Morphological and functional heterogeneity of the mouse intrahepatic biliary epithelium

Laboratory Investigation

Volumn 89, Issue 4, 2009, Pages 456-469

  Glaser, Shannon S ^a   Gaudio, Eugenio ^b   Rao, Arundhati ^a   Pierce, Lisa M ^a   Onori, Paolo ^c   Franchitto, Antonio ^b   Francis, Heather L ^a   Dostal, David E ^a,d   Venter, Julie K ^a   Demorrow, Sharon ^a   Mancinelli, Romina ^a,b   Carpino, Guido ^e   Alvaro, Domenico ^b   Kopriva, Shelley E ^d   Savage, Jennifer M ^a   Alpini, Gianfranco D ^a,d  

^a SCOTT AND WHITE MEMORIAL HOSPITAL   (United States)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF L'AQUILA   (Italy)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

^e UNIVERSITY OF ROME FORO ITALICO   (Italy)

Author keywords

Bicarbonate secretion; cAMP; Cholangiocytes; Secretin; secretin receptor

Indexed keywords

CELL MARKER; CHLORIDE; CYCLIC AMP; CYTOKERATIN 19; EOSIN; HEMATOXYLIN; HORMONE RECEPTOR; PARAFFIN; SECRETIN; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANION EXCHANGE; ARTICLE; BILE DUCT LIGATION; CELL CYCLE; CELL HETEROGENEITY; CELL ISOLATION; CELL PROLIFERATION; CELL SELECTION; CELL SIZE; CELL STRUCTURE; CELLULAR DISTRIBUTION; CHLORIDE TRANSPORT; CONTROLLED STUDY; DISEASE MODEL; DISSECTION; EPITHELIUM; IMMUNOFLUORESCENCE; INTRAHEPATIC BILE DUCT; LIVER; MALE; MORPHOMETRICS; MOUSE; NONHUMAN; ORGAN SIZE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STAINING; TISSUE SECTION; WESTERN BLOTTING;

ANIMALS; ANTIGENS, DIFFERENTIATION; BILE DUCTS, INTRAHEPATIC; CELL CYCLE; CELL PROLIFERATION; CELL SIZE; CHOLESTASIS, INTRAHEPATIC; EPITHELIUM; MALE; MICE; MICE, INBRED C57BL;

EID: 63449090256     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2009.6     Document Type: Article

References (54)

1. Alpini G, Prall RT, LaRusso NF. The pathobiology of biliary epithelia. In: I M Arias, J L Boyer, F V Chisari, N Fausto, W Jakoby, D Schachter, and D A Shafritz D (eds). The Liver; Biology & Pathobiology, 4th edn. Lippincott Williams & Wilkins: Philadelphia, PA, 2001, pp 421-435.
2. Alvaro D, Mancino MG, Glaser S, et al. Proliferating cholangiocytes: a neuroendocrine compartment in the diseased liver. Gastroenterology 2007;132:415-431.
3. Lazaridis KN, Strazzabosco M, LaRusso NF. The cholangiopathies: disorders of biliary epithelia. Gastroenterology 2004;127:1565-1577.
4. Alpini G, Lenzi R, Sarkozi L, et al. Biliary physiology in rats with bile ductular cell hyperplasia. Evidence for a secretory function of proliferated bile ductules. J Clin Invest 1988;81:569-578.
5. Kanno N, LeSage G, Glaser S, et al. Functional heterogeneity of the intrahepatic biliary epithelium. Hepatology 2000;31:555-561.
6. Ludwig J. New concepts in biliary cirrhosis. Sem Liver Dis 1987;7: 293-301.
7. Alpini G, Roberts S, Kuntz SM, et al. Morphological, molecular, and functional heterogeneity of cholangiocytes from normal rat liver. Gastroenterology 1996;110:1636-1643.
8. Benedetti A, Bassotti C, Rapino K, et al. A morphometric study of the epithelium lining the rat intrahepatic biliary tree. J Hepatol 1996;24:335-342.
9. Schaffner F, Popper H. Electron microscopic studies of normal and proliferated bile ductules. Am J Pathol 1961;38:393-410.
10. LeSage G, Benedetti A, Glaser S, et al. Acute carbon tetrachloride feeding selectively damages large, but not small, cholangiocytes from normal rat liver. Hepatology 1999;29:307-319.
11. Kanno N, LeSage G, Glaser S, et al. Regulation of cholangiocyte bicarbonate secretion. Am J Physiol Gastrointest Liver Physiol 2001;281:G612-G625.
12. Neil DA, Hubscher SG. Histologic and biochemical changes during the evolution of chronic rejection of liver allografts. Hepatology 2002;35:639-651.
13. Marzioni M, Glaser SS, Francis H, et al. Functional heterogeneity of cholangiocytes. Semin Liver Dis 2002;22:227-240.
14. Alpini G, Glaser S, Robertson W, et al. Large but not small intrahepatic bile ducts are involved in secretin-regulated ductal bile secretion. Am J Physiol Gastroint Liver Physiol 1997;272:G1064-G1074.
15. Alpini G, Glaser S, Ueno Y, et al. Heterogeneity of the proliferative capacity of rat cholangiocytes after bile duct ligation. Am J Physiol Gastrointest Liver Physiol 1998;274:G767-G775.
16. Alpini G, Ulrich C, Roberts S, et al. Molecular and functional heterogeneity of cholangiocytes from rat liver after bile duct ligation. Am J Physiol Gastrointest Liver Physiol 1997;272: G289-G297.
17. LeSage G, Glaser S, Ueno Y, et al. Regression of cholangiocyte proliferation after cessation of ANIT feeding is coupled with increased apoptosis. Am J Physiol Gastrointest Liver Physiol 2001;281: G182-G190.
18. LeSage G, Glaser SS, Marucci L, et al. Acute carbon tetrachloride feeding induces damage of large but not small cholangiocytes from BDL rat liver. Am J Physiol Gastrointest Liver Physiol 1999;276:G1289-G1301.
19. 3/CaMK I/CREB pathway. Am J Physiol Cell Physiol 2008;295:C499-C513.
20. Steiner JW, Carruthers JS. Studies on the fine structure of the terminal branches of the biliary tree. I. The morphology of normal bile canaliculi, bile preductules (ducts of Hering) and bile ductules. Am J Pathol 1961;38:639-661.
21. Nathanson MH, Boyer JL. Mechanisms and regulation of bile secretion. Hepatology 1991;14:551-566.
22. Alpini G, Glaser S, Robertson W, et al. Bile acids stimulate proliferative and secretory events in large but not small cholangiocytes. Am J Physiol Gastroint Liver Physiol 1997;273:G518-G529.
23. Alpini G, Lenzi R, Zhai W-R, et al. Bile secretory function of intrahepatic biliary epithelium in the rat. Am J Physiol Gastroint Liver Physiol 1989;257:G124-G133.
24. Alvaro D, Cho WKC, Mennone A, et al. Effect of secretin on intracellular pH regulation in isolated rat bile duct epithelial cells. J Clin Invest 1993;92:1314-1325.
25. Alvaro D, Alpini G, Jezequel AM, et al. Role and mechanisms of action of acetylcholine in the regulation of rat cholangiocyte secretory functions. J Clin Invest 1997;100:1349-1362.
26. Glaser S, Rodgers RE, Phinizy JL, et al. Gastrin inhibits secretin-induced ductal secretion by interaction with specific receptors on rat cholangiocytes. Am J Physiol Gastrointest Liver Physiol 1997;273:G1061-G1070.
27. Glaser S, Alvaro D, Roskams T, et al. Dopaminergic inhibition of secretin-stimulated choleresis by increased PKC-γ expression and decrease of PKA activity. Am J Physiol Gastrointest Liver Physiol 2003;284:G683-G694.
28. LeSage G, Alvaro D, Benedetti A, et al. Cholinergic system modulates growth, apoptosis, and secretion of cholangiocytes from bile ductligated rats. Gastroenterology 1999;117:191-199.
29. 2+- and PKC-dependent stimulation of cAMP synthesis. Hepatology 2004;40:1116-1127.
30. LeSage G, Marucci L, Alvaro D, et al. Insulin inhibits secretin-induced ductal secretion by activation of PKC alpha and inhibition of PKA activity. Hepatology 2002;36:641-651.
31. LeSage G, Glaser S, Gubba S, et al. Regrowth of the rat biliary tree after 70% partial hepatectomy is coupled to increased secretin-induced ductal bile secretion. Gastroenterology 1996;111: 1633-1644.
32. 2+)-, and protein kinase C alpha-dependent mechanisms. Hepatology 2000;32:17-25.
33. Tietz PS, Alpini G, Pham LD, et al. Somatostatin inhibits secretininduced ductal hypercholeresis and exocytosis by cholangiocytes. Am J Physiol Gastrointest Liver Physiol 1995;269:G110-G118.
34. Miyoshi H, Rust C, Guicciardi ME, et al. NF-kappaB is activated in cholestasis and functions to reduce liver injury. Am J Pathol 2001;158:967-975.
35. Glaser S, Ueno Y, DeMorrow S, et al. Knockout of alpha-calcitonin gene-related peptide reduces cholangiocyte proliferation in bile duct ligated mice. Lab Invest 2007;87:914-926.
36. Ishii M, Vroman B, LaRusso NF. Isolation and morphological characterization of bile duct epithelial cells from normal rat liver. Gastroenterology 1989;97:1236-1247.
37. Teutsch HF. Improved method for the histochemical demonstration of glucose-6-phosphatase activity. Histochemistry 1978;57:107-117.
38. Kalejta RF, Shenk T, Beavis AJ. Use of a membrane-localized green fluorescent protein allows simultaneous identification of transfected cells and cell cycle analysis by flow cytometry. Cytometry 1997;29: 286-291.
39. Kato A, Gores GJ, LaRusso NF. Secretin stimulates exocytosis in isolated bile duct epithelial cells by a cyclic AMP-mediated mechanism. J Biol Chem 1992;267:15523-15529.
40. - channels in bile duct epithelial cells through a cAMP-dependent mechanism. Am J Physiol Gastroint Liver Physiol 1994;266:G731-G736.
41. Rapundalo ST, Solaro RJ, Kranias EG. Inotropic responses to isoproterenol and phosphodiesterase inhibitors in intact guinea pig hearts: comparison of cyclic AMP levels and phosphorylation of sarcoplasmic reticulum and myofibrillar proteins. Circ Res 1989;64: 104-111.
42. Servetnyk Z, Krjukova J, Gaston B, et al. Activation of chloride transport in CF airway epithelial cell lines and primary CF nasal epithelial cells by S-nitrosoglutathione. Respir Res 2006;7:124.
43. Furuya W, Tarshis T, Law FY, et al. Transmembrane effects of intracellular chloride on the inhibitory potency of extracellular H2DIDS. Evidence for two conformations of the transport site of the human erythrocyte anion exchange protein. J Gen Physiol 1984;83:657-681.
44. Fiorotto R, Spirli C, Fabris L, et al. Ursodeoxycholic acid stimulates cholangiocyte fluid secretion in mice via CFTR-dependent ATP secretion. Gastroenterology 2007;133:1603-1613.
45. Alpini G, Glaser S, Ueno Y, et al. Bile acid feeding induces cholangiocyte proliferation and secretion: evidence for bile acidregulated ductal secretion. Gastroenterology 1999;116:179-186.
46. Ueno Y, Alpini G, Yahagi K, et al. Evaluation of differential gene expression by microarray analysis in small and large cholangiocytes isolated from normal mice. Liver Int 2003;23:449-459.
47. Trauner M, Fickert P, Wagner M. MDR3 (ABCB4) defects: a paradigm for the genetics of adult cholestatic syndromes. Semin Liver Dis 2007;27:77-98.
48. Tsuruoka S, Takeda M, Yoshitomi K, et al. Cellular heterogeneity of ammonium ion transport across the basolateral membrane of the hamster medullary thick ascending limb of Henle's loop. J Clin Invest 1993;92:1881-1888.
49. + transport across the basolateral cell membrane. Am J Physiol Renal Physiol 1986;250:F430-F440.
50. Knickelbein RG, Aronson PS, Dobbins JW. Membrane distribution of sodium-hydrogen and chloride-bicarbonate exchangers in crypt and villus cell membranes from rabbit ileum. J Clin Invest 1988;82: 2158-2163.
51. Fromm M, Hegel U. Segmental heterogeneity of epithelial transport in rat large intestine. Pflugers Arch 1978;378:71-83.
52. Katz N, Jungermann K. Metabolic heterogeneity of the liver. In: Tavoloni N, Berk PD (eds). Hepatic Transport and Bile Secretion: Physiology and Pathophysiology. Raven Press: New York, 1993, pp 55-70.
53. Groothuis GM, Meijer DK. Hepatocyte heterogeneity in bile formation and hepatobiliary transport of drugs. Enzyme 1992;46: 94-138.
54. Nielsen S, Smith BL, Christensen EI, et al. CHIP28 water channels are localized in constitutively water-permeable segments of the nephron. J Cell Biol 1993;120:371-383.