Tauroursodeoxycholic acid reduces endoplasmic reticulum stress, acinar cell damage, and systemic inflammation in acute pancreatitis

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 301, Issue 5, 2011, Pages

  Seyhun, Ersin ^a   Malo, Antje ^a   Schäfer, Claus ^b   Moskaluk, Christopher A ^c   Hoffmann, Ralf Thorsten ^d   Göke, Burkhard ^a   Kubisch, Constanze H ^a  

^a Klinikum Grobhadern   (Germany)

^b Neumarkt Clinic   (Germany)

^c UNIVERSITY OF VIRGINIA   (United States)

^d LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

Chemical chaperone

Indexed keywords

AMYLASE; BINDING PROTEIN; BIOLOGICAL MARKER; CASPASE 12; CASPASE 3; CCAAT ENHANCER BINDING PROTEIN; CERULETIDE; CHAPERONE; MYELOPEROXIDASE; PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE; TAURODEOXYCHOLIC ACID; TAUROURSODEOXYCHOLIC ACID; TRYPSIN; X BOX BINDING PROTEIN 1;

ACINAR CELL; ACUTE PANCREATITIS; AMYLASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DAMAGE; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; HISTOPATHOLOGY; IN VIVO STUDY; LUNG EDEMA; LUNG PARENCHYMA; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; RAT; UNFOLDED PROTEIN RESPONSE; UPREGULATION;

ACINAR CELLS; ANIMALS; CAERULEIN; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; INFLAMMATION; MALE; PANCREAS; PANCREATITIS; RATS; RATS, WISTAR; TAUROCHENODEOXYCHOLIC ACID; UNFOLDED PROTEIN RESPONSE;

EID: 80055060952     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00483.2010     Document Type: Article

References (68)

1. Aho HJ, Nevalainen TJ. Experimental pancreatitis in the rat. Ultrastruc-ture of sodium taurocholate-induced pancreatic lesions. Scand J Gastro-enterol 15: 417-424, 1980.
2. Banks PA, Freeman ML. Practice guidelines in acute pancreatitis. Am J Gastroenterol 101: 2379-2400, 2006.
3. Bardag-Gorce F, Oliva J, Lin A, Li J, French BA, French SW. Proteasome inhibitor up regulates liver antioxidative enzymes in rat model of alcoholic liver disease. Exp Mol Pathol 90: 123-130.
4. Berridge MJ. The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 32: 235-249, 2002.
5. Bhatia M, Neoptolemos JP, Slavin J. Inflammatory mediators as therapeutic targets in acute pancreatitis. Curr Opin Investig Drugs 2: 496-501, 2001.
6. Brodsky JL, McCracken AA. ER protein quality control and protea-some-mediated protein degradation. Semin Cell Dev Biol 10: 507-513, 1999.
7. Browne GW, Pitchumoni CS. Pathophysiology of pulmonary complications of acute pancreatitis. World J Gastroenterol 12: 7087-7096, 2006.
8. Brun-Buisson C, Minelli C, Bertolini G, Brazzi L, Pimentel J, Le-wandowski K, Bion J, Romand JA, Villar J, Thorsteinsson A, Damas P, Armaganidis A, Lemaire F. Epidemiology and outcome of acute lung injury in European intensive care units. Results from the ALIVE study. Intensive Care Med 30: 51-61, 2004.
9. Case RM. Synthesis, intracellular transport and discharge of exportable proteins in the pancreatic acinar cell and other cells. Biol Rev Camb Philos Soc 53: 211-354, 1978.
10. Castro RE, Sola S, Ramalho RM, Steer CJ, Rodrigues CM. The bile acid tauroursodeoxycholic acid modulates phosphorylation and transloca-tion of bad via phosphatidylinositol 3-kinase in glutamate-induced apo-ptosis of rat cortical neurons. J Pharmacol Exp Ther 311: 845-852, 2004.
11. Cohen FE, Kelly JW. Therapeutic approaches to protein-misfolding diseases. Nature 426: 905-909, 2003.
12. Czako L, Hegyi P, Rakonczay Z Jr, Wittmann T, Otsuki M. Interactions between the endocrine and exocrine pancreas and their clinical relevance. Pancreatology 9: 351-359, 2009.
13. de Almeida SF, Picarote G, Fleming JV, Carmo-Fonseca M, Azevedo JE, de Sousa M. Chemical chaperones reduce endoplasmic reticulum stress and prevent mutant HFE aggregate formation. J Biol Chem 282: 27905-27912, 2007.
14. Dorner AJ, Wasley LC, Kaufman RJ. Increased synthesis of secreted proteins induces expression of glucose-regulated proteins in butyrate-treated Chinese hamster ovary cells. J Biol Chem 264: 20602-20607, 1989.
15. Bardag-Gorce F, Oliva J, Lin A, Li J, French BA, French SW. Proteasome inhibitor up regulates liver antioxidative enzymes in rat model of alcoholic liver disease. Exp Mol Pathol 90: 123-130, 2011.
16. Forloni G, Terreni L, Bertani I, Fogliarino S, Invernizzi R, Assini A, Ribizzi G, Negro A, Calabrese E, Volonte MA, Mariani C, Franceschi M, Tabaton M, Bertoli A. Protein misfolding in Alzheimer's and Parkinson's disease: genetics and molecular mechanisms. Neurobiol Aging 23: 957-976, 2002.
17. Frerichs KU, Kennedy C, Sokoloff L, Hallenbeck JM. Local cerebral blood flow during hibernation, a model of natural tolerance to "cerebral ischemia". J Cereb Blood Flow Metab 14: 193-205, 1994.
18. Frerichs KU, Smith CB, Brenner M, DeGracia DJ, Krause GS, Marrone L, Dever TE, Hallenbeck JM. Suppression of protein synthesis in brain during hibernation involves inhibition of protein initiation and elongation. Proc Natl Acad Sci USA 95: 14511-14516, 1998.
19. Gething MJ, Sambrook J. Transport and assembly processes in the endoplasmic reticulum. Semin Cell Biol 1: 65-72, 1990.
20. Halangk W, Lerch MM, Brandt-Nedelev B, Roth W, Ruthenbuerger M, Reinheckel T, Domschke W, Lippert H, Peters C, Deussing J. Role of cathepsin B in intracellular trypsinogen activation and the onset of acute pancreatitis. J Clin Invest 106: 773-781, 2000.
21. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6: 1099-1108, 2000.
22. Harding HP, Zhang Y, Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271-274, 1999.
23. Hegewald G, Nikulin A, Gmaz-Nikulin E, Plamenac P, Barenwald G. Ultrastructural changes of the human pancreas in acute shock. Pathol Res Pract 179: 610-615, 1985.
24. Hinnebusch A. Mechanism and regulation of initiator methionyl-tRNA binding of ribosomes. In: Translational Control of Gene Expression, edited by Sonenberg N HJ, Mathews MB. CSHL Press, Cold Spring Harbor, NY, 2000, p. 185-243.
25. Hofken T, Keller N, Fleischer F, Goke B, Wagner AC. Map kinase phosphatases (MKP's) are early responsive genes during induction of cerulein hyperstimulation pancreatitis. Biochem Biophys Res Commun 276: 680-685, 2000.
26. Ji B, Chen XQ, Misek DE, Kuick R, Hanash S, Ernst S, Najarian R, Logsdon CD. Pancreatic gene expression during the initiation of acute pancreatitis: identification of EGR-1 as a key regulator. Physiol Genomics 14: 59-72, 2003.
27. Kereszturi E, Szmola R, Kukor Z, Simon P, Weiss FU, Lerch MM, Sahin-Toth M. Hereditary pancreatitis caused by mutation-induced mis-folding of human cationic trypsinogen: a novel disease mechanism. Hum Mutat 30: 575-582, 2009.
28. Kim YS, Lee BS, Kim SH, Seong JK, Jeong HY, Lee HY. Is there correlation between pancreatic enzyme and radiological severity in acute pancreatitis? World J Gastroenterol 14: 2401-2405, 2008.
29. Kubisch CH, Logsdon CD. Secretagogues differentially activate endo-plasmic reticulum stress responses in pancreatic acinar cells. Am J Physiol Gastrointest Liver Physiol 292: G1804-G1812, 2007.
30. Kubisch CH, Sans MD, Arumugam T, Ernst SA, Williams JA, Log-sdon CD. Early activation of endoplasmic reticulum stress is associated with arginine-induced acute pancreatitis. Am J Physiol Gastrointest Liver Physiol 291: G238-G245, 2006.
31. Lankisch PG, Burchard-Reckert S, Lehnick D. Underestimation of acute pancreatitis: patients with only a small increase in amylase/lipase levels can also have or develop severe acute pancreatitis. Gut 44: 542-544, 1999.
32. Lee YY, Hong SH, Lee YJ, Chung SS, Jung HS, Park SG, Park KS. Tauroursodeoxycholate (TUDCA), chemical chaperone, enhances function of islets by reducing ER stress. Biochem Biophys Res Commun 397: 735-739.
33. Lerch MM, Adler G. Experimental animal models of acute pancreatitis. Int J Pancreatol 15: 159-170, 1994.
34. Lerch MM, Saluja AK, Dawra R, Ramarao P, Saluja M, Steer ML. Acute necrotizing pancreatitis in the opossum: earliest morphological changes involve acinar cells. Gastroenterology 103: 205-213, 1992.
35. Lu PD, Jousse C, Marciniak SJ, Zhang Y, Novoa I, Scheuner D, Kaufman RJ, Ron D, Harding HP. Cytoprotection by pre-emptive conditional phosphorylation of translation initiation factor 2. EMBO J 23: 169-179, 2004.
36. Malo A, Kruger B, Seyhun E, Schafer C, Hoffmann RT, Goke B, Kubisch CH. Tauroursodeoxycholic acid reduces endoplasmic reticulum stress, trypsin activation and acinar cell apoptosis while increasing secretion in rat pancreatic acini. Am J Physiol Gastrointest Liver Physiol 299: G877-G886, 2010.
37. Melnick J, Dul JL, Argon Y. Sequential interaction of the chaperones BiP and GRP94 with immunoglobulin chains in the endoplasmic reticu-lum. Nature 370: 373-375, 1994.
38. Mizunuma T, Kawamura S, Kishino Y. Effects of injecting excess arginine on rat pancreas. J Nutr 114: 467-471, 1984.
39. Morishima N, Nakanishi K, Takenouchi H, Shibata T, Yasuhiko Y. An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J Biol Chem 277: 34287-34294, 2002.
40. Nagai H, Noguchi T, Takeda K, Ichijo H. Pathophysiological roles of ASK1-MAP kinase signaling pathways. J Biochem Mol Biol 40: 1-6, 2007.
41. Neumann B, Zantl N, Veihelmann A, Emmanuilidis K, Pfeffer K, Heidecke CD, Holzmann B. Mechanisms of acute inflammatory lung injury induced by abdominal sepsis. Int Immunol 11: 217-227, 1999.
42. Ni M, Lee AS. ER chaperones in mammalian development and human diseases. FEBS Lett 581: 3641-3651, 2007.
43. Odinokova IV, Sung KF, Mareninova OA, Hermann K, Evtodienko Y, Andreyev A, Gukovsky I, Gukovskaya AS. Mechanisms regulating cytochrome c release in pancreatic mitochondria. Gut 58: 431-442, 2009.
44. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, Smith RO, Gorgun CZ, Hotamisligil GS. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313: 1137-1140, 2006.
45. Pastor CM, Matthay MA, Frossard JL. Pancreatitis-associated acute lung injury: new insights. Chest 124: 2341-2351, 2003.
46. Perlmutter DH. Chemical chaperones: a pharmacological strategy for disorders of protein folding and trafficking. Pediatr Res 52: 832-836, 2002.
47. Petrov MS. Therapeutic implications of oxidative stress in acute and chronic pancreatitis. Curr Opin Clin Nutr Metab Care 13: 562-568.
48. Rubenfeld GD, Caldwell E, Peabody E, Weaver J, Martin DP, Neff M, Stern EJ, Hudson LD. Incidence and outcomes of acute lung injury. N Engl J Med 353: 1685-1693, 2005.
49. Rubenstein RC, Egan ME, Zeitlin PL. In vitro pharmacologic restoration of CFTR-mediated chloride transport with sodium 4-phenylbutyrate in cystic fibrosis epithelial cells containing delta F508-CFTR. J Clin Invest 100: 2457-2465, 1997.
50. Saraswat VA, Sharma BC, Agarwal DK, Kumar R, Negi TS, Tandon RK. Biliary microlithiasis in patients with idiopathic acute pancreatitis and unexplained biliary pain: response to therapy. J Gastroenterol Hepatol 19: 1206-1211, 2004.
51. Schoenberg MH, Buchler M, Gaspar M, Stinner A, Younes M, Melzner I, Bultmann B, Beger HG. Oxygen free radicals in acute pancreatitis of the rat. Gut 31: 1138-1143, 1990.
52. Schroder M, Kaufman RJ. Divergent roles of IRE1alpha and PERK in the unfolded protein response. Curr Mol Med 6: 5-36, 2006.
53. Schroder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 74: 739-789, 2005.
54. Soto C. Protein misfolding and disease; protein refolding and therapy. FEBS Lett 498: 204-207, 2001.
55. Steer ML, Saluja AK. Experimental acute pancreatitis: studies of the early events that lead to cell injury. In: The Pancreas: Biology. Pathobi-ology, and Disease, second edition, edited by Go VLW, DiMagno EP, Gardner JD, Lebenthal R, Reber HA, Scheele GA. New York: Raven, 1993, p. 489-500.
56. Steer ML. Early events in acute pancreatitis. Baillieres Best Pract Res Clin Gastroenterol 13: 213-225, 1999.
57. Tashiro M, Schafer C, Yao H, Ernst SA, Williams JA. Arginine induced acute pancreatitis alters the actin cytoskeleton and increases heat shock protein expression in rat pancreatic acinar cells. Gut 49: 241-250, 2001.
58. Testoni PA, Caporuscio S, Bagnolo F, Lella F. Idiopathic recurrent pancreatitis: long-term results after ERCP, endoscopic sphincterotomy, or ursodeoxycholic acid treatment. Am J Gastroenterol 95: 1702-1707, 2000.
59. Trombetta ES, Parodi AJ. Quality control and protein folding in the secretory pathway. Annu Rev Cell Dev Biol 19: 649-676, 2003.
60. Tsubakio K, Kiriyama K, Matsushima N, Taniguchi M, Shizusawa T, Katoh T, Manabe N, Yabu M, Kanayama Y, Himeno S. Autoimmune pancreatitis successfully treated with ursodeoxycholic acid. Intern Med 41: 1142-1146, 2002.
61. Ulloa-Aguirre A, Janovick JA, Brothers SP, Conn PM. Pharmacologic rescue of conformationally-defective proteins: implications for the treatment of human disease. Traffic 5: 821-837, 2004.
62. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287: 664-666, 2000.
63. Vonlaufen A, Wilson JS, Apte MV. Molecular mechanisms of pancreatitis: current opinion. J Gastroenterol Hepatol 23: 1339-1348, 2008.
64. Wang L, Piguet AC, Schmidt K, Tordjmann T, Dufour JF. Activation of CREB by tauroursodeoxycholic acid protects cholangiocytes from apoptosis induced by mTOR inhibition. Hepatology 41: 1241-1251, 2005.
65. Welsh MJ, Smith AE. Molecular mechanisms of CFTR chloride channel dysfunction in cystic fibrosis. Cell 73: 1251-1254, 1993.
66. Williams JA, Sans MD, Tashiro M, Schafer C, Bragado MJ, Dab-rowski A. Cholecystokinin activates a variety of intracellular signal transduction mechanisms in rodent pancreatic acinar cells. Pharmacol Toxicol 91: 297-303, 2002.
67. Wu J, Kaufman RJ. From acute ER stress to physiological roles of the Unfolded Protein Response. Cell Death Differ 13: 374-384, 2006.
68. Zhang XP, Li ZJ, Zhang J. Inflammatory mediators and microcirculatory disturbance in acute pancreatitis. Hepatobiliary Pancreat Dis Int 8: 351-357, 2009.