type 2 diabetes: a matter of β-cell life and death? Science 307, 380-384
19. Sheu, L., Pasyk, E. A., Ji, J., Huang, X., Gao, X., Varoqueaux, F., Brose, N., and Gaisano, H. Y. (2003) Regulation of insulin exocytosis by Munc13-1. J. Biol. Chem. 278, 27556-27563
20. Bryant, N. J., Govers, R., and James, D. E. (2002) Regulated transport of the glucose transporter GLUT4. Nat. Rev. Mol. Cell Biol., 3, 267-277
21. Hou, J. C., and Pessin, J. E. (2007) Ins (endocytosis) and outs (exocytosis) of GLUT4 trafficking. Curr. Opin. Cell Biol. 19, 466-473
22. D'Andrea-Merrins, M., Chang, L., Lam, A. D., Ernst, S. A., and Stuenkel, E. L. (2007) Munc18c interaction with syntaxin 4 monomers and SNARE complex intermediates in GLUT4 vesicle trafficking. J. Biol. Chem. 282, 16553-16566
23. Vicogne, J., Vollenweider, D., Smith, J. R., Huang, P., Frohman, M. A., and Pessin, J. E. (2006) Asymmetric phospholipid distribution drives in vitro reconstituted SNARE-dependent membrane fusion. Proc. Natl. Acad. Sci. U.S.A. 103, 14761-14766
24. Latham, C. F., Lopez, J. A., Hu, S. H., Gee, C. L., Westbury, E., Blair, D. H., Armishaw, C. J., Alewood, P. F., Bryant, N. J., James, D. E., and Martin, J. L. (2006) Molecular dissection of the Munc18c/Syntaxin4 interaction: implications for regulation of membrane trafficking. Traffic 7, 1408-1419
25. Spurlin, B.A., and Thurmond, D. C. (2006) Syntaxin 4 facilitates biphasic glucose-stimulated insulin secretion from pancreatic beta-cells. Mol. Endocrinol. 20, 183-193
26. Ohara-Imaizumi, M., Fujiwara, T., Nakamichi, Y., Okamura, T., Akimoto, Y., Kawai, J., Matsushima, S., Kawakami, H., Watanabe, T., Akagawa, K., and Nagamatsu, S. (2007) Imaging analysis reveals mechanistic differences between first- and second-phase insulin exocytosis. J. Cell Biol. 177, 695-705
27. Jewell, J. L., Oh, E., and Thurmond, D. C. (2010) Exocytosis mechanisms underlying insulin release and glucose uptake: conserved roles for Munc18c and syntaxin 4. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298, R517-R531
28. Widberg, C. H., Bryant, N. J., Girotti, M., Rea, S., and James, D. E. (2003) Tomosyn interacts with the t-SNAREs syntaxin4 and SNAP23 and plays a role in insulin-stimulated GLUT4 translocation. J. Biol. Chem. 278, 35093-35101
29. Cheviet, S., Bezzi, P., Ivarsson, R., Renström, E., Viertl, D., Kasas, S., Catsicas, S., and Regazzi, R. (2006) Tomosyn-1 is involved in a post-docking event required for pancreatic beta-cell exocytosis. J. Cell Sci. 119, 2912-2920
30. Zhang, W., Lilja, L., Mandic, S. A., Gromada, J., Smidt, K., Janson, J., Takai, Y., Bark, C., Berggren, P. O., and Meister, B. (2006) Tomosyn is expressed in beta-cells and negatively regulates insulin exocytosis. Diabetes 55, 574-581
31. Yamamoto, Y., Fujikura, K., Sakaue, M., Okimura, K., Kobayashi, Y., Nakamura, T., and Sakisaka, T. (2010) The tail domain of tomosyn controls membrane fusion through tomosyn displacement by VAMP2. Biochem. Biophys. Res. Commun. 399, 24-30
32. Williams, A. L., Bielopolski, N., Meroz, D., Lam, A. D., Passmore, D. R., Ben-Tal, N., Ernst, S. A., Ashery, U., and Stuenkel, E. L. (2011) Structural and functional analysis of tomosyn identifies domains important in exocytotic regulation. J. Biol. Chem. 286, 14542-14553
33. Gladycheva, S. E., Lam, A. D., Liu, J., D'Andrea-Merrins, M., Yizhar, O., Lentz, S. I., Ashery, U., Ernst, S. A., and Stuenkel, E. L. (2007) Receptormediated regulation of tomosyn-syntaxin 1A interactions in bovine adrenal chromaffin cells. J. Biol. Chem. 282, 22887-22899
34. Ashery, U., Bielopolski, N., Barak, B., and Yizhar, O. (2009) Friends and foes in synaptic transmission: the role of tomosyn in vesicle priming. Trends Neurosci. 32, 275-282
35. Chen, K., Richlitzki, A., Featherstone, D. E., Schwärzel, M., and Richmond, J. E. (2011) Tomosyn-dependent regulation of synaptic transmission is required for a late phase of associative odor memory. Proc. Natl. Acad. Sci. U.S.A. 108, 18482-18487
36. Gracheva, E. O., Burdina, A. O., Holgado, A. M., Berthelot-Grosjean, M., Ackley, B. D., Hadwiger, G., Nonet, M. L., Weimer, R. M., and Richmond, J. E. (2006) Tomosyn inhibits synaptic vesicle priming in Caenorhabditis elegans. PLoS Biol. 4, e261
37. Gracheva, E. O., Burdina, A. O., Touroutine, D., Berthelot-Grosjean, M., Parekh, H., and Richmond, J. E. (2007) Tomosyn negatively regulates both synaptic transmitter and neuropeptide release at the C. elegans neuromuscular junction. J. Physiol. 585, 705-709
38. Hu, Z., Tong, X. J., and Kaplan, J. M. (2013) UNC-13L, UNC-13S, and Tomosyn form a protein code for fast and slow neurotransmitter release in Caenorhabditis elegans. Elife 2, e00967
39. Gracheva, E. O., Burdina, A. O., Touroutine, D., Berthelot-Grosjean, M., Parekh, H., and Richmond, J. E. (2007) Tomosyn negatively regulates CAPS-dependent peptide release at Caenorhabditis elegans synapses. J. Neurosci. 27, 10176-10184
40. Dybbs, M., Ngai, J., and Kaplan, J. M. (2005) Using microarrays to facilitate positional cloning: identification of tomosyn as an inhibitor of neurosecretion. PLoS Genet. 1, 6-16
41. Gracheva, E. O., Maryon, E. B., Berthelot-Grosjean, M., and Richmond, J. E. (2010) Differential regulation of synaptic vesicle tethering and docking by UNC-18 and TOM-1. Front. Synaptic Neurosci. 2, 141
42. Fujita, Y., Shirataki, H., Sakisaka, T., Asakura, T., Ohya, T., Kotani, H., Yokoyama, S., Nishioka, H., Matsuura, Y., Mizoguchi, A., Scheller, R. H., and Takai, Y. (1998) Tomosyn: a syntaxin-1-binding protein that forms a novel complex in the neurotransmitter release process. Neuron 20, 905-915
43. Bhatnagar, S., Oler, A. T., Rabaglia, M. E., Stapleton, D. S., Schueler, K. L., Truchan, N. A., Worzella, S. L., Stoehr, J. P., Clee, S. M., Yandell, B. S., Keller, M. P., Thurmond, D. C., and Attie, A. D. (2011) Positional cloning of a type 2 diabetes quantitative trait locus: tomosyn-2, a negative regulator of insulin secretion. PLoS Genet 7, e1002323
44. Yizhar, O., Lipstein, N., Gladycheva, S. E., Matti, U., Ernst, S. A., Rettig, J., Stuenkel, E. L., and Ashery, U. (2007) Multiple functional domains are involved in tomosyn regulation of exocytosis. J. Neurochem. 103, 604-616
45. Burdina, A. O., Klosterman, S. M., Shtessel, L., Ahmed, S., and Richmond, J. E. (2011) In vivo analysis of conserved C. elegans tomosyn domains. PLoS One 6, e26185
46. Shen, J., Tareste, D. C., Paumet, F., Rothman, J. E., and Melia, T. J. (2007) Selective activation of cognate SNAREpins by Sec1/Munc18 proteins. Cell 128, 183-195
47. Scott, B. L., Van Komen, J. S., Liu, S., Weber, T., Melia, T. J., and McNew, J. A. (2003) Liposome fusion assay to monitor intracellular membrane fusion machines. Methods Enzymol. 372, 274-300
48. Yu, H., Rathore, S. S., Lopez, J. A., Davis, E. M., James, D. E., Martin, J. L., and Shen, J. (2013) Comparative studies of Munc18c and Munc18-1 reveal conserved and divergent mechanisms of Sec1/Munc18 proteins. Proc. Natl. Acad. Sci. U.S.A. 110, E3271-E3280
49. Shen, J., Rathore, S. S., Khandan, L., and Rothman, J. E. (2010) SNARE bundle and syntaxin N-peptide constitute a minimal complement for Munc18-1 activation of membrane fusion. J. Cell Biol. 190, 55-63
50. Yu, H., Rathore, S. S., Davis, E. M., Ouyang, Y., and Shen, J. (2013) Doc2b promotes GLUT4 exocytosis by activating the SNARE-mediated fusion reaction in a calcium- and membrane bending-dependent manner. Mol. Biol. Cell 24, 1176-1184
51. Rathore, S. S., Ghosh, N., Ouyang, Y., and Shen, J. (2011) Topological arrangement of the intracellular membrane fusion machinery. Mol. Biol. Cell 22, 2612-2619
52. Yu, H., Rathore, S. S., and Shen, J. (2013) Synip arrests soluble N-ethylmaleimide- sensitive factor attachment protein receptor (SNARE)-dependent membrane fusion as a selective target membrane SNARE-binding inhibitor. J. Biol. Chem. 288, 18885-18893
53. Groffen, A. J., Jacobsen, L., Schut, D., and Verhage, M. (2005) Two distinct genes drive expression of seven tomosyn isoforms in the mammalian brain, sharing a conserved structure with a unique variable domain. J. Neurochem. 92, 554-568
54. Ishiki, M., and Klip, A. (2005) Minireview: recent developments in the regulation of glucose transporter-4 traffic: new signals, locations, and partners. Endocrinology 146, 5071-5078
55. Yizhar, O., Matti, U., Melamed, R., Hagalili, Y., Bruns, D., Rettig, J., and Ashery, U. (2004) Tomosyn inhibits priming of large dense-core vesicles in a calcium-dependent manner. Proc. Natl. Acad. Sci. U.S.A. 101, 2578-2583
56. Masuda, E. S., Huang, B. C., Fisher, J. M., Luo, Y., and Scheller, R. H. (1998) Tomosyn binds t-SNARE proteins via a VAMP-like coiled coil. Neuron 21, 479-480
57. Yamamoto, Y., Mochida, S., Miyazaki, N., Kawai, K., Fujikura, K., Kurooka, T., Iwasaki, K., and Sakisaka, T. (2010) Tomosyn inhibits synaptotagmin- 1-mediated step of Ca2+-dependent neurotransmitter release through its N-terminal WD40 repeats. J. Biol. Chem. 285, 40943-40955
58. Pobbati, A. V., Razeto, A., Böddener, M., Becker, S., and Fasshauer, D. (2004) Structural basis for the inhibitory role of tomosyn in exocytosis. J. Biol. Chem. 279, 47192-47200
59. Novick, P., and Schekman, R. (1979) Secretion and cell-surface growth are blocked in a temperature-sensitive mutant of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 76, 1858-1862
60. Hata, Y., Slaughter, C. A., and Südhof, T. C. (1993) Synaptic vesicle fusion complex contains unc-18 homologue bound to syntaxin. Nature 366, 347-351
61. Dulubova, I., Khvotchev, M., Liu, S., Huryeva, I., Südhof, T. C., and Rizo, J. (2007) Munc18-1 binds directly to the neuronal SNARE complex. Proc. Natl. Acad. Sci. U.S.A. 104, 2697-2702
62. Schollmeier, Y., Krause, J. M., Kreye, S., Malsam, J., and Söllner, T. H. (2011) Resolving the function of distinct Munc18-1/SNARE protein interaction modes in a reconstituted membrane fusion assay. J. Biol. Chem. 286, 30582-30590
63. Hu, S. H., Latham, C. F., Gee, C. L., James, D. E., and Martin, J. L. (2007) Structure of the Munc18c/Syntaxin4 N-peptide complex defines universal features of the N-peptide binding mode of Sec1/Munc18 proteins. Proc. Natl. Acad. Sci. U.S.A. 104, 8773-8778
64. Tellam, J. T., McIntosh, S., and James, D. E. (1995) Molecular identification of two novel Munc-18 isoforms expressed in non-neuronal tissues. J. Biol. Chem. 270, 5857-5863
65. Jewell, J. L., Oh, E., Ramalingam, L., Kalwat, M. A., Tagliabracci, V. S., Tackett, L., Elmendorf, J. S., and Thurmond, D. C. (2011) Munc18c phosphorylation by the insulin receptor links cell signaling directly to SNARE exocytosis. J. Cell Biol. 193, 185-199
66. Oh, E., Spurlin, B. A., Pessin, J. E., and Thurmond, D. C. (2005) Munc18c heterozygous knockout mice display increased susceptibility for severe glucose intolerance. Diabetes 54, 638-647
67. Oh, E., and Thurmond, D. C. (2009) Munc18c depletion selectively impairs the sustained phase of insulin release. Diabetes 58, 1165-1174
68. Bielopolski, N., Lam, A. D., Bar-On, D., Sauer, M., Stuenkel, E. L., and Ashery, U. (2014) Differential interaction of Tomosyn with syntaxin and SNAP25 depends on domains in the WD40 β-propeller core and determines its inhibitory activity. J. Biol. Chem. 289, 17087-17099
69. Ma, C., Su, L., Seven, A. B., Xu, Y., and Rizo, J. (2013) Reconstitution of the vital functions of Munc18 and Munc13 in neurotransmitter release. Science 339, 421-425
70. Rathore, S. S., Bend, E. G., Yu, H., Hammarlund, M., Jorgensen, E. M., and Shen, J. (2010) Syntaxin N-terminal peptide motif is an initiation factor for the assembly of the SNARE-Sec1/Munc18 membrane fusion complex. Proc. Natl. Acad. Sci. U.S.A. 107, 22399-22406
71. Giraudo, C. G., Garcia-Diaz, A., Eng, W. S., Chen, Y., Hendrickson, W. A., Melia, T. J., and Rothman, J. E. (2009) Alternative zippering as an on-off switch for SNARE-mediated fusion. Science 323, 512-516
72. Giraudo, C. G., Eng, W. S., Melia, T. J., and Rothman, J. E. (2006) A clamping mechanism involved in SNARE-dependent exocytosis. Science 313, 676-680
73. Sakisaka, T., Yamamoto, Y., Mochida, S., Nakamura, M., Nishikawa, K., Ishizaki, H., Okamoto-Tanaka, M., Miyoshi, J., Fujiyoshi, Y., Manabe, T., and Takai, Y. (2008) Dual inhibition of SNARE complex formation by tomosyn ensures controlled neurotransmitter release. J. Cell Biol. 183, 323-337
74. Humphrey, S. J., Yang, G., Yang, P., Fazakerley, D. J., Stöckli, J., Yang, J. Y., and James, D. E. (2013) Dynamic adipocyte phosphoproteome reveals that Akt directly regulates mTORC2. Cell Metab. 17, 1009-1020
75. Lehman, K., Rossi, G., Adamo, J. E., and Brennwald, P. (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
76. Hattendorf, D. A., Andreeva, A., Gangar, A., Brennwald, P. J., and Weis, W. I. (2007) Structure of the yeast polarity protein Sro7 reveals a SNARE regulatory mechanism. Nature 446, 567-571