A mouse genetic model for familial cholestasis caused by ATP8B1 mutations reveals pertubed bile salt homeostasis but no impairment in bile secretion

Human Molecular Genetics

Volumn 13, Issue 8, 2004, Pages 881-892

  Pawlikowska, Ludmila ^a,b,d   Groen, Annemiek ^d   Eppens, Elaine F ^d   Kunne, Cindy ^d   Ottenhoff, Roelof ^d   Looije, Norbert ^d   Knisely, A S ^e   Killeen, Nigel P ^c   Bull, Laura N ^a   Elferink, Ronald P J Oude ^d   Freimer, Nelson B ^f  

^a SAN FRANCISCO GENERAL HOSPITAL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d ACADEMIC MEDICAL CENTER   (Netherlands)

^e KING S COLLEGE HOSPITAL   (United Kingdom)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BILE SALT; PROTEIN ATP8B1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE SECRETION; BIOACCUMULATION; BLOOD LEVEL; BODY WEIGHT DISORDER; CHOLESTASIS; CONTROLLED STUDY; DISEASE SEVERITY; FAMILIAL DISEASE; GENE MUTATION; GENETIC MODEL; HOMEOSTASIS; HOMOZYGOSITY; HYDROPHOBICITY; HYDROXYLATION; LIVER DISEASE; LIVER INJURY; MALE; MOUSE; MOUSE MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; WEANING; WILD TYPE;

ADENOSINE TRIPHOSPHATASES; ANIMALS; BILE; BILE ACIDS AND SALTS; CHOLESTASIS; DISEASE MODELS, ANIMAL; LIVER; MALE; MICE; TAUROCHOLIC ACID; TRITIUM;

EID: 11144355538     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddh100     Document Type: Article

References (47)

1. Phillips, M.J. and Suchy, F.J. (2001) Mechanisms and morphology of cholestasis. In Suchy, F.J., Sokol, R.J. and Balistreri, W.F. (eds), Liver Disease in Children, 2nd edn Lipincott, Williams & Wilkins, Philadelphia, PA, pp. 25-37.
2. Gerloff, T., Stieger, B., Hagenbuch, B., Madon, J., Landmann, L., Roth, J., Hofmann, A.F. and Meier, P.J. (1998) The sister of P-glycoprotein represents the canalicular bile salt export pump of mammalian liver. J. Biol. Chem., 273, 10046-10050.
3. Green, R.M., Hoda, F. and Ward, K.L. (2000) Molecular cloning and characterization of the murine bile salt export pump. Gene, 241, 117-123.
4. Wong, M.H., Oelkers, P., Craddock, A.L. and Dawson, P.A. (1994) Expression cloning and characterization of the hamster ileal sodium-dependent bile acid transporter. J. Biol. Chem., 269, 1340-1347.
5. Shneider, B.L., Dawson, P.A., Christie, D.M., Hardikar, W., Wong, M.H. and Suchy, F.J. (1995) Cloning and molecular characterization of the ontogeny of a rat ileal sodium-dependent bile acid transporter. J. Clin. Invest., 95, 745-754.
6. Craddock, A.L., Love, M.W, Daniel, R.W., Kirby, L.C., Walters, H.C., Wong, M.H. and Dawson, P.A. (1998) Expression and transport properties of the human ileal and renal sodium-dependent bile acid transporter. Am. J. Physiol., 274, G157-G169.
7. Shneider, B.L. (2001) Intestinal bile acid transport, biology, physiology, and pathophysiology. J. Pediatr Gastroenterol. Nutr., 32, 407-417.
8. Coleman, R., Iqbal, S., Godfrey, P.P. and Billington, D. (1979) Membranes and bile formation. Composition of several mammalian biles and their membrane-damaging properties. Biochem. J., 178, 201-208.
9. Summerskill, W.H.J. (1965) The syndrome of benign recurrent intrahepatic cholestasis. Am. J. Med., 38, 289-305.
10. Clayton, R.I., Iber, F.L., Ruebner, B.H. and McKusick, V.A. (1969) Byler disease: fatal familial intrahepatic cholestasis in an Amish kindred. Am. J. Dis. Child., 117, 112-124.
11. Linarelli, L.G., Williams, C.N. and Phillips, M.J. (1972) Byler's disease: fatal intrahepatic cholestasis. J. Pediatr., 81, 484-492.
12. Houwen, R.H., Baharloo, S., Blankenship, K., Raeymaekers, P., Juyn, J., Sandkuijl, L.A, and Freimer, N.B. (1994) Genome screening by searching for shared segments: mapping a gene for benign recurrent intrahepatic cholestasis. Nat. Genet., 8, 380-386.
13. Carlton, V.E., Knisely, A.S. and Freimer, N.B. (1995) Mapping of a locus for progressive familial intrahepatic cholestasis (Byler disease) to 18q21-q22, the benign recurrent intrahepatic cholestasis region. Hum. Mol. Genet., 4, 1049-1053.
14. Bull, L.N., van Eijk, M.J., Pawlikowska, L., DeYoung, J.A., Juijn, J.A., Liao, M., Klomp, L.W., Lomri, N., Berger, R., Scharschmidt, B.F. et al. (1998) A gene encoding a P-type ATPase mutated in two forms of hereditary cholestasis. Nat. Genet., 18, 219-224.
15. Strautnieks, S.S., Bull, L.N., Knisely, A.S., Kocoshis, S.A., Dahl, N., Arnell, H., Sokal, E., Dahan, K., Childs, S., Ling et al. (1998) A gene encoding a liver-specific ABC transporter is mutated in progressive familial intrahepatic cholestasis. Nat. Genet., 20, 233-238.
16. Bull, L.N., Carlton, V.E., Stricker, N.L., Baharloo, S., DeYoung, J.A., Freimer, N.B., Magid, M.S., Kahn, E., Markowitz, J., DiCarlo, F.J. et al. (1997) Genetic and morphological findings in progressive familial intrahepatic cholestasis (Byler disease [PFIC-1] and Byler syndrome): evidence for heterogeneity. Hepatology, 26, 155-164.
17. Knisely, A.S. (2000) Progressive familial intrahepatic cholestasis: a personal perspective. Pediatr. Dev. Pathol., 3, 113-125.
18. Chen, H.L., Chang, P.S., Hsu, B.C., Ni, Y.H., Hsu, H.Y., Lee, J.H., Jeng, Y.M., Shan, W.Y. and Chang, M.H. (2002) FIC1 and BSEP defects in Taiwanese patients with chronic intrahepatic cholestasis with low gamma-glutamyltranspeptidase levels. J. Pediatr., 140, 119-124.
19. Lykavieris, P., van Mil, S., Cresteil, D., Fabre, M., Hadchouel, M., Klomp, L., Bernard, O. and Jacquemin, E. (2003) Progressive familial intrahepatic cholestasis type 1 and extrahepatic features: no catch-up of stature growth, exacerbation of diarrhea, and appearance of liver steatosis after liver transplantation. J. Hepatol., 39, 447-452.
20. Eppens, E.F., van Mil, S.W., de Vree, J.M., Mok, K.S., Juijn, J.A., Oude Elferink, R.P., Berger, R., Houwen, R.H. and Klomp, L.W. (2001) FIC1, the protein affected in two forms of hereditary cholestasis, is localized in the cholangiocyte and the canalicular membrane of the hepatocyte. J. Hepatol., 35, 436-443.
21. Ujhazy, P., Ortiz, D., Misra, S., Li, S., Moseley, J., Jones, H. and Arias, I.M. (2001) Familial intrahepatic cholestasis 1: studies of localization and function. Hepatology, 34, 768-775.
22. Tang, X., Halleck, M.S., Schlegel, R.A. and Williamson, P. (1996) A subfamily of P-type ATPases with aminophospholipid transporting activity. Science, 272, 1495-1497.
23. Hua, Z., Fatheddin, P. and Graham, T.R. (2002) An essential subfamily of Drs2p-related P-type ATPases is required for protein trafficking between Golgi complex and endosomal/vacuolar system. Mol. Biol. Cell, 9, 3162-3177.
24. Gall, W.E., Geething, N.C., Hua, Z., Ingram, M.F., Liu, K., Chen, S.I. and Graham, T.R. (2002) Drs2p-dependent formation of exocytic clathrin-coated vesicles in vivo. Curr. Biol., 12, 1623-1627.
25. Axelsen, K.B and Palmgren, M.G. (1998) Evolution of the substrate specificities in the P-type ATPase superfamily. J. Mol. Evol., 46, 84-101.
26. Barnwell, S.G., Tuchweber, B. and Yousef, I.M. (1987) Biliary lipid secretion in the rat during infusion of increasing doses of unconjugated bile acids. Biochim. Biophys. Acta, 922, 221-233.
27. Lu, T.T., Makishima, M., Repa, J.J., Schoonjans, K., Kerr, T.A., Auwerx, J. and Mangelsdorf, D.J. (2000) Molecular basis for feedback regulation of bile acid synthesis by nuclear receptors. Mol. Cell, 3, 507-515.
28. Sinai, C.J., Tohkin, M., Miyata, M., Ward, J.M., Lambert, G. and Gonzalez, F.J. (2000) Targeted disruption of the nuclear receptor FXR/BAR impairs bile acid and lipid homeostasis. Cell, 102, 731-744.
29. Peet, D.J., Turley, S.D., Ma, W., Janowski, B.A., Lobaccaro, J.M., Hammer, R.E. and Mangelsdorf, D.J. (1998) Cholesterol and bile acid metabolism are impaired in mice lacking the nuclear oxysterol receptor LXR alpha. Cell, 93, 693-704.
30. Guo, G.L., Lambert, G., Negishi, M., Ward, J.M., Brewer, H.B. Jr, Kliewer, S.A., Gonzalez, F.J. and Sinai, C.J. (2003) Complementary roles of farnesoid X receptor, pregnane X receptor, and constitutive androstane receptor in protection against bile acid toxicity. J. Biol. Chem., 278, 45062-45071.
31. Makishima, M., Lu, T.T., Xie, W., Whitfield, G.K., Domoto, H., Evans, R.M., Haussler, M.R. and Mangelsdorf, D.J. (2002) Vitamin D receptor as an intestinal bile acid sensor. Science, 296, 1313-1316.
32. Gascon-Barre, M., Demers, C., Mirshahi, A., Neron, S., Zalzal, S. and Nanci, A. (2003) The normal liver harbors the vitamin D nuclear receptor in nonparenchymal and biliary epithelial cells. Hepatology, 37, 1034-1042.
33. Karpen, S.J. (2002) Nuclear receptor regulation of hepatic function. J. Hepatol., 36, 832-850.
34. del Castillo-Olivares, A. and Gil, G. (2000). Alpha 1-fetoprotein transcription factor is required for the expression of sterol 12alpha-hydroxylase, the specific enzyme for cholic acid synthesis. Potential role in the bile acid-mediated regulation of gene transcription. J. Biol. Chem., 275, 17793-17799.
35. Halleck, M.S., Lawler, J.F., Jr, Blackshaw, S., Gao, L., Nagarajan, P., Hacker, C., Pyle, S., Newman, J.T., Nakanishi, Y., Ando, H. et al. (1999) Differential expression of putative transbilayer amphipath transporters. Physiol. Genom., 1, 139-150.
36. Bijleveld, C.M., Vonk, R.J., Kuipers, F., Havinga, R., Boverhof, R., Koopman, B.J., Wolthers, B.G. and Fernandes, J. (1989) Benign recurrent intrahepatic cholestasis: altered bile acid metabolism. Gastroenterology, 97, 427-432.
37. Egawa, H., Yorifuji, T., Sumazaki, R., Kimura, A., Hasegawa, M. and Tanaka, K. (2002) Intractable diarrhea after liver transplantation for Byler's disease: successful treatment with bile adsorptive resin. Liver Transpl., 8, 714-716.
38. Lazaridis, K.N., Pham, L., Tietz, P., Marinelli, R.A., deGroen, P.C., Levine, S., Dawson, P.A. and LaRusso, N.F. (1997) Rat cholangiocytes absorb bile acids at their apical domain via the ileal sodium-dependent bile acid transporter. J. Clin. Invest., 100, 2714-2721.
39. Meier, P.J. and Stieger, B. (2002) Bile salt transporters. A. Rev. Physiol., 64, 635-661.
40. Zachowski, A., Henry, J.P. and Devaux, P.F. (1989) Control of transmembrane lipid asymmetry in chromaffin granules by an ATP-dependent protein. Nature, 340, 75-76.
41. Kipp, H. and Arias, I.M. (2002) Trafficking of canalicular ABC transporters in hepatocytes. A. Rev. Physiol., 64, 595-608.
42. Bourke, B., Goggin, N., Walsh, D., Kennedy, S., Setchell, K.D. and Drumm, B. (1996) Byler-like familial cholestasis in an extended kindred. Arch. Dis. Child., 75, 223-227.
43. Gu, H., Zou, Y.R. and Rajewsky, K. (1993) Independent control of immunoglobulin switch recombination at individual switch regions evidenced through Cre-loxP-mediated gene targeting. Cell, 73, 1155-1164.
44. O'Gorman, S., Dagenais, N.A., Qian, M. and Marchuk, Y. (1997) Protamine-Cre recombinase transgenes efficiently recombine target sequences in the male germ line of mice, but not in embryonic stem cells. Proc. Natl Acad. Sci. USA, 94, 14602-14607.
45. Oude Elferink, R.P.J., Ottenhoff, R., van Wijland, M., Smit, J.J., Schinkel, A.H. and Groen, A.K. (1995) Regulation of biliary lipid secretion by mdr2 P-glycoprotein in the mouse. J. Clin. Invest., 95, 31-38.
46. Elson, D.A., Thurston, G., Huang, L.E., Ginzinger, D.G., McDonald, D.M., Johnson, R.S. and Arbeit, J.M. (2001) Induction of hypervascularity without leakage or inflammation in transgenic mice overexpressing hypoxia-inducible factor-1alpha. Genes Dev., 15, 2520-2532.
47. Ginzinger, D.G. (2002) Gene quantification using real-time quantitative PCR: an emerging technology hits the mainstream. Exp. Hematol., 30, 503-512.