Gastroenterology
Volume 138, Issue 2 , Pages 715-725 , February 2010

Biliary Acute Pancreatitis in Mice is Mediated by the G-Protein−Coupled Cell Surface Bile Acid Receptor Gpbar1

  • George Perides

      Affiliations

    • Department of Surgery, Tufts Medical Center and Tufts University School of Medicine, Boston, Massachusetts
    • Corresponding Author InformationReprint requests Address requests for reprints to: George Perides, PhD, Department of Surgery, Tufts Medical Center, 750 Washington Street, Boston, Massachusetts 02111. fax: (617) 636-1466
    • ,
  • Johanna M. Laukkarinen

      Affiliations

    • Department of Gastroenterology and Alimentary Tract Surgery, Tampere University Hospital, Tampere, Finland
    • ,
  • Galya Vassileva

      Affiliations

    • Department of Discovery Technologies, Schering–Plough Research Institute, Kenilworth, New Jersey
    • ,
  • Michael L. Steer

      Affiliations

    • Department of Surgery, Tufts Medical Center and Tufts University School of Medicine, Boston, Massachusetts

Received 18 May 2009 ,Accepted 23 October 2009.

References 

  1. Opie EL. The etiology of acute hemorrhagic pancreatitis. Bull Johns Hopkins Hosp. 1901;12:182–188
  2. Opie EL. The relationship of cholelithiasis to disease of the pancreas and fat necrosis. Bull Johns Hopkins Hosp. 1901;12:19–21
  3. Lerch MM, Saluja AK, Runzi M, et al. Pancreatic duct obstruction triggers acute necrotizing pancreatitis in the opossum. Gastroenterology. 1993;104:853–861
  4. Aho HJ, Koskensalo SM, Nevalainen TJ. Experimental pancreatitis in the rat (Sodium taurocholate-induced acute hemorrhagic pancreatitis). Scand J Gastroenterol. 1980;15:411–416
  5. Laukkarinen JM, van Acker GJ, Weiss ER, et al. A mouse model of acute biliary pancreatitis induced by retrograde pancreatic duct infusion of Na-taurocholate. Gut. 2007;56:1590–1598
  6. Sherman S, Lehman GA. Endoscopic retrograde cholangiopancreatography- and endoscopic sphincterotomy-induced pancreatitis. In:  Beger HG,  Warshaw AL,  Buchler MW, et al. editor. The pancreas. Blackwell: Oxford; 1998;p. 291–310
  7. Zamniak P, Little JM, Radominska A, et al. Taurine-conjugated bile acids act as Ca2+ ionophores. Biochemistry. 1991;30:8598–8604
  8. Bouscarel B, Kroll SD, Fromm H. Signal transduction and hepatocellular bile acid transport: cross talk between bile acids and second messengers. Gastroenterology. 1999;117:433–452
  9. Voronina S, Longbottom R, Sutton R, et al. Bile acids induce calcium signals in mouse pancreatic acinar cells: implications for bile-induced pancreatic pathology. J Physiol. 2002;540:49–55
  10. Mauricio AC, Sllawik M, Heitzman D, et al. Deoxycholic acid (DOC) affects the transport properties of distal colon. Pflugers Arch. 2000;439:532–540
  11. Kim JY, Kim KH, Lee JA, et al. Transporter-mediated bile acid uptake causes Ca2+-dependent cell death in rat pancreatic acinar cells. Gastroenterology. 2002;122:1941–1953
  12. Fischer L, Gukovskaya AS, Penninger JM, et al. Phosphatidylinositol 3 kinase facilitates bile acid-induced Ca2+ responses in pancreatic acinar cells. Am J Physiol Gastrointest Liver Physiol. 2006;292:G875–G886
  13. Voronina S, Longbottom R, Sutton R, et al. Bile acids induce calcium signals in mose pancreatic acinar cells: implications for bile-induced pancreatic pathology. J Physiol. 2008;540:49–55
  14. Gerasimenko JV, Flowerdew SE, Voronina SG, et al. Bile acids induce Ca2+ release from both the endoplasmic reticulum and acidic intracellular calcium stores through activation of inositol trisphosphate receptors and ryanodine receptors. J Biol Chem. 2006;281:40154–40163
  15. Maruyama T, Miyamoto Y, Nakamura T, et al. Identification of membrane-type receptor for bile acids (M-BAR). Biochem Biophys Res Commun. 2002;298:714–719
  16. Kawamata Y, Fujii R, Hosoya M, et al. A G protein-coupled receptor responsive to bile acids. J Biol Chem. 2003;278:9435–9440
  17. Vassileva G, Golovko A, Markowitz L, et al. Targeted deletion of Gpbar1 protects mice from cholesterol gallstone formation. Biochem J. 2006;398:423–430
  18. Maruyama T, Tanaka K, Suzuki J, et al. Targeted disruption of G protein-coupled bile acid receptor 1 (Gpbar1/M-Bar) in mice. J Endocrinol. 2006;191:197–205
  19. Lampel M, Kern HF. Acute interstitial pancreatitis in the rat induced by excessive doses of a pancreatic secretagogue. Virchows Arch A Pathol Anat Histol. 1977;37:97–117
  20. Frossard JL, Hadengue A, Spahr L. Natural history of long-term lung injury in mouse experimental pancreatitis. Crit Care Med. 2002;30:1541–1546
  21. Van Acker GJ, Perides G, Weiss ER, et al. Tumor progression locus-2 is a critical regulator of pancreatic and lung inflammation during acute pancreatitis. J Biol Chem. 2008;282:22140–22149
  22. Laukkarinen JM, Weiss ER, van Acker GJ, et al. Protease-activated receptor-2 exerts contrasting model-specific effects on acute experimental pancreatitis. J Biol Chem. 2008;283:20703–207012
  23. Sharma A, Tao X, Gopal A, et al. Calcium dependene of proteinase-activated receptor 2 and cholecystokinin-mediated amylase secretion from pancreatic acini. Am J Physiol Gastrointest Liver Physiol. 2005;289:G686–G695
  24. Sharma A, Tao X, Gopal A, et al. Protection against acute pancreatitits by activation of protease-activated receptor-2. Am J Physiol Gastrointest Liver Physiol. 2005;288:G388–G395
  25. Makishima M, Okamoto AY, Repa JJ, et al. Identification of a nuclear receptor for bile acids. Science. 1999;284:1362–1365
  26. Parks DJ, Blanchard SG, Bledsoe RK, et al. Bile acids are ligands for an orphan nuclear receptor. Science. 1999;284:1365–1368
  27. Kliewer SA, Moore JT, Wade L, et al. An orphan nuclear receptor activated by pregnanes defines a novel steroid signaling pathway. Cell. 1998;92:73–82
  28. Qin P, Tang X, Elloso MM, et al. Bile acids induce adhesion molecule expression in endothelial cells trough activation of reactive oxygen species, NF-kappaB, and p38. Am J Physiol. Heart Circ Physiol. 2006;291:H741–H747
  29. Brady LM, Beno DWA, Davis BH. Bile acid stimulation of early growth response gene and mitogen-activated protein kinase is protein kinase C-dependent. Biochem J. 1996;316:765–769
  30. Maruyama T, Miyamoto Y, Nakamura T, et al. Identification of membrane-type receptor for bile acids (M-BAR). Biochem Biophys Res Commun. 2002;298:714–719
  31. Kawamata Y, Fuji R, Hosoya M, et al. A G-protein coupled receptor responsive to bile acids. J Biol Chem. 2003;278:9435–9440
  32. Houten SM, Watanabe M, Auwerx J. Endocrine functions of bile acids. EMBO J. 2006;25:1419–1425
  33. Katsuma S, Hirasawa A, Tsujimoto G. Bile acids promote glucagon-like peptide-1 secretion through TGR5 in a murine enteroendocrine cell line STC-1. Biochem Biophys Res Commun. 2005;329:386–390
  34. Yang JI, Yoon JH, Myung SJ, et al. Bile acid-induced TGR5-dependent cJun-N terminal kinase activation leads to enhanced caspase 8 activation in hepatocytes. Biochem Biophys Res Commun. 2007;361:156–161
  35. Thomas C, Auwerx J, Schoonjans K. Bile acids and the membrane bile acid receptor TGR5 – connecting nutrition and metabolism. Thyroid. 2007;18:167–174
  36. Hofman AF. Biliary secretion and excretion. In:  West JB editors. Physiological basis of medical practice. 11th ed.. Baltimore, MD: Williams and Wilkins; 1990;p. 675–691
  37. Bhoomagoud M, Jung T, Altadottir J, et al. Reducing extracellular pH sensitizes the acinar cell to secretagogue-induced pancreatitis responses in rats. Gastroenterology. 2009;137:1083–1092
  38. Saluja AK, Saluja M, Printz H, et al. Experimental pancreatitis is mediated by low-affinity cholecystokinin receptors that inhibit digestive enzyme secretion. Proc Natl Acad Sci U S A. 1989;86:8968–8971
  39. Saluja AK, Dawra RK, Lerch MM, Steer ML. CCK-JMV-180, an analog of cholecystokinin, releases intracellular calcium from an inositol trisphosphate-independent pool in rat pancreatic acini. J Biol Chem. 1992;267:11202–11207
  40. Grady T, Mah'Moud M, Otani T, et al. Zymogen proteolysis within the pancreatic acinar cell is associated with cellular injury. Am J. Physiol. 1998;275:G1010–G1017

 Conflicts of interest The authors disclose no conflicts.

 Funding Supported by National Institutes of Health grant RO-1 31396 from National Institute of Diabetes, Digestive and Kidney Diseases (M.L.S.), P30-NS047423 and by a fellowship from Sigrid Jusélius Foundation, Finland (J.M.L.).

PII: S0016-5085(09)01949-0

doi: 10.1053/j.gastro.2009.10.052

Gastroenterology
Volume 138, Issue 2 , Pages 715-725 , February 2010

Article Tools

* Image Usage & Resolution