Syntaxin opening by the MUN domain underlies the function of Munc13 in synaptic-vesicle priming

Yang, Xiaoyu; Wang, Shen; Sheng, Yi; Zhang, Mingshu; Zou, Wenjuan; Wu, Lijie; Kang, Lijun; Rizo, Josep; Zhang, Rongguang; Xu, Tao; Ma, Cong

doi:10.1038/nsmb.3038

Title: Syntaxin opening by the MUN domain underlies the function of Munc13 in synaptic-vesicle priming

Journal Article · Mon Jun 01 00:00:00 EDT 2015 · Nature Structural & Molecular Biology

DOI:https://doi.org/10.1038/nsmb.3038· OSTI ID:1259896

Yang, Xiaoyu ^[1];

^[1]; Sheng, Yi ^[1]; Zhang, Mingshu ^[2]; Zou, Wenjuan ^[3]; Wu, Lijie ^[4]; Kang, Lijun ^[3]; Rizo, Josep ^[5]; Zhang, Rongguang ^[6]; Xu, Tao ^[7]; Ma, Cong ^[1]

Huazhong Univ. of Science and Technology, Wuhan (China)
Chinese Academy of Sciences (CAS), Beijing (China)
Zhejiang Univ., Hangzhou (China)
Chinese Academy of Sciences (CAS), Shanghai (China)
Univ. of Texas Southwestern Medical Center, Dallas, TX (United States)
Chinese Academy of Sciences (CAS), Beijing (China); Chinese Academy of Sciences (CAS), Shanghai (China)
Huazhong Univ. of Science and Technology, Wuhan (China); Chinese Academy of Sciences (CAS), Beijing (China); Univ. of Chinese Academy of Sciences, Beijing (China)

UNC-13-Munc13s have a central function in synaptic-vesicle priming through their MUN domains. However, it is unclear whether this function arises from the ability of the MUN domain to mediate the transition from the Munc18-1–closed syntaxin-1 complex to the SNARE complex in vitro. The crystal structure of the rat Munc13-1 MUN domain now reveals an elongated, arch-shaped architecture formed by α-helical bundles, with a highly conserved hydrophobic pocket in the middle. Mutation of two residues (NF) in this pocket abolishes the stimulation caused by the Munc13-1 MUN domain on SNARE-complex assembly and on SNARE-dependent proteoliposome fusion in vitro. Moreover, the same mutation in UNC-13 abrogates synaptic-vesicle priming in Caenorhabditis elegans neuromuscular junctions. Here, these results support the notion that orchestration of syntaxin-1 opening and SNARE-complex assembly underlies the central role of UNC-13-Munc13s in synaptic-vesicle priming.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: National Science Foundation of China; National Key Basic Research Program of China; U.S. National Inst. of Health

Grant/Contract Number:: 31370819; 2014CB910203; 31130065; 91313301; NS37200

OSTI ID:: 1259896

Journal Information:: Nature Structural & Molecular Biology, Vol. 22, Issue 7; ISSN 1545-9993

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

Citation Metrics:

Cited by: 116 works

Citation information provided by
Web of Science

References (49)

A conformational switch in syntaxin during exocytosis: role of munc18 Dulubova, I. The EMBO Journal, Vol. 18, Issue 16 https://doi.org/10.1093/emboj/18.16.4372	journal	August 1999
One GABA and two acetylcholine receptors function at the C. elegans neuromuscular junction Richmond, Janet E.; Jorgensen, Erik M. Nature Neuroscience, Vol. 2, Issue 9 https://doi.org/10.1038/12160	journal	September 1999
REFMAC 5 dictionary: organization of prior chemical knowledge and guidelines for its use Vagin, Alexei A.; Steiner, Roberto A.; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12 https://doi.org/10.1107/S0907444904023510	journal	November 2004
The synaptic SNARE complex is a parallel four-stranded helical bundle Poirier, Michelle A.; Xiao, Wenzhong; Macosko, Jed C. Nature Structural Biology, Vol. 5, Issue 9 https://doi.org/10.1038/1799	journal	September 1998
A minimal domain responsible for Munc13 activity Basu, Jayeeta; Shen, Nan; Dulubova, Irina Nature Structural & Molecular Biology, Vol. 12, Issue 11 https://doi.org/10.1038/nsmb1001	journal	October 2005
Tethering Factors as Organizers of Intracellular Vesicular Traffic Yu, I-Mei; Hughson, Frederick M. Annual Review of Cell and Developmental Biology, Vol. 26, Issue 1 https://doi.org/10.1146/annurev.cellbio.042308.113327	journal	November 2010
An open form of syntaxin bypasses the requirement for UNC-13 in vesicle priming Richmond, Janet E.; Weimer, Robby M.; Jorgensen, Erik M. Nature, Vol. 412, Issue 6844 https://doi.org/10.1038/35085583	journal	July 2001
UNC-13 and UNC-10/Rim Localize Synaptic Vesicles to Specific Membrane Domains Weimer, R. M.; Gracheva, E. O.; Meyrignac, O. Journal of Neuroscience, Vol. 26, Issue 31 https://doi.org/10.1523/JNEUROSCI.2350-06.2006	journal	August 2006
Unraveling the mechanisms of synaptotagmin and SNARE function in neurotransmitter release Rizo, Josep; Chen, Xiaocheng; Araç, Demet Trends in Cell Biology, Vol. 16, Issue 7 https://doi.org/10.1016/j.tcb.2006.04.006	journal	July 2006
Munc18-1 in secretion: lonely Munc joins SNARE team and takes control Toonen, Ruud F. G.; Verhage, Matthijs Trends in Neurosciences, Vol. 30, Issue 11 https://doi.org/10.1016/j.tins.2007.08.008	journal	November 2007
The Crystal Structure of Mouse Exo70 Reveals Unique Features of the Mammalian Exocyst Moore, Brian A.; Robinson, Howard H.; Xu, Zhaohui Journal of Molecular Biology, Vol. 371, Issue 2 https://doi.org/10.1016/j.jmb.2007.05.018	journal	August 2007
Tomosyn Inhibits Synaptic Vesicle Priming in Caenorhabditis elegans Gracheva, Elena O.; Burdina, Anna O.; Holgado, Andrea M. PLoS Biology, Vol. 4, Issue 8 https://doi.org/10.1371/journal.pbio.0040261	journal	July 2006
Drosophila Unc-13 is essential for synaptic transmission Aravamudan, Bharathi; Fergestad, Tim; Davis, Warren S. Nature Neuroscience, Vol. 2, Issue 11 https://doi.org/10.1038/14764	journal	November 1999
A common molecular basis for membrane docking and functional priming of synaptic vesicles Siksou, Léa; Varoqueaux, Frédérique; Pascual, Olivier European Journal of Neuroscience, Vol. 30, Issue 1 https://doi.org/10.1111/j.1460-9568.2009.06811.x	journal	July 2009
Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming Varoqueaux, F.; Sigler, A.; Rhee, J. -S. Proceedings of the National Academy of Sciences, Vol. 99, Issue 13 https://doi.org/10.1073/pnas.122623799	journal	June 2002
RIM Proteins Activate Vesicle Priming by Reversing Autoinhibitory Homodimerization of Munc13 Deng, Lunbin; Kaeser, Pascal S.; Xu, Wei Neuron, Vol. 69, Issue 2 https://doi.org/10.1016/j.neuron.2011.01.005	journal	January 2011
Structural characterization of Tip20p and Dsl1p, subunits of the Dsl1p vesicle tethering complex Tripathi, Arati; Ren, Yi; Jeffrey, Philip D. Nature Structural & Molecular Biology, Vol. 16, Issue 2 https://doi.org/10.1038/nsmb.1548	journal	January 2009
Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles Augustin, Iris; Rosenmund, Christian; Südhof, Thomas C. Nature, Vol. 400, Issue 6743 https://doi.org/10.1038/22768	journal	July 1999
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Conformational Switch of Syntaxin-1 Controls Synaptic Vesicle Fusion Gerber, Stefan H.; Rah, Jong-Cheol; Min, Sang-Won Science, Vol. 321, Issue 5895 https://doi.org/10.1126/science.1163174	journal	August 2008
Munc18-1 binds directly to the neuronal SNARE complex Dulubova, I.; Khvotchev, M.; Liu, S. Proceedings of the National Academy of Sciences, Vol. 104, Issue 8 https://doi.org/10.1073/pnas.0611318104	journal	February 2007
UNC-13 is required for synaptic vesicle fusion in C. elegans Richmond, Janet E.; Davis, Warren S.; Jorgensen, Erik M. Nature Neuroscience, Vol. 2, Issue 11 https://doi.org/10.1038/14755	journal	November 1999
Selective Activation of Cognate SNAREpins by Sec1/Munc18 Proteins Shen, Jingshi; Tareste, David C.; Paumet, Fabienne Cell, Vol. 128, Issue 1 https://doi.org/10.1016/j.cell.2006.12.016	journal	January 2007
Munc13 mediates the transition from the closed syntaxin–Munc18 complex to the SNARE complex Ma, Cong; Li, Wei; Xu, Yibin Nature Structural & Molecular Biology, Vol. 18, Issue 5 https://doi.org/10.1038/nsmb.2047	journal	April 2011
Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution Sutton, R. Bryan; Fasshauer, Dirk; Jahn, Reinhard Nature, Vol. 395, Issue 6700 https://doi.org/10.1038/26412	journal	September 1998
Single-Molecule Studies of the Neuronal SNARE Fusion Machinery Brunger, Axel T.; Weninger, Keith; Bowen, Mark Annual Review of Biochemistry, Vol. 78, Issue 1 https://doi.org/10.1146/annurev.biochem.77.070306.103621	journal	June 2009
UNC-13L, UNC-13S, and Tomosyn form a protein code for fast and slow neurotransmitter release in Caenorhabditis elegans Hu, Zhitao; Tong, Xia-Jing; Kaplan, Joshua M. eLife, Vol. 2 https://doi.org/10.7554/eLife.00967	journal	August 2013
The Membrane Fusion Enigma: SNAREs, Sec1/Munc18 Proteins, and Their Accomplices—Guilty as Charged? Rizo, Josep; Südhof, Thomas C. Annual Review of Cell and Developmental Biology, Vol. 28, Issue 1 https://doi.org/10.1146/annurev-cellbio-101011-155818	journal	November 2012
Definition of the Readily Releasable Pool of Vesicles at Hippocampal Synapses Rosenmund, Christian; Stevens, Charles F. Neuron, Vol. 16, Issue 6 https://doi.org/10.1016/S0896-6273(00)80146-4	journal	June 1996
Reconstitution of the Vital Functions of Munc18 and Munc13 in Neurotransmitter Release Ma, C.; Su, L.; Seven, A. B. Science, Vol. 339, Issue 6118 https://doi.org/10.1126/science.1230473	journal	December 2012
Identification of the Minimal Protein Domain Required for Priming Activity of Munc13-1 Stevens, David R.; Wu, Zheng-Xing; Matti, Ulf Current Biology, Vol. 15, Issue 24 https://doi.org/10.1016/j.cub.2005.10.055	journal	December 2005
SNAREs — engines for membrane fusion Jahn, Reinhard; Scheller, Richard H. Nature Reviews Molecular Cell Biology, Vol. 7, Issue 9 https://doi.org/10.1038/nrm2002	journal	August 2006
The structure of the exocyst subunit Sec6p defines a conserved architecture with diverse roles Sivaram, Mylavarapu V. S.; Furgason, Melonnie L. M.; Brewer, Daniel N. Nature Structural & Molecular Biology, Vol. 13, Issue 6 https://doi.org/10.1038/nsmb1096	journal	May 2006
The Crystal Structure of a Munc13 C-terminal Module Exhibits a Remarkable Similarity to Vesicle Tethering Factors Li, Wei; Ma, Cong; Guan, Rong Structure, Vol. 19, Issue 10 https://doi.org/10.1016/j.str.2011.07.012	journal	October 2011
Remote Homology between Munc13 MUN Domain and Vesicle Tethering Complexes Pei, Jimin; Ma, Cong; Rizo, Josep Journal of Molecular Biology, Vol. 391, Issue 3 https://doi.org/10.1016/j.jmb.2009.06.054	journal	August 2009
The structures of exocyst subunit Exo70p and the Exo84p C-terminal domains reveal a common motif Dong, Gang; Hutagalung, Alex H.; Fu, Chunmei Nature Structural & Molecular Biology, Vol. 12, Issue 12 https://doi.org/10.1038/nsmb1017	journal	October 2005
The CC1-FHA dimer is essential for KIF1A-mediated axonal transport of synaptic vesicles in C. elegans Yue, Yang; Sheng, Yi; Zhang, Hai-Ning Biochemical and Biophysical Research Communications, Vol. 435, Issue 3 https://doi.org/10.1016/j.bbrc.2013.05.005	journal	June 2013
Three-dimensional structure of the neuronal-Sec1–syntaxin 1a complex Misura, Kira M. S.; Scheller, Richard H.; Weis, William I. Nature, Vol. 404, Issue 6776 https://doi.org/10.1038/35006120	journal	March 2000
Open Syntaxin Docks Synaptic Vesicles Hammarlund, Marc; Palfreyman, Mark T.; Watanabe, Shigeki PLoS Biology, Vol. 5, Issue 8 https://doi.org/10.1371/journal.pbio.0050198	journal	July 2007
A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion Söllner, Thomas; Bennett, Mark K.; Whiteheart, Sidney W. Cell, Vol. 75, Issue 3 https://doi.org/10.1016/0092-8674(93)90376-2	journal	November 1993
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
UNC-13 Interaction with Syntaxin Is Required for Synaptic Transmission Madison, Jon M.; Nurrish, Stephen; Kaplan, Joshua M. Current Biology, Vol. 15, Issue 24 https://doi.org/10.1016/j.cub.2005.10.049	journal	December 2005
A post-docking role for active zone protein Rim Koushika, Sandhya P.; Richmond, Janet E.; Hadwiger, Gayla Nature Neuroscience, Vol. 4, Issue 10 https://doi.org/10.1038/nn732	journal	September 2001
C. elegans TRP Family Protein TRP-4 Is a Pore-Forming Subunit of a Native Mechanotransduction Channel Kang, Lijun; Gao, Jingwei; Schafer, William R. Neuron, Vol. 67, Issue 3 https://doi.org/10.1016/j.neuron.2010.06.032	journal	August 2010
Optogenetic analysis of synaptic function Liewald, Jana F.; Brauner, Martin; Stephens, Greg J. Nature Methods, Vol. 5, Issue 10 https://doi.org/10.1038/nmeth.1252	journal	September 2008
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Regulation of transmitter release by Unc-13 and its homologues Brose, Nils; Rosenmund, Christian; Rettig, Jens Current Opinion in Neurobiology, Vol. 10, Issue 3 https://doi.org/10.1016/S0959-4388(00)00105-7	journal	June 2000
GENETIC ORGANIZATION OF THE REGION AROUND UNC-15 (I), A GENE AFFECTING PARAMYOSIN IN CAENORHABDITIS ELEGANS Rose, A. M.; Baillie, D. L. Genetics, Vol. 96, Issue 3 https://doi.org/10.1093/genetics/96.3.639	journal	November 1980
THE GENETICS OF CAENORHABDITIS ELEGANS Brenner, S. Genetics, Vol. 77, Issue 1 https://doi.org/10.1093/genetics/77.1.71	journal	May 1974

Cited By (46)

OSM-9 and an amiloride-sensitive channel, but not PKD-2, are involved in mechanosensation in C. elegans male ray neurons Zhang, Hu; Yue, Xiaomin; Cheng, Hankui Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-25542-1	journal	May 2018
Autoinhibition of Munc18-1 modulates synaptobrevin binding and helps to enable Munc13-dependent regulation of membrane fusion Sitarska, Ewa; Xu, Junjie; Park, Seungmee eLife, Vol. 6 https://doi.org/10.7554/elife.24278	journal	May 2017
Decoding the intensity of sensory input by two glutamate receptors in one C. elegans interneuron. Zou, Wenjuan; Fu, Jiajun; Zhang, Haining Springer Science and Business Media LLC https://doi.org/10.17863/cam.33518	journalarticle	January 2018
Munc18 and Munc13 serve as a functional template to orchestrate neuronal SNARE complex assembly Wang, Shen; Li, Yun; Gong, Jihong Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-018-08028-6	journal	January 2019
Sec3 promotes the initial binary t-SNARE complex assembly and membrane fusion Yue, Peng; Zhang, Yubo; Mei, Kunrong Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms14236	journal	January 2017
Golgi SM protein Sly1 promotes productive trans -SNARE complex assembly through multiple mechanisms Duan, M.; Gao, G.; Banfield, D. K. https://doi.org/10.1101/2020.01.16.909630	preprint	January 2020
Membrane bridging by Munc13-1 is crucial for neurotransmitter release Quade, Bradley; Camacho, Marcial; Zhao, Xiaowei eLife, Vol. 8 https://doi.org/10.7554/elife.42806	journal	February 2019
The Vesicle Priming Factor CAPS Functions as a Homodimer via C2 Domain Interactions to Promote Regulated Vesicle Exocytosis. Petrie, Matt; Esquibel, Joseph; Kabachinski, Greg Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.27895	text	January 2016
HID-1 is required for homotypic fusion of immature secretory granules during maturation Du, Wen; Zhou, Maoge; Zhao, Wei eLife, Vol. 5 https://doi.org/10.7554/elife.18134	journal	October 2016
Heterodimerization of UNC-13/RIM regulates synaptic vesicle release probability but not priming Liu, Haowen; Li, Lei; Nedelcu, Daniel eLife https://doi.org/10.1101/388868	posted_content	August 2018
Munc13-1 MUN domain and Munc18-1 cooperatively chaperone SNARE assembly through a tetrameric complex Shu, Tong; Jin, Huaizhou; Rothman, James E. Proceedings of the National Academy of Sciences, Vol. 117, Issue 2 https://doi.org/10.1073/pnas.1914361117	journal	December 2019
Heterodimerization of UNC-13/RIM regulates synaptic vesicle release probability but not priming in C. elegans Liu, Haowen; Li, Lei; Nedelcu, Daniel eLife, Vol. 8 https://doi.org/10.7554/elife.40585	journal	February 2019
Decoding the intensity of sensory input by two glutamate receptors in one C. elegans interneuron Zou, Wenjuan; Fu, Jiajun; Zhang, Haining Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-06819-5	journal	October 2018
The Vesicle Priming Factor CAPS Functions as a Homodimer via C2 Domain Interactions to Promote Regulated Vesicle Exocytosis Petrie, Matt; Esquibel, Joseph; Kabachinski, Greg Journal of Biological Chemistry, Vol. 291, Issue 40 https://doi.org/10.1074/jbc.m116.728097	journal	August 2016
Munc18-1 is crucial to overcome the inhibition of synaptic vesicle fusion by αSNAP Stepien, Karolina P.; Prinslow, Eric A.; Rizo, Josep Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-12188-4	journal	September 2019
A Stimulation Function of Synaptotagmin-1 in Ternary SNARE Complex Formation Dependent on Munc18 and Munc13 Li, Yun; Wang, Shen; Li, Tianzhi Frontiers in Molecular Neuroscience, Vol. 10 https://doi.org/10.3389/fnmol.2017.00256	journal	August 2017
Open syntaxin overcomes synaptic transmission defects in diverse C. elegans exocytosis mutants Tien, Chi-Wei; Yu, Bin; Huang, Mengjia Nature Communications https://doi.org/10.1101/2020.01.10.901835	posted_content	January 2020
Gβγ SNARE Interactions and Their Behavioral Effects Alford, Simon; Hamm, Heidi; Rodriguez, Shelagh Neurochemical Research, Vol. 44, Issue 3 https://doi.org/10.1007/s11064-018-2531-x	journal	May 2018
Tomosyn guides SNARE complex formation in coordination with Munc18 and Munc13 Li, Yun; Wang, Shen; Li, Tianzhi FEBS Letters, Vol. 592, Issue 7 https://doi.org/10.1002/1873-3468.13018	journal	February 2018
Structure of membrane tethers and their role in fusion Ungermann, Christian; Kümmel, Daniel Traffic, Vol. 20, Issue 7 https://doi.org/10.1111/tra.12655	journal	May 2019
Serotonergic neuron ADF modulates avoidance behaviors by inhibiting sensory neurons in C. elegans Shao, Jiajie; Zhang, Xiaoyan; Cheng, Hankui Pflügers Archiv - European Journal of Physiology, Vol. 471, Issue 2 https://doi.org/10.1007/s00424-018-2202-4	journal	September 2018
Correction: ELKS1 localizes the synaptic vesicle priming protein bMunc13-2 to a specific subset of active zones Kawabe, Hiroshi; Mitkovski, Miso; Kaeser, Pascal S. Journal of Cell Biology, Vol. 216, Issue 4 https://doi.org/10.1083/jcb.20160608603092017c	journal	March 2017
Rare genetic variation in UNC13A may modify survival in amyotrophic lateral sclerosis Gaastra, Benjamin; Shatunov, Aleksey; Pulit, Sara Amyotrophic Lateral Sclerosis and Frontotemporal Degeneration, Vol. 17, Issue 7-8 https://doi.org/10.1080/21678421.2016.1213852	journal	September 2016
Simultaneous lipid and content mixing assays for in vitro reconstitution studies of synaptic vesicle fusion Liu, Xiaoxia; Seven, Alpay Burak; Xu, Junjie Nature Protocols, Vol. 12, Issue 9 https://doi.org/10.1038/nprot.2017.068	journal	August 2017
Munc18-1 catalyzes neuronal SNARE assembly by templating SNARE association Jiao, Junyi; He, Mengze; Port, Sarah A. eLife, Vol. 7 https://doi.org/10.7554/elife.41771	journal	December 2018
ELKS1 localizes the synaptic vesicle priming protein bMunc13-2 to a specific subset of active zones Kawabe, Hiroshi; Mitkovski, Miso; Kaeser, Pascal S. Journal of Cell Biology, Vol. 216, Issue 4 https://doi.org/10.1083/jcb.201606086	journal	March 2017
Identification of a Munc13-sensitive step in chromaffin cell large dense-core vesicle exocytosis Man, Kwun Nok M.; Imig, Cordelia; Walter, Alexander M. eLife, Vol. 4 https://doi.org/10.7554/elife.10635	journal	November 2015
SNARE zippering requires activation by SNARE-like peptides in Sec1/Munc18 proteins Yu, Haijia; Shen, Chong; Liu, Yinghui Proceedings of the National Academy of Sciences, Vol. 115, Issue 36 https://doi.org/10.1073/pnas.1802645115	journal	August 2018
Roles of the fission yeast UNC-13/Munc13 protein Ync13 in late stages of cytokinesis Zhu, Yi-Hua; Hyun, Joanne; Pan, Yun-Zu Molecular Biology of the Cell, Vol. 29, Issue 19 https://doi.org/10.1091/mbc.e18-04-0225	journal	September 2018
C2-domain containing calcium sensors in neuroendocrine secretion Pinheiro, Paulo S.; Houy, Sébastien; Sørensen, Jakob B. Journal of Neurochemistry, Vol. 139, Issue 6 https://doi.org/10.1111/jnc.13865	journal	November 2016
Multiple factors maintain assembled trans-SNARE complexes in the presence of NSF and αSNAP Prinslow, Eric A.; Stepien, Karolina P.; Pan, Yun-Zu eLife, Vol. 8 https://doi.org/10.7554/elife.38880	journal	January 2019
Mechanism of neurotransmitter release coming into focus: Mechanism of Neurotransmitter Release Rizo, Josep Protein Science, Vol. 27, Issue 8 https://doi.org/10.1002/pro.3445	journal	July 2018
A Systematic RNAi Screen Reveals a Novel Role of a Spindle Assembly Checkpoint Protein BuGZ in Synaptic Transmission in C. elegans Han, Mei; Zou, Wenjuan; Chang, Hao Frontiers in Molecular Neuroscience, Vol. 10 https://doi.org/10.3389/fnmol.2017.00141	journal	May 2017
Chaperoning SNARE assembly and disassembly Baker, Richard W.; Hughson, Frederick M. Nature Reviews Molecular Cell Biology, Vol. 17, Issue 8 https://doi.org/10.1038/nrm.2016.65	journal	June 2016
The control of release probability at nerve terminals Dittman, Jeremy S.; Ryan, Timothy A. Nature Reviews Neuroscience, Vol. 20, Issue 3 https://doi.org/10.1038/s41583-018-0111-3	journal	January 2019
Munc18-2, but not Munc18-1 or Munc18-3, controls compound and single-vesicle–regulated exocytosis in mast cells Gutierrez, Berenice A.; Chavez, Miguel A.; Rodarte, Alejandro I. Journal of Biological Chemistry, Vol. 293, Issue 19 https://doi.org/10.1074/jbc.ra118.002455	journal	March 2018
Synaptotagmin-1 C2B domain interacts simultaneously with SNAREs and membranes to promote membrane fusion Wang, Shen; Li, Yun; Ma, Cong eLife, Vol. 5 https://doi.org/10.7554/elife.14211	journal	April 2016
Mechanistic insights into neurotransmitter release and presynaptic plasticity from the crystal structure of Munc13-1 C1C2BMUN Xu, Junjie; Camacho, Marcial; Xu, Yibin eLife, Vol. 6 https://doi.org/10.7554/elife.22567	journal	February 2017
Molecular mechanisms of contractile-ring constriction and membrane trafficking in cytokinesis Gerien, Kenneth S.; Wu, Jian-Qiu Biophysical Reviews, Vol. 10, Issue 6 https://doi.org/10.1007/s12551-018-0479-3	journal	November 2018
Hypothesis - buttressed rings assemble, clamp, and release SNAREpins for synaptic transmission Rothman, James E.; Krishnakumar, Shyam S.; Grushin, Kirill FEBS Letters, Vol. 591, Issue 21 https://doi.org/10.1002/1873-3468.12874	journal	October 2017
Munc18-1 catalyzes neuronal SNARE assembly by templating SNARE association Jiao, Junyi; He, Mengze; Port, Sarah A. eLife https://doi.org/10.1101/413724	posted_content	September 2018
Sequence-specific assignment of methyl groups from the neuronal SNARE complex using lanthanide-induced pseudocontact shifts Pan, Yun-Zu; Quade, Bradley; Brewer, Kyle D. Journal of Biomolecular NMR, Vol. 66, Issue 4 https://doi.org/10.1007/s10858-016-0078-1	journal	December 2016
Intrinsic and extrinsic mechanisms of synapse formation and specificity in C. elegans Hendi, Ardalan; Kurashina, Mizuki; Mizumoto, Kota Cellular and Molecular Life Sciences, Vol. 76, Issue 14 https://doi.org/10.1007/s00018-019-03109-1	journal	April 2019
Polymodal Responses in C. elegans Phasmid Neurons Rely on Multiple Intracellular and Intercellular Signaling Pathways Zou, Wenjuan; Cheng, Hankui; Li, Shitian Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep42295	journal	February 2017
Functional synergy between the Munc13 C-terminal C1 and C2 domains Liu, Xiaoxia; Seven, Alpay Burak; Camacho, Marcial eLife, Vol. 5 https://doi.org/10.7554/elife.13696	journal	May 2016
ELKS active zone proteins as multitasking scaffolds for secretion Held, Richard G.; Kaeser, Pascal S. Open Biology, Vol. 8, Issue 2 https://doi.org/10.1098/rsob.170258	journal	February 2018

Similar Records

Munc18 and Munc13 serve as a functional template to orchestrate neuronal SNARE complex assembly

Journal Article · Tue Jan 08 00:00:00 EST 2019 · Nature Communications · OSTI ID:1259896

Wang, Shen; Li, Yun; Gong, Jihong; +4 more

The interaction of mammalian Class C Vps with nSec-1/Munc18-a and syntaxin 1A regulates pre-synaptic release

Journal Article · Fri Nov 24 00:00:00 EST 2006 · Biochemical and Biophysical Research Communications · OSTI ID:1259896

Kim, Bong Yoon; Sahara, Yoshinori; Yamamoto, Akitsugu; +3 more

Syntaxin1a variants lacking an N-peptide or bearing the LE mutation bind to Munc18a in a closed conformation

Journal Article · Mon Jul 15 00:00:00 EDT 2013 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1259896

Colbert, Karen N.; Hattendorf, Douglas A.; Weiss, Thomas M.; +3 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Nanocrystallography

Title: Syntaxin opening by the MUN domain underlies the function of Munc13 in synaptic-vesicle priming

Citation Formats

References (49)

Cited By (46)

Similar Records

Related Subjects