Functional role of J domain of cysteine string protein in Ca 2+-dependent secretion from acinar cells

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 296, Issue 5, 2009, Pages

  Weng, Ning ^a   Baumler, Megan D ^a   Thomas, Diana D H ^a   Falkowski, Michelle A ^a   Swayne, Leigh Anne ^b   Braun, Janice E A ^b   Groblewski, Guy E ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Heat shock protein 70; Zymogen granules

Indexed keywords

AMYLASE; CALCIUM ION; CYSTEINE STRING PROTEIN; CYSTEINE STRING PROTEIN ALPHA; SYNAPTOBREVIN; UNCLASSIFIED DRUG; VESICLE ASSOCIATED MEMBRANE PROTEIN 8; ZYMOGEN GRANULE; CALCIUM; ENZYME; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); HEAT SHOCK COGNATE PROTEIN 70; HEAT SHOCK PROTEIN 40; HSPA8 PROTEIN, RAT; HYBRID PROTEIN; MEMBRANE PROTEIN; PEPTIDE FRAGMENT; SNARE PROTEIN; VAMP8 PROTEIN, RAT;

ACINAR CELL; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; AMYLASE RELEASE; ANIMAL CELL; ARTICLE; CONCENTRATION RESPONSE; ENZYME RELEASE; EXOCYTOSIS; MALE; NONHUMAN; PANCREAS SECRETION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; RAT; ANIMAL; CHEMISTRY; ENZYMOLOGY; GENETICS; IN VITRO STUDY; METABOLISM; MUTATION; PANCREAS; PROTEIN TERTIARY STRUCTURE; SECRETION; SECRETORY VESICLE; SPRAGUE DAWLEY RAT;

ANIMALS; CALCIUM; ENZYMES; EXOCYTOSIS; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); HSC70 HEAT-SHOCK PROTEINS; HSP40 HEAT-SHOCK PROTEINS; MALE; MEMBRANE PROTEINS; MUTATION; PANCREAS, EXOCRINE; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, TERTIARY; R-SNARE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT FUSION PROTEINS; SECRETORY PATHWAY; SECRETORY VESICLES; SNARE PROTEINS;

EID: 66149118210     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.90592.2008     Document Type: Article

References (53)

1. Bai L, Swayne LA, Braun JE. The CSPalpha/G protein complex in PC12 cells. Biochem Biophys Res Commun 352: 123-129, 2007.
2. Bhagat L, Singh VP, Hietaranta AJ, Agrawal S, Steer ML, Saluja AK. Heat shock protein 70 prevents secretagogue-induced cell injury in the pancreas by preventing intracellular trypsinogen activation. J Clin Invest 106: 81-89, 2000. (Pubitemid 30437243)
3. Blondeau F, Ritter B, Allaire PD, Wasiak S, Girard M, Hussain N, Angers A, Legendre-Guillemin V, Roy L, Boismenu D, Kearney RE, Bell AW, Bergeron JJ, McPherson PS. Tandem MS analysis of brain clathrin-coated vesicles reveals their critical involvement in synaptic vesicle recycling. Proc Natl Acad Sci USA 101: 3833-3838, 2004. (Pubitemid 38381064)
4. Boal F, Zhang H, Tessier C, Scotti P, Lang J. The variable C-terminus of cysteine string proteins modulates exocytosis and protein-protein interactions. Biochemistry 43: 16212-16223, 2004. (Pubitemid 40041034)
5. Braun JE, Scheller RH. Cysteine string protein, a DnaJ family member, is present on diverse secretory vesicles. Neuropharmacology 34: 1361-1369, 1995.
6. Braun JE, Wilbanks SM, Scheller RH. The cysteine string secretory vesicle protein activates Hsc70 ATPase. J Biol Chem 271: 25989-25993, 1996.
7. Brodsky JL, Chiosis G. Hsp70 molecular chaperones: emerging roles in human disease and identification of small molecule modulators. Curr Top Med Chem 6: 1215-1225, 2006. (Pubitemid 44110931)
8. Brown H, Larsson O, Branstrom R, Yang S, Leibiger B, Leibiger I, Fried G, Moede T, Deeney JT, Brown GR, Jacobsson G, Rhodes CJ, Braun JE, Scheller RH, Corkey BE, Berggren P, Meister B. Cysteine string protein (CSP) is an insulin secretory granule-associated protein regulating beta-cell exocytosis. EMBO J 17: 5048-5058, 1998. (Pubitemid 28408470)
9. Chamberlain LH, Burgoyne RD. Identification of a novel cysteine string protein variant and expression of cysteine string proteins in non-neuronal cells. J Biol Chem 271: 7320-7323, 1996.
10. Chamberlain LH, Burgoyne RD. Activation of the ATPase activity of heat-shock proteins Hsc70/Hsp70 by cysteine-string protein. Biochem J 322: 853-858, 1997.
11. Chamberlain LH, Burgoyne RD. Cysteine string protein functions directly in regulated exocytosis. Mol Biol Cell 9: 2259-2267, 1998.
12. Chamberlain LH, Graham ME, Kane S, Jackson JL, Maier VH, Burgoyne RD, Gould GW. The synaptic vesicle protein, cysteine-string protein, is associated with the plasma membrane in 3T3-L1 adipocytes and interacts with syntaxin 4. J Cell Sci 114: 445-455, 2001. (Pubitemid 32149585)
13. Chandra S, Gallardo G, Fernández-Chacón R, Schlüter OM, Südhof TC. Alpha-synuclein cooperates with CSPalpha in preventing neurodegeneration. Cell 123: 383-396, 2005. (Pubitemid 41546670)
14. Chen S, Zheng X, Schulze KL, Morris T, Bellen H, Stanley EF. Enhancement of presynaptic calcium current by cysteine string protein. J Physiol 538: 383-389, 2002. (Pubitemid 35175368)
15. Cosen-Binker LI, Binker MG, Wang CC, Hong W, Gaisano HY. VAMP8 is the v-SNARE that mediates basolateral exocytosis in a mouse model of alcoholic pancreatitis. J Clin Invest 118: 2535-2551, 2008.
16. Evans GJ, Morgan A. Phosphorylation-dependent interaction of the synaptic vesicle proteins cysteine string protein and synaptotagmin I. Biochem J 364: 343-347, 2002. (Pubitemid 34620793)
17. Evans GJ, Morgan A, Burgoyne RD. Tying everything together: the multiple roles of cysteine string protein (CSP) in regulated exocytosis. Traffic 4: 653-659, 2004. (Pubitemid 37168587)
18. Fernandez-Chacon R, Wolfel M, Nishimune H, Tabares L, Schmitz F, Castellano-Munoz M, Rosenmund C, Montesinos ML, Sanes JR, Schneggenburger R, Sudhof TC. The synaptic vesicle protein CSP alpha prevents presynaptic degeneration. Neuron 42: 237-251, 2004. (Pubitemid 38501647)
19. Futatsugi A, Takeshi Nakamura T, Yamada MK, Ebisui E, Nakamura K, Uchida K, Kitaguchi T, Takahashi-Iwanaga H, Noda T, Aruga J, Mikoshiba K. IP3 receptor types 2 and 3 mediate exocrine secretion underlying energy metabolism. Science 309: 2232-2234, 2007.
20. Gaisano HY, Ghai M, Malkus PN, Sheu L, Bouquillon A, Bennett MK, Trimble WS. Distinct cellular locations of the syntaxin family of proteins in rat pancreatic acinar cells. Mol Biol Cell 7: 2019-2027, 1996. (Pubitemid 26415007)
21. Graham ME, Burgoyne RD. Comparison of Cysteine String Protein (Csp) and mutant alpha-SNAP overexpression reveals a role for Csp in late steps of membrane fusion in dense-core granule exocytosis in adrenal chromaffin cells. J Neurosci 20: 1281-1289, 2000.
22. Groblewski GE, Wishart MJ, Yoshida M, Williams JA. Purification and identification of a 28-kDa calcium-regulated heat-stable protein. A novel secretagogue-regulated phosphoprotein in exocrine pancreas. J Biol Chem 271: 31502-31507, 1996. (Pubitemid 26408608)
23. Gundersen CB, Umbach JA. Suppression cloning of the cDNA for a candidate subunit of a presynaptic calcium channel. Neuron 9: 527-537, 1992.
24. Heuck AP, Tweten RK, Johnson AE. Beta-barrel pore-forming toxins: intriguing dimorphic proteins. Biochemistry 40: 9065-9073, 2001.
25. Hwang JH, Ryu JK, Yoon YB, Lee KH, Park YS, Kim JW, Kim N, Jeong JB, Seo JS, Kim YT. Spontaneous activation of pancreas trypsino- gen in heat shock protein 70.1 knock-out mice. Pancreas 31: 332-336, 2005. (Pubitemid 41566881)
26. Kohan SA, Pescatori M, Brecha NC, Mastrogiacomo A, Umbach JA, Gundersen CB. Cysteine string protein immunoreactivity in the nervous system and adrenal gland of rat. J Neurosci 15: 6230-6238, 1995.
27. Lerch MM, Gorelick FS. Early trypsinogen activation in acute pancreatitis. Med Clin North Am 84: 549-563, 2000.
28. Low SH, Li X, Miura M, Kudo N, Quiñones B, Weimbs T. Syntaxin 2 and endobrevin are required for the terminal step of cytokinesis in mammalian cells. Dev Cell 4: 753-759, 2003. (Pubitemid 36564904)
29. Magga JM, Jarvis SE, Arnot MI, Zamponi GW, Braun JE. Cysteine string protein regulates G-protein modulation of N-type calcium channels. Neuron 28: 195-204, 2000.
30. 2+ channels. Science 263: 981-982, 1994.
31. Miller LC, Swayne LA, Kay JG, Feng ZP, Jarvis SE, Zamponi GW, Braun JEA. Molecular determinants of cysteine string protein modulation of N-type calcium channels. J Cell Sci 116: 2967-2974, 2003.
32. Natochin M, Campbell TN, Barren B, Miller LC, Hameed S, Artemyev NO, Braun JE. Characterization of the G alpha(s) regulator cysteine string protein. J Biol Chem 280: 30236-30241, 2005. (Pubitemid 41216203)
33. Nemoto T, Kimura R, Ito K, Tachikawa A, Miyashita Y, Iino M, Kasai H. Sequential-replenishment mechanism of exocytosis in pancreatic acini. Nat Cell Biol 3: 253-258, 2001. (Pubitemid 32201320)
34. Nie Z, Ranjan R, Wenniger JJ, Hong SN, Bronk P, Zinsmaier KF. Overexpression of cysteine-string proteins in Drosophila reveals interactions with syntaxin. J Neurosci 19: 10270-10279, 1999. (Pubitemid 30228034)
35. Ohnishi H, Ernst SA, Yule DI, Baker CW, Williams JA. Heterotrimeric G-protein Gq/11 localized on pancreatic zymogen granule is involved in calcium-regulated amylase secretion. J Biol Chem 272: 16056-16061, 1997. (Pubitemid 27265591)
36. Rosales-Hernandez A, Beck KE, Zhao X, Braun AP, Braun JE. RDJ2 (DNAJA2) chaperones neural G protein signaling pathways. Cell Stress Chaperones 14: 71-82, 2008.
37. Schmitz F, Tabares L, Khimich D, Strenzke N, de La Villa-Pollo P, Castellano-Munoz M, Bulankina A, Moser T, Fernandez-Chacon R, Sudhof TC. CSPalpha-deficiency causes massive and rapid photoreceptor degeneration. Proc Natl Acad Sci USA 103: 2926-2931, 2006. (Pubitemid 43306650)
38. Smith GB, Umbach JA, Hirano A, Gundersen CB. Interaction between constitutively expressed heat shock protein, Hsc70, and cysteine string protein is important for cortical granule exocytosis in Xenopus oocytes. J Biol Chem 280: 32669-32675, 2005. (Pubitemid 41368311)
39. Stahl B, Tobaben S, Südhof TC. Two distinct domains in hsc70 are essential for the interaction with the synaptic vesicle cysteine string protein. Eur J Cell Biol 78: 375-381, 1999. (Pubitemid 29317373)
40. Swayne LA, Beck KE, Braun JE. The cysteine string protein multimeric complex. Biochem Biophys Res Commun 348: 83-91, 2006.
41. Thomas DD, Taft WB, Kaspar KM, Groblewski GE. CRHSP-28 regulates Ca(2+)-stimulated secretion in permeabilized acinar cells. J Biol Chem 276: 28866-28872, 2001.
42. Thomas DD, Weng N, Groblewski GE. Secretagogue-induced translocation of CRHSP-28 within an early apical endosomal compartment in acinar cells. Am J Physiol Gastrointest Liver Physiol 287: G253-G263, 2004. (Pubitemid 38802140)
43. Tobaben S, Thakur P, Fernández-Chacón R, Südhof TC, Rettig J, Stahl B. A trimeric protein complex functions as a synaptic chaperone machine. Neuron 31: 987-999, 2001. (Pubitemid 32925284)
44. Wagner AC, Weber H, Jonas L, Nizze H, Strowski M, Fielder F, Printz H, Steffen H, Goke B. Hyperthermia induces heat shock protein expression and protection against cerulein-induced pancreatitis in rats. Gastroenterology 111: 1333-1342, 1996. (Pubitemid 26362259)
45. Wagner AC, Wishart MJ, Mulders SM, Blevins PM, Andrews PC, Lowe AW, Williams JA. GP-3 a newly characterized glyprotein on the inner surface of the zymogen granule membrane undergoes regulated secretion. J Biol Chem 269: 9099-9104, 1994.
46. Wang CC, Ng CP, Lu L, Atlashkin V, Zhang W, Seet LF, Hong W. A role of VAMP8/endobrevin in regulated exocytosis of pancreatic acinar cells. Dev Cell 7: 359-371, 2004. (Pubitemid 39232972)
47. Wasle B, Edwardson JM. The regulation of exocytosis in the pancreatic acinar cell. Cell Signal 14: 191-197, 2002. (Pubitemid 34102447)
48. Weng N, Thomas DD, Groblewski GE. Pancreatic acinar cells express vesicle-associated membrane protein 2- and 8-specific populations of zymogen granules with distinct and overlapping roles in secretion. J Biol Chem 282: 9635-9645, 2007.
49. Williams JA. Intracellular signaling mechanisms activated by cholecystokinin-regulating synthesis and secretion of digestive enzymes in pancreatic acinar cells. Annu Rev Physiol 63: 77-97, 2001.
50. Zhang H, Kelley WL, Chamberlain LH, Burgoyne RD, Wollheim CB, Lang J. Cysteine-string proteins regulate exocytosis of insulin independent from transmembrane ion fluxes. FEBS Lett 437: 267-272, 1998. (Pubitemid 28511172)
51. Zhang H, Kelley WL, Chamberlain LH, Burgoyne RD, Lang J. Mutational analysis of cysteine string protein in insulin exocytosis. J Cell Sci 112: 1345-1351, 1999. (Pubitemid 29243457)
52. Zhao X, Braun AP, Braun JE. Biological roles of neural J proteins. Cell Mol Life Sci 65: 2385-2396, 2008.
53. Zinsmaier KE, Eberle KK, Buchner E, Walter N, Benzer S. Paralysis and early death in cysteine string protein mutants of Drosophila. Science 263: 977-980, 1994. (Pubitemid 24094564)