Expression, localization and functional role of small GTPases of the Rab3 family in insulin-secreting cells

Journal of Cell Science

Volumn 109, Issue 9, 1996, Pages 2265-2273

  Regazzi, Romano ^a   Ravazzola, Mariella ^a   Iezzi, Mariella ^a   Lang, Jochen ^a   Zahraoui, Ahmed ^b   Andereggen, Elisabeth ^a   Morel, Philippe ^a   Takai, Yoshimi ^c   Wollheim, Claes B ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b INSTITUT CURIE   (France)

^c OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

Author keywords

Exocytosis; Islets of Langerhans; Pancreas

Indexed keywords

BOMBESIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE; INSULIN;

ANIMAL CELL; ARTICLE; ENZYME LOCALIZATION; FLUORESCENCE ACTIVATED CELL SORTER; HUMAN; HUMAN CELL; IMMUNOELECTRON MICROSCOPY; INSULIN RELEASE; NONHUMAN; NORTHERN BLOTTING; PANCREAS ISLET CELL; PRIORITY JOURNAL; RAT; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; CELL LINE; CRICETINAE; GENE EXPRESSION; GTP-BINDING PROTEINS; GUANOSINE TRIPHOSPHATE; HUMANS; HYDROLYSIS; IMMUNOHISTOCHEMISTRY; INSULIN; ISLETS OF LANGERHANS; MOLECULAR WEIGHT; MUTATION; RAB3 GTP-BINDING PROTEINS; RATS; RNA, MESSENGER; SPECIES SPECIFICITY; SUBCELLULAR FRACTIONS; TRANSFECTION;

ANIMALIA; CRICETINAE; STAPHYLOCOCCUS PHAGE 3A;

EID: 0029812387     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (63)

1. Asfari, M., Janjic, D., Meda, P., Li, G., Halban, P. A. and Wollheim, C. B. (1992). Establishment of 2-mercaptoethanol-dependent differentiated insulin-secreting cell lines. Endocrinology 130, 167-178.
2. Baldini, G., Hohl, T., Lin, H. Y. and Lodish, H. F. (1992). Cloning of a Rab3 isotype predominantly expressed in adipocytes. Proc. Nat. Acad. Sci. USA 89, 5049-5052.
3. Baldini, G., Scherer, P. E. and Lodish, H. F. (1995). Nonneuronal expression of Rab3A: Induction during adipogenesis and association with different intracellular membranes than Rab3D. Proc. Nat. Acad. Sci. USA 92, 4284-4288.
4. Bourne, H. R. (1988). Do GTPases direct membrane traffic in secretion? Cell 53, 669-671.
5. Bucci, C., Parton, R. G., Mather, I. H., Stunnenberg, H., Simons, K., Hoflack, B. and Zerial, M. (1992). The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70, 715-728.
6. Chomczynski, P. and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
7. Chung, S.-H., Takai, Y. and Holz, R. W. (1995). Evidence that the Rab3a-binding protein, Rabphilin3a, enhances regulated secretion. J. Biol. Chem. 270, 16714-16718.
8. Darchen, F., Zahraoui, A., Hammel, F., Monteils, M.-P., Tavitian, A. and Scherman, D. (1990). Association of the GTP-binding protein Rab3A with bovine adrenal chromaffin granules. Proc. Nat. Acad. Sci. USA 87, 5692-5696.
9. Darchen, F., Senyshyn, J., Brondyk, W. H., Taatjes, D. J., Holz, R. W., Henry, J. P., Denizot, J. P., Macara, I. G. (1995). The GTPase Rab3a is associated with large dense core vesicles in bovine chromaffin cells and rat PC12 cells. J. Cell Sci. 108, 1639-1649.
10. Elferink, L. A., Anzai, K. and Scheller, R. H. (1992). rab15, a novel low molecular weight GTP-binding protein specifically expressed in rat brain. J. Biol. Chem. 267, 5768-5775.
11. Ferro-Novick, S. and Jahn, R. (1994). Vesicle fusion from yeast to man. Nature 370, 191-193.
12. Fischer von Mollard, G., Mignery, G. A., Baumert, M., Perin, M. S., Hanson, T. J., Burger, P. M., Jahn, R. and Südhof, T. C. (1990) rab3 is a small GTP-binding protein exclusively localized to synaptic vesicles. Proc. Nat. Acad. Sci. USA 87, 1988-1992.
13. Fischer von Mollard, G., Südhof, T. C. and Jahn, R. (1991). A small GTP-binding protein dissociates from synaptic vesicles during exocytosis. Nature 349, 79-81.
14. Fischer von Mollard, G., Stahl, B., Li, C., Südhof, T. C. and Jahn, R. (1994a). Rab proteins in regulated exocytosis. Trends Biochem. Sci. 19, 164-168.
15. Fischer von Mollard, G., Stahl, B., Khokhlatchev, A., Südhof, T. C. and Jahn, R. (1994b). Rab3C is a synaptic vesicle protein that dissociates from synaptic vesicles after stimulation of exocytosis. J. Biol. Chem. 269, 10971-10974.
16. Geppert, M., Bolshakov, V. Y., Siegelbaum, S.A., Takei, K., De Camilli, P., Hammer, R. E. and Südhof, T. C. (1994). The role of Rab3A in neurotransmitter release. Nature 369, 493-497.
17. Gorvel, J.-P., Chavrier, P., Zerial, M. and Gruenberg, J. (1991). Rab5 controls early endosome fusion in vitro. Cell 64, 915-925.
18. Goud, B., Salminen, A., Walworth, N. C. and Novick, P. J. (1988). A GTP-binding protein required for secretion rapidly associates with secretory vesicles and the plasma membrane in yeast. Cell 53, 753-768.
19. 2+-dependent exocytosis from adrenal chromaffin cells. J. Biol. Chem. 269, 10229-10234.
20. Inagaki, N., Mizuta, M. and Seino, S. (1994). Cloning of a mouse rabphilin-3A expressed in hormone-secreting cells. J. Biochem. 116, 239-242.
21. Jena, B. P., Gumkowski, F. D., Konieczko, E. M., Fischer von Mollard, G., Jahn, R. and Jamieson, J. D. (1994). Redistribution of a Rab3-like GTP-binding protein from secretory granules to the Golgi complex in pancreatic acinar cells during regulated exocytosis. J. Cell Biol. 124, 43-53.
22. Johannes, L., Lledo, P.-M., Roa, M., Vincent, J.-D., Henry, J.-P. and Darchen, F. (1994). The GTPase Rab3a negatively controls calcium-dependent exocytosis in neuroendocrine cells. EMBO J. 13, 2029-2037.
23. Kikuchi, A., Yamashita, T., Kawata, M., Yamamoto, K., Ikeda, K., Tanimoto, T. and Takai, Y. (1988). Purification and characterization of a novel GTP-binding protein with molecular weight of 24,000 from bovine brain membranes. J. Biol. Chem. 263, 2897-2904.
24. Kowluru, A., Rabaglia, M. E., Muse, K. E. and Metz, S. A. (1994). Subcellular localization and kinetic characterization of guanine nucleotide binding proteins in normal rat and human pancreatic islets and transformed β cells. Biochim. Biophys. Acta 1222, 348-359.
25. α subunits. EMBO J. 14, 3635-3644.
26. Lankat-Buttgereit, B., Göke, R., Fehmann, H. C., Niess, C. and Göke B. (1992). Expression of the ras-related rab3a gene in insulinoma-derived cell lines. FEBS Lett. 312, 183-186.
27. Lankat-Buttgereit, B., Fehmann, H. C., Hering, B. J., Bretzel, R. G. and Göke, B. (1994). Expression of the ras-related rab3a gene in human insulinomas and normal human pancreatic islets. Pancreas 9, 434-438.
28. 2+/phospholipid-binding protein, depends on rab3A/3C. Neuron 13, 885-898.
29. Li, G., Regazzi, R., Balch, W. E. and Wollheim, C. B. (1993). Stimulation of insulin release from permeabilized HIT-T15 cells by a synthetic peptide corresponding to the effector domain of the small GTP-binding protein rab3. FEBS Lett. 327, 145-149.
30. Lian, J. P., Stone, S., Jiang, Y., Lyons, P. and Ferro-Novick, S. (1994). Ypt1p implicated in v-SNARE activation. Nature 372, 698-701.
31. 2+-dependent exocytosis in rat anterior pituitary cells. Nature 364, 540-544.
32. Martelli, A. M., Bareggi, R., Baldini, G., Scherer, P. E., Lodish, H. F. and Baldini, G. (1995). Diffuse vesicular distribution of Rab3D in the polarized neuroendocrine cell line AtT20. FEBS Lett. 368, 271-275.
33. Matteoli, M., Takei, K., Cameron, R., Hurlbut, P., Johnston, P. A., Südhof, T. C., Jahn, R. and De Camilli, P. (1991). Association of Rab3A with synaptic vesicles at late stages of the secretory pathway. J. Cell Biol. 115, 625-633.
34. Moya, K. L., Tavitian, B., Zahraoui, A. and Tavitian, A. (1992). Localization of the ras-like rab3A protein in the adult rat brain. Brain. Res. 590, 118-127.
35. Oberhauser, A. F., Monck, J. R., Balch, W. E. and Fernandez, J. M. (1992). Exocytotic fusion is activated by Rab3a peptides. Nature 360, 270-273.
36. Olszewski, S., Deeney, J. T., Schuppin, G. T., Williams, K. P., Corkey, B. E. and Rhodes, C. J. (1994). Rab3A effector domain peptides induce insulin exocytosis via a specific interaction with a cytosolic protein doublet. J. Biol. Chem. 269, 27987-27991.
37. Orci, L., Like, A. A., Amherdt, M., Blodel, B., Kanazawa, V., Marliss, E. B., Lambert, A. E., Wollheim, C. B. and Renold, A. E. (1973). Monolayer culture of neonatal rat pancreas: ultrastructural and biochemical study of functioning endocrine cells. J. Ultrastruct. Res. 43, 270-297.
38. Padfield, P. J., Balch, W. E. and Jamieson, J. D. (1992). A synthetic peptide of the rab3a effector domain stimulates amylase release from permeabilized pancreatic acini. Proc. Nat. Acad. Sci. USA 89, 1656-1660.
39. Pfeffer, S. R., Dirac-Svejstrup, A. B. and Soldati, T. (1995). Rab GDP dissociation inhibitor: putting Rab GTPases in the right place. J. Biol. Chem. 270, 17057-17059.
40. 2+ and secretion. EMBO J. 9, 53-60.
41. Reetz, A., Solimena, M., Matteoli, M., Folli, F., Takei, K. and De Camilli, P. (1991). GABA and pancreatic β-cells: colocalization of glutamic acid decarboxylase (GAD) and GABA with synaptic-like microvesicles suggests their role in GABA storage and secretion. EMBO J. 10, 1275-1284.
42. Regazzi, R., Li, G., Deshusses, J. and Wollheim, C. B. (1990). Stimulus-response coupling in insulin-secreting HIT cells. J. Biol. Chem. 265, 15003-15009.
43. Regazzi, R., Ullrich, S., Kahn, R. A. and Wollheim, C. B. (1991). Redistribution of ADP-ribosylation factor during stimulation of permeabilized cells with GTP analogues. Biochem. J. 275, 639-644.
44. Regazzi, R., Kikuchi, A., Takai, Y. and Wollheim, C. B. (1992a). The small GTP-binding proteins in the cytosol of insulin-secreting cells are complexed to GDP dissociation inhibitor proteins. J. Biol. Chem. 267, 17512-17519.
45. Regazzi, R., Vallar, L., Ullrich, S., Ravazzola, M., Kikuchi, A., Takai, Y. and Wollheim, C. B. (1992b). Characterization of small-molecular-mass guanine-nucleotide-binding regulatory proteins in insulin-secreting cells and PC12 cells. Eur. J. Biochem. 208, 729-737.
46. Regazzi, R., Sasaki, T., Takahashi, K., Jonas, J. C., Volker, C., Stock, J. B., Takai, Y. and Wollheim, C. B. (1995a). Prenylcysteine analogs mimicking the C-terminus of GTP-binding proteins stimulate exocytosis from permeabilized HIT-T15 cells. Biochim. Biophys. Acta 1268, 268-278.
47. 2+- but not for GTPγS-induced insulin secretion. EMBO J. 14, 2723-2730.
48. Ricordi, C., Lacy, P. E., Finke, E. H., Olack, B. J. and Sharp, D. W. (1988). Automated method for isolation of human pancreatic islets. Diabetes 37, 413-420.
49. Rorsman, P., Berggren, P.-O., Bokvist, K., Ericson, H., Möhler, H., Oestenson, C.-G. and Smith, P. A. (1989). Glucose-inhibition of glucagon secretion involves activation of GABAA-receptor chloride channels. Nature 341, 233-236.
50. Roth, J., Bendayan, M. and Orci, L. (1978). Ultrastructural localization of intracellular antigens by the use of Protein A-gold complex. J. Histochem. Cytochem. 26, 1074-1078.
51. Rouiller, D. G., Cirulli, V. and Halban, P. A. (1990). Differences in aggregation properties and levels of the neural cell adhesion molecule (NCAM) between islet cell types. Exp. Cell Res. 191, 305-312.
52. Senyshyn, J., Balch, W. E. and Holz, R. W. (1992). Synthetic peptides of the effector-binding domain of rab enhance secretion from digitonin-permeabilized chromaffin cells. FEBS Lett. 309, 41-46.
53. Shirataki, H., Kaibuchi, K., Yamaguchi, T., Wada, K., Horiuchi, H. and Takai, Y. (1992). A possible target protein for smg-25A/rab3A small GTP-binding protein. J. Biol. Chem. 267, 10946-10949.
54. Shirataki, H., Kaibuchi, K., Sakoda, T., Kishida, S., Yamaguchi, T., Wada, K., Miyazaki, M. and Takai, Y. (1993). Rabphilin-3A, a putative target protein for smg p25/rab3A p25 small GTP-binding protein related to synaptotagmin. Mol Cell. Biol. 13, 2061-2068.
55. Sogaard, M., Tani, K., Ye, R. R., Geromanos, S., Tempst, P., Kirchhausen, T., Rothman, J. E. and Sollner, T. (1994) A Rab protein is required for the assembly of SNARE complexes in the docking of transport vesicles. Cell 78, 937-948.
56. Soldati, T., Shapiro, A. D., Dirac-Svejstrup, B. A. and Pfeffer, S. R. (1994). Membrane targeting of the small GTPase Rab9 is accompanied by nucleotide exchange. Nature 369, 76-78.
57. Sorenson, R. L., Garry, D. G. and Brelje, T. C. (1991). Structural and functional considerations of GABA in islets of Langerhans. Diabetes 40, 1365-1374.
58. Takai, Y., Kaibuchi, K., Kikuchi, A. and Kawata, M. (1992). Small GTP-binding proteins. Int. Rev. Cytol. 133, 187-230.
59. Thomas-Reetz, A., Hell, J. W., During, M. J., Walch-Solimena, C., Jahn, R. and De Carnilli, P. (1993). A γ-aminobutyric acid transporter driven by a proton pump is present in synaptic-like microvesicles of pancreatic β cells. Proc. Nat. Acad. Sci. USA 90, 5317-5321.
60. Tokuyasu, K. T. (1980). Immunochemistry on ultrathin frozen sections. Histochem. J. 12, 381-403.
61. Ullrich, O., Stenmark, H., Alexandrov, K., Huber, L. A., Kaibuchi, K., Sasaki, T., Takai, Y. and Zerial, M. (1993). Rab GDP dissociation inhibitor as a general regulator for the membrane association of rab proteins. J. Biol. Chem. 268, 18143-18150.
62. 2+-independent insulin secretion from permeabilized RINm5F cells. J. Biol. Chem. 262, 5049-5056.
63. 2+-binding domains. J. Biol. Chem. 268, 27164-27170.