The SNARE protein vti1a functions in dense-core vesicle biogenesis

Walter AM, Kurps J, de Wit H, Schoening S, Toft-Bertelsen TL, Lauks J, Ziomkiewicz I, Weiss AN, Schulz A, Fischer von Mollard G, Verhage M, et al. (2014)
The EMBO Journal 33(15): 1681-1697.

Download
Es wurde kein Volltext hochgeladen. Nur Publikationsnachweis!
Zeitschriftenaufsatz | Veröffentlicht | Englisch
Autor
; ; ; ; ; ; ; ; ; ; ;
Alle
Abstract / Bemerkung
The SNARE protein vti1a is proposed to drive fusion of intracellular organelles, but recent data also implicated vti1a in exocytosis. Here we show that vti1a is absent from mature secretory vesicles in adrenal chromaffin cells, but localizes to a compartment near the trans-Golgi network, partially overlapping with syntaxin-6. Exocytosis is impaired in vti1a null cells, partly due to fewer Ca2+-channels at the plasma membrane, partly due to fewer vesicles of reduced size and synaptobrevin-2 content. In contrast, release kinetics and Ca2+-sensitivity remain unchanged, indicating that the final fusion reaction leading to transmitter release is unperturbed. Additional deletion of the closest related SNARE, vti1b, does not exacerbate the vti1a phenotype, and vti1b null cells show no secretion defects, indicating that vti1b does not participate in exocytosis. Long-term re-expression of vti1a (days) was necessary for restoration of secretory capacity, whereas strong short-term expression (hours) was ineffective, consistent with vti1a involvement in an upstream step related to vesicle generation, rather than in fusion. We conclude that vti1a functions in vesicle generation and Ca2+-channel trafficking, but is dispensable for transmitter release.
Erscheinungsjahr
Zeitschriftentitel
The EMBO Journal
Band
33
Zeitschriftennummer
15
Seite
1681-1697
ISSN
eISSN
PUB-ID

Zitieren

Walter AM, Kurps J, de Wit H, et al. The SNARE protein vti1a functions in dense-core vesicle biogenesis. The EMBO Journal. 2014;33(15):1681-1697.
Walter, A. M., Kurps, J., de Wit, H., Schoening, S., Toft-Bertelsen, T. L., Lauks, J., Ziomkiewicz, I., et al. (2014). The SNARE protein vti1a functions in dense-core vesicle biogenesis. The EMBO Journal, 33(15), 1681-1697. doi:10.15252/embj.201387549
Walter, A. M., Kurps, J., de Wit, H., Schoening, S., Toft-Bertelsen, T. L., Lauks, J., Ziomkiewicz, I., Weiss, A. N., Schulz, A., Fischer von Mollard, G., et al. (2014). The SNARE protein vti1a functions in dense-core vesicle biogenesis. The EMBO Journal 33, 1681-1697.
Walter, A.M., et al., 2014. The SNARE protein vti1a functions in dense-core vesicle biogenesis. The EMBO Journal, 33(15), p 1681-1697.
A.M. Walter, et al., “The SNARE protein vti1a functions in dense-core vesicle biogenesis”, The EMBO Journal, vol. 33, 2014, pp. 1681-1697.
Walter, A.M., Kurps, J., de Wit, H., Schoening, S., Toft-Bertelsen, T.L., Lauks, J., Ziomkiewicz, I., Weiss, A.N., Schulz, A., Fischer von Mollard, G., Verhage, M., Sorensen, J.B.: The SNARE protein vti1a functions in dense-core vesicle biogenesis. The EMBO Journal. 33, 1681-1697 (2014).
Walter, Alexander M., Kurps, Julia, de Wit, Heidi, Schoening, Susanne, Toft-Bertelsen, Trine L., Lauks, Juliane, Ziomkiewicz, Iwona, Weiss, Annita N., Schulz, Alexander, Fischer von Mollard, Gabriele, Verhage, Matthijs, and Sorensen, Jakob B. “The SNARE protein vti1a functions in dense-core vesicle biogenesis”. The EMBO Journal 33.15 (2014): 1681-1697.

14 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Conserved Oligomeric Golgi and Neuronal Vesicular Trafficking.
Climer LK, Hendrix RD, Lupashin VV., Handb Exp Pharmacol 245(), 2018
PMID: 29063274
Control of insulin granule formation and function by the ABC transporters ABCG1 and ABCA1 and by oxysterol binding protein OSBP.
Hussain SS, Harris MT, Kreutzberger AJB, Inouye CM, Doyle CA, Castle AM, Arvan P, Castle JD., Mol Biol Cell 29(10), 2018
PMID: 29540530
Endosomal and Phagosomal SNAREs.
Dingjan I, Linders PTA, Verboogen DRJ, Revelo NH, Ter Beest M, van den Bogaart G., Physiol Rev 98(3), 2018
PMID: 29790818
Vti1a/b regulate synaptic vesicle and dense core vesicle secretion via protein sorting at the Golgi.
Emperador-Melero J, Huson V, van Weering J, Bollmann C, Fischer von Mollard G, Toonen RF, Verhage M., Nat Commun 9(1), 2018
PMID: 30143604
BAIAP3, a C2 domain-containing Munc13 protein, controls the fate of dense-core vesicles in neuroendocrine cells.
Zhang X, Jiang S, Mitok KA, Li L, Attie AD, Martin TFJ., J Cell Biol 216(7), 2017
PMID: 28626000
The dense-core vesicle maturation protein CCCP-1 binds RAB-2 and membranes through its C-terminal domain.
Cattin-Ortolá J, Topalidou I, Dosey A, Merz AJ, Ailion M., Traffic 18(11), 2017
PMID: 28755404
Phosphatidylinositol 4,5-bisphosphate optical uncaging potentiates exocytosis.
Walter AM, Müller R, Tawfik B, Wierda KD, Pinheiro PS, Nadler A, McCarthy AW, Ziomkiewicz I, Kruse M, Reither G, Rettig J, Lehmann M, Haucke V, Hille B, Schultz C, Sørensen JB., Elife 6(), 2017
PMID: 29068313
The EARP Complex and Its Interactor EIPR-1 Are Required for Cargo Sorting to Dense-Core Vesicles.
Topalidou I, Cattin-Ortolá J, Pappas AL, Cooper K, Merrihew GE, MacCoss MJ, Ailion M., PLoS Genet 12(5), 2016
PMID: 27191843
The mechanisms and functions of spontaneous neurotransmitter release.
Kavalali ET., Nat Rev Neurosci 16(1), 2015
PMID: 25524119
Molecular underpinnings of synaptic vesicle pool heterogeneity.
Crawford DC, Kavalali ET., Traffic 16(4), 2015
PMID: 25620674
Defects in the COG complex and COG-related trafficking regulators affect neuronal Golgi function.
Climer LK, Dobretsov M, Lupashin V., Front Neurosci 9(), 2015
PMID: 26578865
The BAR domain protein PICK1 controls vesicle number and size in adrenal chromaffin cells.
Pinheiro PS, Jansen AM, de Wit H, Tawfik B, Madsen KL, Verhage M, Gether U, Sørensen JB., J Neurosci 34(32), 2014
PMID: 25100601

64 References

Daten bereitgestellt von Europe PubMed Central.

Seven novel mammalian SNARE proteins localize to distinct membrane compartments.
Advani RJ, Bae HR, Bock JB, Chao DS, Doung YC, Prekeris R, Yoo JS, Scheller RH., J. Biol. Chem. 273(17), 1998
PMID: 9553086
Synaptotagmin IV is necessary for the maturation of secretory granules in PC12 cells.
Ahras M, Otto GP, Tooze SA., J. Cell Biol. 173(2), 2006
PMID: 16618809
A SNARE complex mediating fusion of late endosomes defines conserved properties of SNARE structure and function.
Antonin W, Holroyd C, Fasshauer D, Pabst S, Von Mollard GF, Jahn R., EMBO J. 19(23), 2000
PMID: 11101518
Crystal structure of the endosomal SNARE complex reveals common structural principles of all SNAREs.
Antonin W, Fasshauer D, Becker S, Jahn R, Schneider TR., Nat. Struct. Biol. 9(2), 2002
PMID: 11786915
Deletion of the SNARE vti1b in mice results in the loss of a single SNARE partner, syntaxin 8.
Atlashkin V, Kreykenbohm V, Eskelinen EL, Wenzel D, Fayyazi A, Fischer von Mollard G., Mol. Cell. Biol. 23(15), 2003
PMID: 12861006
Syntaxin 6 functions in trans-Golgi network vesicle trafficking.
Bock JB, Klumperman J, Davanger S, Scheller RH., Mol. Biol. Cell 8(7), 1997
PMID: 9243506
v-SNAREs control exocytosis of vesicles from priming to fusion.
Borisovska M, Zhao Y, Tsytsyura Y, Glyvuk N, Takamori S, Matti U, Rettig J, Sudhof T, Bruns D., EMBO J. 24(12), 2005
PMID: 15920476
The v-SNARE Vti1a regulates insulin-stimulated glucose transport and Acrp30 secretion in 3T3-L1 adipocytes.
Bose A, Guilherme A, Huang S, Hubbard AC, Lane CR, Soriano NA, Czech MP., J. Biol. Chem. 280(44), 2005
PMID: 16131485
Homotypic fusion of early endosomes: SNAREs do not determine fusion specificity.
Brandhorst D, Zwilling D, Rizzoli SO, Lippert U, Lang T, Jahn R., Proc. Natl. Acad. Sci. U.S.A. 103(8), 2006
PMID: 16469845
Secretory granule exocytosis.
Burgoyne RD, Morgan A., Physiol. Rev. 83(2), 2003
PMID: 12663867
PICK1 and ICA69 control insulin granule trafficking and their deficiencies lead to impaired glucose tolerance.
Cao M, Mao Z, Kam C, Xiao N, Cao X, Shen C, Cheng KK, Xu A, Lee KM, Jiang L, Xia J., PLoS Biol. 11(4), 2013
PMID: 23630453
Structural determinants of synaptobrevin 2 function in synaptic vesicle fusion.
Deak F, Shin OH, Kavalali ET, Sudhof TC., J. Neurosci. 26(25), 2006
PMID: 16793874
Synaptotagmin-IV modulates synaptic function and long-term potentiation by regulating BDNF release.
Dean C, Liu H, Dunning FM, Chang PY, Jackson MB, Chapman ER., Nat. Neurosci. 12(6), 2009
PMID: 19448629
Functional and spatial segregation of secretory vesicle pools according to vesicle age.
Duncan RR, Greaves J, Wiegand UK, Matskevich I, Bodammer G, Apps DK, Shipston MJ, Chow RH., Nature 422(6928), 2003
PMID: 12634788
Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs.
Fasshauer D, Sutton RB, Brunger AT, Jahn R., Proc. Natl. Acad. Sci. U.S.A. 95(26), 1998
PMID: 9861047
Sodium and calcium channels in bovine chromaffin cells.
Fenwick EM, Marty A, Neher E., J. Physiol. (Lond.) 331(), 1982
PMID: 6296372
A new generation of Ca2+ indicators with greatly improved fluorescence properties.
Grynkiewicz G, Poenie M, Tsien RY., J. Biol. Chem. 260(6), 1985
PMID: 3838314
PICK1 deficiency impairs secretory vesicle biogenesis and leads to growth retardation and decreased glucose tolerance.
Holst B, Madsen KL, Jansen AM, Jin C, Rickhag M, Lund VK, Jensen M, Bhatia V, Sorensen G, Madsen AN, Xue Z, Moller SK, Woldbye D, Qvortrup K, Huganir R, Stamou D, Kjærulff O, Gether U., PLoS Biol. 11(4), 2013
PMID: 23630454
Endosomal sorting of readily releasable synaptic vesicles.
Hoopmann P, Punge A, Barysch SV, Westphal V, Buckers J, Opazo F, Bethani I, Lauterbach MA, Hell SW, Rizzoli SO., Proc. Natl. Acad. Sci. U.S.A. 107(44), 2010
PMID: 20956291
A readily retrievable pool of synaptic vesicles.
Hua Y, Sinha R, Thiel CS, Schmidt R, Huve J, Martens H, Hell SW, Egner A, Klingauf J., Nat. Neurosci. 14(7), 2011
PMID: 21666673
SNAREs--engines for membrane fusion.
Jahn R, Scheller RH., Nat. Rev. Mol. Cell Biol. 7(9), 2006
PMID: 16912714
Role of SNAP23 in insulin-induced translocation of GLUT4 in 3T3-L1 adipocytes. Mediation of complex formation between syntaxin4 and VAMP2.
Kawanishi M, Tamori Y, Okazawa H, Araki S, Shinoda H, Kasuga M., J. Biol. Chem. 275(11), 2000
PMID: 10713150
The SNAREs vti1a and vti1b have distinct localization and SNARE complex partners.
Kreykenbohm V, Wenzel D, Antonin W, Atlachkine V, von Mollard GF., Eur. J. Cell Biol. 81(5), 2002
PMID: 12067063
Syntaxin-6 SNARE involvement in secretory and endocytic pathways of cultured pancreatic beta-cells.
Kuliawat R, Kalinina E, Bock J, Fricker L, McGraw TE, Kim SR, Zhong J, Scheller R, Arvan P., Mol. Biol. Cell 15(4), 2004
PMID: 14742717
Lack of the endosomal SNAREs vti1a and vti1b led to significant impairments in neuronal development.
Kunwar AJ, Rickmann M, Backofen B, Browski SM, Rosenbusch J, Schoning S, Fleischmann T, Krieglstein K, Fischer von Mollard G., Proc. Natl. Acad. Sci. U.S.A. 108(6), 2011
PMID: 21262811
CAPS facilitates filling of the rapidly releasable pool of large dense-core vesicles.
Liu Y, Schirra C, Stevens DR, Matti U, Speidel D, Hof D, Bruns D, Brose N, Rettig J., J. Neurosci. 28(21), 2008
PMID: 18495893
Characterization of a novel yeast SNARE protein implicated in Golgi retrograde traffic.
Lupashin VV, Pokrovskaya ID, McNew JA, Waters MG., Mol. Biol. Cell 8(12), 1997
PMID: 9398683
Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform.
Mallard F, Tang BL, Galli T, Tenza D, Saint-Pol A, Yue X, Antony C, Hong W, Goud B, Johannes L., J. Cell Biol. 156(4), 2002
PMID: 11839770
Characterization of the in vitro retrograde transport of MPR46.
Medigeshi GR, Schu P., Traffic 4(11), 2003
PMID: 14617361
Synaptotagmin interaction with SNAP-25 governs vesicle docking, priming, and fusion triggering.
Mohrmann R, de Wit H, Connell E, Pinheiro PS, Leese C, Bruns D, Davletov B, Verhage M, Sorensen JB., J. Neurosci. 33(36), 2013
PMID: 24005294
Different effects on fast exocytosis induced by synaptotagmin 1 and 2 isoforms and abundance but not by phosphorylation.
Nagy G, Kim JH, Pang ZP, Matti U, Rettig J, Sudhof TC, Sorensen JB., J. Neurosci. 26(2), 2006
PMID: 16407561
Combinatorial SNARE complexes with VAMP7 or VAMP8 define different late endocytic fusion events.
Pryor PR, Mullock BM, Bright NA, Lindsay MR, Gray SR, Richardson SC, Stewart A, James DE, Piper RC, Luzio JP., EMBO Rep. 5(6), 2004
PMID: 15133481
VAMP4 directs synaptic vesicles to a pool that selectively maintains asynchronous neurotransmission.
Raingo J, Khvotchev M, Liu P, Darios F, Li YC, Ramirez DM, Adachi M, Lemieux P, Toth K, Davletov B, Kavalali ET., Nat. Neurosci. 15(5), 2012
PMID: 22406549
Vti1a identifies a vesicle pool that preferentially recycles at rest and maintains spontaneous neurotransmission.
Ramirez DM, Khvotchev M, Trauterman B, Kavalali ET., Neuron 73(1), 2012
PMID: 22243751
Emerging roles of presynaptic proteins in Ca++-triggered exocytosis.
Rettig J, Neher E., Science 298(5594), 2002
PMID: 12399579
A guide to super-resolution fluorescence microscopy.
Schermelleh L, Heintzmann R, Leonhardt H., J. Cell Biol. 190(2), 2010
PMID: 20643879
GLUT4 recycles via a trans-Golgi network (TGN) subdomain enriched in Syntaxins 6 and 16 but not TGN38: involvement of an acidic targeting motif.
Shewan AM, van Dam EM, Martin S, Luen TB, Hong W, Bryant NJ, James DE., Mol. Biol. Cell 14(3), 2003
PMID: 12631717
The SNARE protein SNAP-25 is linked to fast calcium triggering of exocytosis.
Sorensen JB, Matti U, Wei SH, Nehring RB, Voets T, Ashery U, Binz T, Neher E, Rettig J., Proc. Natl. Acad. Sci. U.S.A. 99(3), 2002
PMID: 11830673
Examining synaptotagmin 1 function in dense core vesicle exocytosis under direct control of Ca2+.
Sorensen JB, Fernandez-Chacon R, Sudhof TC, Neher E., J. Gen. Physiol. 122(3), 2003
PMID: 12939392
Differential control of the releasable vesicle pools by SNAP-25 splice variants and SNAP-23.
Sorensen JB, Nagy G, Varoqueaux F, Nehring RB, Brose N, Wilson MC, Neher E., Cell 114(1), 2003
PMID: 12859899
The synaptic vesicle cycle.
Sudhof TC., Annu. Rev. Neurosci. 27(), 2004
PMID: 15217342
Membrane fusion: grappling with SNARE and SM proteins.
Sudhof TC, Rothman JE., Science 323(5913), 2009
PMID: 19164740
Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution.
Sutton RB, Fasshauer D, Jahn R, Brunger AT., Nature 395(6700), 1998
PMID: 9759724
The role of Snapin in neurosecretion: snapin knock-out mice exhibit impaired calcium-dependent exocytosis of large dense-core vesicles in chromaffin cells.
Tian JH, Wu ZX, Unzicker M, Lu L, Cai Q, Li C, Schirra C, Matti U, Stevens D, Deng C, Rettig J, Sheng ZH., J. Neurosci. 25(45), 2005
PMID: 16280592
Dissecting docking and tethering of secretory vesicles at the target membrane.
Toonen RF, Kochubey O, de Wit H, Gulyas-Kovacs A, Konijnenburg B, Sorensen JB, Klingauf J, Verhage M., EMBO J. 25(16), 2006
PMID: 16902411
Munc18-1 promotes large dense-core vesicle docking.
Voets T, Toonen RF, Brian EC, de Wit H, Moser T, Rettig J, Sudhof TC, Neher E, Verhage M., Neuron 31(4), 2001
PMID: 11545717
Synaptobrevin N-terminally bound to syntaxin-SNAP-25 defines the primed vesicle state in regulated exocytosis.
Walter AM, Wiederhold K, Bruns D, Fasshauer D, Sorensen JB., J. Cell Biol. 188(3), 2010
PMID: 20142423
Opposing functions of two sub-domains of the SNARE-complex in neurotransmission.
Weber JP, Reim K, Sorensen JB., EMBO J. 29(15), 2010
PMID: 20562829
Homotypic fusion of immature secretory granules during maturation requires syntaxin 6.
Wendler F, Page L, Urbe S, Tooze SA., Mol. Biol. Cell 12(6), 2001
PMID: 11408578
Docking of secretory vesicles is syntaxin dependent.
de Wit H, Cornelisse LN, Toonen RF, Verhage M., PLoS ONE 1(), 2006
PMID: 17205130
Synaptotagmin-1 docks secretory vesicles to syntaxin-1/SNAP-25 acceptor complexes.
de Wit H, Walter AM, Milosevic I, Gulyas-Kovacs A, Riedel D, Sorensen JB, Verhage M., Cell 138(5), 2009
PMID: 19716167
Early endosomal SNAREs form a structurally conserved SNARE complex and fuse liposomes with multiple topologies.
Zwilling D, Cypionka A, Pohl WH, Fasshauer D, Walla PJ, Wahl MC, Jahn R., EMBO J. 26(1), 2006
PMID: 17159904

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 24902738
PubMed | Europe PMC

Suchen in

Google Scholar