Mechanisms of alcoholic pancreatitis

Journal of Gastroenterology and Hepatology (Australia)

Volumn 25, Issue 12, 2010, Pages 1816-1826

  Apte, Minoti V ^a   Pirola, Romano C ^a   Wilson, Jeremy S ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Alcoholic pancreatitis; Individual susceptibility; Pancreatic fibrosis

Indexed keywords

ACETALDEHYDE; ALCOHOL; CHYMOTRYPSINOGEN; PANCREAS ENZYME; REACTIVE OXYGEN METABOLITE; TRIACYLGLYCEROL LIPASE; TRYPSINOGEN;

ACINAR CELL; ALCOHOL ABUSE; ALCOHOL CONSUMPTION; ALCOHOL OXIDATION; ALCOHOLIC PANCREATITIS; ARTICLE; CELL ACTIVATION; DISEASE PREDISPOSITION; ENZYME ACTIVATION; HUMAN; NONHUMAN; PANCREAS DUCT; PANCREAS INJURY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STELLATE CELL;

EID: 78649568817     PISSN: 08159319     EISSN: 14401746     Source Type: Journal    
DOI: 10.1111/j.1440-1746.2010.06445.x     Document Type: Article

References (101)

1. Freidreich N. Disease of the Pancreas. New York: William Wood, 1878.
2. Lankisch PG, Lohr-Happe A, Otto J et al. Natural course in chronic pancreatitis. Pain, exocrine and endocrine pancreatic insufficiency and prognosis of the disease. Digestion 1993; 54: 148-55.
3. Comfort HW, Gambill EE, Baggenstoss AH. Chronic relapsing pancreatitis: a study of 29 cases without associated disease of the biliary or gastrointestinal tract. Gastroenterology 1946; 6: 239-85.
4. Ammann RW, Muellhaupt B. Progression of alcoholic acute to chronic pancreatitis. Gut 1994; 35: 552-6.
5. Deng X, Wang L, Elm MS et al. Chronic alcohol consumption accelerates fibrosis in response to cerulein-induced pancreatitis in rats. Am. J. Pathol. 2005; 166: 93-106.
6. Elsasser HP, Haake T, Grimmig M et al. Repetitive cerulein-induced pancreatitis and pancreatic fibrosis in the rat. Pancreas. 1992; 7: 385-90.
7. Perides G, Tao X, West N et al. A mouse model of ethanol dependent pancreatic fibrosis. Gut 2005; 54: 1461-7.
8. Renner IG, Savage WT, Pantoja JL et al. Death due to acute pancreatitis. Dig. Dis. Sci. 1985; 30: 1005-18.
9. Bourliere M, Barthet M, Berthezene P et al. Is tobacco a risk factor for chronic pancreatitis and alcoholic cirrhosis? Gut 1991; 32: 1392-5.
10. Durbec JP, Sarles H. Multicenter survey of the etiology of pancreatic diseases. Relationship between the relative risk of developing chronic pancreatitis and alcohol, protein and lipid composition. Digestion 1978; 18: 337-50.
11. Sarles H. Alcoholism and pancreatitis. Scand. J. Gastroenterol. 1971; 6: 193-8.
12. Dreiling DA, Koller M. The natural history of alcoholic pancreatitis: update 1985. Mt. Sinai J. Med. 1985; 52: 340-2.
13. Steinberg W, Tenner S. Acute pancreatitis. N. Engl. J. Med. 1994; 330: 1198-210.
14. Opie EL. The etiology of acute haemorrhagic pancreatitis. Bull. Johns Hopkins Hosp. 1901; 12: 182-8.
15. Goff JS. The effect of alcohol in the pancreatic duct sphincter of Oddi. Am. J. Gastroenterol. 1993; 88: 656-60.
16. Viceconte G. Effect of ethanol on sphincter of Oddi: an endoscopic manometric study. Gut 1983; 24: 20-7.
17. Pirola RC, Davis AE. Effects of intravenous alcohol on motility of the duodenum and the sphincter of Oddi. Australas Ann. Med. 1970; 19: 24-9.
18. Yamasaki K, Okazaki K, Sakamoto Y et al. Effects of ethanol on the motility of papillary sphincter and exocrine pancreas in the monkey. Am. J. Gastroenterol. 1993; 88: 2078-83.
19. Sonoda Y, Woods CM, Toouli J et al. Intragastric ethanol reduces sphincter of Oddi function in the anaesthetised Australian possum. Pancreas. 2005; 31: 469.
20. Hajnal F, Flores MC, Radley S et al. Effect of alcohol and alcoholic beverages on meal-stimulated pancreatic secretion in humans. Gastroenterology 1990; 98: 191-6.
21. Sarles H. Chronic calcifying pancreatitis-chronic alcoholic pancreatitis. Gastroenterology 1974; 66: 604-16.
22. Guy O, Robles DG, Adrich Z et al. Protein content of precipitates present in pancreatic juice of alcoholic subjects and patients with chronic calcifying pancreatitis. Gastroenterology 1983; 84: 102-7.
23. Apte MV, Norton ID, Haber PS et al. Both ethanol and protein deficiency increase messenger RNA levels for pancreatic lithostathine. Life Sci. 1996; 58: 485-92.
24. Rindler MJ, Hoops TC. The pancreatic membrane protein GP2 localises specifically to secretory granules and is shed into the pancreatic juice as a protein aggregate. Eur. J. Cell Biol. 1990; 53: 154-63.
25. Apte MV, Norton ID, Haber PS et al. Chronic ethanol administration decreases rat pancreatic GP2 content. Biochimica Biophys. Acta. 1997; 1336: 89-98.
26. Sarles H, Sarles JC, Camatte R et al. Observations on 205 confirmed cases of acute pancreatitis, recurring pancreatitis, and chronic pancreatitis. Gut 1965; 6: 545-59.
27. Cohn JA, Neoptolemos JP, Feng J et al. Increased risk of idiopathic chronic pancreatitis in cystic fibrosis carriers. Hum. Mutat. 2005; 26: 303-7.
28. Whitcomb DC. Genetic polymorphisms in alcoholic pancreatitis. Dig. Dis. 2005; 23: 247-54.
29. Lindkvist B, Fajardo I, Pejler G et al. Cathepsin B activates human trypsinogen 1 but not proelastase 2 or procarboxypeptidase B. Pancreatology 2006; 6: 224-31.
30. Apte MV, Haber PS, Norton ID et al. Alcohol and the pancreas. Addict. Biol. 1998; 3: 137-50.
31. Sahin-Toth M, Toth M. Gain-of-function mutations associated with hereditary pancreatitis enhance autoactivation of human cationic trypsinogen. Biochem. Biophys. Res. Commun. 2000; 278: 286-9.
32. Teich N, Rosendahl J, Toth M et al. Mutations of human cationic trypsinogen (PRSS1) and chronic pancreatitis. Hum. Mutat. 2006; 27: 721-30.
33. Apte MV, Wilson JS, McCaughan GW et al. Ethanol-induced alterations in messenger RNA levels correlate with glandular content of pancreatic enzymes. J. Lab. Clin. Med. 1995; 125: 634-40.
34. Ponnappa BC, Hoek JB, Waring AJ et al. Effect of ethanol on amylase secretion and cellular calcium homeostasis in pancreatic acini from normal and ethanol-fed rats. Biochem. Pharmacol. 1987; 36: 69-79.
35. Siegmund E, Luthen F, Kunert J et al. Ethanol modifies the actin cytoskeleton in rat pancreatic acinar cells-comparison with effects of CCK. Pancreatology 2004; 4: 12-21.
36. Wilson JS, Apte MV, Thomas MC et al. Effects of ethanol, acetaldehyde and cholesteryl esters on pancreatic lysosomes. Gut 1992; 33: 1099-104.
37. Haber PS, Wilson JS, Apte MV et al. Fatty acid ethyl esters increase rat pancreatic lysosomal fragility. J. Lab. Clin. Med. 1993; 121: 759-64.
38. Lange LG. Nonoxidative ethanol metabolism: formation of fatty acid ethyl esters by cholesterol esterase. Proc. Natl. Acad. Sci. U S A. 1982; 79: 3954-7.
39. Wilson JS, Colley PW, Sosula L et al. Alcohol causes a fatty pancreas. A rat model of ethanol-induced pancreatic steatosis. Alcohol. Clin. Exp. Res. 1982; 6: 117-21.
40. Gukovskaya AS, Mouria M, Gukovsky I et al. Ethanol metabolism and transcription factor activation in pancreatic acinar cells in rats. Gastroenterology 2002; 122: 106-18.
41. Haber PS, Apte MV, Applegate TL et al. Metabolism of ethanol by rat pancreatic acinar cells. J. Lab. Clin. Med. 1998; 132: 294-302.
42. Haber PS, Apte MV, Moran C et al. Non-oxidative metabolism of ethanol by rat pancreatic acini. Pancreatology 2004; 4: 82-9.
43. Chiang CP, Wu CW, Lee SP et al. Expression pattern, ethanol-metabolizing activities, and cellular localization of alcohol and aldehyde dehydrogenases in human pancreas: implications for pathogenesis of alcohol-induced pancreatic injury. Alcohol. Clin. Exp. Res. 2009; 33: 1059-68.
44. Norton I, Apte M, Haber P et al. P4502E1 is present in rat pancreas and is induced by chronic ethanol administration. Gastroenterology 1996; 110: A1280.
45. Ekstrom G, Ingelman-Sundberg M. Rat liver microsomal NADPH-supported oxidase activity and lipid peroxidation dependent on ethanol-inducible cytochrome P-450 (P-450IIE1). Biochem. Pharmacol. 1989; 38: 1313-9.
46. Shaw S, Jayatilleke E. The role of cellular oxidases and catalytic iron in the pathogenesis of ethanol-induced liver injury. Life Sci. 1992; 50: 2045-52.
47. Altomare E, Grattagliano I, Vendemiale G et al. Acute ethanol administration induces oxidative changes in rat pancreatic tissue. Gut 1996; 38: 742-46.
48. Casini A, Galli A, Pignalosa P et al. Collagen type I synthesized by pancreatic periacinar stellate cells (PSC) co-localizes with lipid peroxidation-derived aldehydes in chronic alcoholic pancreatitis. J. Pathol. 2000; 192: 81-9.
49. Norton ID, Apte MV, Lux O et al. Chronic ethanol administration causes oxidative stress in the rat pancreas. J. Lab. Clin. Med. 1998; 131: 442-6.
50. Werner J, Saghir M, Fernandez-del Castillo C et al. Linkage of oxidative and nonoxidative ethanol metabolism in the pancreas and toxicity of nonoxidative ethanol metabolites for pancreatic acinar cells. Surgery. 2001; 129: 736-44.
51. Werner J, Saghir M, Warshaw AL et al. Alcoholic pancreatitis in rats: injury from nonoxidative metabolites of ethanol. Am. J. Physiol. Gastrointest. Liver Physiol. 2002; 283: G65-73.
52. Nordback IH, MacGowan S, Potter J et al. The role of acetaldehyde in the pathogenesis of acute alcoholic pancreatitis. Ann. Surg. 1991; 214: 671-8.
53. Sankaran H, Lewin MB, Wong A et al. Irreversible inhibition by acetaldehyde of cholecystokinin-induced amylase secretion from isolated rat pancreatic acini. Biochem. Pharmacol. 1985; 34: 2859-63.
54. Lieber CS. Metabolism of ethanol. In: Lieber CS, ed. Medical and Nutritional Complications of Alcoholism: Mechanisms and Management. New York: Plenum Publishing Corporation, 1992; 1-35.
55. Dryden GW, Deacuic I, Arteel G et al. Clinical implications of oxidative stress and antioxidant therapy. Curr. Gastroenterol. Rev. 2005; 7: 308-16.
56. Lugea A, Gukovsky I, Gukovskaya AS et al. Nonoxidative ethanol metabolites alter extracellular matrix protein content in rat pancreas. Gastroenterology 2003; 125: 1845-59.
57. Werner J, Laposata M, Fernandez-del Castillo C et al. Pancreatic injury in rats induced by fatty acid ethyl ester, a nonoxidative metabolite of alcohol. Gastroenterology 1997; 113: 286-94.
58. Hungund BL, Goldstein DB, Villegas F et al. Formation of fatty acid ethyl esters during chronic ethanol treatment in mice. Biochem. Pharmacol. 1988; 37: 3001-4.
59. Lange LG, Sobel BE. Mitochondrial dysfunction induced by fatty acid ethyl esters, myocardial metabolites of ethanol. J. Clin. Invest. 1983; 72: 724-31.
60. Criddle DN, Murphy J, Fistetto G et al. Fatty acid ethyl esters cause pancreatic calcium toxicity via inositol trisphosphate receptors and loss of ATP synthesis. Gastroenterology 2006; 130: 781-93.
61. Del Castillo-Vaquero A, Salido GM, Gonzalez A. Increased calcium influx in the presence of ethanol in mouse pancreatic acinar cells. Int. J. Exp. Pathol. 2010; 91: 114-24.
62. Apte M, Pirola R, Wilson J. New insights into alcoholic pancreatitis and pancreatic cancer. J. Gastroenterol. Hepatol. 2009; 24 (Suppl 3): S51-6.
63. Apte MV, Haber PS, Applegate TL et al. Periacinar stellate shaped cells in rat pancreas-identification, isolation, and culture. Gut 1998; 43: 128-33.
64. Bachem MG, Schneider E, Gross H et al. Identification, culture, and characterization of pancreatic stellate cells in rats and humans. Gastroenterology 1998; 115: 421-32.
65. Apte MV, Haber PS, Darby SJ et al. Pancreatic stellate cells are activated by proinflammatory cytokines implications for pancreatic fibrogenesis. Gut 1999; 44: 534-41.
66. Mews P, Phillips P, Fahmy R et al. Pancreatic stellate cells respond to inflammatory cytokines: potential role in chronic pancreatitis. Gut 2002; 50: 535-41.
67. Schneider E, Schmid-Kotsas A, Zhao J et al. Identification of mediators stimulating proliferation and matrix synthesis of rat pancreatic stellate cells. Am. J. Physiol. Cell Physiol. 2001; 281: C532-43.
68. Phillips PA, McCarroll JA, Park S et al. Rat pancreatic stellate cells secrete matrix metalloproteinases: implications for extracellular matrix turnover. Gut 2003; 52: 275-82.
69. Apte MV, Phillips PA, Fahmy RG et al. Does alcohol directly stimulate pancreatic fibrogenesis? Studies with rat pancreatic stellate cells. Gastroenterology 2000; 118: 780-94.
70. Masamune A, Satoh A, Watanabe T et al. Effects of ethanol and its metabolites on human pancreatic stellate cells. Dig. Dis. Sci. 2010; 55: 204-11.
71. Lawrencia C, Charrier A, Huang G et al. Ethanol-mediated expression of connective tissue growth factor (CCN2) in mouse pancreatic stellate cells. Growth Factors 2009; 27: 91-9.
72. Vonlaufen A, Phillips P, Xu Z et al. Withdrawal of alcohol promotes regression while continued alcohol intake promotes persistence of LPS-induced pancreatic injury in alcohol-fed rats. Gut 2010 (in press) accepted June 2010.
73. Vonlaufen A, Xu Z, Daniel B et al. Bacterial endotoxin: a trigger factor for alcoholic pancreatitis? Evidence from a novel, physiologically relevant animal model. Gastroenterology 2007; 133: 1293-303.
74. Apte MV, Pirola RC, Wilson JS. Individual susceptibility to alcoholic pancreatitis. J. Gastroenterol. Hepatol. 2008; 23 (Suppl 1): S63-8.
75. Witt H, Apte MV, Keim V et al. Chronic pancreatitis: challenges and advances in pathogenesis, genetics, diagnosis, and therapy. Gastroenterology 2007; 132: 1557-73.
76. Apte MV, Pirola RC, Wilson JS. Where there's smoke there's not necessarily fire. Gut 2005; 54: 446-7.
77. Law R, Parsi M, Lopez R et al. Cigarette smoking is independently associated with chronic pancreatitis. Pancreatology 2010; 10: 54-9.
78. Maisonneuve P, Lowenfels AB, Mullhaupt B et al. Cigarette smoking accelerates progression of alcoholic chronic pancreatitis. Gut 2005; 54: 510-4.
79. Ammann RW, Raimondi S, Maisonneuve P et al. Is obesity an additional risk factor for alcoholic chronic pancreatitis? Pancreatology 2010; 10: 47-53.
80. Wannamethee SG, Shaper AG. Alcohol, body weight, and weight gain in middle-aged men. Am. J. Clin. Nutr. 2003; 77: 1312-7.
81. Miyasaka K, Ohta M, Takano S et al. Carboxylester lipase gene polymorphism as a risk of alcohol-induced pancreatitis. Pancreas 2005; 30.
82. Witt H, Sahin-Toth M, Landt O et al. A degradation-sensitive anionic trypsinogen (PRSS2) variant protects against chronic pancreatitis. Nat. Genet. 2006; 38: 668-73.
83. Witt H, Luck W, Becker M et al. Mutation in the SPINK1 trypsin inhibitor gene, alcohol use, and chronic pancreatitis. JAMA 2001; 285: 2716-7.
84. Diaconu BL, Ciobanu L, Mocan T et al. Investigation of the SPINK1 N34S mutation in Romanian patients with alcoholic chronic pancreatitis. A clinical analysis based on the criteria of the M-ANNHEIM classification. J. Gastrointestin. Liver Dis. 2009; 18: 143-50.
85. Kuwata K, Hirota M, Shimizu H et al. Functional analysis of recombinant pancreatic secretory trypsin inhibitor protein with amino-acid substitution. J. Gastroenterol. 2002; 37: 928-34.
86. Pandol SJ, Periskic S, Gukovsky I et al. Ethanol diet increases the sensitivity of rats to pancreatitis induced by cholecystokinin octapeptide. Gastroenterology 1999; 117: 706-16.
87. Bode C, Kugler V, Bode JC. Endotoxemia in patients with alcoholic and non-alcoholic cirrhosis and in subjects with no evidence of chronic liver disease following acute alcohol excess. J. Hepatol. 1987; 4: 8-14.
88. Bode JC, Parlesak A, Bode C. Gut derived bacterial toxins (endotoxin) and alcohol liver disease. In: Agarwal DP, Seitz HK, eds. Alcohol in Health and Disease. New York/Basel: Marcel Dekker, 2001; 369-86.
89. Ammori BJ, Leeder PC, King RF et al. Early increase in intestinal permeability in patients with severe acute pancreatitis: correlation with endotoxemia, organ failure, and mortality. J. Gastrointest. Surg. 1999; 3: 252-62.
90. Gullo L, Barbara L, Labo G. Effect of cessation of alcohol use on the course of pancreatic dysfunction in alcoholic pancreatitis. Gastroenterology 1988; 95: 1063-8.
91. Wilson JS, Bernstein L, McDonald C et al. Diet and drinking habits in relation to the development of alcoholic pancreatitis. Gut 1985; 26: 882-7.
92. Nakamura Y, Ishikawa A, Sekiguchi S et al. Spirits increase the risk for chronic pancreatitis more than beer and Sake in 111 Japanese alcoholics. Gastroenterology 2002; 122: A509.
93. Lowenfels AB, Zwemer FL, Jhangiani S et al. Pancreatitis in a native American Indian population. Pancreas 1987; 2: 694-7.
94. Haber PS, Wilson JS, Pirola RC. Smoking and alcoholic pancreatitis. Pancreas 1993; 8: 568-72.
95. Wilson JS, Gossat D, Tait A et al. Evidence for an inherited predisposition to alcoholic pancreatitis. A controlled HLA typing study. Dig. Dis. Sci. 1984; 29: 727-30.
96. Haber PS, Wilson JS, McGarity BH et al. Alpha 1 antitrypsin phenotypes and alcoholic pancreatitis. Gut 1991; 32: 945-8.
97. Norton ID, Apte MV, Dixson H et al. Cystic fibrosis genotypes and alcoholic pancreatitis. J. Gastroenterol. Hepatol. 1998; 13: 496-500.
98. Frenzer A, Butler WJ, Norton ID et al. Polymorphism in alcohol-metabolizing enzymes, glutathione S-transferases and apolipoprotein E and susceptibility to alcohol-induced cirrhosis and chronic pancreatitis. J. Gastroenterol. Hepatol. 2002; 17: 177-82.
99. Schneider A, Barmada MM, Slivka A et al. Transforming growth factor-beta1, interleukin-10 and interferon-gamma cytokine polymorphisms in patients with hereditary, familial and sporadic chronic pancreatitis. Pancreatology 2004; 4: 490-4.
100. Schneider A, Pfutzer RH, Barmada MM et al. SPINK1/PSTI gene mutations in patients with alcoholic chronic pancreatitis from North America. Gastroenterology 2002; 122: A563.
101. Ockenga J, Vogel A, Teich N et al. UDP glucuronosyltransferase (UGT1A7) gene polymorphisms increase the risk of chronic pancreatitis and pancreatic cancer. Gastroenterology 2003; 124: 1802-8.