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Male and Female Placentas Have Divergent Transcriptomic and Epigenomic Responses to Maternal Diets: Not Just Hormones

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Hormones, Intrauterine Health and Programming

Abstract

There is mounting evidence that the placenta can be considered as a programming agent of adult health and diseases. Placental weight and shape at term are correlated with the development of metabolic diseases in adulthood in humans. Maternal obesity and malnutrition predispose the offspring to developing metabolic syndrome, a vicious cycle leading to transmission to subsequent generation(s), with differences in response and susceptibility according to the sex of the individual. Adaptations in placental phenotype in response to maternal diet and body composition alter fetal nutrient provision. This finding implies important epigenetic changes. However, the epigenetics of placental development in studies of developmental origins of health and disease (DOHaD) is still poorly documented, particularly concerning overnutrition. We used histology, microarray analyses and epigenetic techniques to investigate the effects of a high fat diet (HFD) or low protein diet on mouse placental development, respectively. We showed for the first time that not only the gene sets but also their biological functions affected by the HFD differed markedly between the two sexes. Remarkably, genes of the epigenetic machinery as well as global DNA methylation level showed sexual dimorphism. Imprinted gene expression was altered, with locus-specific changes in DNA methylation. Thus, these findings demonstrate a striking sexual dimorphism of programming trajectories in response to the same environmental challenge, implicating sex chromosome genes, not just hormones. Explaining the sex-specific causal variables and how males versus females respond and adapt, and to what extent, to environmental perturbations should help physicians and patients anticipate disease susceptibility.

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References

  • Al-Khan A, Aye IL, Barsoum I, Borbely A, Cebral E, Cerchi G, Clifton VL, Collins S, Cotechini T, Davey A, Flores-Martin J, Fournier T, Franchi AM, Fretes RE, Graham CH, Godbole G, Hansson SR, Headley PL, Ibarra C, Jawerbaum A, Kemmerling U, Kudo Y, Lala PK, Lassance L, Lewis RM, Menkhorst E, Morris C, Nobuzane T, Ramos G, Rote N, Saffery R, Salafia C, Sarr D, Schneider H, Sibley C, Singh AT, Sivasubramaniyam TS, Soares MJ, Vaughan O, Zamudio S, Lash GE (2011) IFPA Meeting 2010 Workshops Report II: placental pathology; trophoblast invasion; fetal sex; parasites and the placenta; decidua and embryonic or fetal loss; trophoblast differentiation and syncytialisation. Placenta 32(Suppl 2):S90–S99

    Article  PubMed  Google Scholar 

  • Armitage JA, Taylor PD, Poston L (2005) Experimental models of developmental programming: consequences of exposure to an energy rich diet during development. J Physiol 565:3–8

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Arnold AP, Lusis AJ (2012) Understanding the sexome: measuring and reporting sex differences in gene systems. Endocrinology 153:2551–2555

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Asaka J, Terada T, Okuda M, Katsura T, Inui K (2006) Androgen receptor is responsible for rat organic cation transporter 2 gene regulation but not for rOCT1 and rOCT3. Pharm Res 23:697–704

    Article  CAS  PubMed  Google Scholar 

  • Attig L, Gabory A, Junien C (2010) Early nutrition and epigenetic programming: chasing shadows. Curr Opin Clin Nutr Metab Care 13:284–293

    Article  CAS  PubMed  Google Scholar 

  • Bale TL (2011) Sex differences in prenatal epigenetic programming of stress pathways. Stress 14:348–356

    PubMed  Google Scholar 

  • Barker DJ (1992) The fetal origins of diseases of old age. Eur J Clin Nutr 46(Suppl 3):S3–S9

    PubMed  Google Scholar 

  • Barker DJ, Osmond C (1988) Low birth weight and hypertension. BMJ 297:134–135

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bermejo-Alvarez P, Rizos D, Rath D, Lonergan P, Gutierrez-Adan A (2008) Epigenetic differences between male and female bovine blastocysts produced in vitro. Physiol Genom 32:264–272

    Article  CAS  Google Scholar 

  • Bermejo-Alvarez P, Rizos D, Rath D, Lonergan P, Gutierrez-Adan A (2010) Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. Proc Natl Acad Sci U S A 107:3394–3399

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bermejo-Alvarez P, Rizos D, Lonergan P, Gutierrez-Adan A (2011) Transcriptional sexual dimorphism during preimplantation embryo development and its consequences for developmental competence and adult health and disease. Reproduction 141:563–570

    Article  CAS  PubMed  Google Scholar 

  • Boloker J, Gertz SJ, Simmons RA (2002) Gestational diabetes leads to the development of diabetes in adulthood in the rat. Diabetes 51:1499–1506

    Article  CAS  PubMed  Google Scholar 

  • Boujendar S, Arany E, Hill D, Remacle C, Reusens B (2003) Taurine supplementation of a low protein diet fed to rat dams normalizes the vascularization of the fetal endocrine pancreas. J Nutr 133:2820–2825

    CAS  PubMed  Google Scholar 

  • Burdge GC, Lillycrop KA (2010) Nutrition, epigenetics, and developmental plasticity: implications for understanding human disease. Ann Rev Nutr 30:1–7

    Article  Google Scholar 

  • Carrel L, Willard HF (2005) X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434:400–404

    Article  CAS  PubMed  Google Scholar 

  • Charalambous M, da Rocha ST, Ferguson-Smith AC (2007) Genomic imprinting, growth control and the allocation of nutritional resources: consequences for postnatal life. Curr Opin Endocrinol Diabetes Obes 14:3–12

    Article  CAS  PubMed  Google Scholar 

  • Clifton VL (2010) Review: sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta 31(Suppl):S33–S39

    Article  PubMed  Google Scholar 

  • Clifton VL, Engel P, Smith R, Gibson P, Brinsmead M, Giles WB (2009) Maternal and neonatal outcomes of pregnancies complicated by asthma in an Australian population. Aust N Z J Obstet Gynaecol 49:619–626

    Article  PubMed  Google Scholar 

  • Clifton VL, Hodyl NA, Murphy VE, Giles WB, Baxter RC, Smith R (2010) Effect of maternal asthma, inhaled glucocorticoids and cigarette use during pregnancy on the newborn insulin-like growth factor axis. Growth Horm IGF Res 20:39–48

    Article  CAS  PubMed  Google Scholar 

  • Coan PM, Vaughan OR, Sekita Y, Finn SL, Burton GJ, Constancia M, Fowden AL (2010) Adaptations in placental phenotype support fetal growth during undernutrition of pregnant mice. J Physiol 588:527–538

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Constância M, Angiolini E, Sandovici I, Smith P, Smith R, Kelsey G, Dean W, Ferguson-Smith A, Sibley CP, Reik W, Fowden A (2005) Adaptation of nutrient supply to fetal demand in the mouse involves interaction between the Igf2 gene and placental transporter systems. Proc Natl Acad Sci U S A 102:19219–19224

    Article  PubMed Central  PubMed  Google Scholar 

  • Cross JC, Mickelson L (2006) Nutritional influences on implantation and placental development. Nutr Rev 64:S12–S18, discussion S72–91

    Article  PubMed  Google Scholar 

  • Cross JC, Baczyk D, Dobric N, Hemberger M, Hughes M, Simmons DG, Yamamoto H, Kingdom JCP (2003) Genes, development and evolution of the placenta. Placenta 24:123–130

    Article  CAS  PubMed  Google Scholar 

  • Dabelea D, Hanson RL, Lindsay RS, Pettitt DJ, Imperatore G, Gabir MM, Roumain J, Bennett PH, Knowler WC (2000) Intrauterine exposure to diabetes conveys risks for type 2 diabetes and obesity: a study of discordant sibships. Diabetes 49:2208–2211

    Article  CAS  PubMed  Google Scholar 

  • Davies W, Wilkinson LS (2006) It is not all hormones: alternative explanations for sexual differentiation of the brain. Brain Res 1126:36–45

    Article  CAS  PubMed  Google Scholar 

  • Deplus R, Brenner C, Burgers WA, Putmans P, Kouzarides T, de Launoit Y, Fuks F (2002) Dnmt3L is a transcriptional repressor that recruits histone deacetylase. Nucleic Acids Res 30:3831–3838

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dolinoy DC, Weidman JR, Waterland RA, Jirtle RL (2006) Maternal genistein alters coat color and protects Avy mouse offspring from obesity by modifying the fetal epigenome. Environ Health Perspect 114:567–572

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dunn GA, Morgan CP, Bale TL (2010) Sex-specificity in transgenerational epigenetic programming. Horm Behav 59:290–295

    Article  PubMed  Google Scholar 

  • Eriksson JG, Kajantie E, Osmond C, Thornburg K, Barker DJ (2009) Boys live dangerously in the womb. Am J Hum Biol 22:330–335

    Article  Google Scholar 

  • Fryer AA, Nafee TM, Ismail KM, Carroll WD, Emes RD, Farrell WE (2009) LINE-1 DNA methylation is inversely correlated with cord plasma homocysteine in man: a preliminary study. Epigenetics 4:394–398

    Article  CAS  PubMed  Google Scholar 

  • Gabory A, Attig L, Junien C (2009) Sexual dimorphism in environmental epigenetic programming. Mol Cell Endocrinol 25:8–18

    Article  Google Scholar 

  • Gabory A, Ferry L, Fajardy I, Jouneau L, Gothie JD, Vige A, Fleur C, Mayeur S, Gallou-Kabani C, Gross MS, Attig L, Vambergue A, Lesage J, Reusens B, Vieau D, Remacle C, Jais JP, Junien C (2012) Maternal diets trigger sex-specific divergent trajectories of gene expression and epigenetic systems in mouse placenta. PLoS One 7:e47986

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gabory A, Roseboom TJ, Moore T, Moore LG, Junien C (2013) Placental contribution to the origins of sexual dimorphism in health and diseases: sex chromosomes and epigenetics. Biol Sex Diff 2013:4–5

    Google Scholar 

  • Gallou-Kabani C, Vige A, Gross MS, Rabes JP, Boileau C, Larue-Achagiotis C, Tome D, Jais JP, Junien C (2007) C57BL/6J and A/J mice fed a high-fat diet delineate components of metabolic syndrome. Obesity (Silver Spring) 15:1996–2005

    Article  CAS  Google Scholar 

  • Gallou-Kabani C, Gabory A, Tost J, Karimi M, Mayeur S, Lesage J, Boudadi E, Gross MS, Taurelle J, Vige A, Breton C, Reusens B, Remacle C, Vieau D, Ekström TJ, Jais JP, Junien C (2010) Sex- and diet-specific changes of imprinted gene expression and DNA methylation in mouse placenta under a high-fat diet. PLoS One 5:e14398

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gheorghe CP, Goyal R, Mittal A, Longo LD (2010) Gene expression in the placenta: maternal stress and epigenetic responses. Int J Dev Biol 54:507–523

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Giraudo SQ, Della-Fera MA, Proctor L, Wickwire K, Ambati S, Baile CA (2010) Maternal high fat feeding and gestational dietary restriction: effects on offspring body weight, food intake and hypothalamic gene expression over three generations in mice. Pharmacol Biochem Behav 97:121–129

    Article  CAS  PubMed  Google Scholar 

  • Graves JA (2010) Review: sex chromosome evolution and the expression of sex-specific genes in the placenta. Placenta 31(Suppl):S27–S32

    Article  PubMed  Google Scholar 

  • Hellman A, Chess A (2007) Gene body-specific methylation on the active X chromosome. Science 315:1141–1143

    Article  CAS  PubMed  Google Scholar 

  • Howerton CL, Bale TL (2012) Prenatal programing: at the intersection of maternal stress and immune activation. Horm Behav 62:237–242

    Article  PubMed Central  PubMed  Google Scholar 

  • Iwase S, Lan F, Bayliss P, de la Torre-Ubieta L, Huarte M, Qi HH, Whetstine JR, Bonni A, Roberts TM, Shi Y (2007) The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell 128:1077–1088

    Article  CAS  PubMed  Google Scholar 

  • Jeong KS, Lee S (2005) Estimating the total mouse DNA methylation according to the B1 repetitive elements. Biochem Biophys Res Commun 335:1211–1216

    Article  CAS  PubMed  Google Scholar 

  • Karimi M, Johansson S, Stach D, Corcoran M, Grander D, Schalling M, Bakalkin G, Lyko F, Larsson C, Ekstrom TJ (2006) LUMA (LUminometric Methylation Assay) – a high throughput method to the analysis of genomic DNA methylation. Exp Cell Res 312:1989–1995

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi H, Sakurai T, Imai M, Takahashi N, Fukuda A, Yayoi O, Sato S, Nakabayashi K, Hata K, Sotomaru Y, Suzuki Y, Kono T (2012) Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS Genet 8:e1002440

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kokalj-Vokac N, Zagorac A, Pristovnik M, Bourgeois CA, Dutrillaux B (1998) DNA methylation of the extraembryonic tissues: an in situ study on human metaphase chromosomes. Chromosome Res 6:161–166

    Article  CAS  PubMed  Google Scholar 

  • Kral JG, Biron S, Simard S, Hould FS, Lebel S, Marceau S, Marceau P (2006) Large maternal weight loss from obesity surgery prevents transmission of obesity to children who were followed for 2 to 18 years. Pediatrics 118:e1644–e1649

    Article  PubMed  Google Scholar 

  • Lampl M, Gotsch F, Kusanovic JP, Gomez R, Nien JK, Frongillo EA, Romero R (2010) Sex differences in fetal growth responses to maternal height and weight. Am J Hum Biol 22:431–443

    Article  PubMed Central  PubMed  Google Scholar 

  • Levin BE, Govek E (1998) Gestational obesity accentuates obesity in obesity-prone progeny. Am J Physiol 275:R1374–R1379

    CAS  PubMed  Google Scholar 

  • Li N, Carrel L (2008) Escape from X chromosome inactivation is an intrinsic property of the Jarid1c locus. Proc Natl Acad Sci U S A 105:17055–17060

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liang C, Decourcy K, Prater MR (2010) High-saturated-fat diet induces gestational diabetes and placental vasculopathy in C57BL/6 mice. Metabolism 59:943–950

    Article  CAS  PubMed  Google Scholar 

  • Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC (2005) Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 135:1382–1386

    CAS  PubMed  Google Scholar 

  • Lubchenco LO, Hansman C, Dressler M, Boyd E (1963) Intrauterine growth as estimated from liveborn birth-weight data at 24 to 42 weeks of gestation. Pediatrics 32:793–800

    CAS  PubMed  Google Scholar 

  • Mao J, Zhang X, Sieli PT, Falduto MT, Torres KE, Rosenfeld CS (2010) Contrasting effects of different maternal diets on sexually dimorphic gene expression in the murine placenta. Proc Natl Acad Sci U S A 107:5557–5562

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • McMillen IC, Robinson JS (2005) Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 85:571–633

    Article  CAS  PubMed  Google Scholar 

  • Mittelstrass K, Ried JS, Yu Z, Krumsiek J, Gieger C, Prehn C, Roemisch-Margl W, Polonikov A, Peters A, Theis FJ, Meitinger T, Kronenberg F, Weidinger S, Wichmann HE, Suhre K, Wang-Sattler R, Adamski J, Illig T (2011) Discovery of sexual dimorphisms in metabolic and genetic biomarkers. PLoS Genet 7:e1002215

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mittwoch U (1993) Blastocysts prepare for the race to be male. Hum Reprod 8:1550–1555

    CAS  PubMed  Google Scholar 

  • Nathanielsz PW, Poston L, Taylor PD (2007) In utero exposure to maternal obesity and diabetes: animal models that identify and characterize implications for future health. Obstet Gynecol Clin North Am 34:201–212, vii–viii

    Article  PubMed  Google Scholar 

  • Ng RK, Dean W, Dawson C, Lucifero D, Madeja Z, Reik W, Hemberger M (2008) Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5. Nat Cell Biol 10:1280–1290

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ (2010) Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 467:963–966

    Article  CAS  PubMed  Google Scholar 

  • Novakovic B, Saffery R (2012) The ever growing complexity of placental epigenetics - role in adverse pregnancy outcomes and fetal programming. Placenta 33:959–970

    Article  CAS  PubMed  Google Scholar 

  • Ooi SK, Qiu C, Bernstein E, Li K, Jia D, Yang Z, Erdjument-Bromage H, Tempst P, Lin SP, Allis CD, Cheng X, Bestor TH (2007) DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448:714–717

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pelis RM, Hartman RC, Wright SH, Wunz TM, Groves CE (2007) Influence of estrogen and xenoestrogens on basolateral uptake of tetraethylammonium by opossum kidney cells in culture. J Pharmacol Exp Ther 323:555–561

    Article  CAS  PubMed  Google Scholar 

  • Penaloza C, Estevez B, Orlanski S, Sikorska M, Walker R, Smith C, Smith B, Lockshin RA, Zakeri Z (2009) Sex of the cell dictates its response: differential gene expression and sensitivity to cell death inducing stress in male and female cells. FASEB J 23:1869–1879

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rawn SM, Cross JC (2008) The evolution, regulation, and function of placenta-specific genes. Annu Rev Cell Dev Biol 24:159–181

    Article  CAS  PubMed  Google Scholar 

  • Reynolds LP, Borowicz PP, Caton JS, Vonnahme KA, Luther JS, Hammer CJ, Maddock Carlin KR, Grazul-Bilska AT, Redmer DA (2010) Developmental programming: the concept, large animal models, and the key role of uteroplacental vascular development. J Anim Sci 88:E61–E72

    Article  CAS  PubMed  Google Scholar 

  • Sleutels F, Zwart R, Barlow DP (2002) The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature 415:810–813

    Article  CAS  PubMed  Google Scholar 

  • Smallwood SA, Tomizawa S, Krueger F, Ruf N, Carli N, Segonds-Pichon A, Sato S, Hata K, Andrews SR, Kelsey G (2011) Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat Genet 43:811–814

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Smith J, Cianflone K, Biron S, Hould FS, Lebel S, Marceau S, Lescelleur O, Biertho L, Simard S, Kral JG, Marceau P (2009) Effects of maternal surgical weight loss in mothers on intergenerational transmission of obesity. J Clin Endocrinol Metab 94:4275–4283

    Article  CAS  PubMed  Google Scholar 

  • Sood R, Zehnder JL, Druzin ML, Brown PO (2006) Gene expression patterns in human placenta. Proc Natl Acad Sci U S A 103:5478–5483

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Srinivasan M, Katewa SD, Palaniyappan A, Pandya JD, Patel MS (2006) Maternal high-fat diet consumption results in fetal malprogramming predisposing to the onset of metabolic syndrome-like phenotype in adulthood. Am J Physiol Endocrinol Metab 291:E792–E799

    Article  CAS  PubMed  Google Scholar 

  • Sturmey RG, Bermejo-Alvarez P, Gutierrez-Adan A, Rizos D, Leese HJ, Lonergan P (2010) Amino acid metabolism of bovine blastocysts: a biomarker of sex and viability. Mol Reprod Dev 77:285–296

    Article  CAS  PubMed  Google Scholar 

  • Suter M, Abramovici A, Showalter L, Hu M, Shope CD, Varner M, Aagaard-Tillery K (2010) In utero tobacco exposure epigenetically modifies placental CYP1A1 expression. Metabolism 59:1481–1490

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Torrens C, Brawley L, Anthony FW, Dance CS, Dunn R, Jackson AA, Poston L, Hanson MA (2006) Folate supplementation during pregnancy improves offspring cardiovascular dysfunction induced by protein restriction. Hypertension 47:982–987

    Article  CAS  PubMed  Google Scholar 

  • Urakami Y, Okuda M, Saito H, Inui K (2000) Hormonal regulation of organic cation transporter OCT2 expression in rat kidney. FEBS Lett 473:173–176

    Article  CAS  PubMed  Google Scholar 

  • van Abeelen AF, de Rooij SR, Osmond C, Painter RC, Veenendaal MV, Bossuyt PM, Elias SG, Grobbee DE, van der Schouw YT, Barker DJ, Roseboom TJ (2011) The sex-specific effects of famine on the association between placental size and later hypertension. Placenta 32:694–698

    Article  PubMed  Google Scholar 

  • van Nas A, Guhathakurta D, Wang SS, Yehya N, Horvath S, Zhang B, Ingram-Drake L, Chaudhuri G, Schadt EE, Drake TA, Arnold AP, Lusis AJ (2009) Elucidating the role of gonadal hormones in sexually dimorphic gene coexpression networks. Endocrinology 150:1235–1249

    Article  PubMed Central  PubMed  Google Scholar 

  • Vucetic Z, Kimmel J, Totoki K, Hollenbeck E, Reyes TM (2010) Maternal high-fat diet alters methylation and gene expression of dopamine and opioid-related genes. Endocrinology 151:4756–4764

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Waddell J, McCarthy MM (2012) Sexual differentiation of the brain and ADHD: what is a sex difference in prevalence telling us? Curr Top Behav Neurosci 9:341–360

    Article  PubMed  Google Scholar 

  • Wagschal A, Feil R (2006) Genomic imprinting in the placenta. Cytogenet Genome Res 113:90–98

    Article  CAS  PubMed  Google Scholar 

  • Wallace JM, Horgan GW, Bhattacharya S (2012) Placental weight and efficiency in relation to maternal body mass index and the risk of pregnancy complications in women delivering singleton babies. Placenta 33:611–618

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Pringle KG, Sykes SD, Marques FZ, Morris BJ, Zakar T, Lumbers ER (2011) Fetal sex affects expression of renin-angiotensin system components in term human decidua. Endocrinology 153:462–468

    Article  PubMed  Google Scholar 

  • Waterland RA, Travisano M, Tahiliani KG (2007) Diet-induced hypermethylation at agouti viable yellow is not inherited transgenerationally through the female. Faseb J 21:3380–3385

    Article  CAS  PubMed  Google Scholar 

  • Watson ED, Cross JC (2005) Development of structures and transport functions in the mouse placenta. Physiology (Bethesda) 20:180–193

    Article  CAS  Google Scholar 

  • Wauthier V, Sugathan A, Meyer RD, Dombkowski AA, Waxman DJ (2010) Intrinsic sex differences in the early growth hormone responsiveness of sex-specific genes in mouse liver. Mol Endocrinol 24:667–678

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Weber M, Davies JJ, Wittig D, Oakeley EJ, Haase M, Lam WL, Schubeler D (2005) Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nat Genet 37:853–862

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Burgoyne PS, Arnold AP (2002) Sex differences in sex chromosome gene expression in mouse brain. Hum Mol Genet 11:1409–1419

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Deng X, Disteche CM (2008) Sex-specific expression of the X-linked histone demethylase gene Jarid1c in brain. PLoS One 3:e2553

    Article  PubMed Central  PubMed  Google Scholar 

  • Yang X, Schadt EE, Wang S, Wang H, Arnold AP, Ingram-Drake L, Drake TA, Lusis AJ (2006) Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res 16:995–1004

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

These studies were supported by the Foundation Cœur et Artères (FCA No 05-T4), the Institut Benjamin Delessert, the Agence Nationale pour la Recherche (ANR 06-PNRA-022-01) and Contrat Cadre d’Aide au Projet d’Innovation Stratégique Industrielle “IT-Diab” OSEO-ISI (18/12/2008).

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Gabory, A. et al. (2014). Male and Female Placentas Have Divergent Transcriptomic and Epigenomic Responses to Maternal Diets: Not Just Hormones. In: Seckl, J., Christen, Y. (eds) Hormones, Intrauterine Health and Programming. Research and Perspectives in Endocrine Interactions, vol 12. Springer, Cham. https://doi.org/10.1007/978-3-319-02591-9_6

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