99
Views
26
CrossRef citations to date
0
Altmetric
Article

Insulin Stimulates Syntaxin4 SNARE Complex Assembly via a Novel Regulatory Mechanism

, &
Pages 1271-1279 | Received 10 Sep 2013, Accepted 07 Jan 2014, Published online: 20 Mar 2023

REFERENCES

  • Bryant NJ, Govers R, James DE. 2002. Regulated transport of the glucose transporter GLUT4. Nat. Rev. Mol. Cell Biol. 3:267–277. http://dx.doi.org/10.1038/nrm782.
  • Bryant NJ, Gould GW. 2011. SNARE proteins underpin insulin-regulated GLUT4 traffic. Traffic 12:657–664. http://dx.doi.org/10.1111/j.1600-0854.2011.01163.x.
  • Ungar D, Hughson FM. 2003. Snare protein structure and function. Annu. Rev. Cell Dev. Biol. 19:493–517. http://dx.doi.org/10.1146/annurev.cellbio.19.110701.155609.
  • Aran V, Bryant NJ, Gould GW. 2011. Tyrosine phosphorylation of Munc18c on residue 521 abrogates binding to Syntaxin 4. BMC Biochem. 12:19. http://dx.doi.org/10.1186/1471-2091-12-19.
  • Jewell JL, Oh E, Ramalingam L, Kalwat MA, Tagliabracci VS, Tackett L, Elmendorf JS, Thurmond DC. 2011. Munc18c phosphorylation by the insulin receptor links cell signaling directly to SNARE exocytosis. J. Cell Biol. 193:185–199. http://dx.doi.org/10.1083/jcb.201007176.
  • Schmelzle K, Kane S, Gridley S, Lienhard GE, White FM. 2006. Temporal dynamics of tyrosine phosphorylation in insulin signaling. Diabetes 55:2171–2179. http://dx.doi.org/10.2337/db06-0148.
  • Aran V, Brandie FM, Boyd AR, Kantidakis T, Rideout EJ, Kelly SM, Gould GW, Bryant NJ. 2009. Characterisation of two distinct binding modes between Syntaxin 4 and Munc18c. Biochem. J. 419:655–660. http://dx.doi.org/10.1042/BJ20082293.
  • Rea S, Martin LB, McIntosh S, Macaulay SL, Ramsdale T, Baldini G, James DE. 1998. Syndet, an adipocyte target SNARE involved in the insulin-induced translocation of GLUT4 to the cell surface. J. Biol. Chem. 273:18784–18792. http://dx.doi.org/10.1074/jbc.273.30.18784.
  • Brandie FM, Aran V, Verma A, McNew JA, Bryant NJ, Gould GW. 2008. Negative regulation of syntaxin4/SNAP-23/VAMP2-mediated membrane fusion by Munc18c in vitro. PLoS One 3:e4074. http://dx.doi.org/10.1371/journal.pone.0004074.
  • Carpp LN, Ciufo LF, Shanks SG, BYoyd A, Bryant NJ. 2006. The Sec1p/Munc18 protein Vps45p binds its cognate SNARE proteins via two distinct modes. J. Cell Biol. 173:927–936. http://dx.doi.org/10.1083/jcb.200512024.
  • Allalou A, Wahlby C. 2009. BlobFinder, a tool for fluorescence microscopy image cytometry. Comput. Methods Programs Biomed. 94:58–65. http://dx.doi.org/10.1016/j.cmpb.2008.08.006.
  • Fredriksson S, Gullberg M, Jarvius J, Olsson C, Pietras K, Gustafsdottir SM, Ostman A, Landegren U. 2002. Protein detection using proximity-dependent DNA ligation assays. Nat. Biotechnol. 20:473–477. http://dx.doi.org/10.1038/nbt0502-473.
  • Söderberg O, Gullberg M, Jarvius M, Ridderstråle K, Leuchowius KJ, Jarvius J, Wester K, Hydbring P, Bahram F, Larsson LG, Landegren U. 2006. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3:995–1000. http://dx.doi.org/10.1038/nmeth947.
  • Weibrecht I, Leuchowius KJ, Clausson CM, Conze T, Jarvius M, Howell WM, Kamali-Moghaddam M, Soderberg O. 2010. Proximity ligation assays: a recent addition to the proteomics toolbox. Expert Rev. Proteomics 7:401–409. http://dx.doi.org/10.1586/epr.10.10.
  • Sutton RB, Fasshauer D, Jahn R, Brunger AT. 1998. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395:347–353. http://dx.doi.org/10.1038/26412.
  • Hickson GR, Chamberlain LH, Maier VH, Gould GW. 2000. Quantification of SNARE protein levels in 3T3-L1 adipocytes: implications for insulin-stimulated glucose transport. Biochem. Biophys. Res. Commun. 270:841–845. http://dx.doi.org/10.1006/bbrc.2000.2525.
  • Chamberlain LH, Gould GW. 2002. The vesicle- and target-SNARE proteins that mediate Glut4 vesicle fusion are localized in detergent-insoluble lipid rafts present on distinct intracellular membranes. J. Biol. Chem. 277:49750–49754. http://dx.doi.org/10.1074/jbc.M206936200.
  • St-Denis JF, Cabaniols JP, Cushman SW, Roche PA. 1999. SNAP-23 participates in SNARE complex assembly in rat adipose cells. Biochem. J. 338:709–715. http://dx.doi.org/10.1042/0264-6021:3380709.
  • Volchuk A, Wang Q, Ewart HS, Liu Z, He L, Bennett MK, Klip A. 1996. Syntaxin 4 in 3T3-L1 adipocytes: regulation by insulin and participation in insulin-dependent glucose transport. Mol. Biol. Cell 7:1075–1082. http://dx.doi.org/10.1091/mbc.7.7.1075.
  • Latham CF, Lopez JA, Hu SH, Gee CL, Westbury E, Blair DH, Armishaw CJ, Alewood PF, Bryant NJ, James DE, Martin JL. 2006. Molecular dissection of the munc18c/syntaxin4 interaction: implications for regulation of membrane trafficking. Traffic 7:1408–1419. http://dx.doi.org/10.1111/j.1600-0854.2006.00474.x.
  • Calakos N, Bennett MK, Peterson KE, Scheller RH. 1994. Protein-protein interactions contributing to the specificity of intracellular vesicular trafficking. Science 263:1146–1149. http://dx.doi.org/10.1126/science.8108733.
  • Hazzard J, Sudhof TC, Rizo J. 1999. NMR analysis of the structure of synaptobrevin and of its interaction with syntaxin. J. Biomol. NMR 14:203–207. http://dx.doi.org/10.1023/A:1008382027065.
  • Liu W, Montana V, Bai J, Chapman ER, Mohideen U, Parpura V. 2006. Single molecule mechanical probing of the SNARE protein interactions. Biophys. J. 91:744–758. http://dx.doi.org/10.1529/biophysj.105.073312.
  • Lang T, Jahn R. 2008. Core proteins of the secretory machinery. Handb. Exp. Pharmacol. 2008:107–127. http://dx.doi.org/10.1007/978-3-540-74805-2_5.
  • Dulubova I, Sugita S, Hill S, Hosaka M, Fernandez I, Südhof TC, Rizo J. 1999. A conformational switch in syntaxin during exocytosis: role of munc18. EMBO J. 18:4372–4382. http://dx.doi.org/10.1093/emboj/18.16.4372.
  • Nicholson KL, Munson M, Miller RB, Filip TJ, Fairman R, Hughson FM. 1998. Regulation of SNARE complex assembly by an N-terminal domain of the t-SNARE Sso1p. Nat. Struct. Biol. 5:793–802. http://dx.doi.org/10.1038/1834.
  • Parlati F, Weber T, McNew JA, Westermann B, Sollner TH, Rothman JE. 1999. Rapid and efficient fusion of phospholipid vesicles by the alpha-helical core of a SNARE complex in the absence of an N-terminal regulatory domain. Proc. Natl. Acad. Sci. U. S. A. 96:12565–12570. http://dx.doi.org/10.1073/pnas.96.22.12565.
  • Flaumenhaft R, Croce K, Chen E, Furie B, Furie BC. 1999. Proteins of the exocytotic core complex mediate platelet alpha-granule secretion. Roles of vesicle-associated membrane protein, SNAP-23, and syntaxin 4. J. Biol. Chem. 274:2492–2501.
  • Scott BL, Van Komen JS, Irshad H, Liu S, Wilson KA, McNew JA. 2004. Sec1p directly stimulates SNARE-mediated membrane fusion in vitro. J. Cell Biol. 167:75–85. http://dx.doi.org/10.1083/jcb.200405018.
  • Shen J, Tareste DC, Paumet F, Rothman JE, Melia TJ. 2007. Selective activation of cognate SNAREpins by Sec1/Munc18 proteins. Cell 128:183–195. http://dx.doi.org/10.1016/j.cell.2006.12.016.
  • Stenkula KG, Lizunov VA, Cushman SW, Zimmerberg J. 2010. Insulin controls the spatial distribution of GLUT4 on the cell surface through regulation of its postfusion dispersal. Cell Metab. 12:250–259. http://dx.doi.org/10.1016/j.cmet.2010.08.005.
  • Hatakeyama H, Kanzaki M. 2011. Molecular basis of insulin-responsive GLUT4 trafficking systems revealed by single molecule imaging. Traffic 12:1805–1820. http://dx.doi.org/10.1111/j.1600-0854.2011.01279.x.
  • Bai L, Wang Y, Fan J, Chen Y, Ji W, Qu A, Xu P, James DE, Xu T. 2007. Dissecting multiple steps of GLUT4 trafficking and identifying the sites of insulin action. Cell Metab. 5:47–57. http://dx.doi.org/10.1016/j.cmet.2006.11.013.
  • Bryant NJ, James DE. 2001. Vps45p stabilizes the syntaxin homologue Tlg2p and positively regulates SNARE complex formation. EMBO J. 20:3380–3388. http://dx.doi.org/10.1093/emboj/20.13.3380.
  • Yu H, Rathore SS, Lopez JA, Davis EM, James DE, Martin JL, 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. http://dx.doi.org/10.1073/pnas.1311232110.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.