Synaptotagmin-7 is an asynchronous calcium sensor for synaptic transmission in neurons expressing SNAP-23

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Weber, Jens P ^a,b,f   Toft Bertelsen, Trine L ^a   Mohrmann, Ralf ^c   Delgado Martinez, Ignacio ^d   Sørensen, Jakob B ^a,e  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c SAARLAND UNIVERSITY   (Germany)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

^f INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

NEURONAL CALCIUM SENSOR; SYNAPTOSOMAL ASSOCIATED PROTEIN 23; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNAPTOTAGMIN; SYNAPTOTAGMIN 7; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG; QB SNARE PROTEIN; QC SNARE PROTEIN; SNAP23 PROTEIN, MOUSE; SYT7 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CELL MIGRATION; CELL VACUOLE; CONTROLLED STUDY; EMBRYO; ENZYME REPRESSION; EXOCYTOSIS; FEMALE; HIPPOCAMPUS; MALE; MOLECULAR IMAGING; MOUSE; NERVE CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; WHOLE CELL PATCH CLAMP; ANIMAL; CELL LINE; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

ANIMALS; CELL LINE; MICE; MICE, KNOCKOUT; NEURONS; QB-SNARE PROTEINS; QC-SNARE PROTEINS; SYNAPTIC TRANSMISSION; SYNAPTOTAGMINS;

EID: 84912567355     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0114033     Document Type: Article

References (78)

1. Sudhof TC (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27: 509-547.
2. Schneggenburger R, Neher E (2005) Presynaptic calcium and control of vesicle fusion. Curr Opin Neurobiol 15: 266-274.
3. Daw MI, Tricoire L, Erdelyi F, Szabo G, McBain CJ (2009) Asynchronous transmitter release from cholecystokinin-containing inhibitory interneurons is widespread and target-cell independent. J Neurosci 29: 11112-11122.
4. Hefft S, Jonas P (2005) Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat Neurosci 8: 1319-1328.
5. Best AR, Regehr WG (2009) Inhibitory regulation of electrically coupled neurons in the inferior olive is mediated by asynchronous release of GABA. Neuron 62: 555-565.
6. Otsu Y, Shahrezaei V, Li B, Raymond LA, Delaney KR, et al. (2004) Competition between phasic and asynchronous release for recovered synaptic vesicles at developing hippocampal autaptic synapses. J Neurosci 24: 420-433.
7. Lu T, Trussell LO (2000) Inhibitory transmission mediated by asynchronous transmitter release. Neuron 26: 683-694.
8. Barrett EF, Stevens CF (1972) The kinetics of transmitter release at the frog neuromuscular junction. J Physiol 227: 691-708.
9. Sakaba T (2006) Roles of the fast-releasing and the slowly releasing vesicles in synaptic transmission at the calyx of held. J Neurosci 26: 5863-5871.
10. Goda Y, Stevens CF (1994) Two components of transmitter release at a central synapse. Proc Natl Acad Sci U S A 91: 12942-12946.
11. Atluri PP, Regehr WG (1998) Delayed release of neurotransmitter from cerebellar granule cells. J Neurosci 18: 8214-8227.
12. Sudhof TC, Rothman JE (2009) Membrane fusion: grappling with SNARE and SM proteins. Science 323: 474-477.
13. Jahn R, Fasshauer D (2012) Molecular machines governing exocytosis of synaptic vesicles. Nature 490: 201-207.
14. Pang ZP, Sudhof TC (2010) Cell biology of Ca2+-triggered exocytosis. Curr Opin Cell Biol 22: 496-505.
15. Li C, Ullrich B, Zhang JZ, Anderson RG, Brose N, et al. (1995) Ca(2+)-dependent and -independent activities of neural and non-neural synaptotagmins. Nature 375: 594-599.
16. Sugita S, Han W, Butz S, Liu X, Fernandez-Chacon R, et al. (2001) Synaptotagmin VII as a plasma membrane Ca(2+) sensor in exocytosis. Neuron 30: 459-473.
17. Maximov A, Shin OH, Liu X, Sudhof TC (2007) Synaptotagmin-12, a synaptic vesicle phosphoprotein that modulates spontaneous neurotransmitter release. J Cell Biol 176: 113-124.
18. Wen H, Linhoff MW, McGinley MJ, Li GL, Corson GM, et al. (2010) Distinct roles for two synaptotagmin isoforms in synchronous and asynchronous transmitter release at zebrafish neuromuscular junction. Proc Natl Acad Sci U S A 107: 13906-13911.
19. Maximov A, Lao Y, Li H, Chen X, Rizo J, et al. (2008) Genetic analysis of synaptotagmin-7 function in synaptic vesicle exocytosis. Proc Natl Acad Sci U S A 105: 3986-3991.
20. Bacaj T, Wu D, Yang X, Morishita W, Zhou P, et al. (2013) Synaptotagmin-1 and synaptotagmin-7 trigger synchronous and asynchronous phases of neurotransmitter release. Neuron 80: 947-959.
21. Liu H, Bai H, Hui E, Yang L, Evans CS, et al. (2014) Synaptotagmin 7 functions as a Ca2+-sensor for synaptic vesicle replenishment. Elife 3: e01524.
22. Schonn JS, Maximov A, Lao Y, Sudhof TC, Sorensen JB (2008) Synaptotagmin-1 and -7 are functionally overlapping Ca2+ sensors for exocytosis in adrenal chromaffin cells. Proc Natl Acad Sci U S A 105: 3998-4003.
23. Gustavsson N, Wei SH, Hoang DN, Lao Y, Zhang Q, et al. (2009) Synaptotagmin-7 is a principal Ca2+ sensor for Ca2+-induced glucagon exocytosis in pancreas. J Physiol 587: 1169-1178.
24. Gustavsson N, Lao Y, Maximov A, Chuang JC, Kostromina E, et al. (2008) Impaired insulin secretion and glucose intolerance in synaptotagmin-7 null mutant mice. Proc Natl Acad Sci U S A 105: 3992-3997.
25. Gauthier BR, Duhamel DL, Iezzi M, Theander S, Saltel F, et al. (2008) Synaptotagmin VII splice variants alpha, beta, and delta are expressed in pancreatic beta-cells and regulate insulin exocytosis. FASEB J 22: 194-206.
26. Li Y, Wang P, Xu J, Gorelick F, Yamazaki H, et al. (2007) Regulation of insulin secretion and GLUT4 trafficking by the calcium sensor synaptotagmin VII. Biochem Biophys Res Commun 362: 658-664.
27. Matsuoka H, Harada K, Nakamura J, Fukuda M, Inoue M (2011) Differential distribution of synaptotagmin-1, -4, -7, and -9 in rat adrenal chromaffin cells. Cell and tissue research 344: 41-50.
28. Martinez I, Chakrabarti S, Hellevik T, Morehead J, Fowler K, et al. (2000) Synaptotagmin VII regulates Ca(2+)-dependent exocytosis of lysosomes in fibroblasts. The Journal of cell biology 148: 1141-1149.
29. Arantes RM, Andrews NW (2006) A role for synaptotagmin VII-regulated exocytosis of lysosomes in neurite outgrowth from primary sympathetic neurons. The Journal of neuroscience: the official journal of the Society for Neuroscience 26: 4630-4637.
30. Virmani T, Han W, Liu X, Sudhof TC, Kavalali ET (2003) Synaptotagmin 7 splice variants differentially regulate synaptic vesicle recycling. The EMBO journal 22: 5347-5357.
31. Rickman C, Jimenez JL, Graham ME, Archer DA, Soloviev M, et al. (2006) Conserved prefusion protein assembly in regulated exocytosis. Mol Biol Cell 17: 283-294.
32. Kim JY, Choi BK, Choi MG, Kim SA, Lai Y, et al. (2012) Solution single-vesicle assay reveals PIP2-mediated sequential actions of synaptotagmin-1 on SNAREs. EMBO J 31: 2144-2155.
33. Mohrmann R, de Wit H, Connell E, Pinheiro PS, Leese C, et al. (2013) Synaptotagmin interaction with SNAP-25 governs vesicle docking, priming, and fusion triggering. J Neurosci 33: 14417-14430.
34. Chieregatti E, Chicka MC, Chapman ER, Baldini G (2004) SNAP-23 functions in docking/fusion of granules at low Ca2+. Mol Biol Cell 15: 1918-1930.
35. Delgado-Martinez I, Nehring RB, Sorensen JB (2007) Differential abilities of SNAP-25 homologs to support neuronal function. J Neurosci 27: 9380-9391.
36. Washbourne P, Thompson PM, Carta M, Costa ET, Mathews JR, et al. (2002) Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat Neurosci 5: 19-26.
37. Bekkers JM, Stevens CF (1991) Excitatory and inhibitory autaptic currents in isolated hippocampal neurons maintained in cell culture. Proc Natl Acad Sci U S A 88: 7834-7838.
38. Diril MK, Wienisch M, Jung N, Klingauf J, Haucke V (2006) Stonin 2 is an AP-2-dependent endocytic sorting adaptor for synaptotagmin internalization and recycling. Dev Cell 10: 233-244.
39. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16: 1197-1207.
40. Mohrmann R, de Wit H, Verhage M, Neher E, Sorensen JB (2010) Fast vesicle fusion in living cells requires at least three SNARE complexes. Science 330: 502-505.
41. Schneggenburger R, Meyer AC, Neher E (1999) Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23: 399-409.
42. Moulder KL, Mennerick S (2005) Reluctant vesicles contribute to the total readily releasable pool in glutamatergic hippocampal neurons. J Neurosci 25: 3842-3850.
43. Stevens CF, Williams JH (2007) Discharge of the readily releasable pool with action potentials at hippocampal synapses. J Neurophysiol 98: 3221-3229.
44. Hagler DJ, Jr., Goda Y (2001) Properties of synchronous and asynchronous release during pulse train depression in cultured hippocampal neurons. Journal of neurophysiology 85: 2324-2334.
45. Maximov A, Sudhof TC (2005) Autonomous function of synaptotagmin 1 in triggering synchronous release independent of asynchronous release. Neuron 48: 547-554.
46. Raingo J, Khvotchev M, Liu P, Darios F, Li YC, et al. (2012) VAMP4 directs synaptic vesicles to a pool that selectively maintains asynchronous neurotransmission. Nat Neurosci 15: 738-745.
47. Miesenbock G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394: 192-195.
48. Fukuda M, Ogata Y, Saegusa C, Kanno E, Mikoshiba K (2002) Alternative splicing isoforms of synaptotagmin VII in the mouse, rat and human. Biochem J 365: 173-180.
49. Dean C, Dunning FM, Liu H, Bomba-Warczak E, Martens H, et al. (2012) Axonal and dendritic synaptotagmin isoforms revealed by a pHluorin-syt functional screen. Mol Biol Cell 23: 1715-1727.
50. Deak F, Liu X, Khvotchev M, Li G, Kavalali ET, et al. (2009) Alpha-latrotoxin stimulates a novel pathway of Ca2+-dependent synaptic exocytosis independent of the classical synaptic fusion machinery. J Neurosci 29: 8639-8648.
51. Yoshihara M, Littleton JT (2002) Synaptotagmin I functions as a calcium sensor to synchronize neurotransmitter release. Neuron 36: 897-908.
52. Littleton JT, Stern M, Perin M, Bellen HJ (1994) Calcium dependence of neurotransmitter release and rate of spontaneous vesicle fusions are altered in Drosophila synaptotagmin mutants. Proc Natl Acad Sci U S A 91: 10888-10892.
53. Geppert M, Goda Y, Hammer RE, Li C, Rosahl TW, et al. (1994) Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell 79: 717-727.
54. Sun J, Pang ZP, Qin D, Fahim AT, Adachi R, et al. (2007) A dual-Ca2+-sensor model for neurotransmitter release in a central synapse. Nature 450: 676-682.
55. Shin OH, Rhee JS, Tang J, Sugita S, Rosenmund C, et al. (2003) Sr2+ binding to the Ca2+ binding site of the synaptotagmin 1 C2B domain triggers fast exocytosis without stimulating SNARE interactions. Neuron 37: 99-108.
56. Burgalossi A, Jung S, Meyer G, Jockusch WJ, Jahn O, et al. (2010) SNARE protein recycling by alphaSNAP and betaSNAP supports synaptic vesicle priming. Neuron 68: 473-487.
57. Nishiki T, Augustine GJ (2004) Synaptotagmin I synchronizes transmitter release in mouse hippocampal neurons. J Neurosci 24: 6127-6132.
58. Liu H, Dean C, Arthur CP, Dong M, Chapman ER (2009) Autapses and networks of hippocampal neurons exhibit distinct synaptic transmission phenotypes in the absence of synaptotagmin I. J Neurosci 29: 7395-7403.
59. Kerr AM, Reisinger E, Jonas P (2008) Differential dependence of phasic transmitter release on synaptotagmin 1 at GABAergic and glutamatergic hippocampal synapses. Proc Natl Acad Sci U S A 105: 15581-15586.
60. Xu J, Pang ZP, Shin OH, Sudhof TC (2009) Synaptotagmin-1 functions as a Ca2+ sensor for spontaneous release. Nat Neurosci 12: 759-766.
61. Pang ZP, Sun J, Rizo J, Maximov A, Sudhof TC (2006) Genetic analysis of synaptotagmin 2 in spontaneous and Ca2+-triggered neurotransmitter release. EMBO J 25: 2039-2050.
62. Wierda KD, Sorensen JB (2014) Innervation by a GABAergic neuron depresses spontaneous release in glutamatergic neurons and unveils the clamping phenotype of synaptotagmin-1. J Neurosci 34: 2100-2110.
63. Xue M, Craig TK, Shin OH, Li L, Brautigam CA, et al. (2010) Structural and mutational analysis of functional differentiation between synaptotagmins-1 and -7. PLoS ONE 5.
64. Rao SK, Huynh C, Proux-Gillardeaux V, Galli T, Andrews NW (2004) Identification of SNAREs involved in synaptotagmin VII-regulated lysosomal exocytosis. The Journal of biological chemistry 279: 20471-20479.
65. Gonelle-Gispert C, Halban PA, Niemann H, Palmer M, Catsicas S, et al. (1999) SNAP-25a and -25b isoforms are both expressed in insulin-secreting cells and can function in insulin secretion. Biochem J 339 (Pt 1): 159-165.
66. Grant NJ, Hepp R, Krause W, Aunis D, Oehme P, et al. (1999) Differential expression of SNAP-25 isoforms and SNAP-23 in the adrenal gland. J Neurochem 72: 363-372.
67. Sadoul K, Berger A, Niemann H, Weller U, Roche PA, et al. (1997) SNAP-23 is not cleaved by botulinum neurotoxin E and can replace SNAP-25 in the process of insulin secretion. J Biol Chem 272: 33023-33027.
68. Verderio C, Pozzi D, Pravettoni E, Inverardi F, Schenk U, et al. (2004) SNAP-25 modulation of calcium dynamics underlies differences in GABAergic and glutamatergic responsiveness to depolarization. Neuron 41: 599-610.
69. Garbelli R, Inverardi F, Medici V, Amadeo A, Verderio C, et al. (2008) Heterogeneous expression of SNAP-25 in rat and human brain. J Comp Neurol 506: 373-386.
70. Tafoya LC, Mameli M, Miyashita T, Guzowski JF, Valenzuela CF, et al. (2006) Expression and function of SNAP-25 as a universal SNARE component in GABAergic neurons. J Neurosci 26: 7826-7838.
71. Frassoni C, Inverardi F, Coco S, Ortino B, Grumelli C, et al. (2005) Analysis of SNAP-25 immunoreactivity in hippocampal inhibitory neurons during development in culture and in situ. Neuroscience 131: 813-823.
72. Suh YH, Terashima A, Petralia RS, Wenthold RJ, Isaac JT, et al. (2010) A neuronal role for SNAP-23 in postsynaptic glutamate receptor trafficking. Nat Neurosci 13: 338-343.
73. Walter AM, Pinheiro PS, Verhage M, Sorensen JB (2013) A sequential vesicle pool model with a single release sensor and a ca(2+)-dependent priming catalyst effectively explains ca(2+)-dependent properties of neurosecretion. PLoS Comput Biol 9: e1003362.
74. Rickman C, Archer DA, Meunier FA, Craxton M, Fukuda M, et al. (2004) Synaptotagmin interaction with the syntaxin/SNAP-25 dimer is mediated by an evolutionarily conserved motif and is sensitive to inositol hexakisphosphate. J Biol Chem 279: 12574-12579.
75. Choi UB, Strop P, Vrljic M, Chu S, Brunger AT, et al. (2010) Single-molecule FRET-derived model of the synaptotagmin 1-SNARE fusion complex. Nat Struct Mol Biol 17: 318-324.
76. Nagy G, Milosevic I, Mohrmann R, Wiederhold K, Walter AM, et al. (2008) The SNAP-25 linker as an adaptation toward fast exocytosis. Mol Biol Cell 19: 3769-3781.
77. Hui E, Bai J, Wang P, Sugimori M, Llinas RR, et al. (2005) Three distinct kinetic groupings of the synaptotagmin family: candidate sensors for rapid and delayed exocytosis. Proc Natl Acad Sci U S A 102: 5210-5214.
78. Weber JP, Reim K, Sorensen JB (2010) Opposing functions of two sub-domains of the SNAREcomplex in neurotransmission. EMBO J 29: 2477-2490.