Rab8 is involved in zymogen granule formation in pancreatic acinar AR42J cells

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Volumn 9, Issue 6, 2008, Pages 964-979

  Faust, Floriane ^a   Gomez Lazaro, Maria ^b   Borta, Heike ^a   Agricola, Brigitte ^a   Schrader, Michael ^a,b  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b UNIVERSITY OF AVEIRO   (Portugal)

Author keywords

Organelle biogenesis; Pancreas; Rab GTPase; Zymogen granule

Indexed keywords

ENZYME PRECURSOR; GUANOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; MESSENGER RNA; RAB PROTEIN; RAB8 PROTEIN; SMALL INTERFERING RNA; ZYMOGEN GRANULE;

ACINAR CELL; ANIMAL CELL; APICAL MEMBRANE; ARTICLE; BIOGENESIS; CELL ISOLATION; CELL VACUOLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME RELEASE; EUKARYOTIC CELL; GENE EXPRESSION REGULATION; GENE SILENCING; GOLGI COMPLEX; INTRACELLULAR TRANSPORT; MEMBRANE FUSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RAT; RNA INTERFERENCE;

ANIMALS; CELL LINE; ELECTROPORATION; GOLGI APPARATUS; MICROSCOPY, FLUORESCENCE; PANCREAS, EXOCRINE; RAB GTP-BINDING PROTEINS; RATS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SECRETORY VESICLES; TRANSFECTION;

EID: 43149088924     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2008.00739.x     Document Type: Article

References (64)

1. Leblond FA, Viau G, Laine J, Lebel D. Reconstitution in vitro of the pH-dependent aggregation of pancreatic zymogens en route to the secretory granule: Implication of GP-2. Biochem J 1993;291:289-296.
2. Freedman SD, Scheele GA. Regulated secretory proteins in the exocrine pancreas aggregate under conditions that mimic the trans-Golgi network. Biochem Biophys Res Commun 1993;197:992-999.
3. Colomer V, Kicska GA, Rindler MJ. Secretory granule content proteins and the luminal domains of granule membrane proteins aggregate in vitro at mildly acidic pH. J Biol Chem 1996;271:48-55.
4. Dartsch H, Kleene R, Kern HF. In vitro condensation-sorting of enzyme proteins isolated from rat pancreatic acinar cells. Eur J Cell Biol 1998;75:211-222.
5. Arvan P, Castle D. Sorting and storage during secretory granule biogenesis: Looking backward and looking forward. Biochem J 1998;332: 593-610.
6. Tooze SA, Martens GJM, Huttner WB. Secretory granule biogenesis: Rafting to the SNARE. Trends Cell Biol 2001;11:116-122.
7. Borgonovo B, Ouwendijk J, Solimena M. Biogenesis of secretory granules. Curr Opin Cell Biol 2006;18:365-370.
8. Wasle B, Edwardson JM. The regulation of exocytosis in the pancreatic acinar cell. Cell Signal 2002;14:191-197.
9. Williams JA. Regulation of pancreatic acinar cell function. Curr Opin Gastroenterol 2006;22:498-504.
10. Beaudoin AR, Grondin G. Secretory pathways in animal cells: With emphasis on pancreatic acinar cells. J Electron Microsc Tech 1991;17:51-69.
11. Rambourg A, Clermont Y, Hermo L. Formation of secretion granules in the Golgi apparatus of pancreatic acinar cells of the rat. Am J Anat 1988;183:187-199.
12. Schrader M. Membrane targeting in secretion. Subcell Biochem 2004;37:391-421.
13. Wagner AC, Williams JA. Pancreatic zymogen granule membrane proteins: molecular details begin to emerge. Digestion 1994;55:191-199.
14. Schmidt K, Dartsch H, Linder D, Kern H, Kleene R. A submembranous matrix of proteoglycans on zymogen granule membranes is involved in granule formation in rat pancreatic acinar cells. J Cell Sci 2000;113:2233-2242.
15. Schmidt K, Schrader M, Kern HF, Kleene R. Regulated apical secretion of zymogens in rat pancreas: Involvement of the GPI-anchored glycoprotein GP-2, the lectin ZG16p and cholesterol-glycosphingolipid enriched microdomains. J Biol Chem 2001;276:14315-14323.
16. Kalus I, Hodel A, Koch A, Kleene R, Michael Edwardson J, Schrader M. Interaction of syncollin with GP-2, the major membrane protein of pancreatic zymogen granules, and association with lipid microdomains. Biochem J 2002;362:433-442.
17. Chen X, Walker AK, Strahler JR, Simon ES, Tomanicek-Volk SL, Nelson BB, Hurley MC, Ernst SA, Williams JA, Andrews PC. Organellar proteomics: analysis of pancreatic zymogen granule membranes. Mol Cell Proteomics 2006;5:306-312.
18. Berkane AA, Nguyen HT, Tranchida F, Waheed AA, Deyris V, Tchiakpe L, Fasano C, Nicoletti C, Desseaux V, Ajandouz el H, Comeau D, Comeau L, Hiol A. Proteomic of lipid rafts in the exocrine pancreas from diet-induced obese rats. Biochem Biophys Res Commun 2007;355:813-819.
19. Rindler MJ, Xu CF, Gumper I, Smith NN, Neubert TA. Proteomic analysis of pancreatic zymogen granules: Identification of new granule proteins. J Proteome Res 2007;6:2978-2992.
20. Goke B. Williams J.A. Wishart M.J. De Lisle R.C. Low molecular mass GTP-binding proteins in subcellular fractions of the pancreas: Regulated phosphoryl G proteins. Am J Physiol 1992;262:C493-C500.
21. Williams JA. Intracellular signaling mechanisms activated by cholecystokinin-regulating synthesis and secretion of digestive enzymes in pancreatic acinar cells. Annu Rev Physiol 2001; 63: 77-97.
22. Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001;2:107-117.
23. Stenmark H, Olkkonen VM. The Rab GTPase family. Genome Biol 2001;2: REVIEWS3007.
24. Grosshans BL, Ortiz D, Novick P. Rabs and their effectors: Achieving specificity in membrane traffic. Proc Natl Acad Sci U S A 2006;103:11821-11827.
25. Hammer JA III, Wu XS. Rabs grab motors: Defining the connections between Rab GTPases and motor proteins. Curr Opin Cell Biol 2002;14:69-75.
26. Seabra MC, Coudrier E. Rab GTPases and myosin motors in organelle motility. Traffic 2004;5:393-399.
27. Jordens I, Marsman M, Kuijl C, Neefjes J. Rab proteins, connecting transport and vesicle fusion. Traffic 2005;6:1070-1077.
28. Riedel D, Antonin W, Fernandez-Chacon R, Alvarez de Toledo G, Jo T, Geppert M, Valentijn JA, Valentijn K, Jamieson JD, Sudhof TC, Jahn R. Rab3D is not required for exocrine exocytosis but for maintenance of normally sized secretory granules. Mol Cell Biol 2002;22:6487-6497.
29. Cronshagen U, Voland P, Kern HF. cDNA cloning and characterization of a novel 16 kDa protein located in zymogen granules of rat pancreas and goblet cells of the gut. Eur J Cell Biol 1994;65:366-377.
30. Rais I, Karas M, Schagger H. Two-dimensional electrophoresis for the isolation of integral membrane proteins and mass spectrometric identification. Proteomics 2004;4:2567-2571.
31. Logsdon CD, Moessner J, Williams JA, Goldfine ID. Glucocorticoids increase amylase mRNA levels, secretory organelles, and secretion in pancreatic acinar AR42J cells. J Cell Biol 1985;100:1200-1208.
32. Piiper A, Leser J, Lutz MP, Beil M, Zeuzem S. Subcellular distribution and function of Rab3A-D in pancreatic acinar AR42J cells. Biochem Biophys Res Commun 2001;287:746-751.
33. Koch A, Schneider G, Luers GH, Schrader M. Peroxisome elongation and constriction but not fission can occur independently of dynamin-like protein 1. J Cell Sci 2004;117:3995-4006.
34. Boll A, Schrader M. Elongation of peroxisomes as an indicator for efficient dynamin-like protein 1 knock down in mammalian cells. J Histochem Cytochem 2005; 53: 1037-1040.
35. Koch A, Thiemann M, Grabenbauer M, Yoon Y, McNiven MA, Schrader M. Dynamin-like protein 1 is involved in peroxisomal fission. J Biol Chem 2003;278:8597-8605.
36. Schrader M. Shared components of mitochondrial and peroxisomal division. Biochim Biophys Acta 2006;1763:531-541.
37. Dahan S, Anderson KL, Weller S, Krueger E, McNiven MA. Agonist-induced vesiculation of the Golgi apparatus in pancreatic acinar cells. Gastroenterology 2005;129:2032-2046.
38. Chabrillat ML, Wilhelm C, Wasmeier C, Sviderskaya EV, Louvard D, Coudrier E. Rab8 regulates the actin-based movement of melanosomes. Mol Biol Cell 2005;16:1640-1650.
39. Chakraborty AK, Funasaka Y, Araki K, Horikawa T, Ichihashi M. Evidence that the small GTPase Rab8 is involved in melanosome traffic and dendrite extension in B16 melanoma cells. Cell Tissue Res 2003;314:381-388.
40. Ihrke G, Martin GV, Shanks MR, Schrader M, Schroer TA, Hubbard AL. Apical plasma membrane proteins and endolyn-78 travel through a subapical compartment in polarized WIF-B hepatocytes. J Cell Biol 1998;141:115-133.
41. Ihrke G, Gray SR, Luzio JP. Endolyn is a mucin-like type I membrane protein targeted to lysosomes by its cytoplasmic tail. Biochem J 2000;345:287-296.
42. Ohnishi H, Ernst SA, Wys N, McNiven M, Williams JA. Rab3D localizes to zymogen granules in rat pancreatic acini and other exocrine glands. Am J Physiol 1996;271:G531-G538.
43. Valentijn JA, Sengupta D, Gumkowski FD, Tang LH, Konieczko EM, Jamieson JD. Rab3D localizes to secretory granules in rat pancreatic acinar cells. Eur J Cell Biol 1996;70:33-41.
44. Ohnishi H, Mine T, Shibata H, Ueda N, Tsuchida T, Fujita T. Involvement of Rab4 in regulated exocytosis of rat pancreatic acini. Gastroenterology 1999;116:943-952.
45. Wagner AC, Strowski MZ, Williams JA. Identification of Rab 5 but not Rab 3A in rat pancreatic zymogen granule membranes. Biochem Biophys Res Commun 1994;200:542-548.
46. Chen X, Li C, Izumi T, Ernst SA, Andrews PC, Williams JA. Rab27b localizes to zymogen granules and regulates pancreatic acinar exocytosis. Biochem Biophys Res Commun 2004;323:1157-1162.
47. Chen X, Edwards JA, Logsdon CD, Ernst SA, Williams JA. Dominant negative Rab3D inhibits amylase release from mouse pancreatic acini. J Biol Chem 2002;277:18002-18009.
48. Huber LA, Pimplikar S, Parton RG, Virta H, Zerial M, Simons K. Rab8, a small GTPase involved in vesicular traffic between the TGN and the basolateral plasma membrane. J Cell Biol 1993;123:35-45.
49. Huber LA, de Hoop MJ, Dupree P, Zerial M, Simons K, Dotti C. Protein transport to the dendritic plasma membrane of cultured neurons is regulated by rab8p. J Cell Biol 1993;123:47-55.
50. Huber LA, Dupree P, Dotti CG. A deficiency of the small GTPase rab8 inhibits membrane traffic in developing neurons. Mol Cell Biol 1995;15:918-924.
51. Ang AL, Folsch H, Koivisto UM, Pypaert M, Mellman I. The Rab8 GTPase selectively regulates AP-1B-dependent basolateral transport in polarized Madin-Darby canine kidney cells. J Cell Biol 2003;163:339-350.
52. Nachury MV, Loktev AV, Zhang Q, Westlake CJ, Peranen J, Merdes A, Slusarski DC, Scheller RH, Bazan JF, Sheffield VC, Jackson PK. A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 2007;129:1201-1213.
53. Kamikura DM, Cooper JA. Clathrin interaction and subcellular localization of Ce-DAB-1, an adaptor for protein secretion in Caenorhabditis elegans. Traffic 2006;7:324-336.
54. Sahlender DA, Roberts RC, Arden SD, Spudich G, Taylor MJ, Luzio JP, Kendrick-Jones J, Buss F. Optineurin links myosin VI to the Golgi complex and is involved in Golgi organization and exocytosis. J Cell Biol 2005;169:285-295.
55. Peranen J, Auvinen P, Virta H, Wepf R, Simons K. Rab8 promotes polarized membrane transport through reorganization of actin and microtubules in fibroblasts. J Cell Biol 1996;135:153-167.
56. Hattula K, Furuhjelm J, Tikkanen J, Tanhuanpaa K, Laakkonen P, Peranen J. Characterization of the Rab8-specific membrane traffic route linked to protrusion formation. J Cell Sci 2006;119:4866-4877.
57. Klumperman J, Kuliawat R, Griffith JM, Geuze HJ, Arvan P. Mannose 6-phosphate receptors are sorted from immature secretory granules via adaptor protein AP-1, clathrin, and syntaxin 6-positive vesicles. J Cell Biol 1998;141:359-371.
58. Gondre-Lewis MC, Petrache HI, Wassif CA, Harries D, Parsegian A, Porter FD, Loh YP. Abnormal sterols in cholesterol-deficiency diseases cause secretory granule malformation and decreased membrane curvature. J Cell Sci 2006;119:1876-1885.
59. Sato T, Mushiake S, Kato Y, Sato K, Sato M, Takeda N, Ozono K, Miki K, Kubo Y, Tsuji A, Harada R, Harada A. The Rab8 GTPase regulates apical protein localization in intestinal cells. Nature 2007;448:366-369.
60. Keller P, Toomre D, Diaz E, White J, Simons K. Multicolour imaging of post-Golgi sorting and trafficking in live cells. Nat Cell Biol 2001;3:140-149.
61. Kleinman HK, McGoodwin EB, Rennard SI, Martin GR. Preparation of collagen substrates for cell attachment: Effect of collagen concentration and phosphate buffer. Anal Biochem 1979;94:308-312.
62. Swarovsky B, Steinhilber W, Scheele GA, Kern HF. Coupled induction of exocrine proteins and intracellular compartments involved in the secretory pathway in AR4-2J cells by glucocorticoids. Eur J Cell Biol 1988;47:101-111.
63. Schrader M, Reuber BE, Morrell JC, Jimenez-Sanchez G, Obie C, Stroh TA, Valle D, Schroer TA, Gould SJ. Expression of PEX11beta mediates peroxisome proliferation in the absence of extracellular stimuli. J Biol Chem 1998;273:29607-29614.
64. Gorr SU, Moore YR. Sorting of a constitutive secretory protein to the regulated secretory pathway of exocrine cells. Biochem Biophys Res Commun 1999;257:545-548.