Increased activity of the vesicular soluble N-ethylmaleimide-sensitive factor attachment protein receptor TI-VAMP/VAMP7 by tyrosine phosphorylation in the Longin domain

Journal of Biological Chemistry

Volumn 288, Issue 17, 2013, Pages 11960-11972

  Burgo, Andrea ^a,b,e   Casano, Alessandra M ^a,b,f   Kuster, Aurelia ^a,b   Arold, Stefan T ^c   Wang, Guan ^a,b   Nola, Sébastien ^a,b   Verraes, Agathe ^a,b   Dingli, Florent ^d   Loew, Damarys ^d   Galli, Thierry ^a,b  

^a INSTITUT JACQUES MONOD   (France)

^b INSERM   (France)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d INSTITUT CURIE   (France)

^e UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

^f EMBL Heidelberg   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEX FORMATIONS; INSULIN-LIKE GROWTH FACTOR-1; INTRACELLULAR CALCIUM; INTRACELLULAR MEMBRANE FUSION; MOLECULAR MECHANISM; N-TERMINAL EXTENSION; SOLUBLE N-ETHYLMALEIMIDE-SENSITIVE FACTOR ATTACHMENT PROTEIN RECEPTOR; TYROSINE PHOSPHORYLATION;

CELL MEMBRANES; INSULIN; PHOSPHORYLATION;

AMINO ACIDS;

CALCIUM; GLUTAMIC ACID; INSULIN; PHENYLALANINE; PROTEIN TI VAMP; PROTEIN TYROSINE KINASE; PROTEIN VAMP7; SNARE PROTEIN; SOMATOMEDIN C; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL STRAIN COS7; CONTROLLED STUDY; DEPOLARIZATION; EXOCYTOSIS; GENETIC TRANSFECTION; HELA CELL; IN VITRO STUDY; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; EXOCYTOSIS; HELA CELLS; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN-LIKE GROWTH FACTOR I; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; R-SNARE PROTEINS; SNARE PROTEINS; SRC-FAMILY KINASES;

EID: 84876936022     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.415075     Document Type: Article

References (51)

1. Filippini, F., Rossi, V., Galli, T., Budillon, A., D'Urso, M., and D'Esposito, M. (2001) Longins. A new evolutionary conserved VAMP family sharing a novel SNARE domain. Trends Biochem. Sci 26, 407-409
2. Chaineau, M., Danglot, L., and Galli, T. (2009) Multiple roles of the vesicular-SNARE TI-VAMP in post-Golgi and endosomal trafficking. FEBS Lett. 583, 3817-3826
3. Burgo, A., Proux-Gillardeaux, V., Sotirakis, E., Bun, P., Casano, A., Verraes, A., Liem, R. K., Formstecher, E., Coppey-Moisan, M., and Galli, T. (2012) A molecular network for the transport of the TI-VAMP/VAMP7 vesicles from cell center to periphery. Dev. Cell 23, 166-180
4. Scheuber, A., Rudge, R., Danglot, L., Raposo, G., Binz, T., Poncer, J. C., and Galli, T. (2006) Loss of AP-3 function affects spontaneous and evoked release at hippocampal mossy fiber synapses. Proc. Natl. Acad. Sci. U. S. A. 103, 16562-16567
5. Hua, Z., Leal-Ortiz, S., Foss, S. M., Waites, C. L., Garner, C. C., Voglmaier, S. M., and Edwards, R. H. (2011) v-SNARE composition distinguishes synaptic vesicle pools. Neuron 71, 474-487
6. Danglot, L., Zylbersztejn, K., Petkovic, M., Gauberti, M., Meziane, H., Combe, R., Champy, M. F., Birling, M. C., Pavlovic, G., Bizot, J. C., Trovero, F., Della Ragione, F., Proux-Gillardeaux, V., Sorg, T., Vivien, D., D'Esposito, M., and Galli, T. (2012) Absence of TI-VAMP/Vamp7 leads to increased anxiety in mice. J. Neurosci. 32, 1962-1968
7. Verderio, C., Cagnoli, C., Bergami, M., Francolini, M., Schenk, U., Colombo, A., Riganti, L., Frassoni, C., Zuccaro, E., Danglot, L., Wilhelm, C., Galli, T., Canossa, M., and Matteoli, M. (2012) TI-VAMP/VAMP7 is the SNARE of secretory lysosomes contributing to ATP secretion from astrocytes. Biol. Cell 104, 213-228
8. Fader, C. M., Aguilera, M. O., and Colombo, M. I. (2012) ATP is released from autophagic vesicles to the extracellular space in a VAMP7-dependent manner. Autophagy 8, 1741-1756
9. Danglot, L., Chaineau, M., Dahan, M., Gendron, M.-C., Boggetto, N., Perez, F., and Galli, T. (2010) Role of TI-VAMP and CD82 in EGFR cellsurface dynamics and signaling. J. Cell Sci. 123, 723-735
10. Martinez-Arca, S., Alberts, P., Zahraoui, A., Louvard, D., and Galli, T. (2000) Role of tetanus neurotoxin insensitive vesicle-associated membrane protein (TI-VAMP) in vesicular transport mediating neurite outgrowth. J. Cell Biol. 149, 889-900
11. Martinez-Arca, S., Rudge, R., Vacca, M., Raposo, G., Camonis, J., Proux-Gillardeaux, V., Daviet, L., Formstecher, E., Hamburger, A., Filippini, F., D'Esposito, M., and Galli, T. (2003) A dual mechanism controlling the localization and function of exocytic v-SNAREs. Proc. Natl. Acad. Sci. U. S. A. 100, 9011-9016
12. Vivona, S., Liu, C. W., Strop, P., Rossi, V., Filippini, F., and Brunger, A. T. (2010) The longin SNARE VAMP7/TI-VAMP adopts a closed conformation. J. Biol. Chem. 285, 17965-17973
13. Gerst, J. E. (2003) SNARE regulators. Matchmakers and matchbreakers. Biochim. Biophys. Acta 1641, 99-110
14. Snyder, D. A., Kelly, M. L., and Woodbury, D. J. (2006) SNARE complex regulation by phosphorylation. Cell Biochem. Biophys. 45, 111-123
15. Gurd, J. W. (1997) Protein tyrosine phosphorylation. Implications for synaptic function. Neurochem. Int. 31, 635-649
16. Shimazaki, Y., Nishiki, T., Omori, A., Sekiguchi, M., Kamata, Y., Kozaki, S., and Takahashi, M. (1996) Phosphorylation of 25-kDa synaptosome-associated protein. Possible involvement in protein kinase C-mediated regulation of neurotransmitter release. J. Biol. Chem. 271, 14548-14553
17. Rickman, C., and Duncan, R. R. (2010) Munc18/Syntaxin interaction kinetics control secretory vesicle dynamics. J. Biol. Chem. 285, 3965-3972
18. Burgo, A., Sotirakis, E., Simmler, M. C., Verraes, A., Chamot, C., Simpson, J. C., Lanzetti, L., Proux-Gillardeaux, V., and Galli, T. (2009) Role of Varp, a Rab21 exchange factor and TI-VAMP/VAMP7 partner, in neurite growth. EMBO Rep. 10, 1117-1124
19. Muzerelle, A., Alberts, P., Martinez-Arca, S., Jeannequin, O., Lafaye, P., Mazié, J.-C., Galli, T., and Gaspar, P. (2003) Tetanus neurotoxin-insensitive vesicle-associated membrane protein localizes to a presynaptic membrane compartment in selected terminal subsets of the rat brain. Neuroscience 122, 59-75
20. McNew, J. A., Weber, T., Parlati, F., Johnston, R. J., Melia, T. J., Söllner, T. H., and Rothman, J. E. (2000) Close is not enough. SNARE-dependent membrane fusion requires an active mechanism that transduces force to membrane anchors. J. Cell Biol. 150, 105-117
21. Fevrier, B., Vilette, D., Archer, F., Loew, D., Faigle, W., Vidal, M., Laude, H., and Raposo, G. (2004) Cells release prions in association with exosomes. Proc. Natl. Acad. Sci. U. S. A. 101, 9683-9688
22. Danglot, L., Triller, A., and Bessis, A. (2003) Association of gephyrin with synaptic and extrasynaptic GABAA receptors varies during development in cultured hippocampal neurons. Mol. Cell. Neurosci. 23, 264-278
23. Pryor, P. R., Jackson, L., Gray, S. R., Edeling, M. A., Thompson, A., Sanderson, C. M., Evans, P. R., Owen, D. J., and Luzio, J. P. (2008) Molecular basis for the sorting of the SNARE VAMP7 into endocytic clathrin-coated vesicles by the ArfGAP Hrb. Cell 134, 817-827
24. Schäfer, I. B., Hesketh, G. G., Bright, N. A., Gray, S. R., Pryor, P. R., Evans, P. R., Luzio, J. P., and Owen, D. J. (2012) The binding of Varp to VAMP7 traps VAMP7ina closed, fusogenically inactive conformation. Nat. Struct. Mol. Biol. 19, 1300-1309
25. Winn, M. D., Murshudov, G. N., and Papiz, M. Z. (2003) Macromolecular TLS refinement in Refmac at moderate resolutions. Methods Enzymol. 374, 300-321
26. 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
27. Sankaranarayanan, S., and Ryan, T. A. (2000) Real-time measurements of vesicle-SNARE recycling in synapses of the central nervous system. Nat Cell Biol. 2, 197-204
28. Gupton, S. L., and Gertler, F. B. (2010) Integrin signaling switches the cytoskeletal and exocytic machinery that drives neuritogenesis. Dev. Cell 18, 725-736
29. Blakesley, V. A., Scrimgeour, A., Esposito, D., and Le Roith, D. (1996) Signaling via the insulin-like growth factor-I receptor. Does it differ from insulin receptor signaling? Cytokine Growth Factor Rev. 7, 153-159
30. Randhawa, V. K., Thong, F. S., Lim, D. Y., Li, D., Garg, R. R., Rudge, R., Galli, T., Rudich, A., and Klip, A. (2004) Insulin and hypertonicity recruit GLUT4 to the plasma membrane of muscle cells using NSF-dependent SNARE mechanisms but different v-SNAREs. Role of TI-VAMP. Mol. Biol. Cell 15, 5565-5573
31. Bondy, C. A., and Cheng, C. M. (2004) Signaling by insulin-like growth factor 1 in brain. Eur. J. Pharmacol. 490, 25-31
32. Zhao, W. Q., and Alkon, D. L. (2001) Role ofinsulin and insulin receptor in learning and memory. Mol. Cell. Endocrinol. 177, 125-134
33. Chiu, S. L., and Cline, H. T. (2010) Insulin receptor signaling in the development of neuronal structure and function. Neural Dev. 5, 7
34. Plum, L., Schubert, M., and Brüning, J. C. (2005) The role of insulin receptor signaling in the brain. Trends Endocrinol. Metab. 16, 59-65
35. Zhao, W., Cavallaro, S., Gusev, P., and Alkon, D. L. (2000) Nonreceptor tyrosine protein kinase pp60c-src in spatial learning. Synapse-specific changes in its gene expression, tyrosine phosphorylation, and proteinprotein interactions. Proc. Natl. Acad. Sci. U. S. A. 97, 8098-8103
36. Luttrell, L. M., Luttrell, D. K., Parsons, S. J., and Rogol, A. D. (1989) Insulin and phorbol ester induce distinct phosphorylations of pp60c-src in the BC3H-1 murine myocyte cell line. Oncogene 4, 317-324
37. Weller, S. G., Capitani, M., Cao, H., Micaroni, M., Luini, A., Sallese, M., and McNiven, M. A. (2010) Src kinase regulates the integrity and function of the Golgi apparatus via activation of dynamin 2. Proc. Natl. Acad. Sci. U. S. A. 107, 5863-5868
38. Cao, H., Chen, J., Krueger, E. W., and McNiven, M. A. (2010) SRC-mediated phosphorylation of dynamin and cortactin regulates the "constitutive" endocytosis of transferrin. Mol. Cell. Biol. 30, 781-792
39. Nada, S., Okada, M., MacAuley, A., Cooper, J. A., and Nakagawa, H. (1991) Cloning of a complementary DNA for a protein-tyrosine kinase that specifically phosphorylates a negative regulatory site of p60c-src. Nature 351, 69-72
40. Kent, H. M., Evans, P. R., Schäfer, I. B., Gray, S. R., Sanderson, C. M., Luzio, J. P., Peden, A. A., and Owen, D. J. (2012) Structural basis of the intracellular sorting ofthe SNARE VAMP7 by the AP3 adaptor complex. Dev. Cell 22, 979-988
41. Chaineau, M., Danglot, L., Proux-Gillardeaux, V., and Galli, T. (2008) Role of HRB in clathrin-dependent endocytosis. J. Biol. Chem. 283, 34365-34373
42. Yudowski, G. A., Puthenveedu, M. A., and von Zastrow, M. (2006) Distinct modes of regulated receptor insertion to the somatodendritic plasma membrane. Nat. Neurosci. 9, 622-627
43. Martinez-Arca, S., Coco, S., Mainguy, G., Schenk, U., Alberts, P., Bouillé, P., Mezzina, M., Prochiantz, A., Matteoli, M., Louvard, D., and Galli, T. (2001) A common exocytotic mechanism mediates axonal and dendritic outgrowth. J. Neurosci. 21, 3830-3838
44. Linstedt, A. D., Vetter, M. L., Bishop, J. M., and Kelly, R. B. (1992) Specific association ofthe proto-oncogene product pp60c-src with anintracellular organelle, the PC12 synaptic vesicle. J. Cell Biol. 117, 1077-1084
45. Bard, F., Mazelin, L., Péchoux-Longin, C., Malhotra, V., and Jurdic, P. (2003) Src regulates Golgi structure and KDEL receptor-dependent retrograde transport to the endoplasmic reticulum. J. Biol. Chem. 278, 46601-46606
46. Chia, J., Goh, G., Racine, V., Ng, S., Kumar, P., and Bard, F. (2012) RNAi screening reveals a large signaling network controlling the Golgi apparatus in human cells. Mol. Syst. Biol. 8, 629
47. Amanchy, R., Periaswamy, B., Mathivanan, S., Reddy, R., Tattikota, S. G., and Pandey, A. (2007) A curated compendium of phosphorylation motifs. Nat. Biotechnol. 25, 285-286
48. Huang, P., Altshuller, Y. M., Hou, J. C., Pessin, J. E., and Frohman, M. A. (2005) Insulin-stimulated plasma membrane fusion of Glut4 glucose transporter-containing vesicles is regulated by phospholipase D1. Mol. Biol. Cell 16, 2614-2623
49. Blom, N., Gammeltoft, S., and Brunak, S. (1999) Sequence and structurebased prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 294, 1351-1362
50. Blom, N., Sicheritz-Pontén, T., Gupta, R., Gammeltoft, S., and Brunak, S. (2004) Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4, 1633-1649
51. Xue, Y., Ren, J., Gao, X., Jin, C., Wen, L., and Yao, X. (2008) GPS 2.0, a tool to predict kinase-specific phosphorylation sites in hierarchy. Mol. Cell. Proteomics 7, 1598-1608