Abcb11 deficiency induces cholestasis coupled to impaired β-fatty acid oxidation in mice

Journal of Biological Chemistry

Volumn 287, Issue 29, 2012, Pages 24784-24794

  Zhang, Yuanyuan ^a   Li, Fei ^b   Patterson, Andrew D ^b   Wang, Yao ^a   Krausz, Kristopher W ^b   Neale, Geoffrey ^a   Thomas, Sarah ^a   Nachagari, Deepa ^a   Vogel, Peter ^a   Vore, Mary ^c   Gonzalez, Frank J ^b   Schuetz, John D ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID METABOLITES; ATP-BINDING CASSETTE TRANSPORTERS; BILE SALTS; DISEASE PROGRESSION; FATTY ACID METABOLISM; FATTY ACID OXIDATION; GENETIC BACKGROUNDS; HUMAN DISEASE; KNOCK OUTS; LIPID METABOLISMS; LIVER DAMAGE; LIVER DISEASE; LIVER INJURIES; LONG-CHAIN FATTY ACIDS; METABOLIC CHANGES; METABOLOMIC ANALYSIS; PRIMARY SYSTEMS; REACTIVE OXYGEN SPECIES;

GENE EXPRESSION; METABOLISM; OXIDATION; PHYSIOLOGY; SALTS;

MAMMALS;

FATTY ACID; LONG CHAIN FATTY ACID; PHENYLACETYLGLYCINE; PHENYLGLYCINE; PHENYLPROPIONYLGLYCINE; UNCLASSIFIED DRUG;

ABCB11 GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLESTASIS; CONTROLLED STUDY; FATTY ACID BLOOD LEVEL; FATTY ACID OXIDATION; GENE; GENE EXPRESSION; GENE INACTIVATION; KNOCKOUT MOUSE; LIPID METABOLISM; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; WHITE ADIPOSE TISSUE;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CHOLESTASIS; FATTY ACIDS; LIVER; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; OXIDATION-REDUCTION; REAL-TIME POLYMERASE CHAIN REACTION;

ANIMALIA; MUS;

EID: 84863788678     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.329318     Document Type: Article

References (55)

1. Chiang, J. Y. (2009) Bile acids. Regulation of synthesis. J. Lipid Res. 50, 1955-1966
2. Trauner, M., and Boyer, J. L. (2003) Bile salt transporters. Molecular characterization, function, and regulation. Physiol. Rev. 83, 633-671 (Pubitemid 36378680)
3. Hayashi, H., Takada, T., Suzuki, H., Akita, H., and Sugiyama, Y. (2005) Two common PFIC2 mutations are associated with the impaired membrane trafficking of BSEP/ABCB11. Hepatology 41, 916-924 (Pubitemid 40462954)
4. Noe, J., Kullak-Ublick, G. A., Jochum, W., Stieger, B., Kerb, R., Haberl, M., Müllhaupt, B., Meier, P. J., and Pauli-Magnus, C. (2005) Impaired expression and function of the bile salt export pump due to three novel ABCB11 mutations in intrahepatic cholestasis. J. Hepatol. 43, 536-543 (Pubitemid 41111438)
5. Stieger, B., Meier, Y., and Meier, P. J. (2007) The bile salt export pump. Pflugers Arch. 453, 611-620 (Pubitemid 46192534)
6. Lam, P., Pearson, C. L., Soroka, C. J., Xu, S., Mennone, A., and Boyer, J. L. (2007) Levels of plasma membrane expression in progressive and benign mutations of the bile salt export pump (Bsep/Abcb11) correlate with severity of cholestatic diseases. Am. J. Physiol. Cell Physiol. 293, C1709-C1716 (Pubitemid 350085643)
7. Jansen, P. L., Strautnieks, S. S., Jacquemin, E., Hadchouel, M., Sokal, E. M., Hooiveld, G. J., Koning, J. H., De Jager-Krikken, A., Kuipers, F., Stellaard, F., Bijleveld, C. M., Gouw, A., Van Goor, H., Thompson, R. J., and Müller, M. (1999) Hepatocanalicular bile salt export pump deficiency in patients with progressive familial intrahepatic cholestasis. Gastroenterology 117, 1370-1379
8. Knisely, A. S., Strautnieks, S. S., Meier, Y., Stieger, B., Byrne, J. A., Portmann, B. C., Bull, L. N., Pawlikowska, L., Bilezikçi, B., Ozçay, F., László, A., Tiszlavicz, L., Moore, L., Raftos, J., Arnell, H., Fischler, B., Németh, A., Papadogiannakis, N., Cielecka-Kuszyk, J., Jankowska, I., Pawłowska, J., Melín-Aldana, H., Emerick, K. M., Whitington, P. F., Mieli-Vergani, G., and Thompson, R. J. (2006) Hepatocellular carcinoma in 10 children under 5 years of age with bile salt export pump deficiency. Hepatology 44, 478-486 (Pubitemid 44214888)
9. Lam, P., Wang, R., and Ling, V. (2005) Bile acid transport in sister of P-glycoprotein (ABCB11) knockout mice. Biochemistry 44, 12598-12605 (Pubitemid 41324350)
10. Wang, R., Salem, M., Yousef, I. M., Tuchweber, B., Lam, P., Childs, S. J., Helgason, C. D., Ackerley, C., Phillips, M. J., and Ling, V. (2001) Targeted inactivation of sister of P-glycoprotein gene (spgp) in mice results in nonprogressive but persistent intrahepatic cholestasis. Proc. Natl. Acad. Sci. U.S.A. 98, 2011-2016 (Pubitemid 32165614)
11. Huang, W., Ma, K., Zhang, J., Qatanani, M., Cuvillier, J., Liu, J., Dong, B., Huang, X., and Moore, D. D. (2006) Nuclear receptor-dependent bile acid signaling is required for normal liver regeneration. Science 312, 233-236
12. Houten, S. M., Watanabe, M., and Auwerx, J. (2006) Endocrine functions of bile acids. EMBO J. 25, 1419-1425
13. Ma, K., Saha, P. K., Chan, L., and Moore, D. D. (2006) Farnesoid X receptor is essential for normal glucose homeostasis. J. Clin. Invest. 116, 1102-1109
14. Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., and Mesirov, J. P. (2005) Gene set enrichment analysis. A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U.S.A. 102, 15545-15550 (Pubitemid 41528093)
15. Irizarry, R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U., and Speed, T. P. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264
16. Cho, J. Y., Matsubara, T., Kang, D. W., Ahn, S. H., Krausz, K. W., Idle, J. R., Luecke, H., and Gonzalez, F. J. (2010) Urinary metabolomics in Fxr-null mice reveals activated adaptive metabolic pathways upon bile acid challenge. J. Lipid Res. 51, 1063-1074
17. Hirschey, M. D., Shimazu, T., Goetzman, E., Jing, E., Schwer, B., Lombard, D. B., Grueter, C. A., Harris, C., Biddinger, S., Ilkayeva, O. R., Stevens, R. D., Li, Y., Saha, A. K., Ruderman, N. B., Bain, J. R., Newgard, C. B., Farese, R. V., Jr., Alt, F. W., Kahn, C. R., and Verdin, E. (2010) SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 464, 121-125
18. Narayan, S. B., Boriack, R. L., Messmer, B., and Bennett, M. J. (2005) Establishing a reference interval for measurement of flux through the mitochondrial fatty acid oxidation pathway in cultured skin fibroblasts. Clin. Chem. 51, 644-646 (Pubitemid 40300245)
19. Evason, K., Bove, K. E., Finegold, M. J., Knisely, A. S., Rhee, S., Rosenthal, P., Miethke, A. G., Karpen, S. J., Ferrell, L. D., and Kim, G. E. (2011) Morphologic findings in progressive familial intrahepatic cholestasis 2 (PFIC2). Correlation with genetic and immunohistochemical studies. Am. J. Surg Pathol. 35, 687-696
20. Hofmann, A. F., and Small, D. M. (1967) Detergent properties of bile salts. Correlation with physiological function. Annu. Rev. Med. 18, 333-376
21. Mühlfeld, A., Kubitz, R., Dransfeld, O., Häussinger, D., and Wettstein, M. (2003) Taurine supplementation induces multidrug resistance protein 2 and bile salt export pump expression in rats and prevents endotoxininduced cholestasis. Arch. Biochem. Biophys. 413, 32-40 (Pubitemid 36434349)
22. Timbrell, J. A., Seabra, V., and Waterfield, C. J. (1995) The in vivo and in vitro protective properties of taurine. Gen. Pharmacol. 26, 453-462
23. Wang, R., Lam, P., Liu, L., Forrest, D., Yousef, I. M., Mignault, D., Phillips, M. J., and Ling, V. (2003) Severe cholestasis induced by cholic acid feeding in knockout mice of sister of P-glycoprotein. Hepatology 38, 1489-1499 (Pubitemid 37466975)
24. Falany, C. N., Johnson, M. R., Barnes, S., and Diasio, R. B. (1994) Glycine and taurine conjugation of bile acids by a single enzyme. Molecular cloning and expression of human liver bile acid CoA:amino acid N-acyltransferase. J. Biol. Chem. 269, 19375-19379
25. Malhi, H., and Gores, G. J. (2008) Molecular mechanisms of lipotoxicity in nonalcoholic fatty liver disease. Semin. Liver Dis. 28, 360-369
26. Malhi, H., and Gores, G. J. (2008) Cellular and molecular mechanisms of liver injury. Gastroenterology 134, 1641-1654 (Pubitemid 351615416)
27. Desvergne, B., Michalik, L., and Wahli, W. (2006) Transcriptional regulation of metabolism. Physiol. Rev. 86, 465-514
28. Desvergne, B. (2007) PPARs special issue. Anchoring the present to explore the future. Biochim. Biophys. Acta 1771, 913-914
29. Zhou, J., Febbraio, M., Wada, T., Zhai, Y., Kuruba, R., He, J., Lee, J. H., Khadem, S., Ren, S., Li, S., Silverstein, R. L., and Xie, W. (2008) Hepatic fatty acid transporter Cd36 is a common target of LXR, PXR, and PPARγin promoting steatosis. Gastroenterology 134, 556-567
30. Zhou, J., Zhai, Y., Mu, Y., Gong, H., Uppal, H., Toma, D., Ren, S., Evans, R. M., and Xie, W. (2006) A novel pregnane X receptor-mediated and sterol regulatory element-binding protein-independent lipogenic pathway. J. Biol. Chem. 281, 15013-15020 (Pubitemid 43855205)
31. Rinaldo, P., O'Shea, J. J., Coates, P. M., Hale, D. E., Stanley, C. A., and Tanaka, K. (1988) Medium-chain acyl-CoA dehydrogenase deficiency. Diagnosis by stable-isotope dilution measurement of urinary n-hexanoylglycine and 3-phenylpropionylglycine. N. Engl. J. Med. 319, 1308-1313 (Pubitemid 19003392)
32. Smith, B. K., Jain, S. S., Rimbaud, S., Dam, A., Quadrilatero, J., Ventura-Clapier, R., Bonen, A., and Holloway, G. P. (2011) FAT/CD36 is located on the outer mitochondrial membrane, upstream of long-chain acyl-CoA synthetase, and regulates palmitate oxidation. Biochem. J. 437, 125-134
33. Talanian, J. L., Holloway, G. P., Snook, L. A., Heigenhauser, G. J., Bonen, A., and Spriet, L. L. (2010) Exercise training increases sarcolemmal and mitochondrial fatty acid transport proteins in human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 299, E180-E188
34. Abumrad, N. A., el-Maghrabi, M. R., Amri, E. Z., Lopez, E., and Grimaldi, P. A. (1993) Cloning of a rat adipocyte membrane protein implicated in binding or transport of long-chain fatty acids that is induced during preadipocyte differentiation. Homology with human CD36. J. Biol. Chem. 268, 17665-17668 (Pubitemid 23260267)
35. Holloway, G. P., Jain, S. S., Bezaire, V., Han, X. X., Glatz, J. F., Luiken, J. J., Harper, M. E., and Bonen, A. (2009) FAT/CD36-null mice reveal that mitochondrial FAT/CD36 is required to up-regulate mitochondrial fatty acid oxidation in contracting muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R960-R967
36. Holloway, G. P., Snook, L. A., Harris, R. J., Glatz, J. F., Luiken, J. J., and Bonen, A. (2011) In obese Zucker rats, lipids accumulate in the heart despite normal mitochondrial content, morphology, and long-chain fatty acid oxidation. J. Physiol. 589, 169-180
37. Hardwick, J. P., Osei-Hyiaman, D., Wiland, H., Abdelmegeed, M. A., and Song, B. J. (2009) PPAR/RXR regulation of fatty acid metabolism and fatty acid ω-hydroxylase (CYP4) isozymes. Implications for prevention of lipotoxicity in fatty liver disease. PPAR Res. 2009, 952734
38. Preiss, B., and Bloch, K. (1964) ω-Oxidation of long chain fatty acids in rat liver. J. Biol. Chem. 239, 85-88
39. Pettersen, J. E., Jellum, E., and Eldjarn, L. (1972) The occurrence of adipic and suberic acid in urine from ketotic patients. Clin. Chim. Acta 38, 17-24
40. Grego, A. V., and Mingrone, G. (1995) Dicarboxylic acids, an alternate fuel substrate in parenteral nutrition. An update. Clin. Nutr. 14, 143-148
41. Savkur, R. S., Bramlett, K. S., Michael, L. F., and Burris, T. P. (2005) Regulation of pyruvate dehydrogenase kinase expression by the farnesoid X receptor. Biochem. Biophys. Res. Commun. 329, 391-396 (Pubitemid 40255466)
42. 2 emission during long-chain fatty acid oxidation. J. Biol. Chem. 285, 5748-5758
43. Cho, H. Y., Reddy, S. P., and Kleeberger, S. R. (2006) Nrf2 defends the lung from oxidative stress. Antioxid. Redox Signal. 8, 76-87 (Pubitemid 43324533)
44. Cho, H. Y., Reddy, S. P., Yamamoto, M., and Kleeberger, S. R. (2004) The transcription factor NRF2 protects against pulmonary fibrosis. FASEB J. 18, 1258-1260 (Pubitemid 39561569)
45. Venugopal, R., and Jaiswal, A. K. (1998) Nrf2 and Nrf1 in association with Jun proteins regulate antioxidant response element-mediated expression and coordinated induction of genes encoding detoxifying enzymes. Oncogene 17, 3145-3156 (Pubitemid 29020810)
46. Kagawa, T., Watanabe, N., Mochizuki, K., Numari, A., Ikeno, Y., Itoh, J., Tanaka, H., Arias, I. M., and Mine, T. (2008) Phenotypic differences in PFIC2 and BRIC2 correlate with protein stability of mutant Bsep and impaired taurocholate secretion in MDCK II cells. Am. J. Physiol. Gastrointest. Liver Physiol. 294, G58-G67
47. Perwaiz, S., Forrest, D., Mignault, D., Tuchweber, B., Phillip, M. J., Wang, R., Ling, V., and Yousef, I. M. (2003) Appearance of atypical 3α,6β,7β,12α-tetrahydroxy-5β-cholan-24-oic acid in spgp knockout mice. J. Lipid Res. 44, 494-502 (Pubitemid 37279697)
48. 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 6, 507-515
49. Lee, F. Y., Lee, H., Hubbert, M. L., Edwards, P. A., and Zhang, Y. (2006) FXR, a multipurpose nuclear receptor. Trends Biochem. Sci. 31, 572-580 (Pubitemid 44436939)
50. Takeuchi, F., Katsuya, T., Chakrewarthy, S., Yamamoto, K., Fujioka, A., Serizawa, M., Fujisawa, T., Nakashima, E., Ohnaka, K., Ikegami, H., Sugiyama, T., Nabika, T., Kasturiratne, A., Yamaguchi, S., Kono, S., Takayanagi, R., Yamori, Y., Kobayashi, S., Ogihara, T., de Silva, A., Wickremasinghe, R., and Kato, N. (2010) Common variants at the GCK, GCKR, G6PC2-ABCB11, and MTNR1B loci are associated with fasting glucose in two Asian populations. Diabetologia 53, 299-308
51. Chen, W. M., Erdos, M. R., Jackson, A. U., Saxena, R., Sanna, S., Silver, K. D., Timpson, N. J., Hansen, T., Orrù, M., Grazia Piras, M., Bonnycastle, L. L., Willer, C. J., Lyssenko, V., Shen, H., Kuusisto, J., Ebrahim, S., Sestu, N., Duren, W. L., Spada, M. C., Stringham, H. M., Scott, L. J., Olla, N., Swift, A. J., Najjar, S., Mitchell, B. D., Lawlor, D. A., Smith, G. D., Ben-Shlomo, Y., Andersen, G., Borch-Johnsen, K., Jørgensen, T., Saramies, J., Valle, T. T., Buchanan, T. A., Shuldiner, A. R., Lakatta, E., Bergman, R. N., Uda, M., Tuomilehto, J., Pedersen, O., Cao, A., Groop, L., Mohlke, K. L., Laakso, M., Schlessinger, D., Collins, F. S., Altshuler, D., Abecasis, G. R., Boehnke, M., Scuteri, A., and Watanabe, R. M. (2008) Variations in the G6PC2/ABCB11 genomic region are associated with fasting glucose levels. J. Clin. Invest. 118, 2620-2628 (Pubitemid 351949789)
52. Randle, P. J. (1998) Regulatory interactions between lipids and carbohydrates. The glucose fatty acid cycle after 35 years. Diabetes Metab. Rev. 14, 263-283
53. Fromenty, B., Berson, A., and Pessayre, D. (1997) Microvesicular steatosis and steatohepatitis. Role of mitochondrial dysfunction and lipid peroxidation. J. Hepatol. 26, Suppl. 1, 13-22 (Pubitemid 127777233)
54. Schönfeld, P., and Wojtczak, L. (2008) Fatty acids as modulators of the cellular production of reactive oxygen species. Free Radic. Biol. Med. 45, 231-241
55. Lewis, D. F., and Sheridan, G. (2001) Cytochromes P450, oxygen, and evolution. ScientificWorldJournal 1, 151-167