Role of synaptotagmin, a Ca2+ and inositol polyphosphate binding protein, in neurotransmitter release and neurite outgrowth

Chemistry and Physics of Lipids

Volumn 98, Issue 1-2, 1999, Pages 59-67

  Mikoshiba, Katsuhiko ^a,b   Fukuda, Mitsunori ^b   Ibata, Keiji ^a   Kabayama, Hiroyuki ^a   Mizutani, Akihiro ^b  

^a THE UNIVERSITY OF TOKYO   (Japan)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Neurite outgrowth; Neurotransmitter release; Synaptotagmin

Indexed keywords

ANTIBODY; BINDING PROTEIN; CALCIUM BINDING PROTEIN; INOSITOL PENTAKISPHOSPHATE; INOSITOL POLYPHOSPHATE; INOSITOL TETRAKISPHOSPHATE; ISOPROTEIN; PHYTIC ACID; SYNAPTOTAGMIN; CALCIUM; INOSITOL PHOSPHATE; MEMBRANE PROTEIN; NERVE PROTEIN; SYNAPTOTAGMIN I; SYT1 PROTEIN, HUMAN; SYT6 PROTEIN, HUMAN;

AMINO ACID SEQUENCE; BINDING AFFINITY; CHICKEN; CONFERENCE PAPER; EXOCYTOSIS; NERVE FIBER GROWTH; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; SPINAL GANGLION; SYNAPSE VESICLE; ANIMAL; BINDING SITE; CHEMISTRY; CYTOLOGY; HUMAN; METABOLISM; MOLECULAR GENETICS; NERVE CELL; NEURITE; PHYSIOLOGY; REVIEW; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CALCIUM; CALCIUM-BINDING PROTEINS; EXOCYTOSIS; HUMANS; INOSITOL PHOSPHATES; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEURITES; NEURONS; SEQUENCE ALIGNMENT; SYNAPTOTAGMIN I; SYNAPTOTAGMINS;

EID: 0032587558     PISSN: 00093084     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0009-3084(99)00018-3     Document Type: Conference Paper

References (46)

1. Babity J.M., Armstrong J.N., Plumier J.C., Currie R.W., Robertson H.A. A novel seizure-induced synaptotagmin gene identified by differential display. Proc. Natl. Acad. Sci. USA. 94:1997;2638-2641.
2. Beckers C.J.M., Balch W.E. Calcium and GTP: essential components in vesicular trafficking between the endoplasmic reticulum and Golgi apparatus. J. Cell Biol. 108:1994;1245-1256.
3. Bennett M.K., Scheller R.H. The molecular machinery for secretion is conserved from yeast to neurons. Proc. Natl. Acad. Sci. USA. 90:1993;2559-2563.
4. Chapman E.R., Hanson P.I., An S., Jahn R. Ca2+ regulates the interaction between synaptotagmin and syntaxin 1. J. Biol. Chem. 270:1995;23667-23671.
5. Craxton M., Goedert M. Synaptotagmin V: a novel synaptotagmin isoform expressed in rat brain. FEBS Lett. 361:1995;196-200.
6. Ferro N.S., Jahn R. Vesicle fusion from yeast to man. Nature. 370:1994;191-193.
7. Fukuda M., Mikoshiba K. The function of inositol high polyphosphate binding proteins. Bioessays. 19:1997;593-603.
8. Fukuda M., Aruga J., Niinobe M., Aimoto S., Mikoshiba K. Inositol-1,3,4,5-tetrakisphosphate binding to C2B domain of IP4BP/synaptotagmin II. J. Biol. Chem. 269:1994;29206-29211.
9. Fukuda M., Moreira J.E., Lewis F.M. et al. 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. 92:1995;10708-10712.
10. Fukuda M., Kojima T., Aruga J., Niinobe M., Mikoshiba K. Functional diversity of C2 domains of synaptotagmin family. Mutational analysis of inositol high polyphosphate binding domain. J. Biol. Chem. 270:1995;26523-26527.
11. Futerman A.H., Banker G.A. The economics of neurite outgrowth-the addition of new membrane to growing axons. Trends Neurosci. 19:1996;144-149.
12. Geppert M., Archer B., Südhof T.C. Synaptotagmin II. A novel differentially distributed form of synaptotagmin. J. Biol. Chem. 266:1991;13548-13552.
13. Goodman, C.S., Shatz, C.J., 1993. Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72/Neuron 10 (Suppl.) 77-98.
14. Hilbush B.S., Morgan J.I. A third synaptotagmin gene, Syt3, in the mouse. Proc. Natl. Acad. Sci. USA. 91:1994;8195-8199.
15. Hudson A.W., Birnbaum M.J. Identification of a nonneuronal isoform of synaptotagmin. Proc. Natl. Acad. Sci. USA. 92:1995;5895-5899.
16. Ibata K., Fukuda M., Mikoshiba K. Inositol 1,3,4,5-tetrakisphosphate binding activities of neuronal and non-neuronal synaptotagmins. J. Biol. Chem. 273:1998;12267-12273.
17. Ide C. Peripheral nerve regeneration. Neurosci. Res. 25:1996;101-121.
18. Igarashi M., Kozaki S., Terakawa S., Kawano S., Ide C., Komiya Y. Growth cone collapse and inhibition of neurite growth by Botulinum neurotoxin C1: A t-SNARE is involved in axonal growth. J. Cell Biol. 134:1996;205-215.
19. Igarashi M., Tagaya M., Komiya Y. The soluble N-ethylmaleimide-sensitive factor attached protein receptor complex in growth cones: molecular aspects of the axon terminal development. J. Neurosci. 17:1997;1460-1470.
20. Kabayama, H., Takei, K., Fukuda, M., Ibata, K., Mikoshiba, K., 1998. Functional involvement of synaptotagmin I/II C2A domain in neurite outgrowth of chick dorsal root ganglion neuron. Neuroscience (in press).
21. Kater S.B., Mills L.R. Regulation of growth cone behavior by calcium. J. Neurosci. 11:1991;891-899.
22. Kojima T., Fukuda M., Aruga J., Mikoshiba K. Calcium-dependent phospholipid binding to the C2A domain of a ubiquitous form of double C2 protein (Doc2β). J. Biochem. 120:1996;671-676.
23. Lang E.J., Zhang H., Fukuda M., Mikoshiba K., Wollheim C.B. The first C2 domain of synaptotagmin is required for exocytosis of insulin from pancreatic b-cells: action of synaptotagmin at low micromolar calcium. EMBO J. 16:1997;5837-5846.
24. Li C., Ullrich B., Zhang J.Z., Anderson R.G., Brose N., Südhof T.C. Ca(2+)-dependent and -independent activities of neural and non-neural synaptotagmins. Nature. 375:1995;594-599.
25. Llinás R., Sugimori M., Lang E.J. et al. The inositol high-polyphosphate series blocks synaptic transmission by preventing vesicular fusion: a squid giant synapse study. Proc. Natl. Acad. Sci. USA. 91:1994;12990-12993.
26. Lou X., Bixby J.L. Coordinate and noncoordinate regulation of synaptic vesicle protein genes during embryonic development. Dev. Biol. 159:1993;327-337.
27. Lupashin V.V., Hamamoto S., Schekman R.W. Biochemical requirements for the targeting and fusion of ER-derived transport vesicles with purified yeast Golgi membranes. J. Cell Biol. 132:1996;277-289.
28. Martin K.C., Hu Y., Armitage B.A., Siegelbaum S.A., Kandel E.R., Kaang B.-K. Evidence for synaptotagmin as an inhibitory clamp on synaptic vesicle release in Aplysia neurons. Proc. Natl. Acad. Sci. USA. 92:1995;11307-11311.
29. Mehrotra B., Elliott J.T., Chen J. et al. Selective photoaffinity labeling of the inositol polyphosphate binding C2B domains of synaptotagmins. J. Biol. Chem. 272:1997;4237-4244.
30. Mikoshiba K., Fukuda M., Moreira J.E. et al. 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. 92:1995;10703-10707.
31. 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. 269:1994;11675-11678.
32. Mizutani A., Fukuda M., Niinobe M., Mikoshiba K. Regulation of AP-2-synaptotagmin interaction by inositol high polyphosphates. Biochem. Biophys. Res. Commun. 240:1997;128-131.
33. Mochida S., Fukuda M., Niinobe M., Kobayashi H., Mikoshiba K. Roles of synaptotagmin C2 domains in neurotransmitter secretion and inositol high-polyphosphate binding at mammalian cholinergic synapses. Neuroscience. 77:1997;937-943.
34. Niinobe M., Yamaguchi Y., Fukuda M., Mikoshiba K. Synaptotagmin is an inositol polyphosphate binding protein: isolation and characterization as an Ins 1,3,4,5-P4 binding protein. Biochem. Biophys. Res. Commun. 205:1994;1036-1042.
35. Nonet M.L., Grundahl K., Meyer B.J., Rand J.B. Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell. 73:1993;1291-1305.
36. Ohara I.M., Fukuda M., Niinobe M. et al. Distinct roles of C2A and C2B domains of synaptotagmin in the regulation of exocytosis in adrenal chromaffin cells. Proc Natl Acad Sci USA. 94:1997;287-291.
37. Osen-Sand A., Staple J.K., Naldi E. et al. Common and distinct fusion proteins in axonal growth and transmitter release. J. Comp. Neurol. 367:1996;222-234.
38. Perin M.S., Fried V.A., Mignery G.A., Jahn R., Südhof T.C. Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nature. 345:1990;260-263.
39. Perin M.S., Johnston P.A., Ozcelik T., Jahn R., Francke U., Südhof T.C. Structural and functional conservation of synaptotagmin (p65) in Drosophila and humans. J. Biol. Chem. 266:1991;615-622.
40. Pind S.N., Nuoffer C., McCaffery J.M. et al. Rab1 and Ca2+ are required for the fusion of carrier vesicles mediating endoplasmic reticulum to Golgi transport. J. Cell Biol. 125:1994;239-252.
41. Shao X., Li C., Fernandez I., Zhang X., Südhof T.C., Rizo J. Synaptotagmin-syntaxin interaction: the C2 domain as a Ca2+-dependent electrostatic switch. Neuron. 18:1997;133-142.
42. Shears S.B. Inositol pentakis- and hexakisphosphate metabolism adds versatility to the actions of inositol polyphosphates. Novel effects on ion channels and protein traffic. Subcell. Biochem. 26:1996;187-226.
43. Sollner T., Rothman J.E. Neurotransmission: harnessing fusion machinery at the synapse. Trends Neurosci. 17:1994;344-348.
44. Südhof T.C., Rizo J. Synaptotagmins: C2-domain proteins that regulate membrane traffic. Neuron. 17:1996;379-388.
45. Sugimori M., Tong C.-K., Fukuda M. et al. Presynaptic injection of syntaxin specific antibodies blocks transmission in the squid giant synapse. Neuroscience. 86:1998;39-51.
46. von P.C., Ichtchenko K., Shao X., Rizo J., Südhof T. C. The evolutionary pressure to inactivate. A subclass of synaptotagmins with an amino acid substitution that abolishes Ca2+ binding. J. Biol. Chem. 272:1997;14314-14319.