RNA interference-mediated silencing of synaptotagmin IX, but not synaptotagmin I, inhibits dense-core vesicle exocytosis in PC12 cells

Biochemical Journal

Volumn 380, Issue 3, 2004, Pages 875-879

  Fukuda, Mitsunori ^a  

^a RIKEN   (Japan)

Author keywords

Ca2+ sensor; Double stranded RNA mediated interference (RNAi); Endocrine cell; Exocytosis; PC12 cell; Synaptotagmin

Indexed keywords

CALCIUM; CELLS; POLYPEPTIDES; POSITIVE IONS; RNA;

EXOCYTOSIS; SYNAPTOTAGMIN ISOFORMS;

BIOCHEMISTRY;

CALCIUM ION; NEUROPEPTIDE Y; POTASSIUM CHLORIDE; SMALL INTERFERING RNA; SYNAPTOTAGMIN; SYNAPTOTAGMIN 9; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIBODY AFFINITY; ARTICLE; CONTROLLED STUDY; EXOCYTOSIS; GENE SILENCING; IMMUNOCYTOCHEMISTRY; NONHUMAN; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEIN SECRETION; RAT; RNA INTERFERENCE; SECRETORY VESICLE;

ANIMALS; CALCIUM-BINDING PROTEINS; CELL LINE; EXOCYTOSIS; GENE EXPRESSION REGULATION; GENE SILENCING; MEMBRANE GLYCOPROTEINS; NERVE TISSUE PROTEINS; PC12 CELLS; RATS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SECRETORY VESICLES; SYNAPTOTAGMIN I; SYNAPTOTAGMINS;

ANIMALIA;

EID: 3042782694     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20040096     Document Type: Article

References (47)

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. Südhof, T. C. (2002) Synaptotagmins: why so many? J. Biol. Chem. 277, 7629-7632
4. 2+ sensor that triggers exocytosis? Nat. Rev. Mol. Cell Biol. 3, 498-508
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. Adolfsen, B. and Littleton, J. T. (2001) Genetic and molecular analysis of the synaptotagmin family. Cell. Mol. Life Sci. 58, 393-402
8. Fukuda, M. (2003) Molecular cloning, expression, and characterization of a novel class of synaptotagmin (Syt XIV) conserved from Drosophila to humans. J. Biochem. (Tokyo) 133, 641-349
9. Fukuda, M. (2003) Molecular cloning and characterization of human, rat, and mouse synaptotagmin XV. Biochem. Biophys. Res. Commun. 306, 64-71
10. 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. U.S.A. 92, 10703-10707
11. 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. U.S.A. 92, 10708-10712
12. 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 (London) 410, 41-49
13. Yoshihara, M. and Littleton, J. T. (2002) Synaptotagmin I functions as a calcium sensor to synchronize neurotransmitter release. Neuron 36, 897-908
14. Poskanzer, K. E., Marek, K. W., Sweeney, S. T. and Davis, G. W. (2003) Synaptotagmin I is necessary for compensatory synaptic vesicle endocytosis in vivo. Nature (London) 426, 559-563
15. Elterink, L. A., Peterson, M. R. and Scheller, R. H. (1993) A role for synaptotagmin (p65) in regulated exocytosis. Cell (Cambridge, Mass.) 72, 153-159
16. 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. U.S.A. 94, 287-291
17. 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
18. Voets, T., Moser, T., Lund, P. E., Chow, R. H., Geppert, M., Südhot, 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. U.S.A. 98, 11680-11685
19. 2+-triggered exocytosis. Neuron 34, 599-611
20. 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
21. Shoji-Kasai, Y., Yoshida, A., Sato, K., Hoshino, T., Ogura, A., Kondo, S., Fujimoto, Y., Kuwahara, R., Kato, R. and Takahashi, M. (1992) Neurotransmitter release from synaptotagmin-deficient clonal variants of PC12 cells. Science 256, 1821-1823
22. 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
23. 2+ sensor in exocytosis. Neuron 30, 459-473
24. 2+ affinities. EMBO J. 21, 270-280
25. 2+-dependent secretion in PC12 cells. J. Biol. Chem. 277, 4601-4604
26. 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
27. 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
28. Thomas, D. M., Ferguson, G. O., 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
29. 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
30. 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
31. Fukuda, M., Kanno, E. and Yamamoto, A. (2004) Rabphilin and Noc2 are recruited to dense-core vesicle exocytosis through specific interaction with Rab27A in PC12 cells. J. Biol. Chem. 279, 13065-13075
32. 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
33. 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
34. Waselle, L., Coppola, T., Fukuda, M., Iezzi, M., El-Amraoui, A., Petit, C. and Regazzi, R. (2003) Involvement of the Rab27 binding protein Slac2c/MyRIP in insulin exocytosis. Mol. Biol. Cell 14, 4103-4113
35. Fukuda, M., Katayama, E. and Mikoshiba, K. (2002) The calcium-binding loops of the tandem C2 domains of synaptotagmin VII cooperatively mediate calcium-dependent oligomerization. J. Biol. Chem. 277, 29315-29320
36. Fukuda, M., Kanno, E., Saegusa, C., Ogata, Y. and Kuroda, T. S. (2002) Slp4-a/granuphilin-a regulates dense-core vesicle exocytosis in PC12 cells. J. Biol. Chem. 277, 39673-39678
37. 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
38. 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
39. Moss, E. G. (2001) RNA interference: it's a small RNA world. Curr. Biol. 11, R772-R775
40. McManus, M. T. and Sharp, P. A. (2002) Gene silencing in mammals by small interfering RNAs. Nat. Rev. Genet. 3, 737-747
41. Shin, O. H., Rizo, J. and Südhof, T. C. (2002) Synaptotagmin function in dense core vesicle exocytosis studied in cracked PC12 cells. Nat. Neurosci. 5, 649-656
42. 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 (London) 424, 943-947
43. 2+-dependent phospholipid binding to the C2A domain of synaptotagmin IV. J. Biol. Chem. 271, 8430-8434
44. Rickman, C., Craxton, M., Osborne, S. and Davletov, B. (2004) Comparative analysis of tandem C2 domains from the mammalian synaptotagmin family. Biochem. J. 378, 681-686
45. 2+-dependent insulin exocytosis. J. Cell Sci., in the press
46. 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, 28180-26185
47. Fukuda, M. and Mikoshiba, K. (2000) Calcium-dependent and -independent hetero-oligomerization in the synaptotagmin family. J. Biochem. (Tokyo) 128, 637-645