Maternal cholestasis during pregnancy programs metabolic disease in offspring

Journal of Clinical Investigation

Volumn 123, Issue 7, 2013, Pages 3172-3181

  Papacleovoulou, Georgia ^a,b   Abu Hayyeh, Shadi ^a,b   Nikolopoulou, Evanthia ^a   Briz, Oscar ^c   Owen, Bryn M ^d   Nikolova, Vanya ^a,b   Ovadia, Caroline ^a   Huang, Xiao ^e   Vaarasmaki, Marja ^f   Baumann, Marc ^e,g   Jansen, Eugene ^h   Albrecht, Christiane ^e   Jarvelin, Marjo Riitta ^f,i,j   Marin, Jose J G ^c   Knisely, A S ^k   Williamson, Catherine ^a,b  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF SALAMANCA   (Spain)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e UNIVERSITY OF BERN   (Switzerland)

^f UNIVERSITY OF OULU   (Finland)

^g UNIVERSITY OF BERN   (Switzerland)

^h NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

ⁱ IMPERIAL COLLEGE LONDON   (United Kingdom)

^j NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^k KING S COLLEGE HOSPITAL   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL;

ADOLESCENT; ADULT; ARTICLE; BODY MASS; CHOLESTASIS; CHOLESTEROL TRANSPORT; COHORT ANALYSIS; DIABETES MELLITUS; DIET; DISEASE SEVERITY; FATTY LIVER; FEMALE; FETOPLACENTAL UNIT; FINLAND; HIP; HUMAN; METABOLIC DISORDER; OBESITY; PHENOTYPE; PREGNANCY; PREGNANCY COMPLICATION; PRIORITY JOURNAL; PROGENY; SEX DIFFERENCE; UTERUS;

ADIPOSE TISSUE, WHITE; ADOLESCENT; ANIMALS; BILE ACIDS AND SALTS; BLOOD GLUCOSE; CASE-CONTROL STUDIES; CELLS, CULTURED; CHOLESTASIS, INTRAHEPATIC; DIET; DISEASE SUSCEPTIBILITY; EPIGENESIS, GENETIC; FATTY LIVER; FEMALE; HOMEOSTASIS; HUMANS; INSULIN; LIPID METABOLISM; LIVER; MALE; MICE; MICE, INBRED C57BL; OBESITY; PLACENTA; PREGNANCY; PREGNANCY COMPLICATIONS; PRENATAL EXPOSURE DELAYED EFFECTS; PRENATAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; TRANSCRIPTOME;

EID: 84879660658     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI68927     Document Type: Article

References (57)

1. Swinburn BA, et al. The global obesity pandemic: shaped by global drivers and local environments. Lancet. 2011;378(9793):804-814.
2. Godfrey KM, Barker DJ. Fetal programming and adult health. Public Health Nutr. 2001;4(2B):611-624. (Pubitemid 32524581)
3. van Abeelen AF, et al. Famine exposure in the young and the risk of type 2 diabetes in adulthood. Diabetes. 2012;61(9):2255-2260.
4. Ravelli AC, et al. Glucose tolerance in adults after prenatal exposure to famine. Lancet. 1998; 351(9097):173-177. (Pubitemid 28037007)
5. Boney CM, Verma A, Tucker R, Vohr BR. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics. 2005;115(3):e290-e296. (Pubitemid 43373011)
6. Tzoulaki I, et al. Relation of immediate postnatal growth with obesity and related metabolic risk factors in adulthood: the northern Finland birth cohort 1966 study. Am J Epidemiol.2010; 171(9):989-998.
7. Samuelsson AM, et al. Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension. 2008;51(2):383-392.
8. Sheau-Fang N, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature. 2010;467(7318):963-966.
9. Burns SP, et al. Gluconeogenesis, glucose handling, and structural changes in livers of the adult offspring of rats partially deprived of protein during pregnancy and lactation. J Clin Invest. 1997;100(7):1768-1774. (Pubitemid 27431334)
10. +-taurocholate Co-transporting polypeptide-mediated bile acid transport by cholestatic sulfated progesterone metabolites. J Biol Chem. 2010;285(22):16504-16512.
11. Dixon PH, et al. Contribution of variant alleles of ABCB11 to susceptibility to intrahepatic cholestasis of pregnancy. Gut. 2009;58(4):537-544.
12. Abu-Hayyeh S, et al. Intrahepatic cholestasis of pregnancy levels of sulfated progesterone metabolites inhibit FXR resulting in a pro-cholestatic phenotype. Hepatology. 2013;57(2):716-726.
13. Van Mil SW, et al. Functional variants of the central bile acid sensor FXR identified in intrahepatic cholestasis of pregnancy. Gastroenterology. 2007; 133(2):507-516.
14. Dixon PH, et al. Heterozygous MDR3 missense mutation associated with intrahepatic cholestasis of pregnancy: evidence for a defect in protein trafficking. Hum Mol Genet. 2000;9(8):1209-1217. (Pubitemid 30248607)
15. Mullenbach R, et al. ABCB4 gene sequence variation in women with intrahepatic cholestasis of pregnancy. J Med Genet. 2003;40(5):e70.
16. Pauli-Magnus 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(2):91-102. (Pubitemid 38253644)
17. Milona A, et al. Raised hepatic bile acid concentrations during pregnancy in mice are associated with reduced farnesoid X receptor function. Hepatology. 2010;52(4):1341-1349.
18. Reyes H, Sjovall J. Bile acids and progesterone metabolites in intrahepatic cholestasis of pregnancy. Ann Med. 2000;32(2):94-106. (Pubitemid 30153904)
19. Papacleovoulou G, Abu-Hayyeh S, Williamson C. Nuclear receptor-driven alterations in bile acid and lipid metabolic pathways during gestation. Biochim Biophys Acta. 2011;1812(8):879-887.
20. 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(1):106-114.
21. Glantz A, Marschall HU, Mattsson LA. Intrahepatic cholestasis of pregnancy: Relationships between bile acid levels and fetal complication rates. Hepatology. 2004;40(2):467-474. (Pubitemid 39062865)
22. Geenes V, Williamson C. Intrahepatic cholestasis of pregnancy. World J Gastroenterol. 2009; 15(17):2049-2066.
23. Goldenberg RL, Culhane JF, Iams JD, Romero R. Epidemiology and causes of preterm birth. Lancet. 2008;371(9606):75-84.
24. Milona A, et al. The normal mechanisms of preg-nancy- induced liver growth are not maintained in mice lacking the bile acid sensor Fxr. Am J Physiol Gastrointest Liver Physiol. 2010;298(2):G151-G158.
25. Um SH, et al. Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature. 2004;431(7005):200-205. (Pubitemid 39243474)
26. Shaw RJ, et al. The kinase LKB1 mediates glucose homeostasis in liver and therapeutic effects of metformin. Science. 2005;310(5754):1642-1646. (Pubitemid 41780780)
27. Jansson T, Ekstrand Y, Bjorn C, Wennergren M, Powell TL. Alterations in the activity of placental amino acid transporters in pregnancies complicated by diabetes. Diabetes. 2002;51(7):2214-2219. (Pubitemid 34729027)
28. Yoshida S, Wada Y. Transfer of maternal cholesterol to embryo and fetus in pregnant mice. J Lipid Res. 2005;46(10):2168-2174. (Pubitemid 41377468)
29. Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nat Rev Genet. 2007;8(4):253-262. (Pubitemid 46439287)
30. Dolinoy DC, Hu D, Jirtle RL. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc Natl Acad Sci U S A. 2007;104(32):13056-13061. (Pubitemid 351737592)
31. Dolinoy DC, Weinhouse C, Jones TR, Rozek LS, Jirtle RL. Variable histone modifications at the A(vy) metastable epiallele. Epigenetics. 2010;5(7):637-644.
32. Miragoli M, et al. A protective antiarrhythmic role of ursodeoxycholic acid in an in vitro rat model of the cholestatic fetal heart. Hepatology. 2011; 54(4):1282-1292.
33. Germain AM, Kato S, Carvajal JA, Valenzuela GJ, Valdes GL, Glasinovic JC. Bile acids increase response and expression of human myometrial oxytocin receptor. Am J Obstet Gynecol. 2003;189(2):577-582.
34. Kim SY, England JL, Sharma JA, Njoroge T. Gestational diabetes mellitus and risk of childhood overweight and obesity in offspring: a systematic review. Exp Diabetes Res. 2011;2011:541308.
35. Davis EF, et al. Pre-eclampsia and offspring cardiovascular health: mechanistic insights from experimental studies. Clin Sci (Lond). 2012;123(2):53-72.
36. Vuguin P, Raab E, Liu B, Barzilai N, Simmons R. Hepatic insulin resistance precedes the development of diabetes in a model of intrauterine growth retardation. Diabetes. 2004;53(10):2617-2622. (Pubitemid 39299270)
37. Aiken CE, Ozanne SE. Sex differences in developmental programming models. Reproduction. 2013;145(1):R1-R13.
38. Uysal KT, Wiesbrock SM, Marino MW, Hotamisligil GS. Protection from obesity-induced insulin resistance in mice lacking TNF-alpha function. Nature. 1997;389(6651):610-614. (Pubitemid 27446179)
39. Gregor MF, Hotamisligil GS. Inflammatory mechanisms in obesity. Annu Rev Immunol. 2011;29:415-445.
40. Nakamura T, et al. Double-stranded RNA-dependent protein kinase links pathogen sensing with stress and metabolic homeostasis. Cell. 2010;140(3):338-348.
41. Barker DJ, Hales CN, Fall CH, Osmond C, Phipps K, Clark PM. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia. 1993;36(1):62-67. (Pubitemid 23018337)
42. Barker DJ, Martyn CN, Osmond C, Hales CN, Fall CH. Growth in utero and serum cholesterol concentrations in adult life. BMJ.1993; 307(6918):1524-1527.
43. Hales CN, et al. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ. 1991; 303(6809):1019-1022.
44. Hales CN, Barker DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992;35(7):595-601.
45. El Hajj N, et al. Metabolic programming of MEST DNA methylation by intrauterine exposure to gestational diabetes mellitus. Diabetes. 2013;62(4):1320-1328.
46. Godfrey KM, et al. Epigenetic gene promoter methylation at birth is associated with child's later adiposity. Diabetes. 2011;60(5):1528-1534.
47. Mouralidarane A, et al. Maternal obesity programs offspring non-alcoholic fatty liver disease via innate immune dysfunction in mice [published online ahead of print January 12, 2013]. Hepatology. doi:10.1002/hep.26248.
48. McCurdy CE, et al. Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. J Clin Invest. 2009;119(2):323-335.
49. Chappell LC, Gurung V, Seed PT, Chambers J, Williamson C, Thornton JG. Ursodeoxycholic acid versus placebo, and early term delivery versus expectant management, in women with intrahepatic cholestasis of pregnancy: semifactorial randomised clinical trial. BMJ. 2012;344:e3799.
50. Bacq Y, et al. Efficacy of ursodeoxycholic acid in treating intrahepatic cholestasis of pregnancy: a meta-analysis. Gastroenterology. 2012;143(6):1492-1501.
51. Glantz A, Marschall HU, Lammert F, Mattsson LA. Intrahepatic cholestasis of pregnancy: a randomized controlled trial comparing dexamethasone and ursodeoxycholic acid. Hepatology. 2005;42(6):1399-1405. (Pubitemid 43260043)
52. Pascual MJ, Serrano MA, El-Mir MY, Macias RI, Jimenez F, Marin JJ. Relationship between asymptomatic hypercholanaemia of pregnancy and progesterone metabolism. Clin Sci (Lond). 2002; 102(5):587-593. (Pubitemid 34494201)
53. Jarvelin MR, et al. Ecological and individual predictors of birthweight in a northern Finland birth cohort 1986. Paediatr Perinat Epidemiol.1997; 11(3):298-312.
54. Brennan K, et al. Intragenic ATM methylation in peripheral blood DNA as a biomarker of breast cancer risk. Cancer Res. 2012;72(9):2304-2313.
55. Gupta RK, et al. Zfp423 expression identifies committed preadipocytes and localizes to adipose endothelial and perivascular cells. Cell Metab. 2012; 15(2):230-239.
56. Vicens M, et al. Inhibition of the intestinal absorption of bile acids using cationic derivatives: mechanism and repercussions. Biochem Pharmacol. 2007; 73(3):394-404. (Pubitemid 44958374)
57. Nikitina L, Wenger F, Baumann M, Surbek D, Korner M, Albrecht C. Expression and localization pattern of ABCA1 in diverse human placental primary cells and tissues. Placenta. 2011;32(6):420-430.