Synaptotagmin III is a critical factor for the formation of the perinuclear endocytic recycling compartment and determination of secretory granules size

Journal of Cell Science

Volumn 116, Issue 1, 2003, Pages 145-154

  Grimberg, Elena ^a   Peng, Ze ^a,b   Hammel, Ilan ^a   Sagi Eisenberg, Ronit ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Endocytic recycling compartment; Endocytosis; RBL 2H3 mast cells; Synaptotagmin; Transferrin

Indexed keywords

BETA N ACETYLHEXOSAMINIDASE; CELL MARKER; COMPLEMENTARY DNA; HISTAMINE; RAB PROTEIN; SEROTONIN; SYNAPTOTAGMIN; TRANSFERRIN;

ANIMAL CELL; CELL GRANULE; CELL MATURATION; CELL ORGANELLE; CELL STRUCTURE; CELL VOLUME; CONTROLLED STUDY; ENDOSOME; GENETIC TRANSFECTION; INTRACELLULAR TRANSPORT; MAST CELL; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; REVIEW; TRANSPORT KINETICS;

ANIMALS; BIOLOGICAL MARKERS; CALCIUM-BINDING PROTEINS; CELL COMPARTMENTATION; CELL NUCLEUS; CELL SIZE; CYTOPLASM; ENDOCYTOSIS; MAST CELLS; MEMBRANE GLYCOPROTEINS; MICROSCOPY, ELECTRON; NERVE TISSUE PROTEINS; OLIGODEOXYRIBONUCLEOTIDES, ANTISENSE; PROTEIN BINDING; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RATS; RECEPTORS, CELL SURFACE; SECRETORY VESICLES; SYNAPTOTAGMINS; TRANSFERRIN; TRANSPORT VESICLES; TUMOR CELLS, CULTURED;

ANIMALIA;

EID: 0037237001     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00186     Document Type: Review

References (39)

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. Baram, D., Mekori, Y. A. and Sagi-Eisenberg, R. (2001). Synaptotagmin regulates mast cell functions. Immunol Rev. 179, 25-34.
4. Barbosa, M. D., Nguyen, Q. A., Tchernev, V. T., Ashley, J. A., Detter, J. C., Blaydes, S. M., Brandt, S. J., Chotai, D., Hodgman, C., Solari, R. C. et al. (1996). Identification of the homologous beige and Chediak-Higashi syndrome genes. Nature 382, 262-265.
5. Bonifacino, J. S., Yuan, L. and Sandoval, I. V. (1989). Internalization and recycling to serotonin-containing granules of the 80K integral membrane protein exposed on the surface of secreting rat basophilic leukaemia cells. J. Cell Sci. 92, 701-712.
6. Butz, S., Fernandez, C. R., Schmitz, F., Jahn, R. and Sudhof, T. C. (1999). The subcellular localizations of atypical synaptotagmins III and VI. Synaptotagmin III is enriched in synapses and synaptic plasma membranes but not in synaptic vesicles. J. Biol. Chem. 274, 18290-18296.
7. Ceresa, B. P., Lotscher, M. and Schmid, S. L. (2001). Receptor and membrane recycling can occur with unaltered efficiency despite dramatic Rab5(q791)-induced changes in endosome geometry. J. Biol. Chem. 276, 9649-9654.
8. 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.
9. Galli, S. J., Gordon, J. R. and Wershil, B. K. (1991). Cytokine production by mast cells and basophils. Curr. Opin. Immunol. 3, 865-872.
10. 2+-induced insulin secretion in pancreatic islet beta cells. J. Biol. Chem. 275, 36079-36085.
11. Geppert, M., Archer, B. D. and Sudhof, T. C. (1991). Synaptotagmin II. A novel differentially distributed form of synaptotagmin. J. Biol. Chem. 266, 13548-13552.
12. 2+ sensor for transmitter release at a central synapse. Cell 79, 717-727.
13. Graham, R. C. and Karnovsky, M. J. (1965). The histochemical demonstration of monoamine oxidase activity by coupled peroxidatic oxidation. J. Histochem. Cytochem. 13, 604-605.
14. Grant, B., Zhang, Y., Paupard, M. C., Lin, S. X., Hall, D. H. and Hirsh, D. (2001). Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling. Nat. Cell Biol. 3, 573-579.
15. Gut, A., Kiraly, C. E., Fukuda, M., Mikoshiba, K., Wollheim, C. B. and Lang, J. (2001). Expression and localisation of synaptotagmin isoforms in endocrine beta-cells: their function in insulin exocytosis. J. Cell Sci. 114, 1709-1716.
16. Hammel, I., Lagunoff, D., Bauza, M. and Chi, E. (1983). Periodic, multimodal distribution of granule volumes in mast cells. Cell Tissue Res. 228, 51-59.
17. Hammel, I., Shiloh, R. H. and Nir, I. (1988). Two populations of mast cells on fibroblast monolayers: correlation of quantitative microscopy and functional activity. J. Cell Sci. 91, 13-19.
18. Hammel, I., Lagunoff, D. and Krüger, P. G. (1989). Recovery of rat mast cells after secretion: a morphometric study. Exp. Cell Res. 184, 518-523.
19. Lin, S. X., Grant, B., Hirsh, D. and Maxfield, F. R. (2001). Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells. Nat. Cell Biol. 3, 562-572.
20. Littleton, J. T., Stern, M., Perin, M. and Bellen, H. J. (1994). Calcium dependence of neurotransmitter release and rate of spontaneous vesicle fusions are altered in Drosophila synaptotagmin mutants. Proc. Natl. Acad. Sci. USA 91, 10888-10892.
21. Mallard, F., Tang, B. L., Galli, T., Tenza, D., Saint-Pol, A., Yue, X., Antony, C., Hong, W., Goud, B. and Johannes, L. (2002). Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. J. Cell Biol. 156, 653-664.
22. McBride, H. M., Rybin, V., Murphy, C., Giner, A., Teasdale, R. and Zerial, M. (1999). Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and syntaxin 13. Cell 98, 377-386.
23. McGraw, T. E., Dunn, K. W. and Maxfield, F. R. (1993). Isolation of a temperature-sensitive variant Chinese hamster ovary cell line with a morphologically altered endocytic recycling compartment. J. Cell. Physiol. 155, 579-594.
24. Mikoshiba, K., Fukuda, M., Moreira, J. E., Lewis, F. M., Sugimori, M., Niinobe, M. and Llinas, 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.
25. Mizuta, M., Kurose, T., Miki, T., Shoji, K.Y., Takahashi, M., Seino, S. and Matsukura, S. (1997). Localization and functional role of synaptotagmin III in insulin secretory vesicles in pancreatic beta-cells. Diabetes 46, 2002-2006.
26. Peng, Z., Grimberg, E. and Sagi-Eisenberg, R. (2002). Suppression of Synaptotagmin II restrains phorbol-ester-induced downregulation of protein kinase Cα by diverting the kinase from a degradative pathway to the recycling endocytic compartment. J. Cell Sci. 115, 3083-3092.
27. Prekeris, R., Klumperman, J., Chen, Y. A. and Scheller, R. H. (1998). Syntaxin 13 mediates cycling of plasma membrane proteins via tubulovesicular recycling endosomes. J. Cell Biol. 143, 957-971.
28. Ren, M., Xu, G., Zeng, J., de Lemos-Chiarandini, C., Adesnik, M. and Sabatini, D. D. (1998). Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc. Natl. Acad. Sci. USA 95, 6187-6192.
29. Shelf, D. R., Daro, E. A., Hull, M. and Mellman, I. (1999). The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions. J. Cell Biol. 145, 123-139.
30. Shelf, D., Pelletier, L., O'Connell, C. B., Warren, G. and Mellman, I. (2002). Transferrin receptor recycling in the absence of perinuclear recycling endosomes. J. Cell Biol. 156, 797-804.
31. Shore, P. A., Burkhalter, A. and Cohn, V. H. (1959). A method for the fluorimetric assay of histamine in tissues. J. Pharmacol. Exp. Ther. 127, 182-185.
32. Sokal, R. R. and Rohlf, F. J. (1995). In Biometry: The Principles and Practice of Statistics in Biological Research. 3rd edn., pp. 571-575. W. H. Freeman Company.
33. Sonnichsen, B., de Renzis, S., Nielsen, E., Rietdorf, J. and Zerial, M. (2000). Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J. Cell Biol. 149, 901-914.
34. Stevens, R. L. and Austen, K. F. (1989). Recent advance in the cellular and molecular biology of mast cells. Immunol. Today 10, 381-385.
35. Tchernev, V. T., Mansfield, T. A., Giot, L., Kumar, A. M., Nandabalan, K., Li, Y., Mishra, V. S., Detter, J. C., Rothberg, J. M., Wallace, M. R., Southwick, F. S. and Kingsmore, S. F. (2002). The Chediak-Higashi protein interacts with SNARE complex and signal transduction proteins. Mol. Med. 8, 56-64.
36. Tooze, S. A., Martens, G. J. and Huttner, W. B. (2001). Secretory granule biogenesis: rafting to the SNARE. Trends Cell Biol. 11, 116-122.
37. Trischler, M., Stoorvogel, W. and Ullrich, O. (1999). Biochemical analysis of distinct Rab5- and Rab11-positive endosomes along the transferrin pathway. J. Cell Sci. 112, 4773-4783.
38. Wilcke, M., Johannes, L., Galli, T., Mayau, V., Goud, B. and Salamero, J. (2000). Rab11 regulates the compartmentalization of early endosomes required for efficient transport from early endosomes to the trans-Golgi network. J. Cell Biol. 151, 1207-1520.
39. Xu, K., Williams, R. M., Holowka, D. and Baird, B. (1998). Stimulated release of fluorescently labeled IgE fragments that efficiently accumulate in secretory granules after endocytosis in RBL-2H3 mast cells. J. Cell Sci. 111, 2385-2396.