Carboxyl methylation of rab3D is developmentally regulated in the rat pancreas: Correlation with exocrine function

European Journal of Cell Biology

Volumn 76, Issue 3, 1998, Pages 204-211

  Valentijn, Jack A ^a   Jamieson, James D ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Carboxyl methylation; Development; Exocrine pancreas; rab3D; Regulated secretion

Indexed keywords

DEXAMETHASONE; RAB PROTEIN;

ACINAR CELL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL SECRETION; EMBRYO; EMBRYO DEVELOPMENT; MALE; NONHUMAN; PANCREAS; PANCREAS TUMOR; PAROTID GLAND; PRIORITY JOURNAL; PROTEIN METHYLATION; RAT;

ANIMALIA;

EID: 0031928546     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0171-9335(98)80035-6     Document Type: Article

References (55)

1. Amsterdam, A., I. Ohad, M. Schramm: Dynamic changes in the ultrastructure of the acinar cell of the rat parotid gland during the secretory cycle. J. Cell Biol. 41, 753-773 (1969).
2. Araki, S., K. Kaibuchi, T. Sasaki, Y. Hata, Y. Takai: Role of the C-terminal region of smg p25A in its interaction with membranes and the GDP/GTP exchange protein. Mol. Cell. Biol. 11, 1438-1447 (1991).
3. Ayad, N., M. Hull, I. Mellman: Mitotic phosphorylation of rab4 prevents binding to a specific receptor on endosome membranes. EMBO J. 16, 4497-507 (1997).
4. Backlund Jr., P. S.: Carboxyl methylation of the low molecular weight GTP-binding protein G25K: regulation of carboxyl methylation by rhoGDI. Biochem. Biophys. Res. Commun. 196, 534-542 (1993).
5. Baldini, G., T. Hohl, H. Y. Lin, H. F. Lodish: Cloning of a rab3 isotype predominantly expressed in adipocytes. Proc. Natl. Acad. Sci. USA 89, 5049-5052 (1992).
6. Baldini, G., P. E. Scherer, H. E. Lodish: Nonneuronal expression of Rab3A: Induction during adipogenesis and association with different intracellular membranes than Rab3D. Proc. Natl. Acad. Sci. USA 92, 4284-4288 (1995).
7. Casey, P. J.: Lipid modifications of G proteins. Curr. Biol. 6, 219-225 (1994).
8. Chang, A., J. D. Jamieson: Stimulus-secretion coupling in the developing exocrine pancreas: secretory responsiveness to cholecystokinin. J. Cell Biol. 103, 2353-2365 (1986).
9. Cope, G. H.: Exocrine glands and protein secretion: a stereological viewpoint. J. Microsc. 131, 187-202 (1983).
10. Cremers, F. P., S. A. Armstrong, M. C. Seabra, M. S. Brown, J. L. Goldstein: REP-2, a rab escort protein encoded by the choroideremia-like gene. J. Biol. Chem. 269, 2111-2117 (1994).
11. De Lisle, R. C.: A plethora of GTPases, large and small. Digestion 54, 3-8 (1993).
12. Doyle, C. M., J. D. Jamieson: Development of secretagogue response in rat pancreatic acinar cells. Dev. Biol. 65, 11-27 (1978).
13. Dunten, R. L., S. J. Wait, P. S. Backlund, Jr.: Fractionation and characterization of protein C-terminal prenyl-cysteine methylesterase activities from rabbit brain. Biochem. Biophys. Res. Commun. 208, 174-182 (1995).
14. Farnsworth, C. C., M. Kawata, Y. Yoshida, Y. Takai, M. H. Gelb, J. A. Glomset: C terminus of the small GTP-binding protein smg p25A contains two geranylgeranylated cysteine residues and a methyl ester. Proc. Natl. Acad. Sci. USA 88, 6196-6200 (1991).
15. Farnsworth, C. C., M. C. Seabra, L. H. Ericsson, M. H. Gelb, J. A. Glomset: Rab geranylgeranyl transferase catalyzes the geranylgeranylation of adjacent cysteines in the small GTPases Rab1A, Rab3A, and Rab5A. Proc. Natl. Acad. Sci. USA 91, 11963-11967 (1994).
16. Glomset, J. A., C. C. Farnsworth: Role of protein modification reactions in programming interactions between Ras-related GTPases and cell membranes. Annu. Rev. Cell Biol. 10, 181-205 (1994).
17. Goke, B., J. A. Williams, M. J. Wishart, R. C. De Lisle: Low molecular mass GTP-binding proteins in subcellular fractions of the pancreas: regulated phosphoryl G proteins. Am. J. Physiol. 262, C493-C500 (1992).
18. Hrycyna, C. A., S. Clarke: Modification of eukaryotic signaling proteins by C-terminal methylation reactions. Pharmacol. Ther. 59, 281-300 (1993).
19. Hrycyna, C. A., S. K. Sapperstein, S. Clarke, S. Michaelis: The Saccharomyces cerevisiae STE14 gene encodes a methyltransferase that mediates C-terminal methylation of a-factor and RAS proteins. EMBO J. 10, 1699-1709 (1991).
20. Iwanij, V, B. E. Hull, J. D. Jamieson: Structural characterization of a rat acinar cell tumor. J. Cell Biol. 95, 727 733 (1982).
21. Iwanij, V., J. D. Jamieson: Biochemical analysis of secretory proteins synthesized by normal rat pancreas and by pancreatic acinar tumor cells. J. Cell Biol. 95, 734-741 (1982).
22. Johannes, L., P.-M. Lledo, M. Roa, J.-D. Vincent, J.-P. Henry, F. Darchen: The GTPase Rab3a negatively controls calcium-dependent exocytosis in neuroendocrine cells. EMBO J. 13, 2029-2037 (1994).
23. Karniguian, A., A. Zahraoui, A. Tavitian: Identification of small GTP-binding rab proteins in human platelets: Thrombin-induced phosphorylation of rab3B, rab6, and rab8 proteins. Proc. Natl. Acad. Sci. USA 90, 7647-7651 (1993).
24. Klengel, R., A. Piiper, S. Pittelkow, S. Zeuzem: Differential expression of Rab3 isoforms during differentiation of pancreatic acinar cell line AR42J. Biochem. Biophys. Res. Commun. 236, 719-722 (1997).
25. Larose, L., J. Morisset: Acinar cell responsiveness to urecholine in the rat pancreas during fetal and early postnatal growth. Gastroenterology 73, 530-533 (1977).
26. Li, G., A. Kowluru, S. A. Metz: Characterization of prenylcysteine methyltransferase in insulin-secreting cells. Biochem. J. 316, 345-351 (1996).
27. Lledo, P.-M., L.Johannes, P. Vernier, R. Zorec, F. Darchen, J. D. Vincent, J.-P. Henry, W. T. Mason: Rab3 proteins: Key players in the control of exocytosis. Trends Neurosci. 17, 426-432 (1994).
28. 2+-dependent exocytosis in rat anterior pituitary cells. Nature 364, 540-544 (1993).
29. Logsdon, C. D., J. Moessner, J. A. Williams, I. D. Goldfine: Glucocorticoids increase amylase mRNA levels secretory organelles and secretion in pancreatic acinar AR42J cells. J. Cell Biol. 100, 1200-1208 (1985).
30. Martelli, A. M., R. Bareggi, G. Baldini, P. E. Scherer, H. F. Lodish: Diffuse vesicular distribution of Rab3D in the polarized neuroendocrine cell line AtT-20. FEBS Lett. 368, 271-275 (1995).
31. Musha, T., M. Kawata, Y. Takai: The geranylgeranyl moiety but not the methyl moiety of the smg-25A/rab3A protein is essential for the interactions with membrane and its inhibitory GDP/GTP exchange protein. J. Biol. Chem. 267, 9821-9825 (1992).
32. Novick, P., M. Zerial: The diversity of rab proteins in vesicle transport. Curr. Opin. Cell Biol. 9, 496-504 (1997).
33. O'Farrell, P. H.: High resolution two dimensional electrophoresis of proteins. J. Biol Chem. 250, 4007-4021 (1975).
34. Oberhauser, A. F., V. Balan, C. L. Fernandez-Badilla, J. M. Fernandez: RT-PCR cloning of rab3 isoforms expressed in peritoneal mast cells. FEBS Lett. 339, 171-174 (1994).
35. Ohnishi, H., S. A. Ernst, N. Wys, M. McNiven, J. A. Williams: Rab3D localizes to zymogen granules in rat pancreatic acini and other exocrine glands. Am. J. Physiol. Gastrointest. Liver Physiol. 271, G531-G538 (1996).
36. Parish, C. A., R. R. Rando: Isoprenylation/methylation of proteins enhances membrane association by a hydrophobic mechanism. Biochemistry 35, 8473-8477 (1996).
37. Parsa, I., W. H. Marsh, P. J. Fitzgerald: Pancreas acinar cell differentiation. I. Morphologic and enzymatic comparisons of embryonic rat pancreas and pancreatic anlage grown in organ culture. Am. J. Pathol. 57, 457-487 (1969).
38. Pfeffer, S. R., A. B. Dirac-Svejstrup, T. Soldati: Rab GDP dissociation inhibitor: Putting Rab GTPases in the right place. J. Biol. Chem. 270, 17057-17059 (1995).
39. Pillinger, M. H., C. Volker, J. B. Stock, G. Weissman, M. R. Philips: Characterization of a plasma membrane-associated prenylcysteine-directed alpha carboxyl methyltransferase in human neutrophils. J. Biol. Chem. 269, 1486-1492 (1994).
40. Raffaniello, R. D., J. Y. Lin, F. S. Wang, J. P. Raufman: Expression of Rab3D in dispersed chief cells from guinea pig stomach. Biochim. Biophys. Acta Mol. Cell Res. 1311, 111-116 (1996).
41. Rando, R. R.: Chemical biology of protein isoprenylation/ methylation. Biochim. Biophys. Acta 1300, 5-16 (1996).
42. Roa, M., F. Paumet, J. Le Mao, B. David, U. Blank: Involvement of the ras-like GTPase rab3d in RBL-2H3 mast cell exocytosis following stimulation via high affinity IgE receptors (FcRI). J. Immunol. 159, 2815-2823 (1997).
43. Sachs, E., J. D. Jamieson: Perturbation of regulated secretion in the pancreatic acinar cell line, AR42J. Am. J. Physiol. 262, G257-G266 (1992).
44. Schnefel, S., P. Zimmermann, A. Pröfrock, R. Jahn, K. Aktories, S. Zeuzem, W. Haase, I. Schulz: High- and small-molecular-weight GTP-binding proteins in zymogen granule membranes of rat pancreatic acinar cells. Cell Physiol. Biochem. 2, 77-89 (1992).
45. Shahinian, S., J. R. Silvius: Doubly-lipid-modified protein sequence motifs exhibit long-lived anchorage to lipid bilayer membranes. Biochemistry 34, 3813-3822 (1995).
46. Smeland, T. E., M. C. Seabra, J. L. Goldstein, M. S. Brown: Geranylgeranylated Rab proteins terminating in Cys-Ala-Cys, but not Cys-Cys, are carboxyl-methylated by bovine brain membranes in vitro. Proc. Natl. Acad. Sci. USA 91, 10712-10716 (1994).
47. Springer, M. S., M. F. Goy, J. Adler: Protein methylation in behavioural control mechanisms and in signal transduction. Nature 280, 279-284 (1979).
48. Tang, L. H., F. D. Gumkowski, D. Sengupta, I. M. Modlin, J. D. Jamieson: Rab3D protein is a specific marker for zymogen granules in gastric chief cells of rats and rabbits. Gastroenterology 110, 809-820 (1996).
49. Valentijn, J. A., F. D. Gumkowski, J. D. Jamieson: The expression pattern of rab3D in the developing rat exocrine pancreas coincides with the acquisition of regulated exocytosis. Eur. J. Cell Biol. 71, 129-136 (1996).
50. Valentijn, J. A-., J. D. Jamieson: On the role of rab GTPases: what can be learned from the developing pancreas. Biochem. Biophys. Res. Commun. 243, 331-336 (1998).
51. Valentijn, J. A., D. Q. La Civita, F. D. Gumkowski, J. D. Jamieson: Rab4 associates with the actin cytoskeleton in developing rat pancreatic acinar cells. Eur. J. Cell Biol. 72, 1-8 (1997).
52. Valentijn, J. A., D. Sengupta, F. D. Gumkowski, L. H. Tang, E. M. Konieczko, J. D. Jamieson: Rab3D localizes to secretory granules in rat pancreatic acinar cells. Eur. J. Cell Biol. 70, 33-41 (1996).
53. Van der Sluijs, P., M. Hull, L. A. Huber, P. Mâle, B. Goud, I. Mellman: Reversible phosphorylation-dephosphorylation determines the localization of rab4 during the cell cycle. EMBO J. 11, 4379-4389 (1992).
54. Volker, C., J. B. Stock: Carboxyl methylation of ras-related proteins. Methods Enzymol. 255, 65-82 (1995).
55. Werlin, S. L., D. G. Colton, J. Harb, E. Reynolds, R. G. Hoffman, J. A. Williams: Ontogeny of secretory function and cholecystokinin binding capacity in immature rat pancreas. Life Sci. 40, 2237-2245 (1987).