Synaptotagmin IV acts as a multi-functional regulator of Ca 2+-dependent exocytosis

Neurochemical Research

Volumn 36, Issue 7, 2011, Pages 1222-1227

  Mori, Yasunori ^a   Fukuda, Mitsunori ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

Ca2+ dependent exocytosis; Immediate early genes; PC12 cells; Phosphorylation; Synaptotagmin IV

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM CHANNEL; CALCIUM ION; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOTAGMIN; SYNAPTOTAGMIN IV; UNCLASSIFIED DRUG;

BINDING AFFINITY; BRAIN REGION; CALCIUM SIGNALING; CELLULAR DISTRIBUTION; EXOCYTOSIS; GENE EXPRESSION REGULATION; HUMAN; IMMEDIATE EARLY GENE; NEUROMUSCULAR SYNAPSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; REGULATORY MECHANISM; REVIEW; SYNAPTOTAGMIN IV GENE;

ANIMALS; CALCIUM; DROSOPHILA; EXOCYTOSIS; PC12 CELLS; RATS; SYNAPTOTAGMINS;

EID: 79959867007     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-010-0352-7     Document Type: Review

References (68)

1. Südhof TC (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27:509-547
2. Fukuda M (2006) The role of synaptotagmin and synaptotagmin-like protein (Slp) in regulated exocytosis. In: Regazzi R (ed) Molecular mechanism of Exocytosis. Landes Bioscience, Austin, TX, pp 42-61
3. Chapman ER (2008) How does synaptotagmin trigger neurotransmitter release? Annu Rev Biochem 77:615-641
4. Fukuda M (2003) Molecular cloning, expression, and characterization of a novel class of synaptotagmin (Syt XIV) conserved from Drosophila to humans. J Biochem 133:641-649
5. Fukuda M (2003) Molecular cloning and characterization of human, rat, and mouse synaptotagmin XV. Biochem Biophys Res Commun 306:64-71
6. Craxton M (2007) Evolutionary genomics of plant genes encoding N-terminal-TM-C2 domain proteins and the similar FAM62 genes and synaptotagmin genes of metazoans. BMC Genomics 8:259
7. Fukuda M, Mikoshiba K (2001) The N-terminal cysteine cluster is essential for membrane targeting of B/K protein. Biochem J 360:441-448 (Pubitemid 33151339)
8. Nalefski EA, Falke JJ (1996) The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci 5:2375-2390 (Pubitemid 26424851)
9. 2+-dependent and -independent activities of neural and non-neural synaptotagmins. Nature 375:594-599
10. 2+ regulates the interaction between synaptotagmin and syntaxin 1. J Biol Chem. 270:23667-23671
11. Fukuda M, Aruga J, Niinobe M, Aimoto S, Mikoshiba K (1994) Inositol-1,3,4,5-tetrakisphosphate binding to C2B domain of IP4BP/synaptotagmin II. J Biol Chem 269:29206-29211
12. 2+-activated neurotransmitter release. Cell 74:1125-1134
13. Nonet ML, Grundahl K, Meyer BJ, Rand JB (1993) Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell 73:1291-1305 (Pubitemid 23201144)
14. 2+ sensor for transmitter release at a central synapse. Cell 79:717-727
15. Fernández-Chacón R, Königstorfer A, Gerber SH, García J, Matos MF, Stevens CF, Brose N, Rizo J, Rosenmund C, Südhof TC (2001) Synaptotagmin I functions as a calcium regulator of release probability. Nature 410:41-49
16. 2A domain. Nature 418:336-340
17. Mackler JM, Drummond JA, Loewen CA, Robinson IM, Reist NE (2002) The C2B Ca2+-binding motif of synaptotagmin is required for synaptic transmission in vivo. Nature 418:340-344 (Pubitemid 34790686)
18. 2+-dependent neurotransmitter release. J Neurosci 24:8542-8550
19. Bommert K, Charlton MP, DeBello WM, Chin GJ, Betz H, Augustine GJ (1993) Inhibition of neurotransmitter release by C2-domain peptides implicates synaptotagmin in exocytosis. Nature 363:163-165 (Pubitemid 23147014)
20. Elferink LA, Peterson MR, Scheller RH (1993) A role for synaptotagmin (p65) in regulated exocytosis. Cell 72:153-159 (Pubitemid 23029702)
21. Mikoshiba K, Fukuda M, Moreira JE, Lewis FMT, Sugimori M, Niinobe M, Llinás R (1995) Role of the C2A domain of synaptotagmin in transmitter release as determined by specific antibody injection into the squid giant synapse preterminal. Proc Natl Acad Sci USA 92:10703-10707
22. Fukuda M, Moreira JE, Lewis FMT, Sugimori M, Niinobe M, Mikoshiba K, Llinás R (1995) Role of the C2B domain of synaptotagmin in vesicular release and recycling as determined by specific antibody injection into the squid giant synapse preterminal. Proc Natl Acad Sci USA 92:10708-10712
23. Mochida S, Fukuda M, Niinobe M, Kobayashi H, Mikoshiba K (1997) Roles of synaptotagmin C2 domains in neurotransmitter secretion and inositol high-polyphosphate binding at mammalian cholinergic synapses. Neuroscience 77:937-943 (Pubitemid 27128769)
24. Ohara-Imaizumi M, Fukuda M, Niinobe M, Misonou H, Ikeda K, Murakami T, Kawasaki M, Mikoshiba K, Kumakura K (1997) Distinct roles of C2A and C2B domains of synaptotagmin in the regulation of exocytosis in adrenal chromaffin cells. Proc Natl Acad Sci USA 94:287-291
25. Fukuda M, Moreira JE, Liu V, Sugimori M, Mikoshiba K, Llinás RR (2000) Role of the conserved WHXL motif in the C terminus of synaptotagmin in synaptic vesicle docking. Proc Natl Acad Sci USA 97:14715-14719 (Pubitemid 32016641)
26. de Wit H, Walter AM, Milosevic I, Gulyás-Kovács A, Riedel D, Sørensen JB, Verhage M (2009) Synaptotagmin-1 docks secretory vesicles to syntaxin-1/SNAP-25 acceptor complexes. Cell 138:935-946
27. Jorgensen EM, Hartwieg E, Schuske K, Nonet ML, Jin Y, Horvitz HR (1995) Defective recycling of synaptic vesicles in synaptotagmin mutants of Caenorhabditis elegans. Nature 378:196-199
28. Poskanzer KE, Marek KW, Sweeney ST, Davis GW (2003) Synaptotagmin I is necessary for compensatory synaptic vesicle endocytosis in vivo. Nature 426:559-563 (Pubitemid 37522641)
29. Llinás RR, Sugimori M, Moran KA, Moreira JE, Fukuda M (2004) Vesicular reuptake inhibition by a synaptotagmin I C2B domain antibody at the squid giant synapse. Proc Natl Acad Sci USA 101:17855-17860 (Pubitemid 40051976)
30. Zhang Q, Fukuda M, Van Bockstaele E, Pascual O, Haydon PG (2004) Synaptotagmin IV regulates glial glutamate release. Proc Natl Acad Sci USA 101:9441-9446 (Pubitemid 38812893)
31. 2+-dependent secretion in PC12 cells. J Biol Chem 277:4601-4604
32. Saegusa C, Fukuda M, Mikoshiba K (2002) Synaptotagmin V is targeted to dense-core vesicles that undergo calcium-dependent exocytosis in PC12 cells. J Biol Chem 277:24499-24505 (Pubitemid 34951975)
33. 2+-dependent insulin exocytosis. J Cell Sci 117:3119-3127
34. 2+-dependent exocytosis of lysosomes in fibroblasts. J Cell Biol 148: 1141-1149
35. Michaut M, De Blas G, Tomes CN, Yunes R, Fukuda M, Mayorga LS (2001) Synaptotagmin VI participates in the acrosome reaction of human spermatozoa. Dev Biol 235:521-529 (Pubitemid 32661189)
36. Hutt DM, Cardullo RA, Baltz JM, Ngsee JK (2002) Synaptotagmin VIII is localized to the mouse sperm head and may function in acrosomal exocytosis. Biol Reprod 66:50-56 (Pubitemid 34020586)
37. Hilbush BS, Morgan JI (1994) A third synaptotagmin gene, Syt3, in the mouse. Proc Natl Acad Sci USA 91:8195-8199 (Pubitemid 24253913)
38. Vician L, Lim IK, Ferguson G, Tocco G, Baudry M, Herschman HR (1995) Synaptotagmin IV is an immediate early gene induced by depolarization in PC12 cells and in brain. Proc Natl Acad Sci USA 92:2164-2168
39. Ferguson GD, Anagnostaras SG, Silva AJ, Herschman HR (2000) Deficits in memory and motor performance in synaptotagmin IV mutant mice. Proc Natl Acad Sci USA 97:5598-5603 (Pubitemid 30313764)
40. Ferguson GD, Chen XN, Korenberg JR, Herschman HR (2000) The human synaptotagmin IV gene defines an evolutionary break point between syntenic mouse and human chromosome regions but retains ligand inducibility and tissue specificity. J Biol Chem 275:36920-36926 (Pubitemid 32002105)
41. Berton F, Iborra C, Boudier JA, Seagar MJ, Marquèze B (1997) Developmental regulation of synaptotagmin I, II, III, and IV mRNAs in the rat CNS. J Neurosci 17:1206-1216 (Pubitemid 27073724)
42. Ibata K, Fukuda M, Hamada T, Kabayama H, Mikoshiba K (2000) Synaptotagmin IV is present at the Golgi and distal parts of neurites. J Neurochem 74:518-526 (Pubitemid 30053723)
43. von Poser C, Ichtchenko K, Shao X, Rizo J, Südhof TC (1997) The evolutionary pressure to inactivate: a subclass of synaptotagmins with an amino acid substitution that abolishes Ca2+ binding. J Biol Chem 272:14314-14319 (Pubitemid 27232845)
44. Ullrich B, Li C, Zhang JZ, McMahon H, Anderson RGW, Geppert M, Südhof TC (1994) Functional properties of multiple synaptotagmins in brain. Neuron 13:1281-1291
45. 2+-dependent phospholipid binding to the C2A domain of synaptotagmin IV. J Biol Chem 271:8430-8434
46. 2+ binding to synaptotagmin 4. Nat Struct Mol Biol 11:844-849
47. Wang Z, Chapman ER (2010) Rat and Drosophila synaptotagmin 4 have opposite effects during SNARE-catalyzed membrane fusion. J Biol Chem 285:30759-30766
48. Littleton JT, Serano TL, Rubin GM, Ganetzky B, Chapman ER (1999) Synaptic function modulated by changes in the ratio of synaptotagmin I and IV. Nature 400:757-760 (Pubitemid 29399535)
49. Wang CT, Grishanin R, Earles CA, Chang PY, Martin TFJ, Chapman ER, Jackson MB (2001) Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of dense-core vesicles. Science 294:1111-1115 (Pubitemid 33041868)
50. Machado HB, Liu W, Vician LJ, Herschman HR (2004) Synaptotagmin IV overexpression inhibits depolarization-induced exocytosis in PC12 cells. J Neurosci Res 76:334-341 (Pubitemid 38580128)
51. Zhang Z, Zhang Z, Jackson MB (2010) Synaptotagmin IV modulation of vesicle size and fusion pores in PC12 cells. Biophys J 98:968-978
52. Wang CT, Lu JC, Bai J, Chang PY, Martin TFJ, Chapman ER, Jackson MB (2003) Different domains of synaptotagmin control the choice between kiss-and-run and full fusion. Nature 424:943-947 (Pubitemid 37051685)
53. Tsuboi T, Rutter GA (2003) Multiple forms of "kiss-and-run" exocytosis revealed by evanescent wave microscopy. Curr Biol 13:563-567
54. Dean C, Liu H, Dunning FM, Chang PY, Jackson MB, Chapman ER (2009) Synaptotagmin-IV modulates synaptic function and long-term potentiation by regulating BDNF release. Nat Neurosci 12:767-776
55. 2+ dependence of vesicle fusion at auditory ribbon synapses. Nat Neurosci 13:45-52
56. 2+-evoked release. EMBO J 27:76-87
57. Fukuda M, Kanno E, Ogata Y, Saegusa C, Kim T, Loh YP, Yamamoto A (2003) Nerve growth factor-dependent sorting of synaptotagmin IV protein to mature dense-core vesicles that undergo calcium-dependent exocytosis in PC12 cells. J Biol Chem. 278:3220-3226 (Pubitemid 36801233)
58. Zhang Z, Bhalla A, Dean C, Chapman ER, Jackson MB (2009) Synaptotagmin IV: a multifunctional regulator of peptidergic nerve terminals. Nat Neurosci 12:163-171
59. Ibata K, Hashikawa T, Tsuboi T, Terakawa S, Liang F, Mizutani A, Fukuda M, Mikoshiba K (2002) Non-polarized distribution of synaptotagmin IV in neurons: evidence that synaptotagmin IV is not a synaptic vesicle protein. Neurosci Res 43:401-406 (Pubitemid 34828240)
60. Ferguson GD, Thomas DM, Elferink LA, Herschman HR (1999) Synthesis, degradation, and subcellular localization of synaptotagmin IV, a neuronal immediate early gene product. J Neurochem 72:1821-1831
61. Thomas DM, Ferguson GD, Herschman HR, Elferink LA (1999) Functional and biochemical analysis of the C2 domains of synaptotagmin IV. Mol Biol Cell 10:2285-2295 (Pubitemid 29343135)
62. Adolfsen B, Saraswati S, Yoshihara M, Littleton JT (2004) Synaptotagmins are trafficked to distinct subcellular domains including the postsynaptic compartment. J Cell Biol 166:249-260 (Pubitemid 38988777)
63. Yoshihara M, Adolfsen B, Galle KT, Littleton JT (2005) Retrograde signaling by Syt 4 induces presynaptic release and synapse-specific growth. Science 310:858-863 (Pubitemid 41567345)
64. Ahras M, Otto GP, Tooze SA (2006) Synaptotagmin IV is necessary for the maturation of secretory granules in PC12 cells. J Cell Biol 173:241-251
65. Fukuda M, Ibata K, Mikoshiba K (2001) A unique spacer domain of synaptotagmin IV is essential for Golgi localization. J Neurochem 77:730-740 (Pubitemid 32466771)
66. Fukuda M, Yamamoto A (2004) Effect of forskolin on synaptotagmin IV protein trafficking in PC12 cells. J Biochem 136:245-253 (Pubitemid 39264979)
67. Lee BH, Min X, Heise CJ, Xu BE, Chen S, Shu H, Luby-Phelps K, Goldsmith EJ, Cobb MH (2004) WNK1 phosphorylates synaptotagmin 2 and modulates its membrane binding. Mol Cell 15:741-751 (Pubitemid 39194904)
68. 2+-triggered exocytosis. Neuron 34:599-611