4-Phenylbutyric acid reduces endoplasmic reticulum stress, Trypsin activation, and acinar cell apoptosis while increasing secretion in rat pancreatic acini

Pancreas

Volumn 42, Issue 1, 2013, Pages 92-101

  Malo, Antje ^a   Krüger, Burkhard ^b   Göke, Burkhard ^a   Kubisch, Constanze H ^a  

^a Campus GroAhadern   (Germany)

^b UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

4 phenylbutyric acid; chemical chaperone; ER stress; exocrine pancreatic acini

Indexed keywords

4 PHENYLBUTYRIC ACID; AMYLASE; CALCIUM; CASPASE 3; CCAAT ENHANCER BINDING PROTEIN; CHOLECYSTOKININ; MEMBRANE PROTEIN; PROTEIN KINASELIKE ER KINASE; STRESS ACTIVATED PROTEIN KINASE; TAUROURSODEOXYCHOLIC ACID; TRYPSIN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ACINAR CELL; AMYLASE RELEASE; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELL DEATH; CELL STIMULATION; CELLULAR SECRETION; DRUG EFFECT; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAT; UNFOLDED PROTEIN RESPONSE; UREA CYCLE;

AMYLASES; ANIMALS; APOPTOSIS; CALCIUM; CHOLECYSTOKININ; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; PANCREAS, EXOCRINE; PHENYLBUTYRATES; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; TAUROCHENODEOXYCHOLIC ACID; TIME FACTORS; TRYPSIN; UNFOLDED PROTEIN RESPONSE;

EID: 84872056918     PISSN: 08853177     EISSN: 15364828     Source Type: Journal    
DOI: 10.1097/MPA.0b013e318259f6ca     Document Type: Article

References (69)

1. Case RM. Synthesis, intracellular transport and discharge of exportable proteins in the pancreatic acinar cell and other cells. Biol Rev Camb Philos Soc. 1978;53:211-354.
2. Gething MJ, Sambrook J. Transport and assembly processes in the endoplasmic reticulum. Semin Cell Biol. 1990;1:65-72.
3. Berridge MJ. The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium. 2002;32:235-249.
4. Schroder M, Kaufman RJ. Divergent roles of Ire1alpha and PERK in the unfolded protein response. Curr Mol Med. 2006;6:5-36.
5. Hammond C, Helenius A. Quality control in the secretory pathway. Curr Opin Cell Biol. 1995;7:523-529.
6. Schroder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem. 2005;74:739-789.
7. 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. 1989;264:20602-20607.
8. Trombetta ES, Parodi AJ. Quality control and protein folding in the secretory pathway. Annu Rev Cell Dev Biol. 2003;19:649-676.
9. Harding HP, Zhang Y, Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature. 1999;397:271-274.
10. Travers KJ, Patil CK, Wodicka L, et al. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell. 2000;101:249-258.
11. Lee AH, Iwakoshi NN, Glimcher LH. Xbp-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol. 2003;23:7448-7459.
12. Wang XZ, Harding HP, Zhang Y, et al. Cloning of mammalian Ire1 reveals diversity in the ER stress responses. EMBO J. 1998;17:5708-5717.
13. Nagai H, Noguchi T, Takeda K, et al. Pathophysiological roles of ask1-map kinase signaling pathways. J Biochem Mol Biol. 2007;40:1-6.
14. Oyadomari S, Mori M. Roles of chop/gadd153 in endoplasmic reticulum stress. Cell Death Differ. 2004;11:381-389.
15. Ron D, Habener JF. Chop, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant-negative inhibitor of gene transcription. Genes Dev. 1992;6:439-453.
16. Morishima N, Nakanishi K, Takenouchi H, et al. An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome cYindependent activation of caspase-9 by caspase-12. J Biol Chem. 2002;277:34287-34294.
17. Schroder M. Endoplasmic reticulum stress responses. Cell Mol Life Sci. 2008;65:862-894.
18. Urano F, Wang X, Bertolotti A, et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase Ire1. Science. 2000;287:664-666.
19. Williams JA, Sans MD, Tashiro M, et al. Cholecystokinin activates a variety of intracellular signal transduction mechanisms in rodent pancreatic acinar cells. Pharmacol Toxicol. 2002;91:297-303.
20. Cagliero E, Apruzzese W, Perlmutter GS, et al. Musculoskeletal disorders of the hand and shoulder in patients with diabetes mellitus. Am J Med. 2002;112:487-490.
21. Steer M. Experimental Acute Pancreatitis: Studies of Early Events That Lead to Cell Injury. 2nd ed. New York: Raven Press; 1993.
22. Kruger B, Albrecht E, Lerch MM. The role of intracellular calcium signaling in premature protease activation and the onset of pancreatitis. Am J Pathol. 2000;157:43-50.
23. van Acker GJ Perides G Steer ML. Co-localization hypothesis a Mechanism For The Intrapancreatic Activation Of Digestive Enzymes During The Early Phases Of Acute Pancreatitis. World J Gastroenterol.2006;121985-1990
24. Bhatia M, Neoptolemos JP, Slavin J. Inflammatory mediators as therapeutic targets in acute pancreatitis. Curr Opin Investig Drugs. 2001;2:496-501.
25. Aho HJ, Nevalainen TJ. Experimental pancreatitis in the rat. Ultrastructure of sodium taurocholate-induced pancreatic lesions. Scand J Gastroenterol. 1980;15:417-424.
26. Hegewald G, Nikulin A, Gmaz-Nikulin E, et al. Ultrastructural changes of the human pancreas in acute shock. Pathol Res Pract. 1985;179:610-615.
27. Lerch MM, Saluja AK, Dawra R, et al. Acute necrotizing pancreatitis in the opossum: earliest morphological changes involve acinar cells. Gastroenterology. 1992;103:205-213.
28. Mizunuma T, Kawamura S, Kishino Y. Effects of injecting excess arginine on rat pancreas. J Nutr. 1984;114:467-471.
29. Ji B, Chen XQ, Misek DE, et al. Pancreatic gene expression during the initiation of acute pancreatitis: identification of EGR-1 as a key regulator. Physiol Genomics. 2003;14:59-72.
30. Kubisch CH, Sans MD, Arumugam T, et al. Early activation of endoplasmic reticulum stress is associated with arginine-induced acute pancreatitis. Am J Physiol Gastrointest Liver Physiol. 2006;291:G238-G245.
31. Lee B, Rhead W, Diaz GA, et al. Phase 2 comparison of a novel ammonia scavenging agent with sodium phenylbutyrate in patients with urea cycle disorders: safety, pharmacokinetics and ammonia control. Mol Genet Metab. 2010;100:221-228.
32. Rubenstein RC, Zeitlin PL. A pilot clinical trial of oral sodium 4-phenylbutyrate (buphenyl) in deltaf508-homozygous cystic fibrosis patients: partial restoration of nasal epithelial CFTR function. Am J Respir Crit Care Med. 1998;157:484-490.
33. Zeitlin PL, Diener-West M, Rubenstein RC, et al. Evidence of CFTR function in cystic fibrosis after systemic administration of 4-phenylbutyrate. Mol Ther. 2002;6:119-126.
34. Kubisch CH, Logsdon CD. Secretagogues differentially activate endoplasmic reticulum stress responses in pancreatic acinar cells. Am J Physiol Gastrointest Liver Physiol. 2007;292:G1804-G1812.
35. Kubisch C, Dimagno MJ, Tietz AB, et al. Overexpression of heat shock protein HSP27 protects against cerulein-induced pancreatitis. Gastroenterology. 2004;127:275-286.
36. Mooren F, Hlouschek V, Finkes T, et al. Early changes in pancreatic acinar cell calcium signaling after pancreatic duct obstruction. J Biol Chem. 2003;278:9361-9369.
37. Basseri S, Lhotak S, Sharma AM, et al. The chemical chaperone 4-phenylbutyrate inhibits adipogenesis by modulating the unfolded protein response. J Lipid Res. 2009;50:2486-2501.
38. Roque T, Boncoeur E, Saint-Criq V, et al. Proinflammatory effect of sodium 4-phenylbutyrate in deltaf508-cystic fibrosis transmembrane conductance regulator lung epithelial cells: involvement of extracellular signal-regulated protein kinase 1/2 and c-Jun-NH2-terminal kinase signaling. J Pharmacol Exp Ther. 2008;326:949-956.
39. Iordache C, Duszyk M. Sodium 4-phenylbutyrate upregulates ENAC and sodium absorption in t84 cells. Exp Cell Res. 2007;313:305-311.
40. Loffing J, Moyer BD, Reynolds D, et al. PBA increases CFTR expression but at high doses inhibits Cl(-) secretion in Calu-3 airway epithelial cells. Am J Physiol. 1999;277:L700-L708.
41. Galas MC, Lignon MF, Rodriguez M, et al. Structure-activity relationship studies on cholecystokinin: analogues with partial agonist activity. Am J Physiol. 1988;254:G176-G182.
42. Williams JA. Receptor-mediated signal transduction pathways and the regulation of pancreatic acinar cell function. Curr Opin Gastroenterol. 2008;24:573-579.
43. Treiman M, Caspersen C, Christensen SB. A tool coming of age: thapsigargin as an inhibitor of sarco-endoplasmic reticulum Ca(2+)-ATPases. Trends Pharmacol Sci. 1998;19:131-135.
44. Wu J, Kaufman RJ. From acute ER stress to physiological roles of the unfolded protein response. Cell Death Differ. 2006;13:374-384.
45. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell. 2008;132:27-42.
46. Tabas I, Ron D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol. 2011;13:184-190.
47. Forloni G, Terreni L, Bertani I, et al. Protein misfolding in Alzheimer's and Parkinson's disease: genetics and molecular mechanisms. Neurobiol Aging. 2002;23:957-976.
48. Collins AF, Pearson HA, Giardina P, et al. Oral sodium phenylbutyrate therapy in homozygous beta thalassemia: a clinical trial. Blood. 1995;85:43-49.
49. He B. Viruses, endoplasmic reticulum stress, and interferon responses. Cell Death Differ. 2006;13:393-403.
50. Seimon TA, Kim MJ, Blumenthal A, et al. Induction of ER stress in macrophages of tuberculosis granulomas. PLoS One. 2010;15:e12772.
51. Kaufman RJ, Back SH, Song B, et al. The unfolded protein response is required to maintain the integrity of the endoplasmic reticulum, prevent oxidative stress and preserve differentiation in beta-cells. Diabetes Obes Metab. 2010;12(suppl 2):99-107.
52. Cohen FE, Kelly JW. Therapeutic approaches to protein-misfolding diseases. Nature. 2003;426:905-909.
53. Perlmutter DH. Chemical chaperones: a pharmacological strategy for disorders of protein folding and trafficking. Pediatr Res. 2002;52:832-836.
54. 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. 1997;100:2457-2465.
55. Engin F, Hotamisligil GS. Restoring endoplasmic reticulum function by chemical chaperones: an emerging therapeutic approach for metabolic diseases. Diabetes Obes Metab. 2010;12(suppl 2):108-115.
56. Ozcan U, Yilmaz E, Ozcan L, et al. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science. 2006;313:1137-1140.
57. Ozcan U, Cao Q, Yilmaz E, et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science. 2004;306:457-461.
58. Gregor MF, Hotamisligil GS. Thematic review series: adipocyte biology. Adipocyte stress: the endoplasmic reticulum and metabolic disease. J Lipid Res. 2007;48:1905-1914.
59. Gabriel SE, Clarke LL, Boucher RC, et al. Cftr and outward rectifying chloride channels are distinct proteins with a regulatory relationship. Nature. 1993;363:263-268.
60. Stutts MJ, Canessa CM, Olsen JC, et al. CFTR as a cAMP-dependent regulator of sodium channels. Science. 1995;269:847-850.
61. Newmark HL, Young CW. Butyrate and phenylacetate as differentiating agents: practical problems and opportunities. J Cell Biochem.1995;22:247-253.
62. Vilatoba M, Eckstein C, Bilbao G, et al. Sodium 4-phenylbutyrate protects against liver ischemia reperfusion injury by inhibition of endoplasmic reticulum-stress mediated apoptosis. Surgery. 2005;138:342-351.
63. Qi X, Hosoi T, Okuma Y, et al. Sodium 4-phenylbutyrate protects against cerebral ischemic injury. Mol Pharmacol. 2004;66:899-908.
64. Malo A, Kruger B, Seyhun E, et al. 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. 2010;299:G877-G886.
65. Kereszturi E, Szmola R, Kukor Z, et al. Hereditary pancreatitis caused by mutation-induced misfolding of human cationic trypsinogen: a novel disease mechanism. Hum Mutat. 2009;30:575-582.
66. Lugea A, Waldron RT, French SW, et al. Drinking and driving pancreatitis: links between endoplasmic reticulum stress and autophagy. Autophagy. 2011;7:783-785.
67. Pandol SJ, Gorelick FS, Gerloff A, et al. Alcohol abuse, endoplasmic reticulum stress and pancreatitis. Dig Dis. 2011;28:776-782.
68. Pandol SJ, Gorelick FS, Lugea A. Environmental and genetic stressors and the unfolded protein response in exocrine pancreatic functionVa hypothesis. Front Physiol. 2011;2:8.
69. Alexandre M, Pandol SJ, Gorelick FS, et al. The emerging role of smoking in the development of pancreatitis. Pancreatology. 2011;11:469-474.