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Originally published In Press as doi:10.1074/jbc.M106340200 on August 16, 2001

J. Biol. Chem., Vol. 276, Issue 42, 39411-39418, October 19, 2001
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Disrupted Bile Acid Homeostasis Reveals an Unexpected Interaction among Nuclear Hormone Receptors, Transporters, and Cytochrome P450*

Erin G. SchuetzDagger , Stephen Strom§, Kazuto YasudaDagger , Valerie LecureurDagger , Mahfoud AssemDagger , Cynthia BrimerDagger , Jatinder LambaDagger , Richard B. Kim, Vinod Ramachandran||, Bernard J. Komoroski||, Raman Venkataramanan§||, Hongbo Cai§, Christopher J. Sinal**, Frank J. Gonzalez**, and John D. SchuetzDagger Dagger Dagger

From the Dagger  Department of Pharmaceutical Sciences, St. Jude Children's Research Hospital, Memphis, Tennessee 38105, the Departments of § Pathology and || Pharmaceutical Sciences, the University of Pittsburgh, Pittsburgh, Pennsylvania 15261, the  Department of Pharmacology, Vanderbilt University, Nashville, Tennessee 37203, and the ** Laboratory of Medicine, National Institutes of Health, Bethesda, Maryland 20892

Sister of P-glycoprotein (SPGP) is the major hepatic bile salt export pump (BSEP). BSEP/SPGP expression varies dramatically among human livers. The potency and hierarchy of bile acids as ligands for the farnesyl/bile acid receptor (FXR/BAR) paralleled their ability to induce BSEP in human hepatocyte cultures. FXR:RXR heterodimers bound to IR1 elements and enhanced bile acid transcriptional activation of the mouse and human BSEP/SPGP promoters. In FXR/BAR nullizygous mice, which have dramatically reduced BSEP/SPGP levels, hepatic CYP3A11 and CYP2B10 were strongly but unexpectedly induced. Notably, the rank order of bile acids as CYP3A4 inducers and activators of pregnane X receptor/steroid and xenobiotic receptor (PXR/SXR) closely paralleled each other but was markedly different from their hierarchy and potency as inducers of BSEP in human hepatocytes. Moreover, the hepatoprotective bile acid ursodeoxycholic acid, which reverses hydrophobic bile acid hepatotoxicity, activates PXR and efficaciously induces CYP3A4 (a bile-metabolizing enzyme) in primary human hepatocytes thus providing one mechanism for its hepatoprotection. Because serum and urinary bile acids increased in FXR/BAR -/- mice, we evaluated hepatic transporters for compensatory changes that might circumvent the profound decrease in BSEP/SPGP. We found weak MRP3 up-regulation. In contrast, MRP4 was substantially increased in the FXR/BAR nullizygous mice and was further elevated by cholic acid. Thus, enhanced hepatocellular concentrations of bile acids, due to the down-regulation of BSEP/SPGP-mediated efflux in FXR nullizygous mice, result in an alternate but apparent compensatory up-regulation of CYP3A, CYP2B, and some ABC transporters that is consistent with activation of PXR/SXR by bile acids.

* This work was supported by National Institutes of Health Research Grants GM60346, ES08648, ES058571, ES08648, ES05780, and P30 CA21745, Cancer Center support grant, the American Lebanese Syrian Associated Charities, and Grant DK92310.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Dagger Dagger To whom correspondence should be addressed: Dept. of Pharmaceutical Sciences, St. Jude Children's Research Hospital, 332 N. Lauderdale Ave., Memphis, TN 38105. Tel.: 901-495-2174; Fax: 901-525-6869; E-mail: John.schuetz@stjude.org.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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B. Goodwin, K. C. Gauthier, M. Umetani, M. A. Watson, M. I. Lochansky, J. L. Collins, E. Leitersdorf, D. J. Mangelsdorf, S. A. Kliewer, and J. J. Repa
Identification of bile acid precursors as endogenous ligands for the nuclear xenobiotic pregnane X receptor
PNAS, January 7, 2003; 100(1): 223 - 228.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
S. A. Kliewer, B. Goodwin, and T. M. Willson
The Nuclear Pregnane X Receptor: A Key Regulator of Xenobiotic Metabolism
Endocr. Rev., October 1, 2002; 23(5): 687 - 702.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
C. Brendel, K. Schoonjans, O. A. Botrugno, E. Treuter, and J. Auwerx
The Small Heterodimer Partner Interacts with the Liver X Receptor {alpha} and Represses Its Transcriptional Activity
Mol. Endocrinol., September 1, 2002; 16(9): 2065 - 2076.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
C. Handschin, M. Podvinec, R. Amherd, R. Looser, J.-C. Ourlin, and U. A. Meyer
Cholesterol and Bile Acids Regulate Xenosensor Signaling in Drug-mediated Induction of Cytochromes P450
J. Biol. Chem., August 9, 2002; 277(33): 29561 - 29567.
[Abstract] [Full Text] [PDF]

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 Mol. Pharmacol.Home page
J. Makinen, C. Frank, J. Jyrkkarinne, J. Gynther, C. Carlberg, and P. Honkakoski
Modulation of Mouse and Human Phenobarbital-Responsive Enhancer Module by Nuclear Receptors
Mol. Pharmacol., August 1, 2002; 62(2): 366 - 378.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
J. Wu, C. Xia, J. Meier, S. Li, X. Hu, and D. S. Lala
The Hypolipidemic Natural Product Guggulsterone Acts as an Antagonist of the Bile Acid Receptor
Mol. Endocrinol., July 1, 2002; 16(7): 1590 - 1597.
[Abstract] [Full Text] [PDF]

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 J. Lipid Res.Home page
S. A. Kliewer and T. M. Willson
Regulation of xenobiotic and bile acid metabolism by the nuclear pregnane X receptor
J. Lipid Res., March 1, 2002; 43(3): 359 - 364.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
H. R. Kast, B. Goodwin, P. T. Tarr, S. A. Jones, A. M. Anisfeld, C. M. Stoltz, P. Tontonoz, S. Kliewer, T. M. Willson, and P. A. Edwards
Regulation of Multidrug Resistance-associated Protein 2 (ABCC2) by the Nuclear Receptors Pregnane X Receptor, Farnesoid X-activated Receptor, and Constitutive Androstane Receptor
J. Biol. Chem., January 18, 2002; 277(4): 2908 - 2915.
[Abstract] [Full Text] [PDF]


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