Functional impact of syntaxin on gating of N-type and Q-type calcium channels (original) (raw)
- Letter
- Published: 07 December 1995
Nature volume 378, pages 623–626 (1995)Cite this article
- 570 Accesses
- 3 Altmetric
- Metrics details
Abstract
RAPID and reliable synaptic transmission depends upon the close proximity of voltage-gated calcium channels and neurotransmitter-containing vesicles in the presynaptic terminal1. Although it is clear that a local Ca2+ rise conveys the crucial signal from Ca2+ channels to the exocytotic mechanism2, little is known about whether communication ever proceeds in the opposite direction, from the release machinery to Ca2+ channels3,4. To look for such signalling, we examined the interaction of various types of voltage-gated Ca2+ channels with syntaxin, a presynaptic membrane protein of relative molecular mass 35,000 (refs 5–7) which may play a key part in synaptic vesicle docking and fusion8 and which interacts strongly with N-type Ca2+ channels5,6,9–12. Here we report that co-expression of syntaxin 1A with N-type channels in Xenopus oocytes sharply decreases the availability of these channels. This is due to the stabilization of channel inactivation rather than to a simple block or lack of channel expression, because it is overcome by strong hyperpolarization. Deletion of syntaxin's carboxy-terminal transmembrane domain abolishes its functional effect on Ca2+ channels. Syntaxin produced a similar effect on Q-type Ca2+ channels encoded by α1A (refs 13-15) but not on L-type Ca2+-channels. Thus, the syntaxin effect is specific for Ca2+ channel types that participate in fast transmitter release in the mammalian central nervous system (ref. 16 and therein). We hypothesize that, in addition to acting as a vesicle-docking site, syntaxin may influence presynaptic Ca2+ channels, opposing Ca2+ entry where it is not advantageous, but allowing it at release sites where synaptic vesicles have become docked and/or ready for fusion.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Additional access options:
Similar content being viewed by others
References
- Llinas, R., Steinberg, I. Z. & Walton, K. Biophys. J. 33, 323–351 (1981).
Article CAS Google Scholar - Katz, B. The Release of Neural Transmitter Substances (Thomas, Springfield, Illinois, 1969).
Google Scholar - Mastrogiacomo, A. et al. Science 263, 981–982 (1994).
Article ADS CAS Google Scholar - Zinsmaier, K. E., Eberle, K. K., Buchner, E., Walter, N. & Benzer, S. Science 263, 977–980 (1994).
Article ADS CAS Google Scholar - Bennett, M. K., Calakos, N. & Scheller, R. H. Science 257, 255–259 (1992).
Article ADS CAS Google Scholar - Yoshida, A. et al. J. biol. Chem. 267, 24925–24928 (1992).
CAS Google Scholar - Bennett, M. K. et al. Cell 74, 863–873 (1993).
Article CAS Google Scholar - Sollner, T., Bennett, M. K., Whiteheart, S. W., Scheller, R. H. & Rothman, J. E. Cell 75, 409–418 (1993).
Article CAS Google Scholar - Horikawa, H. P. M. et al. FEBS Lett. 330, 236–240 (1993).
Article CAS Google Scholar - Leveque, C. et al. J. biol. Chem. 269, 6306–6312 (1994).
CAS PubMed Google Scholar - el Far, O. et al. FEBS Lett. 361, 101–105 (1995).
Article CAS Google Scholar - Sheng, Z. H., Rettig, J., Takahashi, M. & Catterall, W. A. Neuron 13, 1303–1313 (1994).
Article CAS Google Scholar - Randall, A. & Tsien, R. W. J. Neurosci. 15, 2995–3012 (1995).
Article CAS Google Scholar - Sather, W. A. et al. Neuron 11, 291–303 (1993).
Article CAS Google Scholar - Stea, A. et al. Proc. natn. Acad. Sci. U.S.A. 91, 10576–10580 (1994).
Article ADS CAS Google Scholar - Wheeler, D. B., Tsien, R. W. & Randall, A. Science 266, 830–831 (1994).
Article CAS Google Scholar - Bito, H., Honda, Z., Nakamura, M. & Shimizu, T. Eur. J. Biochem. 221, 211–218 (1994).
Article CAS Google Scholar - Liman, E. R., Tytgat, J. & Hess, P. Neuron 9, 861–871 (1992).
Article CAS Google Scholar - Chapman, E. R., An, S., Barton, N. & Jahn, R. J. biol. Chem. 269, 27427–27432 (1994).
CAS PubMed Google Scholar - Kee, Y., Lin, R. C., Hsu, S. C. & Scheller, R. H. Neuron 14, 991–998 (1995).
Article CAS Google Scholar - McMahon, H. T. & Sudhof, T. C. J. biol. Chem. 270, 2213–2217 (1995).
Article CAS Google Scholar - Hayashi, T., Yamasaki, S., Nauenburg, S., Binz, T. & Niemann, H. EMBO J. 14, 2317–2325 (1995).
Article CAS Google Scholar - Walch-Solimena, C. et al. J. Cell. Biol. 128, 637–645 (1995).
Article CAS Google Scholar - Smirnova, T., Fossier, P., Stinnakre, J., Mallet, J. & Baux, G. Neuroscience 68, 125–133 (1995).
Article CAS Google Scholar - Gundersen, C. B. & Umbach, J. A. Neuron 9, 527–537 (1992).
Article CAS Google Scholar - Ellinor, P. T., Zhang, J.-F., Horne, W. A. & Tsien, R. W. Nature 372, 272–275 (1994).
Article ADS CAS Google Scholar - Bezprozvanny, I. & Tsien, R. W. Molec. Pharmac. 48, 540–549 (1995).
CAS Google Scholar - Mikami, A. et al. Nature 340, 230–233 (1989).
Article ADS CAS Google Scholar - Hullin, R. et al. EMBO J. 11, 885–890 (1992).
Article CAS Google Scholar - Mori, Y. et al. Nature 350, 398–402 (1991).
Article ADS CAS Google Scholar
Author information
Author notes
- R.H. Scheller: Howard Hughes Medical Institute, Beckman Center, Stanford University Medical Center, Stanford, California 94305, USA
- R.W. Tsien: To whom correspondence should be addressed.
Authors and Affiliations
- Department of Molecular and Cellular Physiology,
I. Bezprozvanny, R.H. Scheller & R.W. Tsien - Institute of Cytology, Russian Academy of Sciences, St Petersburg, 194064, Russia
I. Bezprozvanny
Authors
- I. Bezprozvanny
You can also search for this author inPubMed Google Scholar - R.H. Scheller
You can also search for this author inPubMed Google Scholar - R.W. Tsien
You can also search for this author inPubMed Google Scholar
Rights and permissions
About this article
Cite this article
Bezprozvanny, I., Scheller, R. & Tsien, R. Functional impact of syntaxin on gating of N-type and Q-type calcium channels.Nature 378, 623–626 (1995). https://doi.org/10.1038/378623a0
- Received: 14 June 1995
- Accepted: 17 October 1995
- Issue Date: 07 December 1995
- DOI: https://doi.org/10.1038/378623a0