Classical protein kinase C(s) regulates targeting of synaptotagmin IX to the endocytic recycling compartment

Journal of Cell Science

Volumn 118, Issue 8, 2005, Pages 1641-1649

  Haberman, Yael ^a   Ziv, Idit ^a   Gorzalczany, Yaara ^a   Fukuda, Mitsunori ^b   Sagi Eisenberg, Ronit ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b RIKEN   (Japan)

Author keywords

Endocytic recycling compartment (ERC); Endocytosis; Protein kinase C; RBL 2H3 mast cells; Synaptotagmin

Indexed keywords

12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; CALCIUM ION; PHORBOL ESTER; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; SYNAPTOTAGMIN; SYNAPTOTAGMIN 10; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL TRANSPORT; CELLULAR DISTRIBUTION; CHO CELL; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME PHOSPHORYLATION; INTRACELLULAR SPACE; LEUKEMIA CELL LINE; MAST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TARGETING; RAT;

ANIMALS; CALCIUM-BINDING PROTEINS; CELL COMPARTMENTATION; CELL LINE, TUMOR; CELL MEMBRANE; CHO CELLS; CRICETINAE; ENDOCYTOSIS; ENDOSOMES; ENZYME INHIBITORS; PHORBOL ESTERS; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASE C-ALPHA; PROTEIN TRANSPORT; RATS; SYNAPTOTAGMINS; TRANSPORT VESICLES;

ANIMALIA;

EID: 18844456346     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02276     Document Type: Article

References (32)

1. Adolfsen, B. and Littleton, J. T. (2001). Genetic and molecular analysis of the synaptotagmin family. Cell Mol. Life. Sci. 58, 393-402.
2. 2+-triggered exocytosis of lysosomes in mast cells. J. Exp. Med. 189, 1649-1658.
3. Becker, K. P. and Hannun, Y. A. (2003). cPKC-dependent sequestration of membrane-recycling components in a subset of recycling endosomes. J. Biol. Chem. 278, 52747-52754.
4. Becker, K. P. and Hannun, Y. A. (2004). Isoenzyme-specific translocation of protein kinase C (PKC)betaII and not PKCbetaI to a juxtanuclear subset of recycling endosomes: involvement of phospholipase D. J. Biol. Chem. 279, 28251-28256.
5. Chapman, E. R., Desai, R. C., Davis, A. F. and Tornehl, C. K. (1998). Delineation of the oligomerization, AP-2 binding, and synprint binding region of the C2B domain of synaptotagmin. J. Biol. Chem. 273, 32966-32972.
6. Feany, M. B., Yee, A. G., Delvy, M. L. and Buckley, K. M. (1993). The synaptic vesicle proteins SV2, synaptotagmin and synaptophysin are sorted to separate cellular compartments in CHO fibroblasts. J. Cell Biol. 123, 575-584.
7. 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.
8. Fukuda, M. and Mikoshiba, K. (2000). Genomic structures of synaptotagmin II protein: comparison of exon-intron organization of the synaptotagmin gene family. Biochem. Biophys. Res. Commun. 270, 528-532.
9. 2+-dependent secretion in PC12 cells. J. Biol. Chem. 277, 4601-4604.
10. Grass, I., Thiel, S., Honing, S. and Haucke, V. (2004). Recognition of a basic AP-2 binding motif within the C2B domain of synaptotagmin is dependent on multimerization. J. Biol. Chem. 279, 54872-54880.
11. Grimberg, E., Peng, Z., Hammel, I. and Sagi-Eisenberg, R. (2003). Synaptotagmin III is a critical factor for the formation of the perinuclear endocytic recycling compartment and determination of secretory granules size. J. Cell Sci. 116, 145-154.
12. Haberman, Y., Grimberg, E., Fukuda, M. and Sagi-Eisenberg, R. (2003). Synaptotagmin IX, a possible linker between the perinuclear endocytic recycling compartment and the microtubules. J. Cell Sci. 116, 4307-4318.
13. Heuser, J. E. and Anderson, R. G. (1989). Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J. Cell Biol. 108, 389-400.
14. 2+-dependent insulin exocytosis. J. Cell Sci. 117, 3119-3127.
15. Le, T. L., Joseph, S. R., Yap, A. S. and Stow, J. L. (2002). Protein kinase C regulates endocytosis and recycling of E-cadherin. Am. J. Physiol. Cell Physiol. 283, 489-499.
16. Lin, S. X., Gundersen, G. G. and Maxfield, F. R. (2002). Export from pericentriolar endocytic recycling compartment to cell surface depends on stable, detyrosinated (glu) microtubules and kinesin. Mol. Biol. Cell 13, 96-109.
17. Lippincott-Schwartz, J., Yuan, L. C., Bonifacino, J. S. and Klausner, R. D. (1989). Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 56, 801-813.
18. Lippincott-Schwartz, J., Yuan, L., Tipper, C., Amherdt, M., Orci, L. and Klausner, R. D. (1991). Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell 67, 601-616.
19. Loder, M. K. and Melikian, H. E. (2003). The dopamine transporter constitutively internalizes and recycles in a protein kinase C-regulated manner in stably transfected PC12 cell lines. J. Biol. Chem. 278, 22168-22174.
20. Mallet, W. G. and Maxfield, F. R. (1999). Chimeric forms of furin and TGN38 are transported with the plasma membrane in the trans-Golgi network via distinct endosomal pathways. J. Cell Biol. 146, 345-359.
21. Marqueze, B., Berton, F. and Seagar, M. (2000). Synaptotagmuns in membrane traffic: which vesicles do the tagmin tag? Biochimie 82, 409-420.
22. Martiny-Baron. G., Kazanietz, M. G., Mischak, H., Blumberg, P. M., Kochs, G., Hug, H., Marme, D. and Schachtele, C. (1993). Selective inhibition of protein kinase C isozymes by the indolocarbazole Go 6976. J. Biol. Chem. 268, 9194-9197.
23. Matlin, K. S. and Simons, K. (1983). Reduced temperature prevents transfer of a membrane glycoprotein to the cell surface but does not prevent terminal glycosylation. Cell 34, 233-243.
24. Peng, Z., Grimberg, E. and Sagi-Eisenberg, R. (2002). Suppression of Synaptotagmin II restrains phorbol ester-induced down-regulation of protein kinase Cα by diverting the kinase from a degradative pathway to the recycling endocytic compartment. J. Cell Sci. 115, 3083-3092.
25. Sudhof, T. C. (2002). Synaptotagmins: why so many? J. Biol. Chem. 277, 7629-7632.
26. Sudhof, T. C. and Rizo, J. (1996). Synaptotagmins: C2-domain proteins that regulate membrane traffic. Neuron 17, 379-388.
27. Sugita, S., Han, W., Butz, S., Liu, X., Fernandez-Chacon, R., Lao, Y. and Sudhof, T. C. (2001). Synaptotagmin VII as a plasma membrane Ca(2+) sensor in exocytosis. Neuron 30, 459-473.
28. 2+ affinities. EMBO J. 21, 270-280.
29. 2+-dependent exocytosis: dynamic action in a flash. Neuron 38, 521-524.
30. Von Poser, C., Zhang, J. Z., Mineo, C., Ding, W., Ying, Y., Sudhof, T. C. and Anderson, R. G. (2000). Synaptotagmin regulation of coated pit assembly. J. Biol. Chem. 275, 30916-30924.
31. Way, K. J., Chou, E. and King, G. L. (2000). Identification of PKC-isoform-specific biological actions using pharmacological approaches. Trends. Pharmacol. Sci. 21, 181-187.
32. Zhang, J. Z., Davletov, B. A., Sudhof, T. C. and Anderson, R. G. (1994). Synaptotagmin I is a high affinity receptor for clathrin AP-2: implications for membrane recycling. Cell 78, 751-760.