The Biliary HCO-3 Umbrella: A Unifying Hypothesis on Pathogenetic and Therapeutic Aspects of Fibrosing Cholangiopathies

Hepatology

Volumn 52, Issue 4, 2010, Pages 1489-1496

  Beuers, Ulrich ^a   Hohenester, Simon ^a   Maillette de Buy Wenniger, Lucas J ^a   Kremer, Andreas E ^a   Jansen, Peter L M ^a   Oude Elferink, Ronald P J ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BICARBONATE; BICARBONATE CHLORIDE ANTIPORTER; BILE ACID; PHOSPHOLIPID; PURINERGIC P2 RECEPTOR;

ANIMAL; BILE DUCT; HUMAN; METABOLISM; MICELLE; PATHOPHYSIOLOGY; PH; PHYSIOLOGY; REVIEW; SCLEROSING CHOLANGITIS; SECRETION;

ADENOSINE TRIPHOSPHATE; ANIMALS; BICARBONATES; BILE ACIDS AND SALTS; BILE DUCTS; CHLORIDE-BICARBONATE ANTIPORTERS; CHOLANGITIS, SCLEROSING; HUMANS; HYDROGEN-ION CONCENTRATION; MICELLES; PHOSPHOLIPIDS; RECEPTORS, PURINERGIC P2;

MLCS; MLOWN;

EID: 77957940106     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.23810     Document Type: Review

References (63)

1. EASL Clinical Practice Guidelines: Management of cholestatic liver diseases. J Hepatol 2009;51:237-267.
2. Gershwin ME, Mackay IR. The causes of primary biliary cirrhosis: convenient and inconvenient truths. HEPATOLOGY 2008;47:737-745.
3. Gotthardt D, Runz H, Keitel V, Fischer C, Flechtenmacher C, Wirtenberger M, et al. A mutation in the canalicular phospholipid transporter gene, ABCB4, is associated with cholestasis, ductopenia, and cirrhosis in adults. HEPATOLOGY 2008;48:1157-1166.
4. Poupon R, Ping C, Chretien Y, Corpechot C, Chazouilleres O, Simon T, et al. Genetic factors of susceptibility and of severity in primary biliary cirrhosis. J Hepatol 2008;49:1038-1045.
5. Prieto J, Qian C, Garcia N, Diez J, Medina JF. Abnormal expression of anion exchanger genes in primary biliary cirrhosis. Gastroenterology 1993;105:572-578.
6. Medina JF, Martinez A, Vazquez JJ, Prieto J. Decreased anion exchanger 2 immunoreactivity in the liver of patients with primary biliary cirrhosis. HEPATOLOGY 1997;25:12-17.
7. Prieto J, Garcia N, Marti-Climent JM, Penuelas I, Richter JA, Medina JF. Assessment of biliary bicarbonate secretion in humans by positron emission tomography. Gastroenterology 1999;117:167-172.
8. Melero S, Spirli C, Zsembery A, Medina JF, Joplin RE, Duner E, et al. Defective regulation of cholangiocyte Cl-/HCO3(-) and Naþ/Hþ exchanger activities in primary biliary cirrhosis. HEPATOLOGY 2002;35: 1513-1521.
9. Beuers U, Oude-Elferink RP. New light on anion exchangers in primary biliary cirrhosis. J Hepatol 2008;49:881-883.
10. Karlsen TH, Franke A, Melum E, Kaser A, Hov JR, Balschun T, et al. Genome-wide association analysis in primary sclerosing cholangitis. Gastroenterology 2010;138:1102-1111.
11. Hofmann AF. Bile acids: trying to understand their chemistry and biology with the hope of helping patients. HEPATOLOGY 2009;49: 1403-1418.
12. Carey MC. Physical-chemical properties of bile acids and their salts. In: Danielsson H, Sjövall J, eds. Sterols and Bile Acids. Amsterdam: Elsevier, 1985:345-403.
13. Rust C, Wild N, Bernt C, Vennegeerts T, Wimmer R, Beuers U. Bile acid-induced apoptosis in hepatocytes is caspase-6-dependent. J Biol Chem 2009;284:2908-2916.
14. Boyer JL. It’s all about bile. HEPATOLOGY 2009;49:711-723.
15. Alpini G, McGill JM, Larusso NF. The pathobiology of biliary epithelia. HEPATOLOGY 2002;35:1256-1268.
16. Boyer JL. Mechanisms of bile secretion and hepatic transport. In: Andreoli TE, Hoffman JF, Fanestil DD, Schultz SG, eds. Physiology of Membrane Disorders. New York: Plenum Publishing Corporation, 1986:609-636.
17. Moschetta A, Xu F, Hagey LR, van Berge-Henegouwen GP, van Erpecum KJ, Brouwers JF, et al. A phylogenetic survey of biliary lipids in vertebrates. J Lipid Res 2005;46:2221-2232.
18. Amelsberg A, Schteingart CD, Ton-Nu HT, Hofmann AF. Carrier-mediated jejunal absorption of conjugated bile acids in the guinea pig. Gastroenterology 1996;110:1098-1106.
19. Eastwood GL. Effect of pH on bile salt injury to mouse gastric mucosa. A light- and electron-microscopic study. Gastroenterology 1975; 68:1456-1465.
20. Duane WC, Wiegand DM, Sievert CE. Bile acid and bile salt disrupt gastric mucosal barrier in the dog by different mechanisms. Am J Physiol 1982;242:G95-G99.
21. Batzri S, Harmon JW, Schweitzer EJ, Toles R. Bile acid accumulation in gastric mucosal cells. Proc Soc Exp Biol Med 1991;197:393-399.
22. Dvorak K, Payne CM, Chavarria M, Ramsey L, Dvorakova B, Bernstein H, et al. Bile acids in combination with low pH induce oxidative stress and oxidative DNA damage: relevance to the pathogenesis of Barrett’s oesophagus. Gut 2007;56:763-771.
23. Fickert P, Trauner M, Fuchsbichler A, Zollner G, Wagner M, Marschall HU, et al. Oncosis represents the main type of cell death in mouse models of cholestasis. J Hepatol 2005;42:378-385.
24. Farina A, Dumonceau JM, Frossard JL, Hadengue A, Hochstrasser DF, Lescuyer P. Proteomic analysis of human bile from malignant biliary stenosis induced by pancreatic cancer. J Proteome Res 2009;8:159-169.
25. Andrianifahanana M, Moniaux N, Batra SK. Regulation of mucin expression: mechanistic aspects and implications for cancer and inflammatory diseases. Biochim Biophys Acta 2006;1765:189-222.
26. Martinez-Anso E, Castillo JE, Diez J, Medina JF, Prieto J. Immunohistochemical detection of chloride/bicarbonate anion exchangers in human liver. HEPATOLOGY 1994;19:1400-1406.
27. Glaser SS, Gaudio E, Rao A, Pierce LM, Onori P, Franchitto A, et al. Morphological and functional heterogeneity of the mouse intrahepatic biliary epithelium. Lab Invest 2009;89:456-469.
28. Kulaksiz H, Heuberger D, Engler S, Stiehl A. Poor outcome in progressive sclerosing cholangitis after septic shock. Endoscopy 2008;40: 214-218.
29. Banales JM, Arenas F, Rodriguez-Ortigosa CM, Saez E, Uriarte I, Doctor RB, et al. Bicarbonate-rich choleresis induced by secretin in normal rat is taurocholate-dependent and involves AE2 anion exchanger. HEPATOLOGY 2006;43:266-275.
30. Alvaro D, Mancino MG, Glaser S, Gaudio E, Marzioni M, Francis H, et al. Proliferating cholangiocytes: a neuroendocrine compartment in the diseased liver. Gastroenterology 2007;132:415-431.
31. Keitel V, Ullmer C, Haussinger D. The membrane-bound bile acid receptor TGR5 (Gpbar-1) is localized in the primary cilium of cholangiocytes. Biol Chem 2010. In press.
32. Gradilone SA, Masyuk AI, Splinter PL, Banales JM, Huang BQ, Tietz PS, et al. Cholangiocyte cilia express TRPV4 and detect changes in luminal tonicity inducing bicarbonate secretion. Proc Natl Acad Sci USA 2007;104:19138-19143.
33. Minagawa N, Nagata J, Shibao K, Masyuk AI, Gomes DA, Rodrigues MA, et al. Cyclic AMP regulates bicarbonate secretion in cholangiocytes through release of ATP into bile. Gastroenterology 2007;133: 1592-1602.
34. Keitel V, Cupisti K, Ullmer C, Knoefel WT, Kubitz R, Haussinger D. The membrane-bound bile acid receptor TGR5 is localized in the epithelium of human gallbladders. HEPATOLOGY 2009;50:861-870.
35. Fiorotto R, Spirli C, Fabris L, Cadamuro M, Okolicsanyi L, Strazzabosco M. Ursodeoxycholic acid stimulates cholangiocyte fluid secretion in mice via CFTR-dependent ATP secretion. Gastroenterology 2007;133: 1603-1613.
36. Feranchak AP, Fitz JG. Thinking outside the cell: the role of extracellular adenosine triphosphate in bile formation. Gastroenterology 2007; 133:1726-1728.
37. Chari RS, Schutz SM, Haebig JE, Shimokura GH, Cotton PB, Fitz JG, et al. Adenosine nucleotides in bile. Am J Physiol 1996;270: G246-G252.
38. Masyuk AI, Gradilone SA, Banales JM, Huang BQ, Masyuk TV, Lee SO, et al. Cholangiocyte primary cilia are chemosensory organelles that detect biliary nucleotides via P2Y12 purinergic receptors. Am J Physiol Gastrointest Liver Physiol 2008;295:G725-G734.
39. Masyuk AI, Masyuk TV, Splinter PL, Huang BQ, Stroope AJ, LaRusso NF. Cholangiocyte cilia detect changes in luminal fluid flow and transmit them into intracellular Ca2þ and cAMP signaling. Gastroenterology 2006;131:911-920.
40. Roman RM, Feranchak AP, Salter KD, Wang Y, Fitz JG. Endogenous ATP release regulates Cl- secretion in cultured human and rat biliary epithelial cells. Am J Physiol 1999;276:G1391-G1400.
41. Dranoff JA, Masyuk AI, Kruglov EA, LaRusso NF, Nathanson MH. Polarized expression and function of P2Y ATP receptors in rat bile duct epithelia. Am J Physiol Gastrointest Liver Physiol 2001;281:G1059-G1067.
42. Dutta AK, Woo K, Doctor RB, Fitz JG, Feranchak AP. Extracellular nucleotides stimulate Cl- currents in biliary epithelia through receptor-mediated IP3 and Ca2þ release. Am J Physiol Gastrointest Liver Physiol 2008;295:G1004-G1015.
43. Yu J, Sheung N, Soliman EM, Spirli C, Dranoff JA. Transcriptional regulation of IL-6 in bile duct epithelia by extracellular ATP. Am J Physiol Gastrointest Liver Physiol 2009;296:G563-G571.
44. Langlois C, Gendron FP. Promoting macrophage transepithelial migration by stimulating the epithelial cell P2Y(2) receptor. Eur J Immunol 2009;39:2895-2905.
45. Schlosser SF, Burgstahler AD, Nathanson MH. Isolated rat hepatocytes can signal to other hepatocytes and bile duct cells by release of nucleotides. Proc Natl Acad Sci USA 1996;93:9948-9953.
46. Reisin IL, Prat AG, Abraham EH, Amara JF, Gregory RJ, Ausiello DA, et al. The cystic fibrosis transmembrane conductance regulator is a dual ATP and chloride channel. J Biol Chem 1994;269:20584-20591.
47. Feranchak AP, Lewis MA, Kresge C, Sathe M, Bugde A, Luby-Phelps K, et al. Initiation of purinergic signaling by exocytosis of ATP-containing vesicles in liver epithelium. J Biol Chem;285:8138-8147.
48. Sabirov RZ, Okada Y. The maxi-anion channel: a classical channel playing novel roles through an unidentified molecular entity. J Physiol Sci 2009;59:3-21.
49. Beuers U, Nathanson MH, Isales CM, Boyer JL. Tauroursodeoxycholic acid stimulates hepatocellular exocytosis and mobilizes extracellular Caþþ mechanisms defective in cholestasis. J Clin Invest 1993;92: 2984-2993.
50. Dombrowski F, Stieger B, Beuers U. Tauroursodeoxycholic acid inserts the bile salt export pump into canalicular membranes of cholestatic rat liver. Lab Invest 2006;86:166-174.
51. Woo K, Dutta AK, Patel V, Kresge C, Feranchak AP. Fluid flow induces mechanosensitive ATP release, calcium signalling and Cl- transport in biliary epithelial cells through a PKCzeta-dependent pathway. J Physiol 2008;586:2779-2798.
52. Mizumori M, Ham M, Guth PH, Engel E, Kaunitz JD, Akiba Y. Intestinal alkaline phosphatase regulates protective surface microclimate pH in rat duodenum. J Physiol 2009;587:3651-3663.
53. Alvaro D, Benedetti A, Marucci L, Delle MM, Monterubbianesi R, Di CE, et al. The function of alkaline phosphatase in the liver: regulation of intrahepatic biliary epithelium secretory activities in the rat. HEPATOLOGY 2000;32:174-184.
54. 0-nucleotidase (CD73)-deficient mice. Pflugers Arch 2008;457:431-440.
55. Beuers U. Drug insight: mechanisms and sites of action of ursodeoxycholic acid in cholestasis. Nat Clin Pract Gastroenterol Hepatol 2006; 3:318-328.
56. Marzioni M, Francis H, Benedetti A, Ueno Y, Fava G, Venter J, et al. Ca2þ-dependent cytoprotective effects of ursodeoxycholic and tauroursodeoxycholic acid on the biliary epithelium in a rat model of cholestasis and loss of bile ducts. Am J Pathol 2006;168:398-409.
57. Wimmer R, Hohenester S, Pusl T, Denk GU, Rust C, Beuers U. Tauroursodeoxycholic acid exerts anticholestatic effects by a cooperative cPKC alpha-/PKA-dependent mechanism in rat liver. Gut 2008;57: 1448-1454.
58. Haussinger D, Kurz AK, Wettstein M, Graf D, Vom Dahl S, Schliess F. Involvement of integrins and Src in tauroursodeoxycholate-induced and swelling-induced choleresis. Gastroenterology 2003;124:1476-1487.
59. Nathanson MH, Burgstahler AD, Masyuk A, Larusso NF. Stimulation of ATP secretion in the liver by therapeutic bile acids. Biochem J 2001;358:1-5.
60. Fickert P, Wagner M, Marschall HU, Fuchsbichler A, Zollner G, Tsybrovskyy O, et al. 24-norUrsodeoxycholic acid is superior to ursodeoxycholic acid in the treatment of sclerosing cholangitis in Mdr2 (Abcb4) knockout mice. Gastroenterology 2006;130:465-481.
61. Halilbasic E, Fiorotto R, Fickert P, Marschall HU, Moustafa T, Spirli C, et al. Side chain structure determines unique physiologic and therapeutic properties of norursodeoxycholic acid in Mdr2-/- mice. HEPATOLOGY 2009;49:1972-1981.
62. Hofmann AF, Zakko SF, Lira M, Clerici C, Hagey LR, Lambert KK, et al. Novel biotransformation and physiological properties of norursodeoxycholic acid in humans. HEPATOLOGY 2005;42:1391-1398.
63. Salas JT, Banales JM, Sarvide S, Recalde S, Ferrer A, Uriarte I, et al. Ae2a,b-deficient mice develop antimitochondrial antibodies and other features resembling primary biliary cirrhosis. Gastroenterology 2008; 134:1482-1493.