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.

Journal Article | Published | English

No fulltext has been uploaded

Author
; ; ; ; ; ; ; ; ; ; ;
All
Abstract
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.
Publishing Year
ISSN
eISSN
PUB-ID

Cite this

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.
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.
This data publication is cited in the following publications:
This publication cites the following data publications:

4 Citations in Europe PMC

Data provided by Europe PubMed Central.

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
Molecular underpinnings of synaptic vesicle pool heterogeneity.
Crawford DC, Kavalali ET., Traffic 16(4), 2015
PMID: 25620674
The mechanisms and functions of spontaneous neurotransmitter release.
Kavalali ET., Nat. Rev. Neurosci. 16(1), 2015
PMID: 25524119
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, Sorensen JB., J. Neurosci. 34(32), 2014
PMID: 25100601

64 References

Data provided by Europe PubMed Central.

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), 2007
PMID: 17159904

Export

0 Marked Publications

Open Data PUB

Web of Science

View record in Web of Science®

Sources

PMID: 24902738
PubMed | Europe PMC

Search this title in

Google Scholar