Skip to main content
SpringerLink
Log in

The Role of Maternal Nutrition During the Periconceptional Period and Its Effect on Offspring Phenotype

  • Chapter
  • First Online:
Periconception in Physiology and Medicine

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1014))

Abstract

The early preimplantation embryo has been rigorously studied for decades to understand inherent reproductive and developmental mechanisms driving its morphogenesis from before fertilisation through to and beyond implantation. Recent research has demonstrated that this short developmental window is also critical for the embryo’s interaction with external, maternal factors, particularly nutritional status. Here, maternal dietary quality has been shown to alter the pattern of development in an enduring way that can influence health throughout the lifetime. Thus, using mouse models, maternal protein restriction exclusively during the preimplantation period with normal nutrition thereafter is sufficient to cause adverse cardiometabolic and neurological outcomes in adult offspring. Evidence for similar effects whereby environmental factors during the periconceptional window can programme postnatal disease risk can be found in human and large animal models and also in response to in vitro conditions such as assisted conception and related infertility treatments. In this review, using mouse malnutrition models, we evaluate the step-by-step mechanisms that lead from maternal poor diet consumption though to offspring disease. We consider how adverse programming within the embryo may be induced, what nutrient factors and signalling pathways may be involved, and how these cues act to change the embryo in distinct ways across placental and foetal lineage paths, leading especially to changes in the growth trajectory which in turn associate with later disease risk. These mechanisms straddle epigenetic, molecular, cellular and physiological levels of biology and suggest, for health outcomes, preimplantation development to be the most important time in our lives.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Artus J, Piliszek A, Hadjantonakis AK (2011) The primitive endoderm lineage of the mouse blastocyst: sequential transcription factor activation and regulation of differentiation by Sox17. Dev Biol 350(2):393–404. doi:10.1016/j.ydbio.2010.12.007

    Article  CAS  PubMed  Google Scholar 

  • Avruch J, Long X, Ortiz-Vega S, Rapley J, Papageorgiou A, Dai N (2009) Amino acid regulation of TOR complex 1. Am J Physiol Endocrinol Metab 296(4):E592–E602. doi:10.1152/ajpendo.90645.2008

    Article  CAS  PubMed  Google Scholar 

  • Barker D, Barker M, Fleming T, Lampl M (2013) Developmental biology: support mothers to secure future public health. Nature 504(7479):209–211

    Article  PubMed  Google Scholar 

  • Barker DJ (2007) The origins of the developmental origins theory. J Intern Med 261(5):412–417. doi:10.1111/j.1365-2796.2007.01809.x

    Article  CAS  PubMed  Google Scholar 

  • Barker DJ, Thornburg KL (2013) The obstetric origins of health for a lifetime. Clin Obstet Gynecol 56(3):511–519. doi:10.1097/GRF.0b013e31829cb9ca

    Article  PubMed  Google Scholar 

  • Bartova E, Krejci J, Harnicarova A, Galiova G, Kozubek S (2008) Histone modifications and nuclear architecture: a review. J Histochem Cytochem Off J Histochem Soc 56(8):711–721. doi:10.1369/jhc.2008.951251

    Article  CAS  Google Scholar 

  • Beckman DA, Lloyd JB, Brent RL (1997) Investigations into mechanisms of amino acid supply to the rat embryo using whole-embryo culture. Int J Dev Biol 41(2):315–318

    CAS  PubMed  Google Scholar 

  • Bedzhov I, Graham SJ, Leung CY, Zernicka-Goetz M (2014) Developmental plasticity, cell fate specification and morphogenesis in the early mouse embryo. Philos Trans R Soc Lond B Biol Sci 369(1657):20130538. doi:10.1098/rstb.2013.0538

  • Bertoli S, Leone A, Ponissi V, Bedogni G, Beggio V, Strepparava MG, Battezzati A (2016) Prevalence of and risk factors for binge eating behaviour in 6930 adults starting a weight loss or maintenance programme. Public Health Nutr 19(1):71–77. doi:10.1017/S1368980015001068

    Article  PubMed  Google Scholar 

  • Brison DR, Roberts SA, Kimber SJ (2013) How should we assess the safety of IVF technologies? Reprod Biomed Online 27(6):710–721. doi:10.1016/j.rbmo.2013.09.006

    Article  PubMed  Google Scholar 

  • Cai KQ, Caslini C, Capo-chichi CD, Slater C, Smith ER, Wu H, Klein-Szanto AJ, Godwin AK, XX X (2009) Loss of GATA4 and GATA6 expression specifies ovarian cancer histological subtypes and precedes neoplastic transformation of ovarian surface epithelia. PLoS One 4(7):e6454. doi:10.1371/journal.pone.0006454

    Article  PubMed  PubMed Central  Google Scholar 

  • Capo-Chichi CD, Smedberg JL, Rula M, Nicolas E, Yeung AT, Adamo RF, Frolov A, Godwin AK, Xu XX (2010) Alteration of differentiation potentials by modulating GATA transcription factors in murine embryonic stem cells. Stem Cells Int 2010:602068. doi:10.4061/2010/602068

    Article  PubMed  PubMed Central  Google Scholar 

  • Cardozo ER, Karmon AE, Gold J, Petrozza JC, Styer AK (2016) Reproductive outcomes in oocyte donation cycles are associated with donor BMI. Hum Reprod 31(2):385–392. doi:10.1093/humrep/dev298

    CAS  PubMed  Google Scholar 

  • Caslini C, Capo-chichi CD, Roland IH, Nicolas E, Yeung AT, XX X (2006) Histone modifications silence the GATA transcription factor genes in ovarian cancer. Oncogene 25(39):5446–5461. doi:10.1038/sj.onc.1209533

    Article  CAS  PubMed  Google Scholar 

  • Ceelen M, van Weissenbruch MM, Vermeiden JP, van Leeuwen FE, Delemarre-van de Waal HA (2008) Cardiometabolic differences in children born after in vitro fertilization: follow-up study. J Clin Endocrinol Metab 93(5):1682–1688. doi:10.1210/jc.2007-2432

    Article  CAS  PubMed  Google Scholar 

  • Cha J, Sun X, Dey SK (2012) Mechanisms of implantation: strategies for successful pregnancy. Nat Med 18(12):1754–1767. doi:10.1038/nm.3012

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Wang D, Wu Z, Ma L, Daley GQ (2010) Molecular basis of the first cell fate determination in mouse embryogenesis. Cell Res 20(9):982–993. doi:10.1038/cr.2010.106

    Article  CAS  PubMed  Google Scholar 

  • Coan PM, Vaughan OR, McCarthy J, Mactier C, Burton GJ, Constancia M, Fowden AL (2011) Dietary composition programmes placental phenotype in mice. J Physiol 589(Pt 14):3659–3670. doi:10.1113/jphysiol.2011.208629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cockburn K, Rossant J (2010) Making the blastocyst: lessons from the mouse. J Clin Invest 120(4):995–1003. doi:10.1172/JCI41229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Rooij SR, Roseboom TJ (2013) The developmental origins of ageing: study protocol for the Dutch famine birth cohort study on ageing. BMJ Open 3(6):e003167. doi:10.1136/bmjopen-2013-003167

  • Denisenko O, Lin B, Louey S, Thornburg K, Bomsztyk K, Bagby S (2011) Maternal malnutrition and placental insufficiency induce global downregulation of gene expression in fetal kidneys. J Dev Orig Health Dis 2(2):124–133. doi:10.1017/S2040174410000632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Denisenko O, Lucas ES, Sun C, Watkins AJ, Mar D, Bomsztyk K, Fleming TP (2016) Regulation of ribosomal RNA expression across the lifespan is fine-tuned by maternal diet before implantation. Biochim Biophys Acta 1859(7):906–913. doi:10.1016/j.bbagrm.2016.04.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dibble CC, Cantley LC (2015) Regulation of mTORC1 by PI3K signaling. Trends Cell Biol 25(9):545–555. doi:10.1016/j.tcb.2015.06.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diskin MG, Kenny DA (2016) Managing the reproductive performance of beef cows. Theriogenology 86(1):379–387. doi:10.1016/j.theriogenology.2016.04.052

    Article  CAS  PubMed  Google Scholar 

  • Dodd JM, O’Brien CM, Grivell RM (2015) Modifying diet and physical activity to support pregnant women who are overweight or obese. Curr Opin Clin Nutr Metab Care 18(3):318–323. doi:10.1097/MCO.0000000000000170

    Article  CAS  PubMed  Google Scholar 

  • Dominguez-Salas P, Moore SE, Baker MS, Bergen AW, Cox SE, Dyer RA, Fulford AJ, Guan Y, Laritsky E, Silver MJ, Swan GE, Zeisel SH, Innis SM, Waterland RA, Prentice AM, Hennig BJ (2014) Maternal nutrition at conception modulates DNA methylation of human metastable epialleles. Nat Commun 5:3746. doi:10.1038/ncomms4746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dunning KR, Russell DL, Robker RL (2014) Lipids and oocyte developmental competence: the role of fatty acids and beta-oxidation. Reproduction 148(1):R15–R27. doi:10.1530/REP-13-0251

    Article  CAS  PubMed  Google Scholar 

  • Eckert JJ, Fleming TP (2008) Tight junction biogenesis during early development. Biochim Biophys Acta 1778(3):717–728. doi:10.1016/j.bbamem.2007.09.031

    Article  CAS  PubMed  Google Scholar 

  • Eckert JJ, Porter R, Watkins AJ, Burt E, Brooks S, Leese HJ, Humpherson PG, Cameron IT, Fleming TP (2012) Metabolic induction and early responses of mouse blastocyst developmental programming following maternal low protein diet affecting life-long health. PLoS One 7(12):e52791. doi:10.1371/journal.pone.0052791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eckert JJ, Velazquez MA, Fleming TP (2015) Cell signalling during blastocyst morphogenesis. Adv Exp Med Biol 843:1–21. doi:10.1007/978-1-4939-2480-6_1

    Article  CAS  PubMed  Google Scholar 

  • Fleming TP, Velazquez MA, Eckert JJ, Lucas ES, Watkins AJ (2012) Nutrition of females during the peri-conceptional period and effects on foetal programming and health of offspring. Anim Reprod Sci 130(3–4):193–197. doi:10.1016/j.anireprosci.2012.01.015

    Article  CAS  PubMed  Google Scholar 

  • Fleming TP, Watkins AJ, Sun C, Velazquez MA, Smyth NR, Eckert JJ (2015) Do little embryos make big decisions? How maternal dietary protein restriction can permanently change an embryo’s potential, affecting adult health. Reprod Fertil Dev 27(4):684–692. doi:10.1071/RD14455

    Article  CAS  PubMed  Google Scholar 

  • Gardner DK, Harvey AJ (2015) Blastocyst metabolism. Reprod Fertil Dev 27:638. doi:10.1071/RD14421

    Article  CAS  PubMed  Google Scholar 

  • Gardner DS, Pearce S, Dandrea J, Walker R, Ramsay MM, Stephenson T, Symonds ME (2004) Peri-implantation undernutrition programs blunted angiotensin II evoked baroreflex responses in young adult sheep. Hypertension 43(6):1290–1296. doi:10.1161/01.HYP.0000126991.67203.7b

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gluckman PD, Cutfield W, Hofman P, Hanson MA (2005) The fetal, neonatal, and infant environments-the long-term consequences for disease risk. Early Hum Dev 81(1):51–59. doi:10.1016/j.earlhumdev.2004.10.003

    Article  PubMed  Google Scholar 

  • Gu L, Liu H, Gu X, Boots C, Moley KH, Wang Q (2015) Metabolic control of oocyte development: linking maternal nutrition and reproductive outcomes. Cell Mol Life Sci CMLS 72(2):251–271. doi:10.1007/s00018-014-1739-4

    Article  CAS  PubMed  Google Scholar 

  • Hales CN, Barker DJ (2001) The thrifty phenotype hypothesis. Br Med Bull 60:5–20

    Article  CAS  PubMed  Google Scholar 

  • Hart R, Norman RJ (2013) The longer-term health outcomes for children born as a result of IVF treatment: part I--General health outcomes. Hum Reprod Update 19(3):232–243. doi:10.1093/humupd/dms062

    Article  CAS  PubMed  Google Scholar 

  • Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, Slagboom PE, Lumey LH (2008) Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A 105(44):17046–17049. doi:10.1073/pnas.0806560105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hernandez CE, Harding JE, Oliver MH, Bloomfield FH, Held SD, Matthews LR (2009) Effects of litter size, sex and periconceptional ewe nutrition on side preference and cognitive flexibility in the offspring. Behav Brain Res 204(1):82–87. doi:10.1016/j.bbr.2009.05.019

    Article  PubMed  Google Scholar 

  • Igosheva N, Abramov AY, Poston L, Eckert JJ, Fleming TP, Duchen MR, McConnell J (2010) Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS One 5(4):e10074. doi:10.1371/journal.pone.0010074

    Article  PubMed  PubMed Central  Google Scholar 

  • Jungheim ES, Louden ED, Chi MM, Frolova AI, Riley JK, Moley KH (2011) Preimplantation exposure of mouse embryos to palmitic acid results in fetal growth restriction followed by catch-up growth in the offspring. Biol Reprod 85(4):678–683. doi:10.1095/biolreprod.111.092148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kermack AJ, Finn-Sell S, Cheong YC, Brook N, Eckert JJ, Macklon NS, Houghton FD (2015) Amino acid composition of human uterine fluid: association with age, lifestyle and gynaecological pathology. Hum Reprod 30(4):917–924. doi:10.1093/humrep/dev008

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim E (2009) Mechanisms of amino acid sensing in mTOR signaling pathway. Nutr Res Pract 3(1):64–71. doi:10.4162/nrp.2009.3.1.64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwong WY, Wild AE, Roberts P, Willis AC, Fleming TP (2000) Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development 127(19):4195–4202

    CAS  PubMed  Google Scholar 

  • Lazaraviciute G, Kauser M, Bhattacharya S, Haggarty P (2014) A systematic review and meta-analysis of DNA methylation levels and imprinting disorders in children conceived by IVF/ICSI compared with children conceived spontaneously. Hum Reprod Update 20(6):840–852. doi:10.1093/humupd/dmu033

    Article  PubMed  Google Scholar 

  • Leary C, Leese HJ, Sturmey RG (2015) Human embryos from overweight and obese women display phenotypic and metabolic abnormalities. Hum Reprod 30(1):122–132. doi:10.1093/humrep/deu276

    Article  PubMed  Google Scholar 

  • Leese HJ (2012) Metabolism of the preimplantation embryo: 40 years on. Reproduction 143(4):417–427. doi:10.1530/REP-11-0484

    Article  CAS  PubMed  Google Scholar 

  • Leroy JL, Valckx SD, Jordaens L, De Bie J, Desmet KL, Van Hoeck V, Britt JH, Marei WF, Bols PE (2015) Nutrition and maternal metabolic health in relation to oocyte and embryo quality: critical views on what we learned from the dairy cow model. Reprod Fertil Dev 27(4):693–703. doi:10.1071/RD14363

    Article  CAS  PubMed  Google Scholar 

  • Li L, Lu X, Dean J (2013) The maternal to zygotic transition in mammals. Mol Aspects Med 34(5):919–938. doi:10.1016/j.mam.2013.01.003

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu X, Zhao D, Zheng Y, Wang L, Qian Y, Xu C, Huang H, Hwa YL, Jin F (2014) Expression of histone acetyltransferase GCN5 and histone deacetylase 1 in the cultured mouse preimplantation embryos. Curr Pharm Des 20(11):1772–1777

    Article  CAS  PubMed  Google Scholar 

  • Luzzo KM, Wang Q, Purcell SH, Chi M, Jimenez PT, Grindler N, Schedl T, Moley KH (2012) High fat diet induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation/brain defects. PLoS One 7(11):e49217. doi:10.1371/journal.pone.0049217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McEvoy TG, Sinclair KD, Young LE, Wilmut I, Robinson JJ (2000) Large offspring syndrome and other consequences of ruminant embryo culture in vitro: relevance to blastocyst culture in human ART. Hum Fertil (Camb) 3(4):238–246

    Article  Google Scholar 

  • McPherson NO, Bell VG, Zander-Fox DL, Fullston T, LL W, Robker RL, Lane M (2015) When two obese parents are worse than one! Impacts on embryo and fetal development. Am J Physiol Endocrinol Metab 309(6):E568–E581. doi:10.1152/ajpendo.00230.2015

    Article  CAS  PubMed  Google Scholar 

  • Moore SE, Cole TJ, Poskitt EM, Sonko BJ, Whitehead RG, McGregor IA, Prentice AM (1997) Season of birth predicts mortality in rural Gambia. Nature 388(6641):434. doi:10.1038/41245

    Article  CAS  PubMed  Google Scholar 

  • Morrisey EE, Musco S, Chen MY, MM L, Leiden JM, Parmacek MS (2000) The gene encoding the mitogen-responsive phosphoprotein Dab2 is differentially regulated by GATA-6 and GATA-4 in the visceral endoderm. J Biol Chem 275(26):19949–19954. doi:10.1074/jbc.M001331200

    Article  CAS  PubMed  Google Scholar 

  • Nardelli AA, Stafinski T, Motan T, Klein K, Menon D (2014) Assisted reproductive technologies (ARTs): evaluation of evidence to support public policy development. Reprod Health 11(1):76. doi:10.1186/1742-4755-11-76

    Article  PubMed  PubMed Central  Google Scholar 

  • Painter RC, de Rooij SR, Bossuyt PM, Simmers TA, Osmond C, Barker DJ, Bleker OP, Roseboom TJ (2006) Early onset of coronary artery disease after prenatal exposure to the Dutch famine. Am J Clin Nutr 84(2):322–327. quiz 466-327

    CAS  PubMed  Google Scholar 

  • Rivera RM, Ross JW (2013) Epigenetics in fertilization and preimplantation embryo development. Prog Biophys Mol Biol 113(3):423–432. doi:10.1016/j.pbiomolbio.2013.02.001

    Article  PubMed  Google Scholar 

  • Roseboom TJ, Painter RC, van Abeelen AF, Veenendaal MV, de Rooij SR (2011) Hungry in the womb: what are the consequences? Lessons from the Dutch famine. Maturitas 70(2):141–145. doi:10.1016/j.maturitas.2011.06.017

    Article  PubMed  Google Scholar 

  • Rossant J, Chazaud C, Yamanaka Y (2003) Lineage allocation and asymmetries in the early mouse embryo. Philos Trans R Soc Lond B Biol Sci 358(1436):1341–1348.; discussion 1349. doi:10.1098/rstb.2003.1329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasson IE, Vitins AP, Mainigi MA, Moley KH, Simmons RA (2015) Pre-gestational vs gestational exposure to maternal obesity differentially programs the offspring in mice. Diabetologia 58(3):615–624. doi:10.1007/s00125-014-3466-7

    Article  CAS  PubMed  Google Scholar 

  • Schrode N, Saiz N, Di Talia S, Hadjantonakis AK (2014) GATA6 levels modulate primitive endoderm cell fate choice and timing in the mouse blastocyst. Dev Cell 29(4):454–467. doi:10.1016/j.devcel.2014.04.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seshagiri PB, Sen Roy S, Sireesha G, Rao RP (2009) Cellular and molecular regulation of mammalian blastocyst hatching. J Reprod Immunol 83(1–2):79–84. doi:10.1016/j.jri.2009.06.264

    Article  CAS  PubMed  Google Scholar 

  • Sim KA, Partridge SR, Sainsbury A (2014) Does weight loss in overweight or obese women improve fertility treatment outcomes? A systematic review. Obes Rev Off J Int Assoc Stud Obes 15(10):839–850. doi:10.1111/obr.12217

    Article  CAS  Google Scholar 

  • Sozen B, Can A, Demir N (2014) Cell fate regulation during preimplantation development: a view of adhesion-linked molecular interactions. Dev Biol 395(1):73–83. doi:10.1016/j.ydbio.2014.08.028

    Article  CAS  PubMed  Google Scholar 

  • Sun C, Denisenko O, Sheth B, Cox A, Lucas ES, Smyth NR, Fleming TP (2015) Epigenetic regulation of histone modifications and Gata6 gene expression induced by maternal diet in mouse embryoid bodies in a model of developmental programming. BMC Dev Biol 15(1):3. doi:10.1186/s12861-015-0053-1

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun C, Velazquez MA, Marfy-Smith S, Sheth B, Cox A, Johnston DA, Smyth N, Fleming TP (2014) Mouse early extra-embryonic lineages activate compensatory endocytosis in response to poor maternal nutrition. Development 141(5):1140–1150. doi:10.1242/dev.103952

    Article  CAS  PubMed  Google Scholar 

  • Todd SEOM, Jaquiery AL, Bloomfield FH, Harding JE (2009) Periconceptional undernutrition of ewes impairs glucose tolerance in their adult offspring. Pediatr Res 65:409–413

    Article  PubMed  Google Scholar 

  • Torrens C, Snelling TH, Chau R, Shanmuganathan M, Cleal JK, Poore KR, Noakes DE, Poston L, Hanson MA, Green LR (2009) Effects of pre- and periconceptional undernutrition on arterial function in adult female sheep are vascular bed dependent. Exp Physiol 94(9):1024–1033. doi:10.1113/expphysiol.2009.047340

    Article  CAS  PubMed  Google Scholar 

  • Turner N, Robker RL (2015) Developmental programming of obesity and insulin resistance: does mitochondrial dysfunction in oocytes play a role? Mol Hum Reprod 21(1):23–30. doi:10.1093/molehr/gau042

    Article  CAS  PubMed  Google Scholar 

  • Van Hoeck V, Leroy JL, Arias Alvarez M, Rizos D, Gutierrez-Adan A, Schnorbusch K, Bols PE, Leese HJ, Sturmey RG (2013) Oocyte developmental failure in response to elevated nonesterified fatty acid concentrations: mechanistic insights. Reproduction 145(1):33–44. doi:10.1530/REP-12-0174

    Article  PubMed  Google Scholar 

  • Van Hoeck V, Sturmey RG, Bermejo-Alvarez P, Rizos D, Gutierrez-Adan A, Leese HJ, Bols PE, Leroy JL (2011) Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology. PLoS One 6(8):e23183. doi:10.1371/journal.pone.0023183

    Article  PubMed  PubMed Central  Google Scholar 

  • Waterland RA, Kellermayer R, Laritsky E, Rayco-Solon P, Harris RA, Travisano M, Zhang W, Torskaya MS, Zhang J, Shen L, Manary MJ, Prentice AM (2010) Season of conception in rural gambia affects DNA methylation at putative human metastable epialleles. PLoS Genet 6(12):e1001252. doi:10.1371/journal.pgen.1001252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watkins AJ, Lucas ES, Marfy-Smith S, Bates N, Kimber SJ, Fleming TP (2015) Maternal nutrition modifies trophoblast giant cell phenotype and fetal growth in mice. Reproduction 149(6):563–575. doi:10.1530/REP-14-0667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watkins AJ, Lucas ES, Torrens C, Cleal JK, Green L, Osmond C, Eckert JJ, Gray WP, Hanson MA, Fleming TP (2010) Maternal low-protein diet during mouse pre-implantation development induces vascular dysfunction and altered renin-angiotensin-system homeostasis in the offspring. Br J Nutr 103(12):1762–1770. doi:10.1017/S0007114509993783

    Article  CAS  PubMed  Google Scholar 

  • Watkins AJ, Lucas ES, Wilkins A, Cagampang FR, Fleming TP (2011) Maternal periconceptional and gestational low protein diet affects mouse offspring growth, cardiovascular and adipose phenotype at 1 year of age. PLoS One 6(12):e28745. doi:10.1371/journal.pone.0028745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watkins AJ, Sinclair KD (2014) Paternal low protein diet affects adult offspring cardiovascular and metabolic function in mice. Am J Physiol Heart Circ Physiol 306(10):H1444–H1452. doi:10.1152/ajpheart.00981.2013

    Article  CAS  PubMed  Google Scholar 

  • Watkins AJ, Ursell E, Panton R, Papenbrock T, Hollis L, Cunningham C, Wilkins A, Perry VH, Sheth B, Kwong WY, Eckert JJ, Wild AE, Hanson MA, Osmond C, Fleming TP (2008a) Adaptive responses by mouse early embryos to maternal diet protect fetal growth but predispose to adult onset disease. Biol Reprod 78(2):299–306. doi:10.1095/biolreprod.107.064220

    Article  CAS  PubMed  Google Scholar 

  • Watkins AJ, Wilkins A, Cunningham C, Perry VH, Seet MJ, Osmond C, Eckert JJ, Torrens C, Cagampang FR, Cleal J, Gray WP, Hanson MA, Fleming TP (2008b) Low protein diet fed exclusively during mouse oocyte maturation leads to behavioural and cardiovascular abnormalities in offspring. J Physiol 586(8):2231–2244. doi:10.1113/jphysiol.2007.149229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou LQ, Dean J (2015) Reprogramming the genome to totipotency in mouse embryos. Trends Cell Biol 25(2):82–91. doi:10.1016/j.tcb.2014.09.006

    Article  CAS  PubMed  Google Scholar 

  • Zohn IE, Sarkar AA (2010) The visceral yolk sac endoderm provides for absorption of nutrients to the embryo during neurulation. Birth Defects Res A Clin Mol Teratol 88(8):593–600. doi:10.1002/bdra.20705

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported through awards from the Biotechnology and Biological Sciences Research Council (BB/I001840/1; BB/F007450/1), The Medical Research Council (G9800781), the NICHD National Cooperative Program (U01 HD044635) and the EU-FP7 EpiHealth and EpiHealthNet programmes to TPF, The Gerald Kerkut Charitable Trust, and NIH awards DK098817 and DK094934 to OD.

Author information

Authors and Affiliations

  1. Biological Sciences, University of Southampton, Mailpoint 840, Southampton General Hospital, Southampton, SO16 6YD, UK

    Tom P. Fleming

  2. Faculty of Medicine, University of Southampton, Mailpoint 840, Southampton General Hospital, Southampton, SO16 6YD, UK

    Judith J. Eckert

  3. Department of Medicine, University of Washington, 850 Republican St, Seattle, WA, 98109, USA

    Oleg Denisenko

Authors
  1. Tom P. Fleming
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Judith J. Eckert
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Oleg Denisenko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tom P. Fleming .

Editor information

Editors and Affiliations

  1. Academic Unit of Reproductive and Developmental Medicine, University of Sheffield, Sheffield, United Kingdom

    Alireza Fazeli

  2. Academic Unit of Reproductive and Developmental Medicine, University of Sheffield, Sheffield, United Kingdom

    William V. Holt

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Fleming, T.P., Eckert, J.J., Denisenko, O. (2017). The Role of Maternal Nutrition During the Periconceptional Period and Its Effect on Offspring Phenotype. In: Fazeli, A., Holt, W. (eds) Periconception in Physiology and Medicine. Advances in Experimental Medicine and Biology, vol 1014. Springer, Cham. https://doi.org/10.1007/978-3-319-62414-3_5

Download citation

Publish with us

Policies and ethics

Search

Navigation