The synaptotagmin juxtamembrane domain is involved in neuroexocytosis

FEBS Open Bio

Volumn 5, Issue , 2015, Pages 388-396

  Caccin, Paola ^a   Scorzeto, Michele ^a   Damiano, Nunzio ^c   Marin, Oriano ^a,c   Megighian, Aram ^a   Montecucco, Cesare ^a,b  

^a UNIVERSITY OF PADOVA   (Italy)

^b CNR   (Italy)

^c CRIBI Biotechnology Centre   (Italy)

Author keywords

Anionic phospholipids; Juxtamembrane domain; Neuroexocytosis; Neuromuscular junction; Synaptotagmin

Indexed keywords

CALCIUM ION; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL; SYNAPTOTAGMIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EXOCYTOSIS; MOUSE; MUSCLE MASS; MUSCLE TWITCH; NERVE ENDING; NEUROEXOCYTOSIS; NEUROMUSCULAR SYNAPSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PARALYSIS; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN DOMAIN; STATIC ELECTRICITY; SYNAPSE VESICLE;

ANIMALIA;

EID: 84930942699     PISSN: 22115463     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.fob.2015.04.013     Document Type: Article

References (54)

1. Südhof T.C., Rizo J. Synaptic vesicle exocytosis. Cold Spring Harbor Perspect. Biol. 2011, 3:201-207.
2. Jahn R., Fasshauer D. Molecular machines governing exocytosis of synaptic vesicles. Nature 2012, 490:201-207.
3. Pantano S., Montecucco C. The blockade of the neurotransmitter release apparatus by botulinum neurotoxins. Cell. Mol. Life Sci. 2014, 71:793-811.
4. Söllner T., Whiteheart S.W., Brunner M., Erdjument-Bromage H., Geromanos S., Tempst P., Rothman J.E. SNAP receptors implicated in vesicle targeting and fusion. Nature 1993, 362:318-324.
5. Sutton R.B., Fasshauer D., Jahn R., Brunger A.T. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 1998, 395:347-353.
6. Südhof T.C. Neurotransmitter release: the last millisecond in the life of a synaptic vesicle. Neuron 2013, 80:675-690.
7. Montecucco C., Schiavo G., Pantano S. SNARE complexes and neuroexocytosis: how many, how close?. Trends Biochem. Sci. 2005, 30:367-372.
8. Hua Y., Scheller R. Three SNARE complexes cooperate to mediate membrane fusion. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:8065-8070.
9. Megighian A., Scorzeto M., Zanini D., Pantano S., Rigoni M., Benna C., Rossetto O., Montecucco C., Zordan M. Arg206 of SNAP-25 is essential for neuroexocytosis at the Drosophila melanogaster neuromuscular junction. J. Cell Sci. 2010, 123:3276-3283.
10. Megighian A., Zordan M., Pantano S., Scorzeto M., Rigoni M., Zanini D., Rossetto O., Montecucco C. Evidence for a radial SNARE super-complex mediating neurotransmitter release at the Drosophila neuromuscular junction. J. Cell Sci. 2013, 126:3134-3140.
11. Sorensen J.B. Conflicting views on the membrane fusion machinery and the fusion pore. Annu. Rev. Cell Dev. Biol. 2009, 25:513-537.
12. Mohrmann R., de Wit H., Verhage M., Neher E., Sørensen J.B. Fast vesicle fusion in living cells requires at least three SNARE complexes. Science 2010, 330:502-505.
13. Mohrmann R., Sørensen J.B. SNARE requirements en route to exocytosis: from many to few. J. Mol. Neurosci. 2012, 48:387-394.
14. Lu X., Zhang Y., Shin Y.-K. Supramolecular SNARE assembly precedes hemifusion in SNARE-mediated membrane fusion. Nat. Struct. Mol. Biol. 2008, 15:700-706.
15. Rizo J., Rosenmund C. Synaptic vesicle fusion. Nat. Struct. Mol. Biol. 2008, 15:665-674.
16. Moghadam P.K., Jackson M.B. The functional significance of synaptotagmin diversity in neuroendocrine secretion. Front. Endocrinol. (Lausanne) 2013, 4:124.
17. Chapman E.R. How does synaptotagmin trigger neurotransmitter release?. Annu. Rev. Biochem. 2008, 77:615-641.
18. Schiavo G., Gu Q.M., Prestwich G.D., Söllner T.H., Rothman J.E. Calcium-dependent switching of the specificity of phosphoinositide binding to synaptotagmin. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:13327-13332.
19. Fernandez I., Araç D., Ubach J., Gerber S.H., Shin O., Gao Y., Anderson R.G., Südhof T.C., Rizo J. Three-dimensional structure of the synaptotagmin 1 C2B-domain: synaptotagmin 1 as a phospholipid binding machine. Neuron 2001, 32:1057-1069.
20. Paddock B.E., Striegel A.R., Hui E., Chapman E.R., Reist N.E. Ca2+-dependent, phospholipid-binding residues of synaptotagmin are critical for excitation-secretion coupling in vivo. J. Neurosci. 2008, 28:7458-7466.
21. Paddock B.E., Wang Z., Biela L.M., Chen K., Getzy M.D., Striegel A., Richmond J.E., Chapman E.R., Featherstone D.E., Reist N.E. Membrane penetration by synaptotagmin is required for coupling calcium binding to vesicle fusion in vivo. J. Neurosci. 2011, 31:2248-2257.
22. Martens S., Kozlov M.M., McMahon H.T. How synaptotagmin promotes membrane fusion. Science 2007, 316:1205-1208.
23. Hui E., Johnson C.P., Yao J., Dunning F.M., Chapman E.R. Synaptotagmin-mediated bending of the target membrane is a critical step in Ca(2+)-regulated fusion. Cell 2009, 138:709-721.
24. Mace K.E., Biela L.M., Sares A.G., Reist N.E. Synaptotagmin I stabilizes synaptic vesicles via its C(2)A polylysine motif. Genesis 2009, 47:337-345.
25. Striegel A.R., Biela L.M., Evans C.S., Wang Z., Delehoy J.B., Sutton R.B., Chapman E.R., Reist N.E. Calcium binding by synaptotagmin's C2A domain is an essential element of the electrostatic switch that triggers synchronous synaptic transmission. J. Neurosci. 2012, 32:1253-1260.
26. Seven A.B., Brewer K.D., Shi L., Jiang Q.X., Rizo J. Prevalent mechanism of membrane bridging by synaptotagmin-1. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:E3243-E3252.
27. Honigmann A., van den Bogaart G., Iraheta E., Risselada H.J., Milovanovic D., Mueller V., Müllar S., Diederichsen U., Fasshauer D., Grubmüller H., Hell S.W., Eggeling C., Kühnel K., Jahn R. Phosphatidylinositol 4,5-bisphosphate clusters act as molecular beacons for vesicle recruitment. Nat. Struct. Mol. Biol. 2013, 20:679-686.
28. Stein A., Radhakrishnan A., Riedel D., Fasshauer D., Jahn R. Synaptotagmin activates membrane fusion through a Ca2+-dependent trans interaction with phospholipids. Nat. Struct. Mol. Biol. 2007, 14:904-911.
29. Changeux J.-P. The nicotinic acetylcholine receptor: the founding father of the pentameric ligand-gated ion channel superfamily. J. Biol. Chem. 2012, 287:40207-40215.
30. Van der Kloot W., Molgó J. Quantal acetylcholine release at the vertebrate neuromuscular junction. Physiol. Rev. 1994, 74:899-991.
31. Kasai H., Takahashi N., Tokumaru H. Distinct initial SNARE configurations underlying the diversity of exocytosis. Physiol. Rev. 2012, 92:1915-1964.
32. Schmidt N., Mishra A., Lai G.H., Wong G.C.L. Arginine-rich cell-penetrating peptides. FEBS Lett. 2010, 584:1806-1813.
33. Said Hassane F., Saleh A.F., Abes R., Gait M.J., Lebleu B. Cell penetrating peptides: overview and applications to the delivery of oligonucleotides. Cell. Mol. Life Sci. 2010, 67:715-726.
34. Debaisieux S., Rayne F., Yezid H., Beaumelle B. The ins and outs of HIV-1 Tat. Traffic 2012, 13:355-363.
35. Pang Z.P., Melicoff E., Padget D., Liu Y., Teich A.F., Dickey B.F., Lin W., Adachi R., Sudhof T.C. Synaptotagmin-2 is essential for survival and contributes to Ca2+ triggering of neurotransmitter release in central and neuromuscular synapses. J. Neurosci. 2006, 26:13493-13504.
36. Zhou P., Bacaj T., Yang X., Pang Z.P., Südhof T.C. Lipid-anchored SNAREs lacking transmembrane regions fully support membrane fusion during neurotransmitter release. Neuron 2013, 80:470-483.
37. Fitzsimonds R.M., Poo M.M. Retrograde signaling in the development and modification of synapses. Physiol. Rev. 1998, 78:143-170.
38. Bai J., Earles C.A., Lewis J.L., Chapman E.R. Membrane-embedded synaptotagmin penetrates cis or trans target membranes and clusters via a novel mechanism. J. Biol. Chem. 2000, 275:25427-25435.
39. Di Paolo G., De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature 2006, 443:651-657.
40. Vennekate W., Schröder S., Lin C.-C., van den Bogaart G., Grunwald M., Jahn R., Walla P.J. Cis- and trans-membrane interactions of synaptotagmin-1. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:11037-11042.
41. Takamori S., Holth M., Stenius K., Lemke E., Gronborg M., Riedel D., Urlaub H., Schenck S., et al. Molecular anatomy of a trafficking organelle. Cell 2006, 127:831-846.
42. Johnsson A.-K., Karlsson R. Synaptotagmin 1 causes phosphatidyl inositol lipid-dependent actin remodeling in cultured non-neuronal and neuronal cells. Exp. Cell Res. 2012, 318:114-126.
43. Lam A.D., Tryoen-Toth P., Tsai B., Vitale N., Stuenkel E.L. SNARE-catalyzed fusion events are regulated by syntaxin 1A-lipid interactions. Mol. Biol. Cell 2008, 19:485-497.
44. Williams D., Vicôgne J., Zaitseva I., McLaughlin S., Pessin J.E. Evidence that electrostatic interactions between vesicle-associated membrane protein 2 andacidic phospholipids may modulate the fusion of transport vesicles with the plasma membrane. Mol. Biol. Cell 2009, 20:4910-4919.
45. Montal M. Electrostatic attraction at the core of membrane fusion. FEBS Lett. 1999, 26:129-130.
46. McLaughlin S., Murray D. Plasma membrane phosphoinositide organization by protein electrostatics. Nature 2005, 438:605-611.
47. Harlow M.L., Szule J.A., Xu J., Jung J.H., Marshall R.M., McMahan U.J. Alignment of synaptic vesicle macromolecules with the macromolecules in active zone material that direct vesicle docking. PLoS One 2013, 8:e69410.
48. Kim J.-Y., Choi B.-K., Choi M.-G., Kim S.-A., Lai Y., Shin Y.-K., Lee N.K. Solution single-vesicle assay reveals PIP2-mediated sequential actions of synaptotagmin-1 on SNAREs. EMBO J. 2012, 31:2144-2155.
49. Chernomordik L.V., Kozlov M.M. Mechanics of membrane fusion. Nat. Struct. Mol. Biol. 2008, 15:675-683.
50. Hernandez J.M., Stein A., Behrmann E., Riedel D., Cypionka A., Farsi Z., Walla P.J., Raunser S., Jahn R. Membrane fusion intermediates via directional and full assembly of the SNARE complex. Science 2012, 336:1581-1584.
51. Fields G.B., Noble R.L. Solid phase peptide synthesis utilizing 9-fluorenylmethoxycarbonyl amino acids. Int. J. Pept. Protein Res. 1990, 35:161-214.
52. Carpino L.A., Henklein P., Foxman B.M., Abdelmoty I., Costisella B., Wray V., Domke T., El-Faham A., Mügge C. The solid state and solution structure of HAPyU. J. Org. Chem. 2001, 66:5245-5247.
53. Bohnert S., Schiavo G. Tetanus toxin is transported in a novel neuronal compartment characterized by a specialized pH regulation. J. Biol. Chem. 2005, 280:42336-42344.
54. Pirazzini M., Azarnia Tehran D., Zanetti G., Megighian A., Scorzeto M., Fillo S., Shone C.C., Binz T., Rossetto O., Lista F., Montecucco C. Thioredoxin and its reductase are present on synaptic vesicles, and their inhibition prevents the paralysis induced by botulinum neurotoxins. Cell Reports 2014, 8:1870-1878.