Molecular diagnosis of hereditary canalicular cholestasis and familial hyperbilirubinemias

1. van Mil SW, Houwen RH, Klomp LW. Genetics of familial intrahepatic cholestasis syndromes. J Med Genet 2005; 42: 449–463.

2. Carlton VE, Pawlikowska L, Bull LN. Molecular basis of intrahepatic cholestasis. Ann Med 2004; 36: 606–617.

3. Chowdhury JR, Wolkoff AW, Chowdhury NR, Arias IM. Hereditary jaundice and disorders of bilirubin metabolism. In: Scriver CR, Beaudet AL, Sly WS, Valle D, eds. The metabolic & molecular bases of inherited disease. 8 ed. New York: McGraw Hill 2001; 3063–3101.

4. Elferink RP, Groen AK. The mechanism of biliary lipid secretion and its defects. Gastroenterol Clin North Am 1999; 28: 59–74, vi.

5. Jansen PL, Muller M. Genetic cholestasis: lessons from the molecular physiology of bile formation. Can J Gastroenterol 2000; 14: 233–238.

6. Thompson R, Strautnieks S. BSEP: function and role in progressive familial intrahepatic cholestasis. Semin Liver Dis 2001; 21: 545–550.

7. Kalicinski PJ, Ismail H, Jankowska I, et al. Surgical treatment of progressive familial intrahepatic cholestasis: comparison of partial external biliary diversion and ileal bypass. Eur J Pediatr Surg 2003; 13: 307–311.

8. Clayton RJ, Iber FL, Ruebner BH, McKusick VA. Byler disease. Fatal familial intrahepatic cholestasis in an Amish kindred. Am J Dis Child 1969; 117: 112–124.

9. Bull LN, van Eijk MJ, Pawlikowska L, et al. A gene encoding a P-type ATPase mutated in two forms of hereditary cholestasis. Nat Genet 1998; 18: 219–224.

10. Klomp LW, Vargas JC, van Mil SW, et al. Characterization of mutations in ATP8B1 associated with hereditary cholestasis. Hepatology 2004; 40: 27–38.

11. Ujhazy P, Ortiz D, Misra S, et al. Familial intrahepatic cholestasis 1: studies of localization and function. Hepatology 2001; 34: 768–775.

12. Paulusma CC, Groen A, Kunne C, et al. Atp8b1 deficiency in mice reduces resistance of the canalicular membrane to hydrophobic bile salts and impairs bile salt transport. Hepatology 2006; 44: 195–204.

13. van Mil SW, Klomp LW, Bull LN, Houwen RH. FIC1 disease: a spectrum of intrahepatic cholestatic disorders. Semin Liver Dis 2001; 21: 535–544.

14. Strautnieks SS, Bull LN, Knisely AS, et al. A gene encoding a liver-specific ABC transporter is mutated in progressive familial intrahepatic cholestasis. Nat Genet 1998; 20: 233–238.

15. Gerloff T, Stieger B, Hagenbuch B, et al. The sister of P-glycoprotein represents the canalicular bile salt export pump of mammalian liver. J Biol Chem 1998; 273: 10046–10050.

16. Jansen PL, Muller M. The molecular genetics of familial intrahepatic cholestasis. Gut 2000; 47: 1–5.

17. Ananthanarayanan M, Balasubramanian N, Makishima M, Mangelsdorf DJ, Suchy FJ. Human bile salt export pump promoter is transactivated by the farnesoid X receptor/bile acid receptor. J Biol Chem 2001; 276: 28857–28865.

18. Davis RA, Miyake JH, Hui TY, Spann NJ. Regulation of cholesterol-7alpha-hydroxylase: BAREly missing a SHP. J Lipid Res 2002; 43: 533–543.

19. Knisely AS, Strautnieks S, Meier Y, et al. Hepatocellular carcinoma in ten children under five years old with bile salt export pump deficiency. Hepatology 2006; 44: 478–486.

20. Scheimann AO, Strautnieks SS, Knisely AS, Byrne JA, Thompson RJ, Finegold MJ. Mutations in bile salt export pump (ABCB11) in two children with progressive familial intrahepatic cholestasis and cholangiocarcinoma. J Pediatr 2007; 150: 556–559.

21. Strautnieks SS, Byrne JA, Pawlikowska L, et al. Severe bile salt export pump deficiency: 82 different ABCB11 mutations in 109 families. Gastroenterology 2008; 134: 1203–1214.

22. de Vree JM, Jacquemin E, Sturm E, et al. Mutations in the MDR3 gene cause progressive familial intrahepatic cholestasis. Proc Natl Acad Sci U S A 1998; 95: 282–287.

23. Smit JJ, Schinkel AH, Oude Elferink RP, et al. Homozygous disruption of the murine mdr2 P–glycoprotein gene leads to a complete absence of phospholipid from bile and to liver disease. Cell 1993; 75: 451–462.

24. Mauad TH, van Nieuwkerk CM, Dingemans KP, et al. Mice with homozygous disruption of the mdr2 P–glycoprotein gene. A novel animal model for studies of nonsuppurative inflammatory cholangitis and hepatocarcinogenesis. Am J Pathol 1994; 145: 1237–1245.

25. Smith AJ, de Vree JM, Ottenhoff R, Oude Elferink RP, Schinkel AH, Borst P. Hepatocyte-specific expression of the human MDR3 P-glycoprotein gene restores the biliary phosphatidylcholine excretion absent in Mdr2 (-/-) mice. Hepatology 1998; 28: 530–536.

26. Fickert P, Fuchsbichler A, Wagner M, et al. Regurgitation of bile acids from leaky bile ducts causes sclerosing cholangitis in Mdr2 (Abcb4) knockout mice. Gastroenterology 2004; 127: 261–274.

27. Elferink RP, Ottenhoff R, van Marle J, Frijters CM, Smith AJ, Groen AK. Class III P-glycoproteins mediate the formation of lipoprotein X in the mouse. J Clin Invest 1998; 102: 1749–1757.

28. Oude Elferink RP, Paulusma CC. Function and patho­physiological importance of ABCB4 (MDR3 P-glycoprotein). Pflugers Arch 2007; 453: 601–610.

29. Jacquemin E, De Vree JM, Cresteil D, et al. The wide spectrum of multidrug resistance 3 deficiency: from neonatal cholestasis to cirrhosis of adulthood. Gastroenterology 2001; 120: 1448–1458.

30. van Ooteghem NA, Klomp LW, van Berge-Henegouwen GP, Houwen RH. Benign recurrent intrahepatic cholestasis progressing to progressive familial intrahepatic cholestasis: low GGT cholestasis is a clinical continuum. J Hepatol 2002; 36: 439–443.

31. Floreani A, Molaro M, Mottes M, et al. Autosomal dominant benign recurrent intrahepatic cholestasis (BRIC) unlinked to 18q21 and 2q24. Am J Med Genet 2000; 95: 450–453.

32. van Mil SW, van der Woerd WL, van der Brugge G, et al. Benign recurrent intrahepatic cholestasis type 2 is caused by mutations in ABCB11. Gastroenterology 2004; 127: 379–384.

33. Stapelbroek JM, van Erpecum KJ, Klomp LW, et al. Nasobiliary drainage induces long–lasting remission in benign recurrent intrahepatic cholestasis. Hepatology 2006; 43: 51–53.

34. Lucena JF, Herrero JI, Quiroga J, et al. A multidrug resistance 3 gene mutation causing cholelithiasis, cholestasis of pregnancy, and adulthood biliary cirrhosis. Gastroenterology 2003; 124: 1037–1042.

35. Rosmorduc O, Hermelin B, Poupon R. Mdr3 gene defect in adults with symptomatic intrahepatic and gallbladder cholesterol cholelithiasis. Gastroenterology 2001; 120: 1459–1467.

36. Rosmorduc O, Hermelin B, Boelle PY, Parc R, Taboury J, Poupon R. ABCB4 gene mutation–associated cholelithiasis in adults. Gastroenterology 2003; 125: 452–459.

37. Ganne-Carrie N, Baussan C, Grando V, Gaudelus J, Cresteil D, Jacquemin E. Progressive familial intrahepatic cholestasis type 3 revealed by oral contraceptive pills. J Hepatol 2003; 38: 693–694.

38. Rosmorduc O, Poupon R. Low phospholipid associated cholelithiasis: association with mutation in the MDR3/ABCB4 gene. Orphanet J Rare Dis 2007; 2: 29.

39. Lammert F, Marschall HU, Glantz A, Matern S. Intrahepatic cholestasis of pregnancy: molecular pathogenesis, diagnosis and management. J Hepatol 2000; 33: 1012–1021.

40. Berkane N, Cocheton JJ, Brehier D, et al. Ursodeoxycholic acid in intrahepatic cholestasis of pregnancy. A retrospective study of 19 cases. Acta Obstet Gynecol Scand 2000; 79: 941–946.

41. Glantz A, Marschall HU, Lammert F, Mattsson LA. Intrahepatic cholestasis of pregnancy: a randomized controlled trial comparing dexamethasone and ursodeoxycholic acid. Hepatology 2005; 42: 1399–1405.

42. Kondrackiene J, Beuers U, Kupcinskas L. Efficacy and safety of ursodeoxycholic acid versus cholestyramine in intrahepatic cholestasis of pregnancy. Gastroenterology 2005; 129: 894–901.

43. Zapata R, Sandoval L, Palma J, et al. Ursodeoxycholic acid in the treatment of intrahepatic cholestasis of pregnancy. A 12-year experience. Liver Int 2005; 25: 548–554.

44. Binder T, Salaj P, Zima T, Vitek L. Randomized prospective comparative study of ursodeoxycholic acid and S-adenosyl-L--methionine in the treatment of intrahepatic cholestasis of pregnancy. J Perinat Med 2006; 34: 383–391.

45. Dixon PH, Weerasekera N, Linton KJ, et al. Heterozygous MDR3 missense mutation associated with intrahepatic cholestasis of pregnancy: evidence for a defect in protein trafficking. Hum Mol Genet 2000; 9: 1209–1217.

46. Gendrot C, Bacq Y, Brechot MC, Lansac J, Andres C. A second heterozygous MDR3 nonsense mutation associated with intrahepatic cholestasis of pregnancy. J Med Genet 2003; 40: e32.

47. Floreani A, Carderi I, Paternoster D, et al. Intrahepatic cholestasis of pregnancy: three novel MDR3 gene mutations. Aliment Pharmacol Ther 2006; 23: 1649–1653.

48. Mullenbach R, Linton KJ, Wiltshire S, et al. ABCB4 gene sequence variation in women with intrahepatic cholestasis of pregnancy. J Med Genet 2003; 40: e70.

49. Painter JN, Savander M, Ropponen A, et al. Sequence variation in the ATP8B1 gene and intrahepatic cholestasis of pregnancy. Eur J Hum Genet 2005; 13: 435–439.

50. Paulusma CC, Oude Elferink RP. The canalicular multispecific organic anion transporter and conjugated hyperbilirubinemia in rat and man. J Mol Med 1997; 75: 420–428.

51. Stockel B, Konig J, Nies AT, Cui Y, Brom M, Keppler D. Characterization of the 5’-flanking region of the human multidrug resistance protein 2 (MRP2) gene and its regulation in comparison withthe multidrug resistance protein 3 (MRP3) gene. Eur J Biochem 2000; 267: 1347–1358.

52. Dubin IN. Chronic idiopathic jaundice; a review of fifty cases. Am J Med 1958; 24: 268–292.

53. Shani M, Seligsohn U, Gilon E, Sheba C, Adam A. Dubin-Johnson syndrome in Israel. I. Clinical, laboratory, and genetic aspects of 101 cases. Q J Med 1970; 39: 549–567.

54. Wolkoff AW, Cohen LE, Arias IM. Inheritance of the Dubin–Johnson syndrome. N Engl J Med 1973; 288: 113–117.

55. Erlinger S, Dhumeaux D, Desjeux JF, Benhamou JP. Hepatic handling of unconjugated dyes in the Dubin-Johnson syndrome. Gastroenterology 1973; 64: 106–110.

56. Bar-Meir S, Baron J, Seligson U, Gottesfeld F, Levy R, Gilat T. 99mTc–HIDA cholescintigraphy in Dubin-Johnson and Rotor syn­dromes. Radiology 1982; 142: 743–746.

57. Bujanover Y, Bar-Meir S, Hayman I, Baron J. 99mTc–HIDA cholescintigraphy in children with Dubin-Johnson syndrome. J Pediatr Gastroenterol Nutr 1983; 2: 311–312.

58. Artiko V, Obradovic VV, Kostic K, Petrovic N, Markovic S, Popovic O. Cholescintigraphy in Dubin-Johnson syndrome. Nucl Med Rev Cent East Eur 1999; 2: 83–84.

59. Arias IM. Studies of chronic familial non-hemolytic jaundice with conjugated bilirubin in the serum with and without an unidentified pigment in the liver cells. Am J Med 1961; 31: 510–518.

60. Shieh CC, Chang MH, Chen CL. Dubin-Johnson syndrome presenting with neonatal cholestasis. Arch Dis Child 1990; 65: 898–899.

61. 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: 1061–1066.

62. Mor-Cohen R, Zivelin A, Rosenberg N, Shani M, Muallem S, Seligsohn U. Identification and functional analysis of two novel mutations in the multidrug resistance protein 2 gene in Israeli patients with Dubin-Johnson syndrome. J Biol Chem 2001; 276: 36923–36930.

63. Wolkoff AW, Wolpert E, Pascasio FN, Arias IM. Rotor’s syndrome. A distinct inheritable pathophysiologic entity. Am J Med 1976; 60: 173–179.

64. Wolpert E, Pascasio FM, Wolkoff AW, Arias IM. Abnormal sulfobromophthalein metabolism in Rotor’s syndrome and obligate heterozygotes. N Engl J Med 1977; 296: 1099–1101.

65. Fretzayas AM, Garoufi AI, Moutsouris CX, Karpathios TE. Cholescintigraphy in the diagnosis of Rotor syndrome. J Nucl Med 1994; 35: 1048–1050.

66. Fretzayas AM, Stavrinadis CS, Koukoutsakis PM, Sinaniotis CA. Diagnostic approach of Rotor syndrome with chole­scintigraphy. Clin Nucl Med 1997; 22: 635–636.

67. Hrebicek M, Jirasek T, Hartmannova H, et al. Rotor-type hyperbilirubinaemia has no defect in the canalicular bilirubin export pump. Liver Int 2007; 27: 485–491.

68. Cebecauerova D, Jirasek T, Budisova L, et al. Dual hereditary jaundice: simultaneous occurrence of mutations causing Gilbert’s and Dubin-Johnson syndrome. Gastroenterology 2005; 129: 315–320.

69. Byrne JA, Strautnieks SS, Ihrke G, et al. Missense mutations and single nucleotide polymorphisms in ABCB11 impair bile salt export pump processing and function or disrupt pre-messenger RNA splicing. Hepatology 2009; 49: 553–567.

70. Treepongkaruna S, Gaensan A, Pienvichit P, et al. Novel ABCB11 mutations in a Thai infant with progressive familial intrahepatic cholestasis. World J Gastroenterol 2009; 15: 4339–4342.

71. Lang C, Meier Y, Stieger B, et al. Mutations and polymorphisms in the bile salt export pump and the multidrug resistance protein 3 associated with drug–induced liver injury. Pharmacogenet Genomics 2007; 17: 47–60.