Genetic cholestasis, causes and consequences for hepatobiliary transport

Liver International

Volumn 23, Issue 5, 2003, Pages 315-322

  Jansen, Peter L M ^a   Sturm, Ekkehard ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Benign recurrent intrahepatic cholestasis; Bile acid synthesis; Bile acids; Bile salt export pump; Farnesoid X receptor; Hepatobiliary transport; Intrahepatic cholestasis of pregnancy; Progressive familial intrahepatic cholestasis

Indexed keywords

BILE SALT; CARRIER PROTEIN; CHOLESTEROL; CYTOCHROME P450; GAMMA GLUTAMYLTRANSFERASE; GLYCOPROTEIN P; LIGAND; PHOSPHOLIPID; TAUROCHOLIC ACID; TRANSCRIPTION FACTOR; URSODEOXYCHOLIC ACID;

BASOLATERAL MEMBRANE; BILE FLOW; BILE SECRETION; BILIARY TRACT SURGERY; CHOLESTEROL METABOLISM; DISEASE CLASSIFICATION; ENTEROHEPATIC CIRCULATION; ENZYME ACTIVITY; GENE MUTATION; GENETIC CODE; GENETIC TRANSCRIPTION; HEPATOBILIARY SYSTEM; HUMAN; INHIBITION KINETICS; INTRAHEPATIC BILE DUCT; INTRAHEPATIC CHOLESTASIS; LIVER PROTECTION; LIVER SINUSOID; LIVER TRANSPLANTATION; PATHOGENESIS; PATHOPHYSIOLOGY; PROTEIN EXPRESSION; RELAPSE; REVIEW; SMALL INTESTINE ABSORPTION; TRANSPORT KINETICS;

EID: 0141891445     PISSN: 14783223     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1478-3231.2003.00856.x     Document Type: Review

References (63)

1. Kullak-Ublick G A, Stieger B, Hagenbuch B, Meier P J. Hepatic transport of bile salts. Semin Liver Dis 2000; 20(3): 273-92.
2. Stieger B, Hagenbuch B, Landmann L, Hochli M, Schroeder A, Meier P J. In situ localization of the hepatocytic Na+/taurocholate cotransporting polypeptide in rat liver. Gastroenterology 1994; 107(6): 1781-7.
3. Kullak-Ublick G A, Ismair M G, Stieger B, Landmann L, Huber R, Pizzagalli F, et al. Organic anion-transporting polypeptide B (OATP-B) and its functional comparison with three other OATPs of human liver. Gastroenterology 2001; 120(2): 525-33.
4. Gerloff T, Stieger B, Hagenbuch B, Madon J, Landmann L, Roth J, et al. The sister of P-glycoprotein represents the canalicular bile salt export pump of mammalian liver. J Biol Chem 1998; 273(16): 10046-50.
5. Green R M, Hoda F, Ward K L. Molecular cloning and characterization of the murine bile salt export pump. Gene 2000; 241(1): 117-23.
6. Lecureur V, Sun D, Hargrove P, Schuetz E G, Kim R B, Lan L B, et al. Cloning and expression of murine sister of P-glycoprotein reveals a more discriminating transporter than MDR1/P-glycoprotein. Mol Pharmacol 2000; 57(1): 24-35.
7. Wang R, Salem M, Yousef I M, Tuchweber B, Lam P, Childs S J, et al. Targeted inactivation of sister of P-glycoprotein gene (spgp) in mice results in nonprogressive but persistent intrahepatic cholestasis. Proc Natl Acad Sci USA 2001; 98(4): 2011-6.
8. Hirohashi T, Suzuki H, Takikawa H, Sugiyama Y. ATP-dependent transport of bile salts by rat multidrug resistance-associated protein 3 (Mrp3). J Biol Chem 2000; 275(4): 2905-10.
9. Zelcer N, Reid G, Wielinga P, Kuil A, van D H I, Schuetz J D, et al. Steroid and bile acid conjugates are substrates of human multidrug-resistance protein (MRP) 4 (ATP-binding cassette C4). Biochem J 2003; 371(Part 2): 361-7.
10. Ogawa K, Suzuki H, Hirohashi T, Ishikawa T, Meier PJ, Hirose K, et al. Characterization of inducible nature of MRP3 in rat liver. Am J Physiol Gastrointest Liver Physiol 2000; 278(3): G438-46.
11. Schuetz E G, Strom S, Yasuda K, Lecureur V, Assem M, Brimer C, et al. Disrupted bile acid homeostasis reveals an unexpected interaction among nuclear hormone receptors, transporters, and cytochrome P450. J Biol Chem 2001; 276(42): 39411-8.
12. Oelkers P, Kirby L C, Heubi J E, Dawson PA. Primary bile acid malabsorption caused by mutations in the ileal sodium-dependent bile acid transporter gene (SLC10A2). J Clin Invest 1997; 99(8): 1880-7.
13. Wong M H, Oelkers P, Dawson PA. Identification of a mutation in the ileal sodium-dependent bile acid transporter gene that abolishes transport activity. J Biol Chem 1995; 270(45): 27228-34.
14. Kipp H, Pichetshote N, Arias I M. Transporters on demand: intrahepatic pools of canalicular ATP binding cassette transporters in rat liver. J Biol Chem 2001; 276(10): 7218-24.
15. Ananthanarayanan M, Balasubramanian N, Makishima M, Mangelsdorf D J, Suchy F J. Human bile salt export pump promoter is transactivated by the farnesoid X receptor/bile acid receptor. J Biol Chem 2001; 276(31): 28857-65.
16. Lu T T, Makishima M, Repa J J, Schoonjans K, Kerr T A, Auwerx J, et al. Molecular basis for feedback regulation of bile acid synthesis by nuclear receptors. Mol Cell 2000; 6(3): 507-15.
17. Denson L A, Sturm E, Echevarria W, Zimmerman T L, Makishima M, Mangelsdorf D J, et al. The orphan nuclear receptor, shp, mediates bile acid-induced inhibition of the rat bile acid transporter, ntcp. Gastroenterology 2001; 121(1): 140-7.
18. Sinal C J, Tohkin M, Miyata M, Ward J M, Lambert G, Gonzalez F J. Targeted disruption of the nuclear receptor FXR/BAR impairs bile acid and lipid homeostasis. Cell 2000; 102(6): 731-44.
19. Gartung C, Ananthanarayanan M, Rahman M A, Schuele S, Nundy S, Soroka C J, et al. Down-regulation of expression and function of the rat liver Na+/bile acid cotransporter in extrahepatic cholestasis. Gastroenterology 1996; 110(1): 199-209.
20. Kerr T A, Saeki S, Schneider M, Schaefer K, Berdy S, Redder T, et al. Loss of nuclear receptor SHP impairs but does not eliminate negative feedback regulation of bile acid synthesis. Dev Cell 2002; 2(6): 713-20.
21. Holt J A, Luo G, Billin A N, Bisi J, McNeill Y Y, Kozarsky K F, et al. Definition of a novel growth factor-dependent signal cascade for the suppression of bile acid synthesis. Genes Dev 2003; 17: 1581-91.
22. Zollner G, Fickert P, Zenz R, Fuchsbichler A, Stumptner C, Kenner L, et al. Hepatobiliary transporter expression in percutaneous liver biopsies of patients with cholestatic liver diseases. Hepatology 2001; 33(3): 633-46.
23. Fickert P, Zollner G, Fuchsbichler A, Stumptner C, Weiglein A H, Lammert F, et al. Ursodeoxycholic acid aggravates bile infarcts in bile duct-ligated and Mdr2 knockout mice via disruption of cholangioles. Gastroenterology 2002; 123(4): 1238-51.
24. Inokuchi A, Hinoshita E, Iwamoto Y, Kohno K, Kuwano M, Uchiumi T. Enhanced expression of the human multidrug resistance protein 3 by bile salt in human enterocytes. A transcriptional control of a plausible bile acid transporter. J Biol Chem 2001; 276(50): 46822-9.
25. Bohan A, Chen S-W, Denson L A, Held M A, Boyer J L. TNF alpha dependent up-regulation of Lrh-1 and Mrp3(Abcc3) reduces liver injury in obstructive cholestasis. J Biol Chem 2003, in press.
26. Thompson R, Jansen P L. Genetic defects in hepatocanalicular transport. Semin Liver Dis 2000; 20(3): 365-72.
27. Bull L N, van Eijk M J, Pawlikowska L, DeYoung J A, Juijn J A, Liao M, et al. A gene encoding a P-type ATPase mutated in two forms of hereditary cholestasis. Nat Genet 1998; 18(3): 219-24.
28. De Vree J M, Jacquemin E, Sturm E, Cresteil D, Bosma P J, Aten J, et al. Mutations in the MDR3 gene cause progressive familial intrahepatic cholestasis. Proc Natl Acad Sci USA 1998; 95(1): 282-7.
29. Jacquemin E, Cresteil D, Manouvrier S, Boute O, Hadchouel M. Heterozygous non-sense mutation of the MDR3 gene in familial intrahepatic cholestasis of pregnancy. Lancet 1999; 353(9148): 210-1.
30. Rosmorduc O, Hermelin B, Poupon R. MDR3 gene defect in adults with symptomatic intrahepatic and gallbladder cholesterol cholelithiasis. Gastroenterology 2001; 120(6): 1459-67.
31. Zielenski J, Tsui L C. Cystic fibrosis: genotypic and phenotypic variations. Annu Rev Genet 1995; 29: 777-807.
32. Mosser J, Lutz Y, Stoeckel M E, Sarde C O, Kretz C, Douar A M, et al. The gene responsible for adrenoleukodystrophy encodes a peroxisomal membrane protein. Hum Mol Genet 1994; 3(2): 265-71.
33. Paulusma C C, Kool M, Bosma P J, Scheffer G L, ter Borg F, Scheper R J, et al. A mutation in the human canalicular multispecific organic anion transporter gene causes the Dubin-Johnson syndrome. Hepatology 1997; 25(6): 1539-42.
34. Kartenbeck J, Leuschner U, Mayer R, Keppler D. Absence of the canalicular isoform of the MRP gene-encoded conjugate export pump from the hepatocytes in Dubin-Johnson syndrome. Hepatology 1996; 23(5): 1061-6.
35. Bull L N, Carlton V E, Stricker N L, Baharloo S, DeYoung J A, Freimer N B, et al. Genetic and morphological findings in progressive familial intrahepatic cholestasis (Byler disease [PFIC-1] and Byler syndrome): evidence for heterogeneity. Hepatology 1997; 26(1): 155-64.
36. Alonso E M, Snover D C, Montag A, Freese D K, Whitington P F. Histologic pathology of the liver in progressive familial intrahepatic cholestasis. J Pediatr Gastroenterol Nutr 1994; 18(2): 128-33.
37. Bourke B, Goggin N, Walsh D, Kennedy S, Setchell K D, Drumm B. Byler-like familial cholestasis in an extended kindred. Arch Dis Child 1996; 75(3): 223-7.
38. Arnell H, Nemeth A, Anneren G, Dahl N. Progressive familial intrahepatic cholestasis (PFIC): evidence for genetic heterogeneity by exclusion of linkage to chromosome 18q21-q22. Hum Genet 1997; 100(3-4): 378-81.
39. Naveh Y, Bassan L, Rosenthal E, Berkowitz D, Jaffe M, Mandel H, et al. Progressive familial intrahepatic cholestasis among the Arab population in Israel. J Pediatr Gastroenterol Nutr 1997; 24(5): 548-54.
40. Kagalwalla A F, Al Amir A R, Khalifa A, Sylven M, Al Ajaji S, Kagalwalla Y A. Progressive familial intrahepatic cholestasis (Byler's disease) in Arab children. Ann Trop Paediatr 1995; 15(4): 321-7.
41. Floreani A, Molaro M, Mottes M, Sangalli A, Baragiotta A, Roda A, et al. Autosomal dominant benign recurrent intrahepatic cholestasis (BRIC) unlinked to 18q21 and 2q24. Am J Med Genet 2000; 95(5): 450-3.
42. Brenard R, Geubel A P, Benhamou J P. Benign recurrent intrahepatic cholestasis. A report of 26 cases. J Clin Gastroenterol 1989; 11(5): 546-51.
43. Cancado E L, Leitao R M, Carrilho F J, Laudanna A A. Unexpected clinical remission of cholestasis after rifampicin therapy in patients with normal or slightly increased levels of gamma-glutamyl transpeptidase. Am J Gastroenterol 1998; 93(9): 1510-7.
44. Balsells F, Wyllie R, Steffen R, Kay M. Benign recurrent intrahepatic cholestasis: improvement of pruritus and shortening of the symptomatic phase with rifampin therapy: a case report. Clin Pediatr (Phila) 1997; 36(8): 483-5.
45. Strautnieks S S, Bull L N, Knisely A S, Kocoshis S A, Dahl N, Arnell H, et al. A gene encoding a liver-specific ABC transporter is mutated in progressive familial intrahepatic cholestasis. Nat Genet 1998; 20(3): 233-8.
46. Jansen P L, Strautnieks S S, Jacquemin E, Hadchouel M, Sokal E M, Hooiveld G J, et al. Hepatocanalicular bile salt export pump deficiency in patients with progressive familial intrahepatic cholestasis. Gastroenterology 1999; 117(6): 1370-9.
47. Deleuze J F, Jacquemin E, Dubuisson C, Cresteil D, Dumont M, Erlinger S, et al. Defect of multidrug-resistance 3 gene expression in a subtype of progressive familial intrahepatic cholestasis. Hepatology 1996; 23(4): 904-8.
48. Jacquemin E, De Vree J M, Cresteil D, Sokal E M, Sturm E, Dumont M, et al. The wide spectrum of multidrug resistance 3 deficiency: from neonatal cholestasis to cirrhosis of adulthood. Gastroenterology 2001; 120(6): 1448-58.
49. Jacquemin E, Hermans D, Myara A, Habes D, Debray D, Hadchouel M, et al. Ursodeoxycholic acid therapy in pediatric patients with progressive familial intrahepatic cholestasis. Hepatology 1997; 25(3): 519-23.
50. Jacquemin E. Progressive familial intrahepatic cholestasis. J Gastroenterol Hepatol 1999; 14(6): 594-9.
51. Emond J C, Whitington P F. Selective surgical management of progressive familial intrahepatic cholestasis (Byler's disease). J Pediatr Surg 1995; 30(12): 1635-41.
52. Melter M, Rodeck B, Kardorff R, Hoyer P F, Petersen C, Ballauff A, et al. Progressive familial intrahepatic cholestasis: partial biliary diversion normalizes serum lipids and improves growth in noncirrhotic patients. Am J Gastroenterol 2000; 95(12): 3522-8.
53. Rebhandl W, Felberbauer F X, Turnbull J, Paya K, Barcik U, Huber W D, et al. Biliary diversion by use of the appendix (cholecystoappendicostomy) in progressive familial intrahepatic cholestasis. J Pediatr Gastroenterol Nutr 1999; 28(2): 217-9.
54. Whitington P F, Whitington G L. Partial external diversion of bile for the treatment of intractable pruritus associated with intrahepatic cholestasis. Gastroenterology 1988; 95(1): 130-6.
55. Soubrane O, Gauthier F, Devictor D, Bernard O, Valayer J, Houssin D, et al. Orthotopic liver transplantation for Byler disease. Transplantation 1990; 50(5): 804-6.
56. Dixon P H, Weerasekera N, Linton K J, Donaldson O, Chambers J, Egginton E, et al. Heterozygous MDR3 missense mutation associated with intrahepatic cholestasis of pregnancy: evidence for a defect in protein trafficking. Hum Mol Genet 2000; 9(8): 1209-17.
57. de Pagter A G, Berge Henegouwen G P, Bokkel Huinink J A, Brandt K H. Familial benign recurrent intrahepatic cholestasis. Interrelation with intrahepatic cholestasis of pregnancy and from oral contraceptives. Gastroenterology 1976; 71(2): 202-7.
58. Mazzella G, Nicola R, Francesco A, Patrizia S, Luciano B, Anna M, et al. Ursodeoxycholic acid administration in patients with cholestasis of pregnancy: effects on primary bile acids in babies and mothers. Hepatology 2001; 33(3): 504-8.
59. Palma J, Reyes H, Ribalta J, Hernandez I, Sandoval L, Almuna R, et al. Ursodeoxycholic acid in the treatment of cholestasis of pregnancy: a randomized, double-blind study controlled with placebo. J Hepatol 1997; 27(6): 1022-8.
60. Aagenaes O. Hereditary cholestasis with lymphoedema (Aagenaes syndrome, cholestasis-lymphoedema syndrome). New cases and follow-up from infancy to adult age. Scand J Gastroenterol 1998; 33(4): 335-45.
61. Bull L N, Roche E, Song E J, Pedersen J, Knisely A S, Der Hagen C B, et al. Mapping of the locus for cholestasis-lymphedema syndrome (Aagenaes syndrome) to a 6.6-cM interval on chromosome 15q. Am J Hum Genet 2000; 67(4): 994-9.
62. Fruhwirth M, Janecke A R, Muller T, Carlton V E, Kronenberg F, Offner F, et al. Evidence for genetic heterogeneity in lymphedema-cholestasis syndrome. J Pediatr 2003; 142(4): 441-7.
63. Carlton V E, Harris B Z, Puffenberger E G, Batta A K, Knisely A S, Robinson D L, et al. Complex inheritance of familial hypercholanemia with associated mutations in TJP2 and BAAT. Nat Genet 2003; 34(1): 91-6.