Hostname: page-component-76fb5796d-r6qrq Total loading time: 0 Render date: 2024-04-27T18:48:09.074Z Has data issue: false hasContentIssue false
  • English
  • Français

Alteration of the embryonic microenvironment and sex-specific responses of the preimplantation embryo related to a maternal high-fat diet in the rabbit model

Published online by Cambridge University Press:  12 October 2023

Sophie Calderari Open the ORCID record for Sophie Calderari [Opens in a new window] ,
Catherine Archilla ,
Luc Jouneau ,
Nathalie Daniel ,
Nathalie Peynot ,
Michele Dahirel ,
Christophe Richard ,
Eve Mourier ,
Barbara Schmaltz-Panneau  and
Anaïs Vitorino Carvalho
...Show all authors
Sophie Calderari*
Affiliation:
Université Paris-Saclay, UVSQ, INRAE, BREED, Jouy-en-Josas 78350, France Ecole Nationale Vétérinaire d’Alfort, BREED, Maisons-Alfort 94700, France
Catherine Archilla
Affiliation:
Université Paris-Saclay, UVSQ, INRAE, BREED, Jouy-en-Josas 78350, France Ecole Nationale Vétérinaire d’Alfort, BREED, Maisons-Alfort 94700, France
Luc Jouneau
Affiliation:
Université Paris-Saclay, UVSQ, INRAE, BREED, Jouy-en-Josas 78350, France Ecole Nationale Vétérinaire d’Alfort, BREED, Maisons-Alfort 94700, France
Nathalie Daniel
Affiliation:
Université Paris-Saclay, UVSQ, INRAE, BREED, Jouy-en-Josas 78350, France Ecole Nationale Vétérinaire d’Alfort, BREED, Maisons-Alfort 94700, France
Nathalie Peynot
Affiliation:
Université Paris-Saclay, UVSQ, INRAE, BREED, Jouy-en-Josas 78350, France Ecole Nationale Vétérinaire d’Alfort, BREED, Maisons-Alfort 94700, France
Michele Dahirel
Affiliation:
Université Paris-Saclay, UVSQ, INRAE, BREED, Jouy-en-Josas 78350, France Ecole Nationale Vétérinaire d’Alfort, BREED, Maisons-Alfort 94700, France
Christophe Richard
Affiliation:
Université Paris-Saclay, UVSQ, INRAE, BREED, Jouy-en-Josas 78350, France Ecole Nationale Vétérinaire d’Alfort, BREED, Maisons-Alfort 94700, France Plateforme MIMA2-CIMA, Jouy en Josas, France
Eve Mourier
Affiliation:
Université Paris-Saclay, UVSQ, INRAE, BREED, Jouy-en-Josas 78350, France Ecole Nationale Vétérinaire d’Alfort, BREED, Maisons-Alfort 94700, France Plateforme MIMA2-CIMA, Jouy en Josas, France
Barbara Schmaltz-Panneau
Affiliation:
Université Paris-Saclay, UVSQ, INRAE, BREED, Jouy-en-Josas 78350, France Ecole Nationale Vétérinaire d’Alfort, BREED, Maisons-Alfort 94700, France
Anaïs Vitorino Carvalho
Affiliation:
Université Paris-Saclay, UVSQ, INRAE, BREED, Jouy-en-Josas 78350, France Ecole Nationale Vétérinaire d’Alfort, BREED, Maisons-Alfort 94700, France
Delphine Rousseau-Ralliard
Affiliation:
Université Paris-Saclay, UVSQ, INRAE, BREED, Jouy-en-Josas 78350, France Ecole Nationale Vétérinaire d’Alfort, BREED, Maisons-Alfort 94700, France
Franck Lager
Affiliation:
Université Paris Cité, Institut Cochin, Inserm, CNRS, Paris F-75014, France
Carmen Marchiol
Affiliation:
Université Paris Cité, Institut Cochin, Inserm, CNRS, Paris F-75014, France
Gilles Renault
Affiliation:
Université Paris Cité, Institut Cochin, Inserm, CNRS, Paris F-75014, France
Julie Gatien
Affiliation:
Research and Development Department, Eliance, Nouzilly, France
Lydie Nadal-Desbarats
Affiliation:
UMR 1253, iBrain, University of Tours, Inserm, Tours, France PST-ASB, University of Tours, Tours, France
Anne Couturier-Tarrade
Affiliation:
Université Paris-Saclay, UVSQ, INRAE, BREED, Jouy-en-Josas 78350, France Ecole Nationale Vétérinaire d’Alfort, BREED, Maisons-Alfort 94700, France
Véronique Duranthon
Affiliation:
Université Paris-Saclay, UVSQ, INRAE, BREED, Jouy-en-Josas 78350, France Ecole Nationale Vétérinaire d’Alfort, BREED, Maisons-Alfort 94700, France
Pascale Chavatte-Palmer
Affiliation:
Université Paris-Saclay, UVSQ, INRAE, BREED, Jouy-en-Josas 78350, France Ecole Nationale Vétérinaire d’Alfort, BREED, Maisons-Alfort 94700, France
*
Corresponding author: S. Calderari; Email: sophie.calderari@inrae.fr
Get access Rights & Permissions [Opens in a new window]

Abstract

The maternal metabolic environment can be detrimental to the health of the offspring. In a previous work, we showed that maternal high-fat (HH) feeding in rabbit induced sex-dependent metabolic adaptation in the fetus and led to metabolic syndrome in adult offspring. As early development representing a critical window of susceptibility, in the present work we aimed to explore the effects of the HH diet on the oocyte, preimplantation embryo and its microenvironment. In oocytes from females on HH diet, transcriptomic analysis revealed a weak modification in the content of transcripts mainly involved in meiosis and translational control. The effect of maternal HH diet on the embryonic microenvironment was investigated by identifying the metabolite composition of uterine and embryonic fluids collected in vivo by biomicroscopy. Metabolomic analysis revealed differences in the HH uterine fluid surrounding the embryo, with increased pyruvate concentration. Within the blastocoelic fluid, metabolomic profiles showed decreased glucose and alanine concentrations. In addition, the blastocyst transcriptome showed under-expression of genes and pathways involved in lipid, glucose and amino acid transport and metabolism, most pronounced in female embryos. This work demonstrates that the maternal HH diet disrupts the in vivo composition of the embryonic microenvironment, where the presence of nutrients is increased. In contrast to this nutrient-rich environment, the embryo presents a decrease in nutrient sensing and metabolism suggesting a potential protective process. In addition, this work identifies a very early sex-specific response to the maternal HH diet, from the blastocyst stage.

Keywords

preimplantation embryoDOHaDhigh-fat dietmicroenvironmentrabbit model
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 14 , Issue 5 , October 2023 , pp. 602 - 613
Check for updates
Copyright
© The Author(s), 2023. Published by Cambridge University Press in association with The International Society for Developmental Origins of Health and Disease (DOHaD)

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

a

These three authors contributed equally to this study.

References

Food-based dietary guidelines in the WHO European Region. https://www.euro.who.int/en/health-topics/disease-prevention/nutrition/publications/technical-documents/dietary-recommendations-and-nutritional-requirements/food-based-dietary-guidelines-in-the-who-european-region. Accessed June 16, 2021.Google Scholar
WHO | Global status report on noncommunicable diseases 2014. WHO. http://www.who.int/nmh/publications/ncd-status-report-2014/en/. Accessed June 7, 2021.Google Scholar
Obesity and overweight. https://www.who.int/news-room/fact-sheets/detail/obesity-and-overweight. Accessed June 9, 2021.Google Scholar
Lin, X, Xu, Y, Pan, X, et al. Global, regional, and national burden and trend of diabetes in 195 countries and territories: an analysis from 1990 to 2025. Sci Rep. 2020; 10(1), 14790.CrossRefGoogle ScholarPubMed
Poston, L, Caleyachetty, R, Cnattingius, S, et al. Preconceptional and maternal obesity: epidemiology and health consequences. Lancet Diabetes Endocrinol. 2016; 4(12), 1025–1036.CrossRefGoogle ScholarPubMed
Laz, TH, Rahman, M, Berenson, AB. Trends in serum lipids and hypertension prevalence among non-pregnant reproductive-age women: United States national health and nutrition examination survey 1999-2008. Matern Child Health J. 2013; 17(8), 1424–1431.CrossRefGoogle ScholarPubMed
Guelinckx, I, Devlieger, R, Beckers, K, Vansant, G. Maternal obesity: pregnancy complications, gestational weight gain and nutrition. Obes Rev. 2008; 9(2), 140–150.CrossRefGoogle ScholarPubMed
Palinski, W. Effect of maternal cardiovascular conditions and risk factors on offspring cardiovascular disease. Circulation. 2014; 129(20), 2066–2077.CrossRefGoogle ScholarPubMed
Williams, L, Seki, Y, Vuguin, PM, Charron, MJ. Animal models of in utero exposure to a high fat diet: a review. Biochim Biophys Acta. 2014; 1842(3), 507–519.10.1016/j.bbadis.2013.07.006CrossRefGoogle ScholarPubMed
Langley-Evans, SC. Developmental programming of health and disease. Proc Nutr Soc. 2006; 65(1), 97–105.CrossRefGoogle ScholarPubMed
Gluckman, PD, Hanson, MA, Beedle, AS. Early life events and their consequences for later disease: a life history and evolutionary perspective. Am J Hum Biol Off J Hum Biol Counc. 2007; 19(1), 1–19.10.1002/ajhb.20590CrossRefGoogle ScholarPubMed
Aiken, CE, Ozanne, SE. Sex differences in developmental programming models. Reprod Camb Engl. 2013; 145(1), R1–13.CrossRefGoogle ScholarPubMed
Palinski, W, D’Armiento, FP, Witztum, JL, et al. Maternal hypercholesterolemia and treatment during pregnancy influence the long-term progression of atherosclerosis in offspring of rabbits. Circ Res. 2001; 89(11), 991–996.CrossRefGoogle ScholarPubMed
Picone, O, Laigre, P, Fortun-Lamothe, L, et al. Hyperlipidic hypercholesterolemic diet in prepubertal rabbits affects gene expression in the embryo, restricts fetal growth and increases offspring susceptibility to obesity. Theriogenology. 2011; 75(2), 287–299.CrossRefGoogle ScholarPubMed
Tarrade, A, Rousseau-Ralliard, D, Aubrière, M-C, et al. Sexual dimorphism of the feto-placental phenotype in response to a high fat and control maternal diets in a rabbit model. PloS One. 2013; 8(12), e83458.CrossRefGoogle ScholarPubMed
Watkins, AJ, Lucas, ES, Fleming, TP. Impact of the periconceptional environment on the programming of adult disease. J Dev Orig Health Dis. 2010; 1(2), 87–95.CrossRefGoogle ScholarPubMed
Fleming, TP, Watkins, AJ, Velazquez, MA, et al. Origins of lifetime health around the time of conception: causes and consequences. Lancet Lond Engl. 2018; 391(10132), 1842–1852.CrossRefGoogle ScholarPubMed
Duranthon, V, Watson, AJ, Lonergan, P. Preimplantation embryo programming: transcription, epigenetics, and culture environment. Reprod Camb Engl. 2008; 135(2), 141–150.CrossRefGoogle ScholarPubMed
Rousseau-Ralliard, D, Couturier-Tarrade, A, Thieme, R, et al. A short periconceptional exposure to maternal type-1 diabetes is sufficient to disrupt the feto-placental phenotype in a rabbit model. Mol Cell Endocrinol. 2019; 480, 42–53.CrossRefGoogle Scholar
Nicholas, LM, Morrison, JL, Rattanatray, L, Zhang, S, Ozanne, SE, McMillen, IC. The early origins of obesity and insulin resistance: timing, programming and mechanisms. Int J Obes. 2016; 40(2), 229–238.CrossRefGoogle ScholarPubMed
Edwards, LJ, McMillen, IC. Periconceptional nutrition programs development of the cardiovascular system in the fetal sheep. Am J Physiol-Regul Integr Comp Physiol. 2002; 283(3), R669–R679.CrossRefGoogle ScholarPubMed
Calderari, S, Daniel, N, Mourier, E, et al. Metabolomic differences in blastocoel and uterine fluids collected in vivo by ultrasound biomicroscopy on rabbit embryos. Biol. Reprod. 2021; 104(4), 794–805.CrossRefGoogle ScholarPubMed
Okamoto, I, Patrat, C, Thépot, D, et al. Eutherian mammals use diverse strategies to initiate X-chromosome inactivation during development. Nature. 2011; 472(7343), 370–374.CrossRefGoogle ScholarPubMed
Jolivet, G, Daniel-Carlier, N, Harscoët, E, et al. Fetal estrogens are not involved in sex determination but critical for early ovarian differentiation in rabbits. Endocrinology. 2022; 163(1), bqab210. DOI: 10.1210/endocr/bqab210.10.1210/endocr/bqab210CrossRefGoogle Scholar
Rousseau-Ralliard, D, Valentino, SA, Aubrière, M-C, et al. Effects of first-generation in utero exposure to diesel engine exhaust on second-generation placental function, fatty acid profiles and foetal metabolism in rabbits: preliminary results. Sci Rep. 2019; 9(1), 9710.10.1038/s41598-019-46130-xCrossRefGoogle ScholarPubMed
Tapponnier, Y, Afanassieff, M, Aksoy, I, et al. Reprogramming of rabbit induced pluripotent stem cells toward epiblast and chimeric competency using Krüppel-like factors. Stem Cell Res. 2017; 24, 106–117.CrossRefGoogle ScholarPubMed
Subramanian, A, Tamayo, P, Mootha, VK, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005; 102(43), 15545–15550.CrossRefGoogle ScholarPubMed
Hutt, KJ, McLaughlin, EA, Holland, MK. Primordial follicle activation and follicular development in the juvenile rabbit ovary. Cell Tissue Res. 2006; 326(3), 809–822.CrossRefGoogle ScholarPubMed
Hennet, M1, Combelles, CMH. The antral follicle: a microenvironment for oocyte differentiation. Int J Dev Biol. 2013; 56(10-11-12), 819–831.CrossRefGoogle Scholar
Cordier, A-G, Léveillé, P, Dupont, C, et al. Dietary lipid and cholesterol induce ovarian dysfunction and abnormal LH response to stimulation in rabbits. PloS One. 2013; 8(5), e63101.CrossRefGoogle ScholarPubMed
Brevini Gandolfi, TAL, Gandolfi, F. The maternal legacy to the embryo: cytoplasmic components and their effects on early development. Theriogenology. 2001; 55(6), 1255–1276.CrossRefGoogle Scholar
Watson, AJ, De Sousa, P, Caveney, A, et al. Impact of bovine oocyte maturation media on oocyte transcript levels, blastocyst development, cell number, and Apoptosis1. Biol Reprod. 2000; 62(2), 355–364.CrossRefGoogle Scholar
Chang, AS, Dale, AN, Moley, KH. Maternal diabetes adversely affects preovulatory oocyte maturation, development, and granulosa cell apoptosis. Endocrinology. 2005; 146(5), 2445–2453.CrossRefGoogle ScholarPubMed
Ma, J-Y, Li, M, Ge, Z-J, et al. Whole transcriptome analysis of the effects of type I diabetes on mouse oocytes. PloS One. 2012; 7(7), e41981.CrossRefGoogle ScholarPubMed
Reynolds, KA, Boudoures, AL, Chi, MM-Y, Wang, Q, Moley, KH. Adverse effects of obesity and/or high-fat diet on oocyte quality and metabolism are not reversible with resumption of regular diet in mice. Reprod Fertil Dev. 2015; 27(4), 716–724.CrossRefGoogle Scholar
Chaffin, CL, Latham, KE, Mtango, NR, Midic, U, VandeVoort, CA. Dietary sugar in healthy female primates perturbs oocyte maturation and in vitro preimplantation embryo development. Endocrinology. 2014; 155(7), 2688–2695.CrossRefGoogle ScholarPubMed
Snider, AP, Wood, JR. Obesity induces ovarian inflammation and reduces oocyte quality. Reproduction. 2019; 158(3), R79–R90.CrossRefGoogle ScholarPubMed
Gonzalez, MB, Robker, RL, Rose, RD. Obesity and oocyte quality: significant implications for ART and emerging mechanistic insights. Biol Reprod. 2022; 106(2), 338–350.CrossRefGoogle ScholarPubMed
Fuchimoto, D, Mizukoshi, A, Schultz, RM, Sakai, S, Aoki, F. Posttranscriptional regulation of cyclin A1 and cyclin A2 during mouse oocyte meiotic maturation and preimplantation development. Biol Reprod. 2001; 65(4), 986–993.CrossRefGoogle ScholarPubMed
Radonova, L, Pauerova, T, Jansova, D, et al. Cyclin A1 in oocytes prevents chromosome segregation and anaphase entry. Sci Rep. 2020; 10(1), 7455.CrossRefGoogle ScholarPubMed
Biot, M, de Massy, B. Reading the epigenetic code for exchanging DNA. eLife. 2020; 9, e61820.CrossRefGoogle ScholarPubMed
Ibba, M, Soll, D. Aminoacyl-tRNA synthesis. Annu Rev Biochem. 2000; 69(1), 617–650.CrossRefGoogle ScholarPubMed
Angermayr, M, Bandlow, W. RIO1, an extraordinary novel protein kinase. FEBS Lett. 2002; 524(1-3), 31–36.CrossRefGoogle ScholarPubMed
Cheong, A, Lingutla, R, Mager, J. Expression analysis of mammalian mitochondrial ribosomal protein genes. Gene Expr Patterns. 2020; 38, 119147.10.1016/j.gep.2020.119147CrossRefGoogle ScholarPubMed
Tselykh, TV, Roos, C, Heino, TI. The mitochondrial ribosome-specific MrpL55 protein is essential in Drosophila and dynamically required during development. Exp Cell Res. 2005; 307(2), 354–366.CrossRefGoogle ScholarPubMed
Rousseau-Ralliard, D, Aubrière, M-C, Daniel, N, et al. Importance of windows of exposure to maternal high-fat diet and feto-placental effects: discrimination between pre-conception and gestational periods in a rabbit model. Front Physiol. 2021; 12, 784268.CrossRefGoogle ScholarPubMed
Leese, HJ, Tay, JI, Reischl, J, Downing, SJ. Formation of Fallopian tubal fluid: role of a neglected epithelium. Reprod Camb Engl. 2001; 121(3), 339–346.CrossRefGoogle ScholarPubMed
Li, S, Winuthayanon, W. Oviduct: roles in fertilization and early embryo development. J Endocrinol. 2017; 232(1), R1–R26.CrossRefGoogle ScholarPubMed
Yang, Y, Wang, L, Chen, C, et al. Metabolic changes of maternal uterine fluid, uterus, and plasma during the peri-implantation period of early pregnancy in mice. Reprod Sci Thousand Oaks Calif. 2020; 27(2), 488–502.CrossRefGoogle ScholarPubMed
Kermack, AJ, Finn-Sell, S, Cheong, YC, et al. Amino acid composition of human uterine fluid: association with age, lifestyle and gynaecological pathology. Hum Reprod Oxf Engl. 2015; 30(4), 917–924.CrossRefGoogle ScholarPubMed
Eckert, JJ, Porter, R, Watkins, AJ, et al. Metabolic induction and early responses of mouse blastocyst developmental programming following maternal low protein diet affecting life-long health. PloS One. 2012; 7(12), e52791.CrossRefGoogle ScholarPubMed
Tripathi, SK, Farman, M, Nandi, S, Girish Kumar, V, Gupta, PSP. Oviductal and uterine fluid analytes as biomarkers of metabolic stress in ewes (Ovis aries). Small Rumin Res. 2016; 144, 225–228.CrossRefGoogle Scholar
Leese, HJ, Hugentobler, SA, Gray, SM, et al. Female reproductive tract fluids: composition, mechanism of formation and potential role in the developmental origins of health and disease. Reprod Fertil Dev. 2008; 20(1), 1–8.CrossRefGoogle ScholarPubMed
Aguilar, J, Reyley, M. The uterine tubal fluid: secretion, composition and biological effects. Anim. Reprod. 2005; 2, 91–105. Google Scholar
Chi, F, Sharpley, MS, Nagaraj, R, Roy, SS, Banerjee, U. Glycolysis-independent glucose metabolism distinguishes TE from ICM fate during Mammalian embryogenesis. Dev Cell. 2020; 53(1), 9–26.e4.10.1016/j.devcel.2020.02.015CrossRefGoogle ScholarPubMed
Gardner, DK, Gardner, DK, Harvey, AJ, Harvey, AJ. Blastocyst metabolism. Reprod Fertil Dev. 2015; 27(4), 638. DOI: 10.1071/RD14421.CrossRefGoogle ScholarPubMed
Zhang, H, Yan, K, Sui, L, et al. Low-level pyruvate inhibits early embryonic development and maternal mRNA clearance in mice. Theriogenology. 2021; 166, 104–111.CrossRefGoogle ScholarPubMed
Zhang, T, Zheng, Y, Han, R, et al. Effects of pyruvate on early embryonic development and zygotic genome activation in pigs. Theriogenology. 2022; 189, 77–85.CrossRefGoogle ScholarPubMed
Nono Nankam, PA, Blüher, M. Retinol-binding protein 4 in obesity and metabolic dysfunctions. Mol Cell Endocrinol. 2021; 531, 111312.CrossRefGoogle ScholarPubMed
Welles, JE, Toro, AL, Sunilkumar, S, et al. Retinol-binding protein 4 mRNA translation in hepatocytes is enhanced by activation of mTORC1. Am J Physiol Endocrinol Metab. 2021; 320(2), E306–E315.CrossRefGoogle ScholarPubMed
Xu, C, Li, H, Tang, C-K. Sterol carrier protein 2 in lipid metabolism and non-alcoholic fatty liver disease: pathophysiology, molecular biology, and potential clinical implications. Metabolis. 2022; 131, 155180.10.1016/j.metabol.2022.155180CrossRefGoogle ScholarPubMed
Schroeder, F, Atshaves, BP, McIntosh, AL, et al. Sterol carrier protein-2: new roles in regulating lipid rafts and signaling. Biochim Biophys Acta. 2007; 1771(6), 700–718.CrossRefGoogle ScholarPubMed
Quirós, PM, Ramsay, AJ, Sala, D, et al. Loss of mitochondrial protease OMA1 alters processing of the GTPase OPA1 and causes obesity and defective thermogenesis in mice. EMBO J. 2012; 31(9), 2117–2133.CrossRefGoogle ScholarPubMed
Zhou, D, Sun, M-H, Lee, S-H, Cui, X-S. ROMO1 is required for mitochondrial metabolism during preimplantation embryo development in pigs. Cell Div. 2021; 16(1), 7.CrossRefGoogle ScholarPubMed
Ye, Q, Zeng, X, Cai, S, Qiao, S, Zeng, X. Mechanisms of lipid metabolism in uterine receptivity and embryo development. Trends Endocrinol Metab TEM. 2021; 32(12), 1015–1030.CrossRefGoogle ScholarPubMed
Sharpley, MS, Chi, F, Hoeve, JT, Banerjee, U. Metabolic plasticity drives development during mammalian embryogenesis. Dev Cell. 2021; 56(16), 2329–2347.e6.CrossRefGoogle ScholarPubMed
Baardman, J, Verberk, SGS, Prange, KHM, et al. A defective pentose phosphate pathway reduces inflammatory macrophage responses during hypercholesterolemia. Cell Rep. 2018; 25(8), 2044–2052.e5.CrossRefGoogle ScholarPubMed
Gandasi, NR, Arapi, V, Mickael, ME, et al. Glutamine uptake via SNAT6 and caveolin regulates glutamine-glutamate cycle. Int J Mol Sci. 2021; 22(3), 1167.CrossRefGoogle ScholarPubMed
Orsi, NM, Leese, HJ. Ammonium exposure and pyruvate affect the amino acid metabolism of bovine blastocysts in vitro. Reproduction. 2004; 127(1), 131–140.CrossRefGoogle ScholarPubMed
Humpherson, PG, Leese, HJ, Sturmey, RG. Amino acid metabolism of the porcine blastocyst. Theriogenology. 2005; 64(8), 1852–1866.CrossRefGoogle ScholarPubMed
Van Winkle, LJ, Tesch, JK, Shah, A, Campione, AL. System B0,+ amino acid transport regulates the penetration stage of blastocyst implantation with possible long-term developmental consequences through adulthood. Hum Reprod Update. 2006; 12(2), 145–157.CrossRefGoogle ScholarPubMed
Gopichandran, N, Leese, HJ. Metabolic characterization of the bovine blastocyst, inner cell mass, trophectoderm and blastocoel fluid. Reprod Camb Engl. 2003; 126(3), 299–308.CrossRefGoogle ScholarPubMed
Martínez, Y, Li, X, Liu, G, et al. The role of methionine on metabolism, oxidative stress, and diseases. Amino Acids. 2017; 49(12), 2091–2098.CrossRefGoogle ScholarPubMed
Liu, GY, Sabatini, DM. MTOR at the nexus of nutrition, growth, ageing and disease. Nat Rev Mol Cell Biol. 2020; 21(4), 183–203.CrossRefGoogle ScholarPubMed
Gürke, J, Hirche, F, Thieme, R, et al. Maternal diabetes leads to adaptation in embryonic amino acid metabolism during early pregnancy. PloS One. 2015; 10(5), e0127465.CrossRefGoogle ScholarPubMed
Fleming, TP, Sun, C, Denisenko, O, et al. Environmental exposures around conception: developmental pathways leading to lifetime disease risk. Int J Environ Res Public Health. 2021; 18(17), 9380.CrossRefGoogle ScholarPubMed
Dzeja, P, Terzic, A. Adenylate kinase and AMP signaling networks: metabolic monitoring, signal communication and body energy sensing. Int J Mol Sci. 2009; 10(4), 1729–1772.CrossRefGoogle ScholarPubMed
Leprivier, G, Rotblat, B. How does mTOR sense glucose starvation? AMPK is the usual suspect. Cell Death Discov. 2020; 6(1), 1–5.CrossRefGoogle ScholarPubMed
Chen, H-F, Chuang, H-C, Tan, T-H. Regulation of dual-specificity phosphatase (DUSP) ubiquitination and protein stability. Int J Mol Sci. 2019; 20(11), 2668.CrossRefGoogle ScholarPubMed
Dunn, C, Wiltshire, C, MacLaren, A, Gillespie, DAF. Molecular mechanism and biological functions of c-Jun N-terminal kinase signalling via the c-Jun transcription factor. Cell Signal. 2002; 14(7), 585–593.CrossRefGoogle ScholarPubMed
Chinenov, Y, Kerppola, TK. Close encounters of many kinds: Fos-Jun interactions that mediate transcription regulatory specificity. Oncogene. 2001; 20(19), 2438–2452.CrossRefGoogle ScholarPubMed
Parfitt, D-E, Shen, MM. From blastocyst to gastrula: gene regulatory networks of embryonic stem cells and early mouse embryogenesis. Philos Trans R Soc B Biol Sci. 2014; 369(1657), 20130542.CrossRefGoogle ScholarPubMed
Ozawa, M, Sakatani, M, Yao, J, et al. Global gene expression of the inner cell mass and trophectoderm of the bovine blastocyst. BMC Dev Biol. 2012; 12(1), 33.CrossRefGoogle ScholarPubMed
Guo, B, Tian, X-C, Li, D-D, et al. Expression, regulation and function of Egr1 during implantation and decidualization in mice. Cell Cycle Georget Tex. 2014; 13(16), 2626–2640.CrossRefGoogle ScholarPubMed
O’Donovan, KJ, Tourtellotte, WG, Millbrandt, J, Baraban, JM. The EGR family of transcription-regulatory factors: progress at the interface of molecular and systems neuroscience. Trends Neurosci. 1999; 22(4), 167–173.CrossRefGoogle ScholarPubMed
Pérez-Cerezales, S, Ramos-Ibeas, P, Rizos, D, Lonergan, P, Bermejo-Alvarez, P, Gutiérrez-Adán, A. Early sex-dependent differences in response to environmental stress. Reprod Camb Engl. 2018; 155(1), R39–R51.Google ScholarPubMed
Bermejo-Alvarez, P, Rizos, D, Lonergan, P, Gutierrez-Adan, A. Transcriptional sexual dimorphism during preimplantation embryo development and its consequences for developmental competence and adult health and disease. Reprod Camb Engl. 2011; 141(5), 563–570.CrossRefGoogle ScholarPubMed
Murayama, A, Ohmori, K, Fujimura, A, et al. Epigenetic control of rDNA loci in response to intracellular energy status. Cell. 2008; 133(4), 627–639.CrossRefGoogle ScholarPubMed
Supplementary material: File

Calderari et al. supplementary material

Table S1

Download Calderari et al. supplementary material(File)
File 47.6 KB
Supplementary material: File

Calderari et al. supplementary material

Table S2

Download Calderari et al. supplementary material(File)
File 18.3 KB
Supplementary material: File

Calderari et al. supplementary material

Table S3

Download Calderari et al. supplementary material(File)
File 14 KB