Intrahepatic cholestasis of pregnancy levels of sulfated progesterone metabolites inhibit farnesoid X receptor resulting in a cholestatic phenotype

Hepatology

Volumn 57, Issue 2, 2013, Pages 716-726

  Abu Hayyeh, Shadi ^a   Papacleovoulou, Georgia ^a   Lövgren Sandblom, Anita ^b   Tahir, Mehreen ^a   Oduwole, Olayiwola ^a   Jamaludin, Nurul Akmal ^a   Ravat, Sabiha ^a   Nikolova, Vanya ^a   Chambers, Jenny ^a   Selden, Clare ^c   Rees, Myrddin ^d   Marschall, Hanns Ulrich ^e   Parker, Malcolm G ^a   Williamson, Catherine ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^d NORTH HAMPSHIRE HOSPITAL   (United Kingdom)

^e UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BILE ACID; CHOLIC ACID; EPIALLOPREGNANOLONE SULFATE; FARNESOID X RECEPTOR; FIBROBLAST GROWTH FACTOR 19; GESTAGEN; PROGESTERONE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HEPATOMA CELL; INTRAHEPATIC CHOLESTASIS; INTRAHEPATIC CHOLESTASIS OF PREGNANCY; LIVER CELL; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PHENOTYPE; PREGNANCY; PREGNANCY DISORDER; PRIORITY JOURNAL;

ANIMALS; BILE ACIDS AND SALTS; CHOLESTASIS; CHOLESTASIS, INTRAHEPATIC; CHOLIC ACID; FEMALE; HOMEOSTASIS; HUMANS; MICE; MICE, INBRED C57BL; PHENOTYPE; PREGNANCY; PREGNANCY COMPLICATIONS; PREGNANOLONE; PROGESTERONE; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SULFURIC ACID ESTERS;

EID: 84873279850     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.26055     Document Type: Article

References (46)

1. Geenes V, Williamson C. Intrahepatic cholestasis of pregnancy. World J Gastroenterol 2009; 15: 2049-2066.
2. Fisk NM, Storey GN. Fetal outcome in obstetric cholestasis. Br J Obstet Gynaecol 1988; 95: 1137-1143.
3. Glantz A, Marschall HU, Mattsson LA. Intrahepatic cholestasis of pregnancy: relationships between bile acid levels and fetal complication rates. HEPATOLOGY 2004; 40: 467-474.
4. Van Mil SW, Milona A, Dixon PH, Mullenbach R, Geenes VL, Chambers J, et al. Functional variants of the central bile acid sensor FXR identified in intrahepatic cholestasis of pregnancy. Gastroenterology 2007; 133: 507-516.
5. Pauli-Magnus C, Lang T, Meier Y, Zodan-Marin T, Jung D, Breymann C, et al. Sequence analysis of bile salt export pump (ABCB11) and multidrug resistance p-glycoprotein 3 (ABCB4, MDR3) in patients with intrahepatic cholestasis of pregnancy. Pharmacogenetics 2004; 14: 91-102.
6. Dixon PH, Van Mil SW, Chambers J, Strautnieks S, Thompson RJ, Lammert F, et al. Contribution of variant alleles of ABCB11 to susceptibility to intrahepatic cholestasis of pregnancy. Gut 2009; 58: 537-544.
7. de Vree JM, Jacquemin E, Sturm E, Cresteil D, Bosma PJ, Aten J, et al. Mutations in the MDR3 gene cause progressive familial intrahepatic cholestasis. Proc Natl Acad Sci U S A 1998; 95: 282-287.
8. 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: 210-211.
9. Dixon PH, Weerasekera N, Linton KJ, 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: 1209-1217.
10. Mullenbach R, Linton KJ, Wiltshire S, Weerasekera N, Chambers J, Elias E, et al. ABCB4 gene sequence variation in women with intrahepatic cholestasis of pregnancy. J Med Genet 2003; 40: e70.
11. Sookoian S, Castano G, Burgueno A, Gianotti TF, Pirola CJ. Association of the multidrug-resistance-associated protein gene (ABCC2) variants with intrahepatic cholestasis of pregnancy. J Hepatol 2008; 48: 125-132.
12. Kreek MJ, Weser E, Sleisenger MH, Jeffries GH. Idiopathic cholestasis of pregnancy. The response to challenge with the synthetic estrogen, ethinyl estradiol. N Engl J Med 1967; 277: 1391-1395.
13. Williamson C, Hems LM, Goulis DG, Walker I, Chambers J, Donaldson O, et al. Clinical outcome in a series of cases of obstetric cholestasis identified via a patient support group. BJOG 2004; 111: 676-681.
14. Sjovall K, Sjovall J. Serum bile acid levels in pregnancy with pruritus (bile acids and steroids 158). Clin Chim Acta 1966; 13: 207-211.
15. Meng LJ, Reyes H, Palma J, Hernandez I, Ribalta J, Sjovall J. Profiles of bile acids and progesterone metabolites in the urine and serum of women with intrahepatic cholestasis of pregnancy. J Hepatol 1997; 27: 346-357.
16. Meng LJ, Reyes H, Axelson M, Palma J, Hernandez I, Ribalta J, et al. Progesterone metabolites and bile acids in serum of patients with intrahepatic cholestasis of pregnancy: effect of ursodeoxycholic acid therapy. HEPATOLOGY 1997; 26: 1573-1579.
17. Reyes H, Sjovall J. Bile acids and progesterone metabolites in intrahepatic cholestasis of pregnancy. Ann Med 2000; 32: 94-106.
18. Sjovall J, Sjovall K. Steroid sulphates in plasma from pregnant women with pruritus and elevated plasma bile acid levels. Ann Clin Res 1970; 2: 321-337.
19. +-taurocholate Co-transporting polypeptide-mediated bile acid transport by cholestatic sulfated progesterone metabolites. J Biol Chem 2010; 285: 16504-16512.
20. Vallejo M, Briz O, Serrano MA, Monte MJ, Marin JJ. Potential role of trans-inhibition of the bile salt export pump by progesterone metabolites in the etiopathogenesis of intrahepatic cholestasis of pregnancy. J Hepatol 2006; 44: 1150-1157.
21. 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.
22. Huang L, Zhao A, Lew JL, Zhang T, Hrywna Y, Thompson JR, et al. Farnesoid X receptor activates transcription of the phospholipid pump MDR3. J Biol Chem 2003; 278: 51085-51090.
23. Denson LA, Sturm E, Echevarria W, Zimmerman TL, Makishima M, Mangelsdorf DJ, et al. The orphan nuclear receptor, shp, mediates bile acid-induced inhibition of the rat bile acid transporter, ntcp. Gastroenterology 2001; 121: 140-147.
24. Goodwin B, Jones SA, Price RR, Watson MA, McKee DD, Moore LB, et al. A regulatory cascade of the nuclear receptors FXR, SHP-1, and LRH-1 represses bile acid biosynthesis. Mol Cell 2000; 6: 517-526.
25. Milona A, Owen BM, Cobbold JF, Willemsen EC, Cox IJ, Boudjelal M, et al. Raised hepatic bile acid concentrations during pregnancy in mice are associated with reduced farnesoid X receptor function. HEPATOLOGY 2010; 52: 1341-1349.
26. Mullenbach R, Bennett A, Tetlow N, Patel N, Hamilton G, Cheng F, et al. ATP8B1 mutations in British cases with intrahepatic cholestasis of pregnancy. Gut 2005; 54: 829-834.
27. Kullak-Ublick GA, Beuers U, Paumgartner G. Hepatobiliary transport. J Hepatol 2000; 32: 3-18.
28. Song KH, Li T, Owsley E, Strom S, Chiang JY. Bile acids activate fibroblast growth factor 19 signaling in human hepatocytes to inhibit cholesterol 7alpha-hydroxylase gene expression. HEPATOLOGY 2009; 49: 297-305.
29. Heery DM, Kalkhoven E, Hoare S, Parker MG. A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature 1997; 387: 733-736.
30. Yu J, Lo JL, Huang L, Zhao A, Metzger E, Adams A, et al. Lithocholic acid decreases expression of bile salt export pump through farnesoid X receptor antagonist activity. J Biol Chem 2002; 277: 31441-31447.
31. Makishima M, Okamoto AY, Repa JJ, Tu H, Learned RM, Luk A, et al. Identification of a nuclear receptor for bile acids. Science 1999; 284: 1362-1365.
32. Parks DJ, Blanchard SG, Bledsoe RK, Chandra G, Consler TG, Kliewer SA, et al. Bile acids: natural ligands for an orphan nuclear receptor. Science 1999; 284: 1365-1368.
33. Wang H, Chen J, Hollister K, Sowers LC, Forman BM. Endogenous bile acids are ligands for the nuclear receptor FXR/BAR. Mol Cell 1999; 3: 543-553.
34. Sinal CJ, Tohkin M, Miyata M, Ward JM, Lambert G, Gonzalez FJ. Targeted disruption of the nuclear receptor FXR/BAR impairs bile acid and lipid homeostasis. Cell 2000; 102: 731-744.
35. 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: 10046-10050.
36. Strautnieks SS, Bull LN, Knisely AS, Kocoshis SA, 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: 233-238.
37. Zhao A, Yu J, Lew JL, Huang L, Wright SD, Cui J. Polyunsaturated fatty acids are FXR ligands and differentially regulate expression of FXR targets. DNA Cell Biol 2004; 23: 519-526.
38. Kemper JK. Regulation of FXR transcriptional activity in health and disease: emerging roles of FXR cofactors and post-translational modifications. Biochim Biophys Acta 2011; 1812: 842-850.
39. Kaimal R, Song X, Yan B, King R, Deng R. Differential modulation of farnesoid X receptor signaling pathway by the thiazolidinediones. J Pharmacol Exp Ther 2009; 330: 125-134.
40. Reschly EJ, Ai N, Ekins S, Welsh WJ, Hagey LR, Hofmann AF, et al. Evolution of the bile salt nuclear receptor FXR in vertebrates. J Lipid Res 2008; 49: 1577-1587.
41. Li G, Lin W, Araya JJ, Chen T, Timmermann BN, Guo GL. A tea catechin, epigallocatechin-3-gallate, is a unique modulator of the farnesoid X receptor. Toxicol Appl Pharmacol 2012; 258: 268-274.
42. Meng LJ, Reyes H, Palma J, Hernandez I, Ribalta J, Sjovall J. Effects of ursodeoxycholic acid on conjugated bile acids and progesterone metabolites in serum and urine of patients with intrahepatic cholestasis of pregnancy. J Hepatol 1997; 27: 1029-1040.
43. Glantz A, Reilly SJ, Benthin L, Lammert F, Mattsson LA, Marschall HU. Intrahepatic cholestasis of pregnancy: amelioration of pruritus by UDCA is associated with decreased progesterone disulphates in urine. HEPATOLOGY 2008; 47: 544-551.
44. Dann AT, Kenyon AP, Wierzbicki AS, Seed PT, Shennan AH, Tribe RM. Plasma lipid profiles of women with intrahepatic cholestasis of pregnancy. Obstet Gynecol 2006; 107: 106-114.
45. Lammert F, Marschall HU, Glantz A, Matern S. Intrahepatic cholestasis of pregnancy: molecular pathogenesis, diagnosis and management. J Hepatol 2000; 33: 1012-1021.
46. Moschetta A, Bookout AL, Mangelsdorf DJ. Prevention of cholesterol gallstone disease by FXR agonists in a mouse model. Nat Med 2004; 10: 1352-1358.