Cholecystokinin-58 and cholecystokinin-8 exhibit similar actions on calcium signaling, zymogen secretion, and cell fate in murine pancreatic acinar cells

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 297, Issue 6, 2009, Pages

  Criddle, David N ^a   Booth, David M ^a   Mukherjee, Rajarshi ^b   McLaughlin, Euan ^b   Green, Gary M ^c   Sutton, Robert ^b   Petersen, Ole H ^a   Reeve Jr , Joseph R ^d  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b ROYAL LIVERPOOL AND BROADGREEN UNIVERSITY HOSPITALS NHS TRUST   (United Kingdom)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apoptosis; Mitochondria; Necrosis

Indexed keywords

CALCIUM; CHOLECYSTOKININ; CHOLECYSTOKININ 58; CHOLECYSTOKININ OCTAPEPTIDE; ENZYME PRECURSOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG;

ACINAR CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CELL ACTIVITY; CELL FATE; CELL SECRETION; CONCENTRATION (PARAMETERS); CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENZYME ACTIVITY; ENZYME RELEASE; FLUORESCENCE MICROSCOPY; HORMONE ACTION; IN VITRO STUDY; MOUSE; NONHUMAN; PANCREAS CELL; PATCH CLAMP; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

AMYLASES; ANIMALS; CALCIUM SIGNALING; CELL DIFFERENTIATION; CHOLECYSTOKININ; ENZYME PRECURSORS; EXOCYTOSIS; HUMANS; MEMBRANE POTENTIALS; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; NECROSIS; PANCREAS, EXOCRINE; PATCH-CLAMP TECHNIQUES; PEPTIDE FRAGMENTS; TIME FACTORS;

EID: 72749090107     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00119.2009     Document Type: Article

References (36)

1. Bi Y, Page SL, Williams JA. Rho and Rac promote acinar morphological changes, actin reorganization, and amylase secretion. Am J Physiol Gastrointest Liver Physiol 289: G561-G570, 2005. (Pubitemid 41216394)
2. Campos-Toimil M, Edwardson JM, Thomas P. Real-time studies of zymogen granule exocytosis in intact rat pancreatic acinar cells. J Physiol 528: 317-326, 2000. (Pubitemid 30810736)
3. Criddle DN, Gerasimenko JV, Baumgartner HK, Jaffar M, Voronina S, Sutton R, Petersen OH, Gerasimenko OV. Calcium signalling and pancreatic cell death: apoptosis or necrosis? Cell Death Differ 14: 1285-1294, 2007. (Pubitemid 46965259)
4. Criddle DN, Gillies S, Baumgartner-Wilson HK, Jaffar M, Chinje EC, Passmore S, Chvanov M, Barrow S, Gerasimenko OV, Tepikin AV, Sutton R, Petersen OH. Menadione-induced reactive oxygen species generation via redox cycling promotes apoptosis of murine pancreatic acinar cells. J Biol Chem 281: 40485-40492, 2006. (Pubitemid 46041851)
5. Criddle DN, Murphy J, Fistetto G, Barrow S, Tepikin AV, Neoptolemos JP, Sutton R, Petersen OH. Fatty acid ethyl esters cause pancreatic calcium toxicity via inositol trisphosphate receptors and loss of ATP synthesis. Gastroenterology 130: 781-793, 2006. (Pubitemid 43374528)
6. Criddle DN, Raraty MG, Neoptolemos JP, Tepikin AV, Petersen OH, Sutton R. Ethanol toxicity in pancreatic acinar cells: mediation by nonoxidative fatty acid metabolites. Proc Natl Acad Sci USA 101: 10738-10743, 2004. (Pubitemid 38955812)
7. Dufresne M, Seva C, Fourmy D. Cholecystokinin and gastrin receptors. Physiol Rev 86: 805-847, 2006.
8. Eberlein GA, Eysselein VE, Hesse WH, Goebell H, Schaefer M, Reeve JR Jr. Detection of cholecystokinin-58 in human blood by inhibition of degradation. Am J Physiol Gastrointest Liver Physiol 253: G477-G482, 1987.
9. Eysselein VE, Eberlein GA, Hesse WH, Singer MV, Goebell H, Reeve JR Jr. Cholecystokinin-58 is the major circulating form of cholecystokinin in canine blood. J Biol Chem 262: 214-217, 1987.
10. Grady T, Mah'Moud M, Otani T, Rhee S, Lerch MM, Gorelick FS. Zymogen proteolysis within the pancreatic acinar cell is associated with cellular injury. Am J Physiol Gastrointest Liver Physiol 275: G1010-G1017, 1998. (Pubitemid 28538955)
11. Hajnoczky G, Robb-Gaspers LD, Seitz MB, Thomas AP. Decoding of cytosolic calcium oscillations in the mitochondria. Cell 82: 415-424, 1995.
12. Holst JJ, Knuhtsen S, Jensen SL, Fahrenkrug J, Larsson LI, Nielsen OV. Interrelation of nerves and hormones in stomach and pancreas. Scand J Gastroenterol Suppl 82: 85-99, 1983.
13. Iwatsuki N, Petersen OH. In vitro action of bombesin on amylase secretion, membrane potential, and membrane resistance in rat and mouse pancreatic acinar cells. A comparison with other secretagogues. J Clin Invest 61: 41-46, 1978. (Pubitemid 8262327)
14. Ji B, Bi Y, Simeone D, Mortensen RM, Logsdon CD. Human pancreatic acinar cells lack functional responses to cholecystokinin and gastrin. Gastroenterology 121: 1380-1390, 2001. (Pubitemid 33140455)
15. Kruger B, Albrecht E, Lerch MM. The role of intracellular calcium signaling in premature protease activation and the onset of pancreatitis. Am J Pathol 157: 43-50, 2000. (Pubitemid 30641723)
16. Maruyama Y, Inooka G, Li YX, Miyashita Y, Kasai H. Agonist-induced localized Ca2+ spikes directly triggering exocytotic secretion in exocrine pancreas. EMBO J 12: 3017-3022, 1993. (Pubitemid 23232732)
17. 2+ signaling and enzyme secretion by cholecystokinin in human pancreatic acinar cells. Gastroenterology 135: 632-641, 2008.
18. Owyang C, Logsdon CD. New insights into neurohormonal regulation of pancreatic secretion. Gastroenterology 127: 957-969, 2004. (Pubitemid 39208427)
19. Pandol SJ, Gukovsky I, Satoh A, Lugea A, Gukovskaya AS. Animal and in vitro models of alcoholic pancreatitis: role of cholecystokinin. Pancreas 27: 297-300, 2003. (Pubitemid 37337893)
20. Park MK, Lee M, Petersen OH. Morphological and functional changes of dissociated single pancreatic acinar cells: testing the suitability of the single cell as a model for exocytosis and calcium signaling. Cell Calcium 35: 367-379, 2004. (Pubitemid 38351205)
21. 2+-activated ion channels in exocrine acinar cells. Cell Calcium 38: 171-200, 2005.
22. Petersen OH, Findlay I, Iwatsuki N, Singh J, Gallacher DV, Fuller CM, Pearson GT, Dunne MJ, Morris AP. Human pancreatic acinar cells: studies of stimulus-secretion coupling. Gastroenterology 89: 109-117, 1985. (Pubitemid 15057920)
23. Petersen OH, Sutton R, Criddle DN. Failure of calcium microdomain generation and pathological consequences. Cell Calcium 40: 593-600, 2006. (Pubitemid 44660725)
24. Petersen OH, Tepikin AV. Polarized calcium signaling in exocrine gland cells. Annu Rev Physiol 70: 273-299, 2008.
25. Raraty M, Ward J, Erdemli G, Vaillant C, Neoptolemos JP, Sutton R, Petersen OH. Calcium-dependent enzyme activation and vacuole formation in the apical granular region of pancreatic acinar cells. Proc Natl Acad Sci USA 97: 13126-13131, 2000.
26. Reeve JR Jr, Green GM, Chew P, Eysselein VE, Keire DA. CCK-58 is the only detectable endocrine form of cholecystokinin in rat. Am J Physiol Gastrointest Liver Physiol 285: G255-G265, 2003. (Pubitemid 36875196)
27. Reeve JR Jr, Liddle RA, Shively JE, Lee TD, Keire DA, Chew P, Vigna SR. Sequence variation outside the "active" region of dog and rabbit cholecystokinin-58 results in bioactivity differences. Pancreas 32: 306-313, 2006.
28. Reeve JR Jr, McVey DC, Bunnett NW, Solomon TE, Keire DA, Ho FJ, Davis MT, Lee TD, Shively JE, Vigna SR. Differences in receptor binding and stability to enzymatic digestion between CCK-8 and CCK-58. Pancreas 25: e50-e55, 2002.
29. Reeve JR Jr, Wu SV, Keire DA, Faull K, Chew P, Solomon TE, Green GM, Coskun T. Differential bile-pancreatic secretory effects of CCK-58 and CCK-8. Am J Physiol Gastrointest Liver Physiol 286: G395-G402, 2004. (Pubitemid 38250311)
30. Saluja A, Logsdon C, Garg P. Direct versus indirect action of cholecystokinin on human pancreatic acinar cells: is it time for a judgment after a century of trial? Gastroenterology 135: 357-360, 2008.
31. Saluja AK, Lerch MM, Phillips PA, Dudeja V. Why does pancreatic overstimulation cause pancreatitis? Annu Rev Physiol 69: 249-269, 2007. (Pubitemid 46457643)
32. Tinel H, Cancela JM, Mogami H, Gerasimenko JV, Gerasimenko OV, Tepikin AV, Petersen OH. Active mitochondria surrounding the pancreatic acinar granule region prevent spreading of inositol trisphosphate-evoked local cytosolic Ca(2+) signals. EMBO J 18: 4999-5008, 1999. (Pubitemid 29443802)
33. Voronina S, Sukhomlin T, Johnson PR, Erdemli G, Petersen OH, Tepikin A. Correlation of NADH and Ca2+ signals in mouse pancreatic acinar cells. J Physiol 539: 41-52, 2002. (Pubitemid 35190095)
34. Wu SV, Harikumar KG, Burgess RJ, Reeve J Jr, Miller LJ. Effects of cholecystokinin-58 on Type 1 cholecystokinin receptor function and regulation. Receptor binding, activation, internalization and oligomerization. Am J Physiol Gastrointest Liver Physiol 295: G641-G647, 2008.
35. Yamamoto M, Reeve JR Jr, Green GM. Supramaximal CCK-58 does not induce pancreatitis in the rat: role of pancreatic water secretion. Am J Physiol Gastrointest Liver Physiol 292: G964-G974, 2007. (Pubitemid 46557768)
36. Yamamoto M, Reeve JR Jr, Keire DA, Green GM. Water and enzyme secretion are tightly coupled in pancreatic secretion stimulated by food or CCK-58 but not by CCK-8. Am J Physiol Gastrointest Liver Physiol 288: G866-G879, 2005. (Pubitemid 40563126)