Effect of forskolin on synaptotagmin IV protein trafficking in PC12 cells

Journal of Biochemistry

Volumn 136, Issue 2, 2004, Pages 245-253

  Fukuda, Mitsunori ^a   Yamamoto, Akitsugu ^b  

^a INST OF PHYS AND CHEMICAL RESEARCH   (Japan)

^b NAGAHAMA INSTITUTE OF BIO SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

Dense core vesicle; Forskolin; Golgi; Immediate early gene; Regulated exocytosis; Synaptotagmin

Indexed keywords

FORSKOLIN; GENE PRODUCT; SYNAPTOTAGMIN;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL SELECTION; CELL STRAIN; CELLULAR DISTRIBUTION; EXOCYTOSIS; GENETIC REGULATION; IMMEDIATE EARLY GENE; IMMUNOELECTRON MICROSCOPY; MEMBRANE DEPOLARIZATION; MOUSE; NEUROTRANSMITTER RELEASE; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT;

ANIMALS; BIOLOGICAL TRANSPORT; CALCIUM; CALCIUM-BINDING PROTEINS; CELL MEMBRANE; CULTURE MEDIA; CYCLIC AMP; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EXOCYTOSIS; FORSKOLIN; GOLGI APPARATUS; IMMUNOHISTOCHEMISTRY; LONG-TERM POTENTIATION; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICROSCOPY, IMMUNOELECTRON; MICROTUBULES; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; PC12 CELLS; PROTEIN ISOFORMS; PROTEIN TRANSPORT; RATS; SUBCELLULAR FRACTIONS; SYNAPTOTAGMINS; TRANS-GOLGI NETWORK;

ANIMALIA;

EID: 4644341973     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: 10.1093/jb/mvh116     Document Type: Article

References (64)

1. Schiavo, G., Osborne, S.L., and Sgouros, J.G. (1998) Synaptotagmins: more isoforms than functions? Biochem. Biophys. Res. Commun. 248, 1-8
2. Marquèze, B., Berton, F., and Seagar, M. (2000) Synaptotagmins in membrane traffic: which vesicles do the tagmins tag? Biochimie 82, 409-420
3. 2+ sensor that triggers exocytosis? Nat. Rev. Mol. Cell Biol. 3, 498-508
4. Südhof, T.C. (2002) Synaptotagmins: why so many? J Biol. Chem. 277, 7629-7632
5. 2+-regulated membrane trafficking. Recent Res. Dev. Chem. Phys. Lipids 1, 15-51
6. Craxton, M. (2001) Genomic analysis of synaptotagmin genes. Genomics 77, 43-49
7. 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
8. Fukuda, M. (2003) Molecular cloning and characterization of human, rat, and mouse synaptotagmin XV. Biochem. Biophys. Res. Commun. 306, 64-71
9. Adolfsen, B. and Littleton, J.T. (2001) Genetic and molecular analysis of the synaptotagmin family. Cell. Mol. Life Sci. 58, 393-402
10. Fernandez-Chacon, R., Konigstorfer, A., Gerber, S.H., Garcia, J., Matos, M.F., Stevens, C.F., Brose, N., Rizo, J., Rosenmund, C., and Südhof, T.C. (2001) Synaptotagmin I functions as a calcium regulator of release probability. Nature 410, 41-49
11. 2+-binding motif of synaptotagmin is required for synaptic transmission in vivo. Nature 418, 340-344
12. Yoshihara, M. and Littleton, J.T. (2002) Synaptotagmin I functions as a calcium sensor to synchronize neurotransmitter release. Neuron 36, 897-908
13. Bommert, K., Charlton, M.P., DeBello, W.M., Chin, G.J., Betz, H., and Augustine, G.J. (1993) Inhibition of neurotransmitter release by C2-domain peptides implicates synaptotagmin in exocytosis. Nature 363, 163-165
14. Mikoshiba, K., Fukuda, M., Moreira, J.E., Lewis, F.M.T., Sugimori, M., Niinobe, M., and 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
15. Fukuda, M., Moreira, J.E., Lewis, F.M.T., Sugimori, M., Niinobe, M., Mikoshiba, K., and 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
16. Fukuda, M., Moreira, J.E., Liu, V., Sugimori, M., Mikoshiba, K., and Llinás, R.R. (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
17. 2+-dependent reversible docking of granules to the plasma membrane. Traffic 3, 496-511
18. Lang, J., Fukuda, M., Zhang, H., Mikoshiba, K., and Wollheim, C.B. (1997) The first C2 domain of synaptotagmin is required for exocytosis of insulin from pancreatic β-cells: action of synaptotagmin at low micromolar calcium. EMBO J. 16, 5837-5846
19. Ohara-Imaizumi, M., Fukuda, M., Niinobe, M., Misonou, H., Ikeda, K., Murakami, T., Kawasaki, M., Mikoshiba, K., and 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
20. Voets, T., Moser, T., Lund, P.E., Chow, R.H., Geppert, M., Südhof, T.C., and Neher, E. (2001) Intracellular calcium dependence of large dense-core vesicle exocytosis in the absence of synaptotagmin I. Proc. Natl. Acad. Sci. USA 98, 11680-11685
21. 2+-dependent secretion in PC12 cells. J. Biol. Chem. 277, 4601-4604
22. Saegusa, C., Fukuda, M., and 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
23. Tucker, W.C., Edwardson, J.M., Bai, J., Kim, H.J., Martin, T.F.J., and Chapman, E.R. (2003) Identification of synaptotagmin effectors via acute inhibition of secretion from cracked PC12 cells. J. Cell Biol. 162, 199-209
24. 2+] in pituitary cells. Amer. J. Physiol. Cell Physiol. 284, C547-C554
25. 2+-dependent insulin exocytosis. J. Cell Sci. 117, 3119-3127
26. Fukuda, M. (2004) RNA interference-mediated silencing of synaptotagmin IX, but not synaptotagmin I, inhibits dense-core vesicle exocytosis in PC12 cells. Biochem. J. 380, 875-879
27. Michaut, M., De Blas, G., Tomes, C.N., Yunes, R., Fukuda, M., and Mayorga, L.S. (2001) Synaptotagmin VI participates in the acrosome reaction of human spermatozoa. Dev. Biol. 235, 521-529
28. 2+-dependent exocytosis of lysosomes in fibroblasts. J. Cell Biol. 148, 1141-1149
29. 2+-regulated exocytosis of lysosomes. Cell 106, 157-169
30. Chakrabarti, S., Kobayashi, K.S., Flavell, R.A., Marks, C.B., Miyake, K., Liston, D.R., Fowler, K.T., Gorelick, F.S., and Andrews, N.W. (2003) Impaired membrane resealing and autoimmune myositis in synaptotagmin VII-deficient mice. J. Cell Biol. 162, 543-549
31. Mizuta, M., Kurose, T., Miki, T., Shoji-Kasai, Y., Takahashi, M., Seino, S., and Matsukura, S. (1997) Localization and functional role of synaptotagmin III in insulin secretory vesicles in pancreatic β-cells. Diabetes 46, 2002-2006
32. Ferguson, G.D., Thomas, D.M., Elferink, L.A., and Herschman, H.R. (1999) Synthesis degradation, and subcellular localization of synaptotagmin IV, a neuronal immediate early gene product. J. Neurochem. 72, 1821-1831
33. Gut, A., Kiraly, C.E., Fukuda, M., Mikoshiba, K., Wollheim, C.B., and Lang, J. (2001) Expression and localisation of synaptotagmin isoforms in endocrine β-cells: their function in insulin exocytosis. J. Cell Sci. 114, 1709-1716
34. 2+ sensor in exocytosis. Neuron 30, 459-473
35. Fukuda, M., Ogata, Y., Saegusa, C., Kanno, E., and Mikoshiba, K. (2002) Alternative splicing isoforms of synaptotagmin VII in the mouse, rat and human. Biochem. J. 365, 173-180
36. Fukuda, M., Kanno, E., Ogata, Y., Saegusa, C., Kim, T., Peng Loh, Y., and 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
37. Hilbush, B.S. and Morgan, J.I. (1994) A third synaptotagmin gene, Syt3, in the mouse. Proc. Natl. Acad. Sci. USA 91, 8195-8199.
38. Vician, L., Lim, I.K., Ferguson, G., Tocco, G., Baudry, M., and Herschman, H.R. (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. Babity, J.M., Armstrong, J.N., Plumier, J.C., Currie, R.W., and Robertson, H.A. (1997) A novel seizure-induced synaptotagmin gene identified by differential display. Proc. Natl. Acad. Sci. USA 94, 2638-2641
40. Ibata, K., Fukuda, M., Hamada, T., Kabayama, H., and Mikoshiba, K. (2000) Synaptotagmin IV is present at the Golgi and distal parts of neurites. J. Neurochem. 74, 518-526
41. Ferguson, G.D., Vician, L., and Herschman, H.R. (2001) Synaptotagmin IV: biochemistry, genetics, behavior, and possible links to human psychiatric disease. Mol. Neurobiol. 23, 173-185
42. Ferguson, G.D., Anagnostaras, S.G., Silva, A.J., and Herschman, H.R. (2000) Deficits in memory and motor performance in synaptotagmin IV mutant mice. Proc. Natl. Acad. Sci. USA 97, 5598-5603
43. Littleton, J.T., Serano, T.L., Rubin, G.M., Ganetzky, B., and Chapman, E.R. (1999) Synaptic function modulated by changes in the ratio of synaptotagmin I and IV. Nature 400, 757-760
44. Thomas, D.M., Ferguson, G.D., Herschman, H.R., and Elferink, L.A. (1999) Functional and biochemical analysis of the C2 domains of synaptotagmin IV. Mol. Biol. Cell 10, 2285-2295
45. Wang, C.T., Grishanin, R., Earles, C.A., Chang, P.Y., Martin, T.F.J., Chapman, E.R., and Jackson, M.B. (2001) Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of dense-core vesicles. Science 294, 1111-1115
46. Tsuboi, T. and Rutter, G.A. (2003) Multiple forms of "kiss-and- run" exocytosis revealed by evanescent wave microscopy. Curr. Biol. 13, 563-567
47. Wang, C.T., Lu, J.C., Bai, J., Chang, P.Y., Martin, T.F.J., Chapman, E.R., and Jackson, M.B. (2003) Different domains of synaptotagmin control the choice between kiss-and-run and full fusion. Nature 424, 943-947
48. Berton, F., Cornet, V., Iborra, C., Garrido, J., Dargent, B., Fukuda, M., Seagar, M., and Marquèze, B. (2000) Synaptotagmin I and IV define distinct populations of neuronal transport vesicles. Eur. J. Neurosci. 12, 1294-1302
49. Eaton, B.A., Haugwitz, M., Lau, D., and Moore, H.P. (2000) Biogenesis of regulated exocytotic carriers in neuroendocrine cells. J. Neurosci. 20, 7334-7344
50. Fukuda, M., Ibata, K., and Mikoshiba, K. (2001) A unique spacer domain of synaptotagmin IV is essential for Golgi localization. J. Neurochem. 77, 730-740
51. Ibata, K., Hashikawa, T., Tsuboi, T., Terakawa, S., Liang, F., Mizutani, A., Fukuda, M., and 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
52. Fukuda, M., Yamamoto, A., and Mikoshiba, K. (2001) Formation of crystalloid endoplasmic reticulum induced by expression of synaptotagmin lacking the conserved WHXL motif in the C terminus: structural importance of the WHXL motif in the C2B domain. J. Biol. Chem. 276, 41112-41119
53. Fukuda, M. and Mikoshiba, K. (1999) A novel alternatively spliced variant of synaptotagmin VI lacking a transmembrane domain: implications for distinct functions of the two isoforms. J. Biol. Chem. 274, 31428-31434
54. Fukuda, M., Kanno, E., and Mikoshiba, K. (1999) Conserved N-terminal cysteine motif is essential for homo- and heterodimer formation of synaptotagmins III, V, VI, and X. J. Biol. Chem. 274, 31421-31427
55. Fukuda, M. (2003) Slp4-a/granuphilin-a inhibits dense-core vesicle exocytosis through interaction with the GDP-bound form of Rab27A in PC12 cells. J. Biol. Chem. 278, 15390-15396
56. Fukuda, M. and Mikoshiba, K. (2000) Distinct self-oligomerization activities of synaptotagmin family: unique calcium-dependent oligomerization properties of synaptotagmin VII. J. Biol. Chem. 275, 28180-28185
57. 2+-triggered exocytosis. Neuron 34, 599-611
58. Rabe, C.S. and McGee, R., Jr. (1983) Regulation of depolarization- dependent release of neurotransmitters by adenosine: cyclic AMP-dependent enhancement of release from PC12 cells. J. Neurochem. 41, 1623-1634
59. Fukuda, M., Kanno, E., and Yamamoto, A. (2004) Rabphilin and Noc2 are recruited to dense-core vesicles through specific interaction with Rab27A in PC12 cells. J. Biol. Chem. 279, 13065-13075
60. Ferguson, G.D., Chen, X.N., Korenberg, J.R., and Herschman, H.R. (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
61. 2+-dependent phospholipid binding to the C2A domain of synaptotagmin IV. J. Biol. Chem. 271, 8430-8434
62. 2+ binding in the C2A domain. Nature 418, 336-340
63. Zhang, Q., Fukuda, M., Van Bockstaele, E., Pascual, O., and Haydon, P.G. (2004) Synaptotagmin IV regulates glial glutamate release. Proc. Natl. Acad. Sci. USA 101, 9441-9446
64. Salin, P.A., Malenka, R.C., and Nicoll, R.A. (1996) Cyclic AMP mediates a presynaptic form of LTP at cerebellar parallel fiber synapses. Neuron 16, 797-803