Bile acid-FXRa pathways regulate male sexual maturation in mice

Oncotarget

Volumn 7, Issue 15, 2016, Pages 19468-19482

  Baptissart, Marine ^a,b,c,d   Martinot, Emmanuelle ^a,b,c,d   Vega, Aurélie ^a,b,c,d   Sédes, Lauriane ^a,b,c,d   Rouaisnel, Betty ^a,b,c,d   De Haze, Angélique ^a,b,c,d   Baron, Silvère ^a,b,c,d   Schoonjans, Kristina ^e   Caira, Françoise ^a,b,c,d   Volle, David H ^a,b,c,d  

^a Faculté de Médecine   (France)

^b laboratoire des adaptations métaboliques à l'exercice en conditions physiologiques et pathologiques   (France)

^c CNRS   (France)

^d CRNH AUVERGNE   (France)

^e EPFL   (Switzerland)

Author keywords

Bile acid; Germ cell apoptosis; Hypothalamo pituitary axis; Nuclear receptors; Testicular steroidogenesis

Indexed keywords

BILE ACID; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FARNESOL; FARNESOL X RECEPTOR ALPHA; LUTEINIZING HORMONE RECEPTOR; NUCLEAR RECEPTOR DAX 1; PROTEIN TYROSINE PHOSPHATASE SHP; TESTOSTERONE; UNCLASSIFIED DRUG; 3 [2 [2 CHLORO 4 [3 (2,6 DICHLOROPHENYL) 5 ISOPROPYL 4 ISOXAZOLYLMETHOXY]PHENYL]VINYL]BENZOIC ACID; CELL RECEPTOR; CHOLIC ACID; FARNESOID X-ACTIVATED RECEPTOR; ISOXAZOLE DERIVATIVE;

ANIMAL CELL; APOPTOSIS; ARTICLE; BILE ACID BLOOD LEVEL; BODY HEIGHT; CELL DEATH; CELL DIFFERENTIATION; CELL SURVIVAL; CONTROLLED STUDY; DAX 1 GENE; DOWN REGULATION; GENE EXPRESSION REGULATION; GERM CELL; GROWTH DISORDER; HYPOTHALAMUS HYPOPHYSIS SYSTEM; INTRACELLULAR SIGNALING; LEYDIG CELL; LHCGR GENE; MALE; MALE INFERTILITY; MALE SEXUAL MATURATION; MOUSE; NONHUMAN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PUBERTY; SEXUAL MATURATION; SHP GENE; SPERMATOZOON COUNT; TESTIS FUNCTION; TESTOSTERONE METABOLISM; TESTOSTERONE SYNTHESIS; WEIGHT GAIN; AGONISTS; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; CELL LINE; CYTOLOGY; DRUG EFFECTS; FERTILITY; GENETICS; KNOCKOUT MOUSE; METABOLISM; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TESTIS;

ANIMALS; BILE ACIDS AND SALTS; CELL LINE; CHOLIC ACID; FERTILITY; ISOXAZOLES; LEYDIG CELLS; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, BIOLOGICAL; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RNA INTERFERENCE; SEXUAL MATURATION; SIGNAL TRANSDUCTION; TESTIS; TESTOSTERONE;

EID: 84964792501     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.7153     Document Type: Article

References (30)

1. Volle DH, Duggavathi R, Magnier BC, Houten SM, Cummins CL, Lobaccaro J-MA, Verhoeven G, Schoonjans K, Auwerx J. The small heterodimer partner is a gonadal gatekeeper of sexual maturation in male mice. Genes Dev 2007; 21:303-15.
2. Van Thiel DH, Gavaler JS, Zajko AB, Cobb CF. Consequences of complete bile-duct ligation on the pubertal process in the male rat. J Pediatr Gastroenterol Nutr 1985; 4:616-21.
3. Wilson JD, Leihy MW, Shaw G, Renfree MB. Androgen physiology: unsolved problems at the millennium. Mol Cell Endocrinol 2002; 198:1-5.
4. Watanabe M, Houten SM, Mataki C, Christoffolete MA, Kim BW, Sato H, Messaddeq N, Harney JW, Ezaki O, Kodama T, Schoonjans K, Bianco AC, Auwerx J. Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature 2006; 439:484-9.
5. Volle DH, Mouzat K, Duggavathi R, Siddeek B, Déchelotte P, Sion B, Veyssière G, Benahmed M, Lobaccaro J-MA. Multiple roles of the nuclear receptors for oxysterols liver X receptor to maintain male fertility. Mol Endocrinol 2007; 21:1014-27.
6. Delbès G, Levacher C, Duquenne C, Racine C, Pakarinen P, Habert R. Endogenous estrogens inhibit mouse fetal Leydig cell development via estrogen receptor alpha. Endocrinology 2005; 146:2454-61.
7. Vaucher L, Funaro MG, Mehta A, Mielnik A, Bolyakov A, Prossnitz ER, Schlegel PN, Paduch DA. Activation of GPER-1 estradiol receptor downregulates production of testosterone in isolated rat Leydig cells and adult human testis. PLoS ONE 2014; 9:e92425.
8. Cederroth CR, Schaad O, Descombes P, Chambon P, Vassalli J-D, Nef S. Estrogen receptor alpha is a major contributor to estrogen-mediated fetal testis dysgenesis and cryptorchidism. Endocrinology 2007; 148:5507-19.
9. Burnett LA, Light MM, Mehrotra P, Nowak RA. Stimulation of GPR30 Increases Release of EMMPRINContaining Microvesicles in Human Uterine Epithelial Cells. The Journal of Clinical Endocrinology & Metabolism 2012; 97:4613-22.
10. Volle DH, Decourteix M, Garo E, McNeilly J, Fenichel P, Auwerx J, McNeilly AS, Schoonjans K, Benahmed M. The orphan nuclear receptor small heterodimer partner mediates male infertility induced by diethylstilbestrol in mice. J Clin Invest 2009; 119:3752-64.
11. Baptissart M, Vega A, Martinot E, Pommier AJ, Houten SM, Marceau G, de Haze A, Baron S, Schoonjans K, Lobaccaro JM, Volle DH. Bile acids alter male fertility through G-protein-coupled bile acid receptor 1 signaling pathways in mice. Hepatology 2014; 60:1054-65.
12. Meeks JJ, Russell TA, Jeffs B, Huhtaniemi I, Weiss J, Jameson JL. Leydig cell-specific expression of DAX1 improves fertility of the Dax1-deficient mouse. Biol Reprod 2003; 69:154-60.
13. Jeffs B, Ito M, Yu RN, Martinson FA, Wang ZJ, Doglio LT, Jameson JL. Sertoli cell-specific rescue of fertility, but not testicular pathology, in Dax1 (Ahch)-deficient male mice. Endocrinology 2001; 142:2481-8.
14. Volle DH, Repa JJ, Mazur A, Cummins CL, Val P, Henry-Berger J, Caira F, Veyssiere G, Mangelsdorf DJ, Lobaccaro J-MA. Regulation of the aldo-keto reductase gene akr1b7 by the nuclear oxysterol receptor LXRalpha (liver X receptor-alpha) in the mouse intestine: putative role of LXRs in lipid detoxification processes. Mol Endocrinol 2004; 18:888-98.
15. Omezzine A, Chater S, Mauduit C, Florin A, Tabone E, Chuzel F, Bars R, Benahmed M. Long-term apoptotic cell death process with increased expression and activation of caspase-3 and-6 in adult rat germ cells exposed in utero to flutamide. Endocrinology 2003; 144:648-61.
16. Li J, Lu Y, Liu R, Xiong X, Zhang Z, Zhang X, Ning G, Li X. DAX1 suppresses FXR transactivity as a novel co-repressor. Biochem Biophys Res Commun 2011; 412:660-6.
17. Vega A, Martinot E, Baptissart M, de Haze A, Saru J-P, Baron S, Caira F, Schoonjans K, Lobaccaro J-MA, Volle DH. Identification of the link between the hypothalamopituitary axis and the testicular orphan nuclear receptor NR0B2 in adult male mice. Endocrinology 2014;:en20141418.
18. Ahn SW, Gang G-T, Kim YD, Ahn R-S, Harris RA, Lee C-H, Choi H-S. Insulin directly regulates steroidogenesis via induction of the orphan nuclear receptor DAX-1 in testicular Leydig cells. J Biol Chem 2013; 288:15937-46.
19. Kim JW, Peng N, Rainey WE, Carr BR, Attia GR. Liver receptor homolog-1 regulates the expression of steroidogenic acute regulatory protein in human granulosa cells. J Clin Endocrinol Metab 2004; 89:3042-7.
20. Manna PR, Chandrala SP, Jo Y, Stocco DM. cAMPindependent signaling regulates steroidogenesis in mouse Leydig cells in the absence of StAR phosphorylation. J Mol Endocrinol 2006; 37:81-95.
21. Howard WR, Pospisil JA, Njolito E, Noonan DJ. Catabolites of Cholesterol Synthesis Pathways and Forskolin as Activators of the Farnesoid X-Activated Nuclear Receptor. Toxicology and Applied Pharmacology 2000; 163:195-202.
22. Wang S, Lai K, Moy FJ, Bhat A, Hartman HB, Evans MJ. The Nuclear Hormone Receptor Farnesoid X Receptor (FXR) Is Activated by Androsterone. Endocrinology 2006; 147:4025-33.
23. Baptissart M, Vega A, Martinot E, Baron S, Lobaccaro J-MA, Volle DH. Farnesoid X receptor alpha: a molecular link between bile acids and steroid signaling? Cell Mol Life Sci 2013;
24. Hoekstra M, van der Sluis RJ, Li Z, Oosterveer MH, Groen AK, Van Berkel TJC. FXR agonist GW4064 increases plasma glucocorticoid levels in C57BL/6 mice. Mol Cell Endocrinol 2012; 362:69-75.
25. Vega A, Baptissart M, Caira F, Brugnon F, Lobaccaro J-MA, Volle DH. Epigenetic: a molecular link between testicular cancer and environmental exposures. Front Endocrinol (Lausanne) 2012; 3:150.
26. Foresta C, Schipilliti M, Ciarleglio FA, Lenzi A, D'Amico D. Male hypogonadism in cirrhosis and after liver transplantation. J Endocrinol Invest 2008; 31:470-8.
27. Knisely AS, Bull LN, Shneider BL. ATP8B1 Deficiency [Internet]. In: Pagon RA, Adam MP, Ardinger HH, Bird TD, Dolan CR, Fong C-T, Smith RJ, Stephens K, editors. GeneReviews(®). Seattle (WA): University of Washington, Seattle; 1993 [cited 2015 Jan 5]. Available from: http://www.ncbi.nlm.nih.gov/books/NBK1297/
28. Pols TW, Nomura M, Harach T, Lo Sasso G, Oosterveer MH, Thomas C, Rizzo G, Gioiello A, Adorini L, Pellicciari R, Auwerx J, Schoonjans K. TGR5 activation inhibits atherosclerosis by reducing macrophage inflammation and lipid loading. Cell Metab 2011; 14:747-57.
29. Milona A, Owen BM, van Mil S, Dormann D, Mataki C, Boudjelal M, Cairns W, Schoonjans K, Milligan S, Parker M, White R, Williamson C. The normal mechanisms of pregnancy-induced liver growth are not maintained in mice lacking the bile acid sensor Fxr. Am J Physiol Gastrointest Liver Physiol 2010; 298:G151-8.
30. García-Aragoncillo E, Carrillo J, Lalli E, Agra N, Gómez-López G, Pestaña A, Alonso J. DAX1, a direct target of EWS/FLI1 oncoprotein, is a principal regulator of cellcycle progression in Ewing's tumor cells. Oncogene 2008; 27:6034-43.