Neuronal SNARE Complex Assembly Guided by Munc18-1 and Munc13-1

Overview

Journal FEBS Open Bio

Specialty Biology

Date 2022 Mar 12

PMID 35278279

Authors

Shen Wang

Cong Ma

Affiliations

Soon will be listed here.

Abstract

Neurotransmitter release by Ca -triggered synaptic vesicle exocytosis is essential for information transmission in the nervous system. The soluble N-ethylmaleimide sensitive factor attachment protein receptors (SNAREs) syntaxin-1, SNAP-25, and synaptobrevin-2 form the SNARE complex to bring synaptic vesicles and the plasma membranes together and to catalyze membrane fusion. Munc18-1 and Munc13-1 regulate synaptic vesicle priming via orchestrating neuronal SNARE complex assembly. In this review, we summarize recent advances toward the functions and molecular mechanisms of Munc18-1 and Munc13-1 in guiding neuronal SNARE complex assembly, and discuss the functional similarities and differences between Munc18-1 and Munc13-1 in neurons and their homologs in other intracellular membrane trafficking systems.

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References

Pertsinidis A, Mukherjee K, Sharma M, Pang Z, Park S, Zhang Y . Ultrahigh-resolution imaging reveals formation of neuronal SNARE/Munc18 complexes in situ. Proc Natl Acad Sci U S A. 2013; 110(30):E2812-20. PMC: 3725074. DOI: 10.1073/pnas.1310654110. View

Kloepper T, Kienle C, Fasshauer D . SNAREing the basis of multicellularity: consequences of protein family expansion during evolution. Mol Biol Evol. 2008; 25(9):2055-68. DOI: 10.1093/molbev/msn151. View

Han G, Bin N, Kang S, Han L, Sugita S . Domain 3a of Munc18-1 plays a crucial role at the priming stage of exocytosis. J Cell Sci. 2013; 126(Pt 11):2361-71. DOI: 10.1242/jcs.126862. View

Yoon T, Munson M . SNARE complex assembly and disassembly. Curr Biol. 2018; 28(8):R397-R401. DOI: 10.1016/j.cub.2018.01.005. View

Zorman S, Rebane A, Ma L, Yang G, Molski M, Coleman J . Common intermediates and kinetics, but different energetics, in the assembly of SNARE proteins. Elife. 2014; 3:e03348. PMC: 4166003. DOI: 10.7554/eLife.03348. View

Imig C, Min S, Krinner S, Arancillo M, Rosenmund C, Sudhof T . The morphological and molecular nature of synaptic vesicle priming at presynaptic active zones. Neuron. 2014; 84(2):416-31. DOI: 10.1016/j.neuron.2014.10.009. View

Magdziarek M, Bolembach A, Stepien K, Quade B, Liu X, Rizo J . Re-examining how Munc13-1 facilitates opening of syntaxin-1. Protein Sci. 2020; 29(6):1440-1458. PMC: 7255523. DOI: 10.1002/pro.3844. View

Camacho M, Basu J, Trimbuch T, Chang S, Pulido-Lozano C, Chang S . Heterodimerization of Munc13 CA domain with RIM regulates synaptic vesicle docking and priming. Nat Commun. 2017; 8:15293. PMC: 5436228. DOI: 10.1038/ncomms15293. View

Perez-Victoria F, Bonifacino J . Dual roles of the mammalian GARP complex in tethering and SNARE complex assembly at the trans-golgi network. Mol Cell Biol. 2009; 29(19):5251-63. PMC: 2747979. DOI: 10.1128/MCB.00495-09. View

10.

Margittai M, Fasshauer D, Pabst S, Jahn R, Langen R . Homo- and heterooligomeric SNARE complexes studied by site-directed spin labeling. J Biol Chem. 2001; 276(16):13169-77. DOI: 10.1074/jbc.M010653200. View

11.

Wang S, Choi U, Gong J, Yang X, Li Y, Wang A . Conformational change of syntaxin linker region induced by Munc13s initiates SNARE complex formation in synaptic exocytosis. EMBO J. 2017; 36(6):816-829. PMC: 5350566. DOI: 10.15252/embj.201695775. View

12.

Burgalossi A, Jung S, Meyer G, Jockusch W, Jahn O, Taschenberger H . SNARE protein recycling by αSNAP and βSNAP supports synaptic vesicle priming. Neuron. 2010; 68(3):473-87. DOI: 10.1016/j.neuron.2010.09.019. View

13.

Kienle N, Kloepper T, Fasshauer D . Phylogeny of the SNARE vesicle fusion machinery yields insights into the conservation of the secretory pathway in fungi. BMC Evol Biol. 2009; 9:19. PMC: 2639358. DOI: 10.1186/1471-2148-9-19. View

14.

van der Beek J, Jonker C, van der Welle R, Liv N, Klumperman J . CORVET, CHEVI and HOPS - multisubunit tethers of the endo-lysosomal system in health and disease. J Cell Sci. 2019; 132(10). DOI: 10.1242/jcs.189134. View

15.

Kloepper T, Kienle C, Fasshauer D . An elaborate classification of SNARE proteins sheds light on the conservation of the eukaryotic endomembrane system. Mol Biol Cell. 2007; 18(9):3463-71. PMC: 1951749. DOI: 10.1091/mbc.e07-03-0193. View

16.

Yip C, Berscheminski J, Walz T . Molecular architecture of the TRAPPII complex and implications for vesicle tethering. Nat Struct Mol Biol. 2010; 17(11):1298-304. PMC: 2988884. DOI: 10.1038/nsmb.1914. View

17.

Bonifacino J, Hierro A . Transport according to GARP: receiving retrograde cargo at the trans-Golgi network. Trends Cell Biol. 2010; 21(3):159-67. PMC: 3073588. DOI: 10.1016/j.tcb.2010.11.003. View

18.

Li Y, Wang S, Li T, Zhu L, Ma C . Tomosyn guides SNARE complex formation in coordination with Munc18 and Munc13. FEBS Lett. 2018; 592(7):1161-1172. DOI: 10.1002/1873-3468.13018. View

19.

de Wit H, Walter A, Milosevic I, Gulyas-Kovacs A, Riedel D, Sorensen J . Synaptotagmin-1 docks secretory vesicles to syntaxin-1/SNAP-25 acceptor complexes. Cell. 2009; 138(5):935-46. DOI: 10.1016/j.cell.2009.07.027. View

20.

Jahn R, Scheller R . SNAREs--engines for membrane fusion. Nat Rev Mol Cell Biol. 2006; 7(9):631-43. DOI: 10.1038/nrm2002. View