A look beyond the QR code of SNARE proteins.
coiled coil
compartments
eukaryotic cell
four‐helix bundle
membrane fusion
snare protein
vesicle trafficking
Journal
Protein science : a publication of the Protein Society
ISSN: 1469-896X
Titre abrégé: Protein Sci
Pays: United States
ID NLM: 9211750
Informations de publication
Date de publication:
Sep 2024
Sep 2024
Historique:
revised:
29
07
2024
received:
26
04
2024
accepted:
03
08
2024
medline:
24
8
2024
pubmed:
24
8
2024
entrez:
24
8
2024
Statut:
ppublish
Résumé
Soluble N-ethylmaleimide-sensitive factor Attachment protein REceptor (SNARE) proteins catalyze the fusion process of vesicles with target membranes in eukaryotic cells. To do this, they assemble in a zipper-like fashion into stable complexes between the membranes. Structural studies have shown that the complexes consist of four different helices, which we subdivide into Qa-, Qb-, Qc-, and R-helix on the basis of their sequence signatures. Using a combination of biochemistry, modeling and molecular dynamics, we investigated how the four different types are arranged in a complex. We found that there is a matching pattern in the core of the complex that dictates the position of the four fundamental SNARE types in the bundle, resulting in a QabcR complex. In the cell, several different cognate QabcR-SNARE complexes catalyze the different transport steps between the compartments of the endomembrane system. Each of these cognate QabcR complexes is compiled from a repertoire of about 20 SNARE subtypes. Our studies show that exchange within the four types is largely tolerated structurally, although some non-cognate exchanges lead to structural imbalances. This suggests that SNARE complexes have evolved for a catalytic mechanism, a mechanism that leaves little scope for selectivity beyond the QabcR rule.
Substances chimiques
SNARE Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e5158Subventions
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
Organisme : Swiss National Science Foundation
ID : 31003A_182732
Pays : Switzerland
Organisme : Swiss National Science Foundation
ID : 310030_219549
Pays : Switzerland
Informations de copyright
© 2024 The Author(s). Protein Science published by Wiley Periodicals LLC on behalf of The Protein Society.
Références
Abriata LA, Palzkill T, Peraro MD. How structural and physicochemical determinants shape sequence constraints in a functional enzyme. PLoS One. 2015;10(2):e0118684.
Antonin W, Riedel D, Mollard GF v. The SNARE Vti1a‐β is localized to small synaptic vesicles and participates in a novel SNARE complex. J Neurosci. 2000;20(15):5724–5732.
Apostolovic B, Danial M, Klok H‐A. Coiled coils: attractive protein folding motifs for the fabrication of self‐assembled, responsive and bioactive materials. Chem Soc Rev. 2010;39(9):3541–3575.
Bethani I, Lang T, Geumann U, Sieber JJ, Jahn R, Rizzoli SO. The specificity of SNARE pairing in biological membranes is mediated by both proof‐reading and spatial segregation. EMBO J. 2007;26(17):3981–3992.
Bock JB, Matern HT, Peden AA, Scheller RH. A genomic perspective on membrane compartment organization. Nature. 2001;409(6822):839–841.
Bonifacino JS, Glick BS. The mechanisms of vesicle budding and fusion. Cell. 2004;116(2):153–166.
Cai H, Reinisch K, Ferro‐Novick S. Coats, tethers, rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev Cell. 2007;12(5):671–682.
Crooks GE, Hon G, Chandonia J‐M, Brenner SE. WebLogo: A sequence logo generator. Genome Res. 2004;14(6):1188–1190.
Dacks JB, Field MC, Buick R, Eme L, Gribaldo S, Roger AJ, et al. The changing view of eukaryogenesis: fossils, cells, lineages and how they all come together. J Cell Sci. 2016;129(20):3695–3703.
Diao J, Liu R, Rong Y, Zhao M, Zhang J, Lai Y, et al. ATG14 promotes membrane tethering and fusion of autophagosomes to endolysosomes. Nature. 2015;520(7548):563–566.
Fasshauer D, Antonin W, Margittai M, Pabst S, Jahn R. Mixed and non‐cognate SNARE complexes characterization of assembly and biophysical properties*. J Biol Chem. 1999;274(22):15440–15446.
Fasshauer D, Sutton RB, Brunger AT, Jahn R. Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q‐ and R‐SNAREs. Proc Natl Acad Sci. 1998;95(26):15781–15786.
Fauchère J, Charton M, Kier LB, Verloop A, Pliska V. Amino acid side chain parameters for correlation studies in biology and pharmacology. Int J Pept Prot Res. 1988;32(4):269–278.
Feller SE, Zhang Y, Pastor RW, Brooks BR. Constant pressure molecular dynamics simulation: the Langevin piston method. J Chem Phys. 1995;103(11):4613–4621.
Furukawa N, Mima J. Multiple and distinct strategies of yeast SNAREs to confer the specificity of membrane fusion. Sci Rep. 2014;4(1):4277.
Gabaldón T. Origin and early evolution of the eukaryotic cell. Annu Rev Microbiol. 2021;75(1):1–17.
Grigoryan G, Keating AE. Structural specificity in coiled‐coil interactions. Curr Opin Struct Biol. 2008;18(4):477–483.
Hohenstein AC, Roche PA. SNAP‐29 is a promiscuous Syntaxin‐binding SNARE. Biochem Biophys Res Commun. 2001;285(2):167–171.
Huang J, MacKerell AD. CHARMM36 all‐atom additive protein force field: validation based on comparison to NMR data. J Comput Chem. 2013;34(25):2135–2145.
Izawa R, Onoue T, Furukawa N, Mima J. Distinct contributions of vacuolar Qabc‐ and R‐SNARE proteins to membrane fusion specificity*. J Biol Chem. 2012;287(5):3445–3453.
Jahn R, Cafiso DC, Tamm LK. Mechanisms of SNARE proteins in membrane fusion. Nat Rev Mol Cell Biol. 2024;25(2):101–118.
Jahn R, Fasshauer D. Molecular machines governing exocytosis of synaptic vesicles. Nature. 2012;490(7419):201–207.
Jahn R, Scheller RH. SNAREs: engines for membrane fusion. Nat Rev Mol Cell Biol. 2006;7(9):631–643.
Jo S, Kim T, Iyer VG, Im W. CHARMM‐GUI: a web‐based graphical user interface for CHARMM. J Comput Chem. 2008;29(11):1859–1865.
Khalifeh D, Neveu E, Fasshauer D. Megaviruses contain various genes encoding for eukaryotic vesicle trafficking factors. Traffic. 2022;23(8):414–425.
Khvotchev M, Soloviev M. SNARE modulators and SNARE mimetic peptides. Biomolecules. 2022;12(12):1779.
Kienle N, Kloepper TH, 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(1):19.
Kloepper TH, Kienle CN, Fasshauer D. An elaborate classification of SNARE proteins sheds light on the conservation of the eukaryotic endomembrane system. Mol Biol Cell. 2007;18(9):3463–3471.
Kloepper TH, Kienle CN, Fasshauer D. SNAREing the basis of multicellularity: consequences of protein family expansion during evolution. Mol Biol Evol. 2008;25(9):2055–2068.
Koike S, Jahn R. SNARE proteins: zip codes in vesicle targeting? Biochem J. 2022;479(3):273–288.
Koonin EV. The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol. 2010;11(5):209.
Kreykenbohm V, Wenzel D, Antonin W, Atlachkine V, Mollard GF v. The SNAREs vti1a and vti1b have distinct localization and SNARE complex partners. Eur J Cell Biol. 2002;81(5):273–280.
Kweon Y, Rothe A, Conibear E, Stevens TH. Ykt6p is a multifunctional yeast R‐SNARE that is required for multiple membrane transport pathways to the vacuole. Mol Biol Cell. 2003;14(5):1868–1881.
Linial M. SNARE proteins‐why so many, why so few? J Neurochem. 1997;69(5):1781–1792.
Lupas AN, Bassler J. Coiled coils: a model system for the 21st century. Trends Biochem Sci. 2017;42(2):130–140.
Martyna GJ, Tobias DJ, Klein ML. Constant pressure molecular dynamics algorithms. J Chem Phys. 1994;101(5):4177–4189.
Mason JM, Arndt KM. Coiled coil domains: stability, specificity, and biological Implications. Chembiochem. 2004;5(2):170–176.
McNew JA, Parlati F, Fukuda R, Johnston RJ, Paz K, et al. Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature. 2000;407(6801):153–159.
Neveu E, Khalifeh D, Salamin N, Fasshauer D. Prototypic SNARE proteins are encoded in the genomes of Heimdallarchaeota, potentially bridging the gap between the prokaryotes and eukaryotes. Curr Biol. 2020;30(13):2468–2480.e5.
Ollikainen N, Jong RM, Kortemme T. Coupling protein side‐chain and backbone flexibility improves the Re‐design of protein‐ligand specificity. PLoS Comput Biol. 2015;11(9):e1004335.
Paez‐Perez M, Russell IA, Cicuta P, Michele LD. Modulating membrane fusion through the design of fusogenic DNA circuits and bilayer composition. Soft Matter. 2022;18(37):7035–7044.
Parlati F, McNew JA, Fukuda R, Miller R, Söllner TH, Rothman JE. Topological restriction of SNARE‐dependent membrane fusion. Nature. 2000;407(6801):194–198.
Parlati F, Varlamov O, Paz K, McNew JA, Hurtado D, et al. Distinct SNARE complexes mediating membrane fusion in Golgi transport based on combinatorial specificity. Proc Natl Acad Sci. 2002;99(8):5424–5429.
Paumet F, Rahimian V, Rothman JE. The specificity of SNARE‐dependent fusion is encoded in the SNARE motif. Proc Natl Acad Sci. 2004;101(10):3376–3380.
Paumet F, Wesolowski J, Garcia‐Diaz A, Delevoye C, Aulner N, Shuman HA, et al. Intracellular bacteria encode inhibitory SNARE‐like proteins. PLoS One. 2009;4(10):e7375.
Pelham HRB. SNAREs and the specificity of membrane fusion. Trends Cell Biol. 2001;11(3):99–101.
Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, et al. Scalable molecular dynamics with NAMD. J Comput Chem. 2005;26(16):1781–1802.
Rizo J. Molecular mechanisms underlying neurotransmitter release. Annu Rev Biophys. 2022;51(1):377–408.
Rothman JE. Mechanisms of intracellular protein transport. Nature. 1994;372(6501):55–63.
Sadek M, Berndt D, Milovanovic D, Jahn R, Diederichsen U. Distance regulated vesicle fusion and docking mediated by β‐peptide nucleic acid SNARE protein analogues. Chembiochem. 2016;17(6):479–485.
Sanderfoot A. Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants. Plant Physiol. 2007;144(1):6–17.
Schreiber G, Keating AE. Protein binding specificity versus promiscuity. Curr Opin Struct Biol. 2011;21(1):50–61.
Seeman NC, Sleiman HF. DNA nanotechnology. Nat Rev Mater. 2017;3(1):17068.
Sharpe HJ, Stevens TJ, Munro S. A comprehensive comparison of transmembrane domains reveals organelle‐specific properties. Cell. 2010;142(1):158–169.
Shi X, Halder P, Yavuz H, Jahn R, Shuman HA. Direct targeting of membrane fusion by SNARE mimicry: convergent evolution of legionella effectors. Proc Natl Acad Sci. 2016;113(31):8807–8812.
Söllner T, Whiteheart SW, Brunner M, Erdjument‐Bromage H, Geromanos S, Tempst P, et al. SNAP receptors implicated in vesicle targeting and fusion. Nature. 1993;362(6418):318–324.
Sørensen JB, Wiederhold K, Müller EM, Milosevic I, Nagy G, de Groot BL, et al. Sequential N‐ to C‐terminal SNARE complex assembly drives priming and fusion of secretory vesicles. EMBO J. 2006;25(5):955–966.
Stanton AE, Hughson FM. The machinery of vesicle fusion. Curr Opin Cell Biol. 2023;83:102191.
Strop P, Kaiser SE, Vrljic M, Brunger AT. The structure of the yeast plasma membrane SNARE complex reveals destabilizing water‐filled cavities*. J Biol Chem. 2008;283(2):1113–1119.
Südhof TC, Rothman JE. Membrane fusion: grappling with SNARE and SM proteins. Science. 2009;323(5913):474–477.
Sutton RB, Fasshauer D, Jahn R, Brunger AT. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4Å resolution. Nature. 1998;395(6700):347–353.
Tanford C. Contribution of hydrophobic interactions to the stability of the globular conformation of proteins. J Am Chem Soc. 1962;84(22):4240–4247.
Truebestein L, Leonard TA. Coiled‐coils: the long and short of it. Bioessays. 2016;38(9):903–916.
Tsui MM, Banfield DK. Yeast Golgi SNARE interactions are promiscuous. J Cell Sci. 2000;113(1):145–152.
Tsui MMK, Tai WCS, Banfield DK. Selective formation of Sed5p‐containing SNARE complexes is mediated by combinatorial binding interactions. Mol Biol Cell. 2001;12(3):521–538.
Volchuk A, Ravazzola M, Perrelet A, Eng WS, Liberto MD, et al. Countercurrent distribution of two distinct SNARE complexes mediating transport within the Golgi stack. Mol Biol Cell. 2004;15(4):1506–1518.
Walter AM, Wiederhold K, Bruns D, Fasshauer D, Sørensen JB. Synaptobrevin N‐terminally bound to syntaxin‐SNAP‐25 defines the primed vesicle state in regulated exocytosis. J Cell Biol. 2010;188(3):401–413.
Weber T, Zemelman BV, McNew JA, Westermann B, Gmachl M, et al. SNAREpins: minimal machinery for membrane fusion. Cell. 1998;92(6):759–772.
Weimbs T, Low SH, Chapin SJ, Mostov KE, Bucher P, Hofmann K. A conserved domain is present in different families of vesicular fusion proteins: a new superfamily. Proc Natl Acad Sci. 1997;94(7):3046–3051.
Weimbs T, Mostov K, Low SH, Hofmann K. A model for structural similarity between different SNARE complexes based on sequence relationships. Trends Cell Biol. 1998;8(7):260–262.
Wendler F, Tooze S. Syntaxin 6: the promiscuous behaviour of a SNARE protein. Traffic. 2001;2(9):606–611.
Wiederhold K, Kloepper TH, Walter AM, Stein A, Kienle N, Sørensen JB, et al. A coiled coil trigger site is essential for rapid binding of synaptobrevin to the SNARE acceptor complex. J Biol Chem. 2010;285(28):21549–21559.
Woolfson DN. The design of coiled‐coil structures and assemblies. Adv Protein Chem. 2005;70:79–112.
Woolfson DN. Understanding a protein fold: the physics, chemistry, and biology of α‐helical coiled coils. J Biol Chem. 2023;299(4):104579.
Xu H, Mohtashami M, Stewart B, Boulianne G, Trimble WS. Drosophila SNAP‐29 is an essential SNARE that binds multiple proteins involved in membrane traffic. PLoS One. 2014;9(3):e91471.
Yang B, Gonzalez L, Prekeris R, Steegmaier M, Advani RJ, Scheller RH. SNARE interactions are not selective implications for membrane fusion specificity. J Biol Chem. 1999;274(9):5649–5653.
Zhang H, Chen J, Wang Y, Peng L, Dong X, Lu Y, et al. A computationally guided protein‐interaction screen uncovers coiled‐coil interactions involved in vesicular trafficking. J Mol Biol. 2009;392(1):228–241.
Zimmerman JM, Eliezer N, Simha R. The characterization of amino acid sequences in proteins by statistical methods. J Theor Biol. 1968;21(2):170–201.