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Articles, Cellular/Molecular

Membrane-Proximal Tryptophans of Synaptobrevin II Stabilize Priming of Secretory Vesicles

Maria Borisovska, Yvonne N. Schwarz, Madhurima Dhara, Antonio Yarzagaray, Sandra Hugo, Daniele Narzi, Shirley W. I. Siu, Jaideep Kesavan, Ralf Mohrmann, Rainer A. Böckmann and Dieter Bruns
Journal of Neuroscience 7 November 2012, 32 (45) 15983-15997; DOI: https://doi.org/10.1523/JNEUROSCI.6282-11.2012
Maria Borisovska
1Institute for Physiology, School of Medicine, University of Saarland, D-66421 Homburg/Saar, Germany, and
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Yvonne N. Schwarz
1Institute for Physiology, School of Medicine, University of Saarland, D-66421 Homburg/Saar, Germany, and
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Madhurima Dhara
1Institute for Physiology, School of Medicine, University of Saarland, D-66421 Homburg/Saar, Germany, and
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Antonio Yarzagaray
1Institute for Physiology, School of Medicine, University of Saarland, D-66421 Homburg/Saar, Germany, and
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Sandra Hugo
1Institute for Physiology, School of Medicine, University of Saarland, D-66421 Homburg/Saar, Germany, and
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Daniele Narzi
2Computational Biology, Department of Biology, University of Erlangen-Nürnberg, D-91054 Erlangen, Germany
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Shirley W. I. Siu
2Computational Biology, Department of Biology, University of Erlangen-Nürnberg, D-91054 Erlangen, Germany
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Jaideep Kesavan
1Institute for Physiology, School of Medicine, University of Saarland, D-66421 Homburg/Saar, Germany, and
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Ralf Mohrmann
1Institute for Physiology, School of Medicine, University of Saarland, D-66421 Homburg/Saar, Germany, and
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Rainer A. Böckmann
2Computational Biology, Department of Biology, University of Erlangen-Nürnberg, D-91054 Erlangen, Germany
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Dieter Bruns
1Institute for Physiology, School of Medicine, University of Saarland, D-66421 Homburg/Saar, Germany, and
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Abstract

Trans-soluble N-ethylmaleimide-sensitive factor attachment protein (SNAP) receptor (SNARE) complexes formed between the SNARE motifs of synaptobrevin II, SNAP-25, and syntaxin play an essential role in Ca2+-regulated exocytosis. Apart from the well studied interactions of the SNARE domains, little is known about the functional relevance of other evolutionarily conserved structures in the SNARE proteins. Here, we show that substitution of two highly conserved tryptophan residues within the juxtamembrane domain (JMD) of the vesicular SNARE Synaptobrevin II (SybII) profoundly impairs priming of granules in mouse chromaffin cells without altering catecholamine release from single vesicles. Using molecular dynamic simulations of membrane-embedded SybII, we show that Trp residues of the JMD influence the electrostatic surface potential by controlling the position of neighboring lysine and arginine residues at the membrane–water interface. Our observations indicate a decisive role of the tryptophan moiety of SybII in keeping the vesicles in the release-ready state and support a model wherein tryptophan-mediated protein–lipid interactions assist in bridging the apposing membranes before fusion.

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The Journal of Neuroscience: 32 (45)
Journal of Neuroscience
Vol. 32, Issue 45
7 Nov 2012
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Membrane-Proximal Tryptophans of Synaptobrevin II Stabilize Priming of Secretory Vesicles
Maria Borisovska, Yvonne N. Schwarz, Madhurima Dhara, Antonio Yarzagaray, Sandra Hugo, Daniele Narzi, Shirley W. I. Siu, Jaideep Kesavan, Ralf Mohrmann, Rainer A. Böckmann, Dieter Bruns
Journal of Neuroscience 7 November 2012, 32 (45) 15983-15997; DOI: 10.1523/JNEUROSCI.6282-11.2012

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Membrane-Proximal Tryptophans of Synaptobrevin II Stabilize Priming of Secretory Vesicles
Maria Borisovska, Yvonne N. Schwarz, Madhurima Dhara, Antonio Yarzagaray, Sandra Hugo, Daniele Narzi, Shirley W. I. Siu, Jaideep Kesavan, Ralf Mohrmann, Rainer A. Böckmann, Dieter Bruns
Journal of Neuroscience 7 November 2012, 32 (45) 15983-15997; DOI: 10.1523/JNEUROSCI.6282-11.2012
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