Synaptotagmin III isoform is compartmentalized in pancreatic β-cells and has a functional role in exocytosis

Diabetes

Volumn 49, Issue 3, 2000, Pages 383-391

  Brown, Hilary ^a   Meister, Björn ^a   Deeney, Jude ^a,b   Corkey, Barbara E ^b   Yang, Shao Nian ^a   Larsson, Olof ^a   Rhodes, C J ^c   Seino, Susumu ^d   Berggren, Per Olof ^a   Fried, Gabriel ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d CHIBA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM CHANNEL; CALCIUM SENSING RECEPTOR; SYNAPTOTAGMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL COMPARTMENTALIZATION; ENDOCRINE CELL; EXOCYTOSIS; INSULINOMA; MALE; NERVE CELL; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT;

EID: 0034089335     PISSN: 00121797     EISSN: None     Source Type: Journal    
DOI: 10.2337/diabetes.49.3.383     Document Type: Article

References (79)

1. Matthew WD, Tsavaler L, Reichardt LF: Identification of a synaptic vesicle-specific membrane protein with a wide distribution in neuronal and neurosecretory tissue. J Cell Biol 91:257-269, 1981
2. Geppert M, Archer BT, Südhof TC: Synaptotagmin II: a novel differentially distributed form of synaptotagmin. J Biol Chem 266:13548-13552, 1991
3. Hilbush BS, Morgan JI: A third synaptotagmin gene, Syt3, in the mouse. Proc Natl Acad Sci U S A 91:8195-8199, 1994
4. Mizuta M, Inagaki N, Nemoto Y, Matsukura S, Takahashi M, Seino S: Synaptotagmin III is a novel isoform of rat synaptotagmin expressed in endocrine and neuronal cells. J Biol Chem 269:11675-11678, 1994
5. Ullrich B, Li C, Zhang JZ, McMahon H, Anderson RG, Geppert M, Südhof TC: Functional properties of multiple synaptotagmins in brain. Neuron 13:1281-1291, 1994
6. Hudson AW, Birnbaum MJ: Identification of a nonneuronal isoform of synaptotagmin. Proc Natl Acad Sci USA 92:5895-5899, 1995
7. Li C, Ullrich B, Zhang JZ, Anderson RG, Brose N, Südhof TC: Ca(2+)-dependent and -independent activities of neural and non-neural synaptotagmins. Nature 375:594-599, 1995
8. Marquéze B, Boudier JA, Mizuta M, Inagaki N, Seino S, Seagar M: Cellular localization of synaptotagmin I, II, and III mRNAs in the central nervous system and pituitary and adrenal glands of the rat. J Neurosci 15:4906-4917, 1995
9. Ullrich B, Südhof TC: Differential distributions of novel synaptotagmins: comparison to synapsins. Neuropharmacology 34:1371-1377, 1995
10. von Poser C, Ichtchenko K, Shao X, Rizo J, Südhof TC: The evolutionary pressure to inactivate: a subclass of synaptotagmins with an amino acid substitution that abolishes Ca2+ binding. J Biol Chem 272:14314-14319, 1997
11. Perin MS, Brose N, Jahn R, Südhof TC: Domain structure of synaptotagmin (p65) [Erratum published in J Biol Chem 266:10018, 1991]. J Biol Chem 266:623-629, 1991
12. Perin MS: The COOH terminus of synaptotagmin mediates interaction with the neurexins. J Biol Chem 269:8576-8581, 1994
13. Sutton RB, Davletov BA, Berghuis AM, SüdhofTC, Sprang SR: Structure of the first C2 domain of synaptotagmin I: a novel Ca2+/phospholipid-binding fold. Cell 80:929-938, 1995
14. Davletov BA, Südhof TC: A single C2 domain from synaptotagmin I is sufficient for high affinity Ca2+/phospholipid binding. J Biol Chem 268:26386-26390, 1993
15. Chapman ER, Jahn R: Calcium-dependent interaction of the cytoplasmic region of synaptotagmin with membranes: autonomous function of a single C2-homologous domain. J Biol Chem 269:5735-5741, 1994
16. Brose N, Hofmann K, Hata Y, Südhof TC: Mammalian homologues of Caenorhabditis elegans unc-13 gene define novel family of C2-domain proteins. J Biol Chem 270:25273-25280, 1995
17. Miyazaki M, Kaibuchi K, Shirataki H, Kohno H, Ueyama T, Nishikawa J, Takai Y: Rabphilin-3A binds to a M(r) 115,000 polypeptide in a phosphatidylserine- and Ca(2+)-dependent manner. Brain Res Mol Brain Res 28:29-36, 1995
18. Shao X, Davletov BA, Sutton RB, Südhof TC, Rizo J: Bipartite Ca2+-binding motif in C2 domains of synaptotagmin and protein kinase C. Science 273:248-251, 1996
19. Südhof TC, Rizo J: Synaptotagmins: C2-domain proteins that regulate membrane traffic. Neuron 17:379-388, 1996
20. Südhof TC, Jahn R: Proteins of synaptic vesicles involved in exocytosis and membrane recycling. Neuron 6:665-677, 1991
21. Brose N, Petrenko AG, Südhof TC, Jahn R: Synaptotagmin: a calcium sensor on the synaptic vesicle surface. Science 256:1021-1025, 1992
22. Jahn R, Südhof TC: Synaptic vesicle traffic: rush hour in the nerve terminal. J Neurochem 61:12-21, 1993
23. Elferink LA, Peterson MR, Scheller RH: A role for synaptotagmin (p65) in regulated exocytosis. Cell 72:153-159, 1993
24. O'Connor V, Augustine GJ, Betz H: Synaptic vesicle exocytosis: molecules and models. Cell 76:785-787, 1994
25. Bennett MK, Scheller RH: Molecular correlates of synaptic vesicle docking and fusion. Curr Opin Neurobiol 4:324-329, 1994
26. Geppert M, Goda Y, Hammer RE, Li C, Rosahl TW, Stevens CF, Südhof TC: Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell 79:717-727, 1994
27. Littleton JT, Bellen HJ: Synaptotagmin controls and modulates synaptic-vesicle fusion in a Ca(2+)-dependent manner. Trends Neurosci 18:177-183, 1995
28. Kelly RB: Neural transmission: synaptotagmin is just a calcium sensor. Curr Biol 5:257-259, 1995
29. Fried G: Synaptic vesicles and release of transmitters: new insights at the molecular level. Acta Physiol Scand 154:1-15, 1995
30. Südhof TC: The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375:645-653, 1995
31. Bauerfeind R, Jelinek R, Huttner WB: Synaptotagmin I- and II-deficient PC12 cells exhibit calcium-independent, depolarization-induced neurotransmitter release from synaptic-like microvesicles. FEBS Lett 364:328-334, 1995
32. Bennett MK, Garcia-Arraras JE, Elferink LA, Peterson K, Fleming AM, Hazuka CD, Scheller RH: The syntaxin family of vesicular transport receptors. Cell 74:863-873, 1993
33. Hess DT, Slater TM, Wilson MC, Skene JH: The 25 kDa synaptosomal-associated protein SNAP-25 is the major methionine-rich polypeptide in rapid axonal transport and a major substrate for palmitoylation in adult CNS. J Neurosci 12:4634-4641, 1992
34. Rothman JE, Orci L: Molecular dissection of the secretory pathway. Nature 355:409-415, 1992
35. Söllner T, Bennett MK, Whiteheart SW, Scheller RH, Rothman JE: A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75:409-418, 1993
36. Söllner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE: SNAP receptors implicated in vesicle targeting and fusion. Nature 362:318-324, 1993
37. Nonet ML, Grundahl K, Meyer BJ, Rand JB: Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell 73:1291-1305, 1993
38. Broadie K, Bellen HJ, DiAntonio A, Littleton JT, Schwarz TL: Absence of synaptotagmin disrupts excitation-secretion coupling during synaptic transmssion. Proc Natl Acad Sci. U S A 91:10727-10731, 1994
39. DiAntonio A, Schwarz TL: The effect on synaptic physiology of synaptotagmin mutations in Drosophila. Neuron 12:909-920, 1994
40. Littleton JT, Stern M, Perin M, Bellen HJ: 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, 1994
41. Hutton JC: The insulin secretory granule. Diabetologia 32:271-281, 1989
42. Efendic S, Kindmark H, Berggren PO: Mechanisms involved in the regulation of the insulin secretory process. J Intern Med 735:9-22, 1991
43. Newgard CB, McGarry JD: Metabolic coupling factors in pancreatic beta-cell signal transduction. Ann Rev Biochem 64:689-719, 1995
44. Brun T, Roche E, Assimacopoulos-Jeannet F, Corkey BE, Kim KH, Prentki M: Evidence for an anaplerotic/malonyl-CoA pathway in pancreatic beta-cell nutrient signaling. Diabetes 45:190-198, 1996
45. Prentki M: New insights into pancreatic beta-cell metabolic signaling in insulin secretion. Eur J Endocrinol 134:272-286, 1996
46. Asanuma N, Aizawa T, Sato Y, Schermerhorn T, Komatsu M, Sharp GW, Hashizume K: Two signaling pathways, from the upper glycolytic flux and from the mitochondria, converge to potentiate insulin release. Endocrinology 138:751-755, 1997
47. Berggren PO, Larsson O: Ca2+ and pancreatic B-cell function. Biochem Soc Transact 22:12-18, 1994
48. Larsson O, Kindmark H, Brändström R, Fredholm B, Berggren PO: Oscillations in K-ATP channel activity promote oscillations in cytoplasmic free Ca2+ concentration in the pancreatic beta cell. Proc Natl Acad Sci U S A 9:3:5161-5165, 1996
49. Nilsson T, Schultz V, Berggren PO, Corkey BE, Tornheim I: Temporal patterns of changes in ATP/ADP ratio, glucose 6-phosphate and cytoplasmic free Ca2+ in glucose-stimulated pancreatic beta-cells. Biochim J 31:91-94, 1996
50. Jacobsson G, Bean AJ, Scheller RH, Juntti-Berggren L, Deeney JT, Berggren PO, Meister B: Identification of synaptic proteins and their isoform mRNAs in compartments of pancreatic endocrine relis. Proc Natl Acad Sci U S A 91:12487-12491, 1994
51. Mizuta M, Kurose T, Mike T, Shoji-Kasai Y, Takahashi M, Seino S, Matsukura S: Localization and functional role of synaptotagmin III in insulin secretory vesicles in pancreatic β-cells. Diabetes 46:2002-2006, 1997
52. Santerre RF, Cook RA, Crisel RM, Sharp JD, Schmidt RJ, Williams DC, Wilson CP: Insulin synthesis in a clonal cell line of simian virus 40-transformed hamster pancreatic beta cells. Proc Natl Acad Sci U S A 78:4339-4343, 1981
53. Buchan AMJ, Sikora LKJ, Levy JG, McIntosh CHS, Dyck I, Brown JC: An immunocytochemical investigation with monoclonal antibodies to somatostatin. Histochemistry 83:175-180, 1985
54. Hill RS, Boyd AE: Perifusion of a clonal cell line of Simian virus 40-transformed beta-cells: insulin secretory dynamics in response to glucose, 3-isobutyl-1-methylxanthine, and potassium. Diabetes 34:115-120, 1985
55. Grill V, Pigon J, Hartling SG, Binder C, Efendic S: Effects of dexamethasone on glucose-induced insulin and proinsulin release in low and high responders. Metabolism 39:251-258, 1990
56. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ: Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391:85-100, 1981
57. Reetz A, Solimena M, Matteoli M, Folli F, Takei K, De Camilli P: GABA and pancreatic beta-cells: colocalization of glutamic acid decarboxylase (GAD) and GABA with synaptic-like microvesicles suggests their role in GABA storage and secretion. EMBO J 10:1275-1284, 1991
58. Rhodes CJ, Brennan SO, Hutton JC: Proalbumin to albumin conversion by a proinsulin processing endopeptidase of insulin secretory granules. J Biol Chem 254:14240-14245, 1989
59. Towbin H, Staehelin T, Gordon J: Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76:4350-4354, 1979
60. Wendland B, Miller KG, Schilling J, Scheller RH: Differential expression of the p65 gene family. Neuron 9:99:3-1007, 1991
61. Vician L, Lim IK, Ferguson G, Tocco G, Baudry M, Herschman HR: Synaptotagmin IV is an immediate early gene induced by depolarization in PC12 cells and in brain. Proc Natl Acad Sci U S A 92:2164-2168, 1995
62. Helle KB: Chromogranins: universal proteins in secretory organelles from Paramecium to man. Neurochem Int 17:165-175, 1990
63. Winkler H, Fischer-Colbrie R: The chromogranins A and B: the first 25 years and future perspectives. Neurosrience 49:497-528, 1992
64. Eisenberg D, Schwartz E, Komaromy M, Wall R: Analysis of membrane and surface protein sequences with the Hydrophobic moment plot. J Mol Biol 179:125-142, 1984
65. Thomas-Reetz A, Hell JW, During MJ, Walch-Solimena C, Jahn R, De Camilli P: A gamma-aminobutyric acid transporter driven by a proton pump is present in synaptic-like microvesicles of pancreatic beta cells. Proc Natl Acad Sci U S A 90:51317-5321, 1993
66. Jahn R, Schiebler W, Ouimet CC, Greengard P: A 38,000-dalton membrane protein (p38) present in synaptic vesicles. Proc Natl Acad Sci U S A 82:4137-4141, 1985
67. Poitout V, Olson LK, Robertson RP: Insulin-secreting cell lines: classification, characteristics and potential applications. Diabetes 22:7-14, 1996
68. Goda Y, Stevens CF: Two components of transmitter release at a central synapse. Proc Natl Acad Sci U S A 91:12942-12946, 1994
69. Lundberg JM, Rudehill A, Sollevi A, Fried G, Wallin G: Frequency- and reserpine-dependent chemical coding of sympathetic transmission: differential release of noradrenaline and neuropeptide Y from pig spleen. Neurosci Lett 63:96-100, 1986
70. Iverfeldt K, Serfozo P, Diaz Arnesto LL, Bartfai T: Differential release of coexisting transmitters: frequency dependence of the efflux of substance P, thyrotropin releasing honnone and 3H-serotonin from tissue slices of rat ventral spinal cord. Acta Physiol Scand 137:63-71, 1989
71. Verhage M, McMahon HT, Ghijsen WE, Boomsma F, Scholten G, Wiegant VM, Nicholls DG: Differential release of amino acids, neuropeptides, and catecholamines from isolated nerve terminals. Neuron 6:517-524, 1991
72. Franck J, Brodin E, Fried G: Differential release of endogenous 5-hydroxytryptamine, substance P and neurokinin A from ventral spinal cord in response to electrical stimulation. J Neurochem 61:704-711, 1993
73. Augustine GJ, Neher E: Calcium requirements for secretion in bovine chromaffin cells. J Physiol (Lond) 450:247-271, 1992
74. Theler JM, Mollard P, Guérinau N, Vacher P, Pralong WF, Schlegel W, Wollheim CB: Video imaging of cytosolic Ca2+ in pancreatic beta-cells stimulated by glucose, carbachol, and ATP. J Biol Chem 267:18110-18117, 1992
75. Ämmälä C, Eliasson L, Bokvist K, Larsson O, Ashcroft FM, Rorsman P: Exocytosis elicited by action potentials and voltage-clamp calcium currents in individual mouse pancreatic B-cells. J Physiol (Lond) 472:665-688, 1993
76. Bokvist K, Eliasson L, Ämmälä C, Renström E, Rorsman P: Co-localization of L-type Ca2+ channels and insulin-containing secretory granules and its significance for the initiation of exocytosis in mouse pancreatic B-cells. EMBO J 14:50-57, 1995
77. Heinemann C, Chow RH, Neher E, Zucker RS: Kinetics of the secretory response in bovine chromaffin cells following flash photolysis of caged Ca2+. Biophys J 67:2540-2557, 1994
78. Neher E, von Ruden L: Depression and augmentation of quantal release in adrenal chromaffin cell. Adv Second Messenger Phosphoprotein Res 29:353-362, 1994
79. Henquin JC: Specificity of divalent cation requirement for insulin release: effects of strontium. Pflügers Arch 383:123-129, 1980