Caerulein-induced acute pancreatitis inhibits protein synthesis through effects on eIF2B and eIF4F

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 285, Issue 3 48-3, 2003, Pages

  Sans, Maria Dolors ^a,b   DiMagno, Matthew J ^a   D'Alecy, Louis G ^a   Williams, John A ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b 7737 Med Sci II ^*  (United States)

Author keywords

Mice; Protein translation

Indexed keywords

CERULETIDE; CHOLECYSTOKININ; GUANINE NUCLEOTIDE EXCHANGE FACTOR; INITIATION FACTOR 2; INITIATION FACTOR 4E BINDING PROTEIN 1; INITIATION FACTOR 4F; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN; PROTEIN KINASE B; RIBOSOME PROTEIN; S6 KINASE; UNCLASSIFIED DRUG;

ACUTE PANCREATITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; PROTEIN SYNTHESIS INHIBITION; REGULATORY MECHANISM; TRANSLATION INITIATION;

EID: 0041965742     PISSN: 01931857     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpgi.00540.2002     Document Type: Article

References (69)

1. Anderson P and Kedersha N. Stressful initiations. J Cell Sci 115: 3227-3234, 2002.
2. Bauduin H, Colin M, and Dumont JE. Energy sources for protein synthesis and enzymatic secretion in rat pancreas in vitro. Biochim Biophys Acta 174: 722-733, 1969.
3. Beil M, Leser J, Lutz MP, Gukovskaya A, Seufferlein T, Lynch G, Pandol SJ, and Adler G. Caspase 8-mediated cleavage of plectin precedes F-actin breakdown in acinar cells during pancreatitis. Am J Physiol Gastrointest Liver Physiol 282: G450-G460, 2002.
4. Bianchi BR, Miller TR, Witte DG, and Lin CW. Novel CCK analogues and bombesin: a detailed analysis between phosphoinositide breakdown and high-dose inhibition of pancreatic enzyme secretion in three rodent species. J Pharmacol Exp Ther 268: 996-1002, 1994.
5. Boyd EJS, Wood H, Clarke G, Neill GD, Hutchison F, and Wormsley KG. Pancreatic synthetic rates: a new test of pancreatic function. Scand J Gastroenterol 17: 225-231, 1982.
6. s6k is activated by CCK in rat pancreatic acini. Am J Physiol Cell Physiol 273: C101-C109, 1997.
7. Bragado MJ, Groblewski GE, and Williams JA. Regulation of protein synthesis by cholecystokinin in rat pancreatic acini involves PHAS-I and the p70 S6 kinase pathway. Gastroenterology 115: 733-742, 1998.
8. Bragado MJ, Tashiro M, and Williams JA. Regulation of the initiation of pancreatic digestive enzyme protein synthesis by cholecystokinin in rat pancreas in vivo. Gastroenterology 119: 1731-1739, 2000.
9. Burgering BM and Coffer PJ. Protein kinase B (c-Akt) in phosphotidylinositol-3-OH kinase signal transduction. Nature 376: 599-602, 1995.
10. Caso G, Ford GC, Nair KS, Garlick PJ, and McNurlan MA. Aminoacyl-tRNA enrichment after a flood of labeled phenylalanine: insulin effect on muscle protein synthesis. Am J Physiol Endocrinol Metab 282: E1029-E1038, 2002.
11. Chen X, Ji B, Han B, Ernst SA, Simeone D, and Logsdon CD. NF-κB activation in pancreas induces pancreatic and systemic inflammatory response. Gastroenterology 122: 448-457, 2002.
12. Dabrowski A, Boguslowicz C, Dabrowska M, Tribillo I, and Gabryelewicz A. Reactive oxygen species activate mitogen-activated protein kinases in pancreatic acinar cells. Pancreas 21: 376-384, 2000.
13. Davis TA, Fiorotto ML, Nguyen HV, and Burrin DG. Aminoacyl-tRNA and tissue free amino acid pools are equilibrated after a flooding dose of phenylalanine. Am J Physiol Endocrinol Metab 277: E103-E109, 1999.
14. DiMagno M, Williams J, and Owyang C. eNOS is protective in the initiation of experimental acute pancreatitis. Gastroenterology 122: A-284, 2002.
15. Gardner JD and Jensen RT. Receptors for secretagogues on pancreatic acinar cells. In: The Pancreas. Biology, pathobiology and disease (2nd ed.), edited by Go VLW, DiMagno EP, Gardner JD, Lebenthal E, Reber HA, and Scheele GA. New York: Raven, 1993, p. 151-166.
16. 3H]phenylalanine. Biochem J 192: 719-723, 1980.
17. Gilliland L and Steer ML. Effects of ethionine on digestive enzyme synthesis and discharge by mouse pancreas. Am J Physiol Gastrointest Liver Physiol 239: G418-G426, 1980.
18. Gingras A, Raught B, and Sonenberg N. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 68: 913-963, 1999.
19. Gukovskaya AS, Gukovsky I, Jung Y, Mouria M, and Pandol SJ. Cholecystokinin induces caspase activation and mitochondrial dysfunction in pancreatic acinar cells. Roles in cell injury processes of pancreatitis. J Biol Chem 277: 22595-22604, 2002.
20. Hofbauer B, Saluja AK, Lerch MM, Bhagat L, Bhatia M, Lee HS, Frossard JL, Adler G, and Steer ML. Intra-acinar cell activation of trypsinogen during caerulein-induced pancreatitis in rats. Am J Physiol Gastrointest Liver Physiol 275: G352-G362, 1998.
21. Iovanna JL, Keim V, Michel R, and Dagorn JC. Pancreatic gene expression is altered during acute experimental pancreatitis in the rat. Am J Physiol Gastrointest Liver Physiol 261: G485-G489, 1991.
22. Jefferson LS, Fabian JR, and Kimball SR. Glycogen synthase kinase-3 is the predominant insulin-regulated eukaryotic initiation factor 2B kinase in skeletal muscle. Int J Biochem Cell Biol 31: 191-200, 1999.
23. Jefferson LS and Kimball SR. Amino acid regulation of gene expression. J Nutr 131: 2460S-2466S, 2001.
24. A receptors determine the divergent acinar cell response to the cholecystokinin analog JMV-180. J Biol Chem 275: 19115-19120, 2000.
25. Kaufman RJ. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 13: 1211-1233, 1999.
26. Kern HF, Adler G, and Scheele GA. Structural and biochemical characterization of maximal and supramaximal hormonal stimulation of rat exocrine pancreas. Scand J Gastroenterol 20: 20-29, 1985.
27. Kimball SR. Eukaryotic initiation factor eIF2. Int J Biochem Cell Biol 31: 25-29, 1999.
28. Kimball SR, Everson WV, Flaim KE, and Jefferson LS. Initiation of protein synthesis in a cell-free system prepared from rat hepatocytes. Am J Physiol Cell Physiol 256: C28-C34, 1989.
29. Kimball SR, Jurasinski CV, Lawrence JC Jr, and Jefferson LS. Insulin stimulates protein synthesis in skeletal muscle by enhancing the association of eIF-4E and eIF-4G. Am J Physiol Cell Physiol 272: C754-C759, 1997.
30. Koike H, Steer ML, and Meldolesi J. Pancreatic effects of ethionine: blockade of exocytosis and appearance of crinophagy and autophagy precede cellular necrosis. Am J Physiol Gastrointest Liver Physiol 242: G297-G307, 1982.
31. Korc M, Bailey AC, and Williams JA. Regulation of protein synthesis in normal and diabetic rat pancreas by cholecystokinin. Am J Physiol Gastrointest Liver Physiol 241: G116-G121, 1981.
32. Lampel M and Kern HF. Acute interstitial pancreatitis in the rat induced by excessive doses of a pancreatic secretagogue. Virchows Arch A Path Anat Histol 373: 97-117, 1977.
33. Lundholm K, Ternell M, Zachrisson H, Moldawer L, and Lindstrom L. Measurement of hepatic protein synthesis in unrestrained mice-evaluation of the 'flooding technique.' Acta Physiol Scand 141: 207-219, 1991.
34. Luthen R, Niederau C, and Grendell JH. Intrapancreatic zymogen activation and levels of ATP and glutathione during caerulein pancreatitis in rats. Am J Physiol Gastrointest Liver Physiol 268: G592-G604, 1995.
35. Luthen RE, Niederau C, Ferrell LD, and Grendell JH. Energy metabolism in mouse pancreas in response to different dosages of a CCK analogue. Pancreas 112: 141-146, 1995.
36. Machovich R, Papp M, and Fodor I. Protein synthesis in acute pancreatitis. Biochem Med 3: 376-383, 1970.
37. Marissen WE and Lloyd RE. Eukaryotic translation initiation factor 4G is targeted for proteolytic cleavage by caspase 3 during inhibition of translation in apoptotic cells. Mol Cell Biol 18: 7565-7574, 1998.
38. Matozaki T, Martinez J, and Williams JA. A new CCK analogue differentiates two functionally distinct CCK receptors in rat and mouse pancreatic acini. Am J Physiol Gastrointest Liver Physiol 257: G594-G600, 1989.
39. Meyuhas O. Synthesis of the translational apparatus is regulated at the translational level. Eur J Biochem 267: 6321-6330, 2000.
40. Meyuhas O and Hornstein E. Translational control of TOP mRNAs. In: Translational Control of Gene Expression, edited by Sonenberg N, Hershey JW, and Mathews M. Cold Spring Harbor, New York: Cold Spring Harbor, 2000, p. 671-693.
41. Mitsui K, Brady M, Palfrey HC, and Nairn AC. Purification and characterization of calmodulin-dependent protein kinase III from rabbit reticulocytes and rat pancreas. J Biol Chem 268: 13422-13433, 1993.
42. Morley SJ, Jeffrey I, Bushell M, Pain VM, and Clemens MJ. Differential requirements for caspase-8 activity in the mechanism of phosphorylation of eIF2α, cleavage of eIF4GI and signaling events associated with the inhibition of protein synthesis in apoptotic Jurkat T cells. FEBS Lett 477: 229-236, 2000.
43. Mothe-Satney I, Yang D, Fadden P, Haystead TA, and Lawrence JC. Multiple mechanisms control phosphorylation of PHAS-I in five (S/T) sites that govern translational repression. Mol Cell Biol 20: 3558-3567, 2000.
44. Nairn AC, Bhagat B, and Palfrey HC. Identification of calmodulin-dependent protein kinase III and its major Mr 100,000 substrate in mammalian tissues. Proc Natl Acad Sci USA 82: 7939-7943, 1985.
45. Niederau C, Ferrell LD, and Grendell JH. Caerulein-induced acute necrotizing pancreatitis in mice: protective effects of proglumide, benzotript, and secretin. Gastroenterology 88: 1192-1204, 1985.
46. Ogden JM, Modlin IM, Gorelick FS, and Marks IN. Effect of buprenorphine on pancreatic enzyme synthesis and secretion in normal rats and rats with acute edematous pancreatitis. Dig Dis Sci 39: 2407-2415, 1994.
47. Perkins PS, Bahrami LH, Lenhard LW, and Pandol SJ. Intracellular mechanisms involved in short-term regulation of net protein synthesis in pancreatic acini. Biochim Biophys Acta 1092: 145-152, 1991.
48. Perkins PS and Pandol SJ. Cholecystokinin-induced changes in polysome structure regulate protein synthesis in pancreas. Biochim Biophys Acta 1136: 265-271, 1992.
49. Powers RE, Grady T, Orchard JL, and Gilrane TB. Different effects of hyperstimulation by similar classes of secretagogues on the exocrine pancreas. Pancreas 8: 58-63, 1993.
50. Proud CG. Control of the elongation phase of protein synthesis. In: Translational Control of Gene Expression, edited by Sonenberg N, Hershey JW, and Mathews M. Cold Spring Harbor, New York: Cold Spring Harbor, 2000, p. 719-739.
51. Proud CG and Denton RM. Molecular mechanisms for the control of translation by insulin. Biochem J 328: 329-341, 1997.
52. Ron D. Translational control in the endoplasmic reticulum stress response. J Clin Invest 110: 1383-1388, 2002.
53. 2+/calmodulin-dependent system of protein phosphorylation. Biochimie 70: 619-626, 1988.
54. Saelens X, Kalai M, and Vandenabeele P. Translation inhibition in apoptosis: caspase-dependent PKR activation and eIF2-α phosphorylation. J Biol Chem 276: 41620-41628, 2001.
55. Saluja AK, Saito I, Saluja M, Houlihan MJ, Powers RE, Meldolesi J, and Steer ML. In vivo rat pancreatic acinar cell function during supramaximal stimulation with caerulein. Am J Physiol Gastrointest Liver Physiol 249: G702-G710, 1985.
56. Sans MD, Kimball SR, and Williams JA. Effect of CCK and intracellular calcium to regulate eIF2B and protein synthesis in rat pancreatic acinar cells. Am J Physiol Gastrointest Liver Physiol 282: G267-G276, 2002.
57. Schulz HU, Niederau C, Klonowski-Stumpe H, Halangk W, Luthen R, and Lippert H. Oxidative stress in acute pancreatitis. Hepatogastroenterology 46: 2736-2750, 1999.
58. Scorsone KA, Panniers R, Rowlands AG, and Henshaw EC. Phosphorylation of eukaryotic initiation factor 2 during physiological stresses, which affect protein synthesis. J Biol Chem 262: 14538-14543, 1987.
59. 2 or heat shock is mediated by phosphoinositide 3-kinase and not by mitogen-activated protein kinase-activated protein kinase-2. Biochem J 336: 241-246, 1998.
60. Steer ML and Saluja AK. Experimental acute pancreatitis: studies of the early events that lead to cell injury. In: The Pancreas. Biology, Pathobiology and Disease (2nd ed.), edited by Go VLW, DiMagno EP, Gardner JD, Lebenthal E, Reber HA, and Scheele GA. New York: Raven, 1993, p. 489-500.
61. Sweiry JH, Emery PW, Munoz M, Doolabh K, and Mann GE. Influx and incorporation into protein of L-phenylalanine in the perfused rat pancreas: effects of amino acid deprivation and carbachol. Biochim Biophys Acta 1070: 135-142, 1991.
62. Welsh GI, Miller CM, Loughlin AJ, Price NT, and Proud CG. Regulation of eukaryotic initiation factor eIF2B: glycogen synthase kinase-3 phosphorylates a conserved serine, which undergoes dephosphorylation in response to insulin. FEBS Lett 421: 125-130, 1998.
63. Welsh GI, Stokes CM, Wang X, Sakaue H, Ogawa W, Kasuga M, and Proud CG. Activation of translation initiation factor eIF2B by insulin requires phosphatidyl inositol 3-kinase. FEBS Lett 410: 418-422, 1997.
64. White B, Sullivan J, DeGracia D, O'Neil B, Neumar R, Grossman L, Rafols J, and Krause G. Brain ischemia and reperfusion: molecular mechanisms of neuronal injury. J Neurol Sci 179: 1-33, 2000.
65. 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.
66. Wisner JRJ, Ozawa S, and Renner IG. Pancreatic exocrine function in unconscious rats treated with submaximal, maximal, and supramaximal doses of bombesin tetradecapeptide. Pancreas 4: 83-89, 1989.
67. Yuan S, Rosenberg L, Ilieva A, Agapitos D, and Duguid WP. Early changes of gene expression during cerulein supramaximal stimulation. Pancreas 19: 45-50, 1999.
68. Zamora M, Marissen WE, and Lloyd RE. Multiple eIF4GI-specific protease activities present in uninfected and poliovirus-infected cells. J Virol 76: 165-177, 2002.
69. Zhou W, Shen F, Miller JE, Han Q, and Olson MS. Evidence for altered cellular calcium in the pathogenic mechanism of acute pancreatitis in rats. J Surg Res 60: 147-155, 1996.