Maternal glucose homeostasis is impaired in mouse models of gestational cholestasis

被引:16
作者
Bellafante, Elena [1 ]
McIlvride, Saraid [1 ]
Nikolova, Vanya [1 ]
Fan, Hei Man [1 ]
Manna, Luiza Borges [1 ]
Chambers, Jenny [1 ,2 ]
Machirori, Mavis [2 ]
Banerjee, Anita [3 ]
Murphy, Kevin [4 ]
Martineau, Marcus [5 ]
Schoonjans, Kristina [6 ]
Marschall, Hanns-Ulrich [7 ]
Jones, Peter [1 ]
Williamson, Catherine [1 ,8 ]
机构
[1] Kings Coll London, Sch Life Course Sci, London, England
[2] Imperial Coll London, Womens Hlth Res Ctr, London, England
[3] Guys & St Thomas NHS Fdn Trust, London, England
[4] Imperial Coll London, Dept Med, London, England
[5] Imperial Coll London, Dept Surg & Canc, London, England
[6] Ecole Polytech Fed Lausanne, Lab Integrat & Syst Physiol, Lausanne, Switzerland
[7] Univ Gothenburg, Sahlgrenska Acad, Dept Mol & Clin Med, Gothenburg, Sweden
[8] Kings Coll London, Maternal & Fetal Dis Grp, Hodgkin Bldg,Guys Campus, London SE1 1UL, England
基金
英国惠康基金; 欧盟地平线“2020”;
关键词
FARNESOID-X-RECEPTOR; BILE-ACID RECEPTOR; INTRAHEPATIC CHOLESTASIS; INSULIN-SECRETION; DIFFERENTIAL REGULATION; BETA-CELLS; PREGNANCY; ACTIVATION; MICE; FXR;
D O I
10.1038/s41598-020-67968-6
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Women with intrahepatic cholestasis of pregnancy (ICP), a disorder characterised by raised serum bile acids, are at increased risk of developing gestational diabetes mellitus and have impaired glucose tolerance whilst cholestatic. FXR and TGR5 are modulators of glucose metabolism, and FXR activity is reduced in normal pregnancy, and further in ICP. We aimed to investigate the role of raised serum bile acids, FXR and TGR5 in gestational glucose metabolism using mouse models. Cholic acid feeding resulted in reduced pancreatic beta-cell proliferation and increased apoptosis in pregnancy, without altering insulin sensitivity, suggesting that raised bile acids affect beta-cell mass but are insufficient to impair glucose tolerance. Conversely, pregnant Fxr(-/-) and Tgr5(-/-) mice are glucose intolerant and have reduced insulin secretion in response to glucose challenge, and Fxr(-/-) mice are also insulin resistant. Furthermore, fecal bile acids are reduced in pregnant Fxr(-/-) mice. Lithocholic acid and deoxycholic acid, the principal ligands for TGR5, are decreased in particular. Therefore, we propose that raised serum bile acids and reduced FXR and TGR5 activity contribute to the altered glucose metabolism observed in ICP.
引用
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页数:10
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[31]   Changes in LXR signaling influence early-pregnancy lipogenesis and protect against dysregulated fetoplacental lipid homeostasis [J].
Nikolova, Vanya ;
Papacleovoulou, Georgia ;
Bellafante, Elena ;
Manna, Luiza Borges ;
Jansen, Eugene ;
Baron, Silvere ;
Abu-Hayyeh, Shadi ;
Parker, Malcolm ;
Williamson, Catherine .
AMERICAN JOURNAL OF PHYSIOLOGY-ENDOCRINOLOGY AND METABOLISM, 2017, 313 (04) :E463-E472
[33]   Association of adverse perinatal outcomes of intrahepatic cholestasis of pregnancy with biochemical markers: results of aggregate and individual patient data meta-analyses [J].
Ovadia, Caroline ;
Seed, Paul T. ;
Sklavounos, Alexandros ;
Geenes, Victoria ;
Di Illio, Chiara ;
Chambers, Jenny ;
Kohari, Katherine ;
Bacq, Yannick ;
Bozkurt, Nuray ;
Brun-Furrer, Romana ;
Bull, Laura ;
Estiu, Maria C. ;
Grymowicz, Monika ;
Gunaydin, Berrin ;
Hague, William M. ;
Haslinger, Christian ;
Hu, Yayi ;
Kawakita, Tetsuya ;
Kebapcilar, Ayse G. ;
Kebapcilar, Levent ;
Kondrackiene, Jurate ;
Koster, Maria P. H. ;
Kowalska-Kanka, Aneta ;
Kupcinskas, Limas ;
Lee, Richard H. ;
Locatelli, Anna ;
Macias, Rocio I. R. ;
Marschall, Hanns-Ulrich ;
Oudijk, Martijn A. ;
Raz, Yael ;
Rimon, Eli ;
Shan, Dan ;
Shao, Yong ;
Tribe, Rachel ;
Tripodi, Valeria ;
Abide, Cigdem Yayla ;
Yenidede, Ilter ;
Thornton, Jim G. ;
Chappell, Lucy C. ;
Williamson, Catherine .
LANCET, 2019, 393 (10174) :899-909
[34]   Maternal cholestasis during pregnancy programs metabolic disease in offspring [J].
Papacleovoulou, Georgia ;
Abu-Hayyeh, Shadi ;
Nikolopoulou, Evanthia ;
Briz, Oscar ;
Owen, Bryn M. ;
Nikolova, Vanya ;
Ovadia, Caroline ;
Huang, Xiao ;
Vaarasmaki, Marja ;
Baumann, Marc ;
Jansen, Eugene ;
Albrecht, Christiane ;
Jarvelin, Marjo-Riitta ;
Marin, Jose J. G. ;
Knisely, A. S. ;
Williamson, Catherine .
JOURNAL OF CLINICAL INVESTIGATION, 2013, 123 (07) :3172-3181
[35]   Intestine farnesoid X receptor agonist and the gut microbiota activate G-protein bile acid receptor-1 signaling to improve metabolism [J].
Pathak, Preeti ;
Xie, Cen ;
Nichols, Robert G. ;
Ferrell, Jessica M. ;
Boehme, Shannon ;
Krausz, Kristopher W. ;
Patterson, Andrew D. ;
Gonzalez, Frank J. ;
Chiang, John Y. L. .
HEPATOLOGY, 2018, 68 (04) :1574-1588
[36]   Farnesoid X receptor induces Takeda G-protein receptor 5 cross-talk to regulate bile acid synthesis and hepatic metabolism [J].
Pathak, Preeti ;
Liu, Hailiang ;
Boehme, Shannon ;
Xie, Cen ;
Krausz, Kristopher W. ;
Gonzalez, Frank ;
Chiang, John Y. L. .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2017, 292 (26) :11055-11069
[37]   The nuclear receptor FXR is expressed in pancreatic β-cells and protects human islets from lipotoxicity [J].
Popescu, Iuliana Ristea ;
Helleboid-Chapman, Audrey ;
Lucas, Anthony ;
Vandewalle, Brigitte ;
Dumont, Julie ;
Bouchaert, Emmanuel ;
Derudas, Bruno ;
Kerr-Conte, Julie ;
Caron, Sandrine ;
Pattou, Francois ;
Staels, Bart .
FEBS LETTERS, 2010, 584 (13) :2845-2851
[38]   Gut Microbiota Regulates Bile Acid Metabolism by Reducing the Levels of Tauro-beta-muricholic Acid, a Naturally Occurring FXR Antagonist [J].
Sayin, Sama I. ;
Wahlstrom, Annika ;
Felin, Jenny ;
Jantti, Sirkku ;
Marschall, Hanns-Ulrich ;
Bamberg, Krister ;
Angelin, Bo ;
Hyotylainen, Tuulia ;
Oresic, Matej ;
Backhed, Fredrik .
CELL METABOLISM, 2013, 17 (02) :225-235
[39]   Bile acids in glucose metabolism in health and disease [J].
Shapiro, Hagit ;
Kolodziejczyk, Aleksandra A. ;
Halstuch, Daniel ;
Elinav, Eran .
JOURNAL OF EXPERIMENTAL MEDICINE, 2018, 215 (02) :383-396
[40]   Intrahepatic cholestasis of pregnancy and associated adverse pregnancy and fetal outcomes: a 12-year population-based cohort study [J].
Shemer, E. Wikstroem ;
Marschall, H. U. ;
Ludvigsson, J. F. ;
Stephansson, O. .
BJOG-AN INTERNATIONAL JOURNAL OF OBSTETRICS AND GYNAECOLOGY, 2013, 120 (06) :717-723