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Effects of Prenatal Nutrition and the Role of the Placenta in Health and Disease

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Investigations of Early Nutrition Effects on Long-Term Health

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1735))

Abstract

Epidemiologic studies identified the linkage between exposures to stresses, including the type and plane of nutrition in utero with development of disease in later life. Given the critical roles of the placenta in mediating transport of nutrients between the mother and fetus and regulation of maternal metabolism, recent attention has focused on the role of the placenta in mediating the effect of altered nutritional exposures on the development of disease in later life. In this chapter we describe the mechanisms of nutrient transport in the placenta, the influence of placental metabolism on this, and how placental energetics influence placental function in response to a variety of stressors. Further the recent “recognition” that the placenta itself has a sex which affects its function may begin to help elucidate the mechanisms underlying the well-known dimorphism in development of disease in adult life.

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References

  1. Barker DJ, Osmond C (1986) Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 1(8489):1077–1081

    Article  CAS  PubMed  Google Scholar 

  2. Barker DJ, Osmond C, Golding J, Kuh D, Wadsworth ME (1989) Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ 298(6673):564–567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ (1989) Weight in infancy and death from ischaemic heart disease. Lancet 2(8663):577–580

    Article  CAS  PubMed  Google Scholar 

  4. Barker DJ, Eriksson JG, Forsen T, Osmond C (2002) Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol 31(6):1235–1239

    Article  CAS  PubMed  Google Scholar 

  5. Leon DA, Lithell HO, Vagero D, Koupilova I, Mohsen R, Berglund L et al (1998) Reduced fetal growth rate and increased risk of death from ischaemic heart disease: cohort study of 15 000 Swedish men and women born 1915-29. BMJ 317(7153):241–245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Stein CE, Fall CH, Kumaran K, Osmond C, Cox V, Barker DJ (1996) Fetal growth and coronary heart disease in south India. Lancet 348(9037):1269–1273

    Article  CAS  PubMed  Google Scholar 

  7. Rich-Edwards JW, Stampfer MJ, Manson JE, Rosner B, Hankinson SE, Colditz GA et al (1976) Birth weight and risk of cardiovascular disease in a cohort of women followed up since 1976. BMJ 315(7105):396–400

    Article  Google Scholar 

  8. Fan Z, Zhang ZX, Li Y, Wang Z, Xu T, Gong X et al (2010) Relationship between birth size and coronary heart disease in China. Ann Med 42(8):596–602

    Article  PubMed  PubMed Central  Google Scholar 

  9. Barker D (2003) The midwife, the coincidence, and the hypothesis. BMJ 327(7429):1428–1430

    Article  PubMed  PubMed Central  Google Scholar 

  10. Kapral N, Miller SE, Scharf RJ, Gurka MJ, DeBoer MD (2017) Associations between birthweight and overweight and obesity in school-age children. Pediatr Obes. https://doi.org/10.1111/ijpo.12227

  11. Roseboom TJ, Painter RC, de Rooij SR, van Abeelen AF, Veenendaal MV, Osmond C et al (2011) Effects of famine on placental size and efficiency. Placenta 32(5):395–399

    Article  CAS  PubMed  Google Scholar 

  12. Zoller B, Sundquist J, Sundquist K, Crump C (2015) Perinatal risk factors for premature ischaemic heart disease in a Swedish national cohort. BMJ Open 5(6):e007308. https://doi.org/10.1136/bmjopen-2014-007308

    Article  PubMed  PubMed Central  Google Scholar 

  13. Barker DJ, Osmond C, Kajantie E, Eriksson JG (2009) Growth and chronic disease: findings in the Helsinki Birth Cohort. Ann Hum Biol 36(5):445–458

    Article  PubMed  Google Scholar 

  14. Bagby SP (2007) Maternal nutrition, low nephron number, and hypertension in later life: pathways of nutritional programming. J Nutr 137(4):1066–1072

    Article  CAS  PubMed  Google Scholar 

  15. Hales CN, Barker DJ (2013) Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Int J Epidemiol 42(5):1215–1222

    Article  CAS  PubMed  Google Scholar 

  16. Ravelli AC, van Der Meulen JH, Osmond C, Barker DJ, Bleker OP (1999) Obesity at the age of 50 y in men and women exposed to famine prenatally. Am J Clin Nutr 70(5):811–816

    CAS  PubMed  Google Scholar 

  17. Barker DJ (1995) Fetal origins of coronary heart disease. BMJ 311(6998):171–174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Cooper C, Walker-Bone K, Arden N, Dennison E (2000) Novel insights into the pathogenesis of osteoporosis: the role of intrauterine programming. Rheumatology (Oxford) 39(12):1312–1315

    Article  CAS  Google Scholar 

  19. Buss C, Entringer S, Wadhwa PD (2012) Fetal programming of brain development: intrauterine stress and susceptibility to psychopathology. Sci Signal 5(245):pt7. https://doi.org/10.1126/scisignal.2003406

    Article  PubMed  CAS  Google Scholar 

  20. Wilson ME, Ford SP (2001) Comparative aspects of placental efficiency. Reprod Suppl 58:223–232

    CAS  PubMed  Google Scholar 

  21. Tamimi RM, Lagiou P, Mucci LA, Hsieh CC, Adami HO, Trichopoulos D (2003) Average energy intake among pregnant women carrying a boy compared with a girl. BMJ 326(7401):1245–1246

    Article  PubMed  PubMed Central  Google Scholar 

  22. Eriksson JG, Kajantie E, Osmond C, Thornburg K, Barker DJ (2010) Boys live dangerously in the womb. Am J Hum Biol 22(3):330–335

    Article  PubMed  PubMed Central  Google Scholar 

  23. Song S (2014) Malnutrition, sex ratio, and selection: a study based on the great leap forward famine. Hum Nat 25(4):580–595

    Article  PubMed  Google Scholar 

  24. Barker DJ, Thornburg KL (2013) The obstetric origins of health for a lifetime. Clin Obstet Gynecol 56(3):511–519

    Article  PubMed  Google Scholar 

  25. Barker DJ, Thornburg KL, Osmond C, Kajantie E, Eriksson JG (2010) The prenatal origins of lung cancer. II. The placenta. Am J Hum Biol 22(4):512–516

    Article  PubMed  Google Scholar 

  26. Barker DJ, Osmond C, Thornburg KL, Kajantie E, Eriksson JG (2013) The intrauterine origins of Hodgkin’s lymphoma. Cancer Epidemiol 37(3):321–323

    Article  PubMed  Google Scholar 

  27. Hamilton S, Bosman FT, Boffetta P, Ilyas M, Morreau H, Nakamura S-I et al (2010) Carcinoma of the colon and rectum. In: Bosman FT, Carneiro F, Hruban RH, Theise ND (eds) WHO classification of tumours of the digestive system, WHO/IARC classification of tumours, vol 3, 4th edn. IARC Press, Lyon, pp 134–146. ISBN-10: 9283224329

    Google Scholar 

  28. Barker DJ, Osmond C, Thornburg KL, Kajantie E, Eriksson JG (2013) The shape of the placental surface at birth and colorectal cancer in later life. Am J Hum Biol 25(4):566–568

    Article  PubMed  Google Scholar 

  29. McMillen IC, Robinson JS (2005) Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 85(2):571–633

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  31. Eriksson JG, Kajantie E, Thornburg KL, Osmond C, Barker DJ (2011) Mother’s body size and placental size predict coronary heart disease in men. Eur Heart J 32(18):2297–2303

    Article  PubMed  PubMed Central  Google Scholar 

  32. Barker DJ, Larsen G, Osmond C, Thornburg KL, Kajantie E, Eriksson JG (2012) The placental origins of sudden cardiac death. Int J Epidemiol 41(5):1394–1399

    Article  PubMed  Google Scholar 

  33. Barker DJ, Gelow J, Thornburg K, Osmond C, Kajantie E, Eriksson JG (2010) The early origins of chronic heart failure: impaired placental growth and initiation of insulin resistance in childhood. Eur J Heart Fail 12(8):819–825

    Article  PubMed  PubMed Central  Google Scholar 

  34. Barker DJ, Osmond C, Forsen TJ, Kajantie E, Eriksson JG (2005) Trajectories of growth among children who have coronary events as adults. N Engl J Med 353(17):1802–1809

    Article  CAS  PubMed  Google Scholar 

  35. Myatt L (2006) Placental adaptive responses and fetal programming. J Physiol 572(Pt 1):25–30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Hauguel S, Desmaizieres V, Challier JC (1986) Glucose uptake, utilization, and transfer by the human placenta as functions of maternal glucose concentration. Pediatr Res 20(3):269–273

    Article  CAS  PubMed  Google Scholar 

  37. Rofey DL, Kolko RP, Iosif AM, Silk JS, Bost JE, Feng W et al (2009) A longitudinal study of childhood depression and anxiety in relation to weight gain. Child Psychiatry Hum Dev 40(4):517–526

    Article  PubMed  PubMed Central  Google Scholar 

  38. Waring ME, Lapane KL (2008) Overweight in children and adolescents in relation to attention-deficit/hyperactivity disorder: results from a national sample. Pediatrics 122(1):e1–e6. https://doi.org/10.1542/peds.2007-1955

    Article  PubMed  Google Scholar 

  39. Pasinetti GM, Eberstein JA (2008) Metabolic syndrome and the role of dietary lifestyles in Alzheimer’s disease. J Neurochem 106(4):1503–1514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Peterson LJ, Flood PM (2012) Oxidative stress and microglial cells in Parkinson’s disease. Mediators Inflamm 2012:401264. https://doi.org/10.1155/2012/401264

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  41. Priyadarshini M, Kamal MA, Greig NH, Reale M, Abuzenadah AM, Chaudhary AG et al (2012) Alzheimer’s disease and type 2 diabetes: exploring the association to obesity and tyrosine hydroxylase. CNS Neurol Disord Drug Targets 11(4):482–489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Muralimanoharan S, Maloyan A, Mele J, Guo C, Myatt LG, Myatt L (2012) MIR-210 modulates mitochondrial respiration in placenta with preeclampsia. Placenta 33(10):816–823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Mele J, Muralimanoharan S, Maloyan A, Myatt L (2014) Impaired mitochondrial function in human placenta with increased maternal adiposity. Am J Physiol Endocrinol Metab 307(5):E419–E425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Muralimanoharan S, Maloyan A, Myatt L (2016) Mitochondrial function and glucose metabolism in the placenta with gestational diabetes mellitus: role of miR-143. Clin Sci (Lond) 130(11):931–941

    Article  CAS  Google Scholar 

  45. Mayeur S, Lancel S, Theys N, Lukaszewski MA, Duban-Deweer S, Bastide B et al (2013) Maternal calorie restriction modulates placental mitochondrial biogenesis and bioenergetic efficiency: putative involvement in fetoplacental growth defects in rats. Am J Physiol Endocrinol Metab 304(1):E14–E22

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  47. Sood R, Zehnder JL, Druzin ML, Brown PO (2006) Gene expression patterns in human placenta. Proc Natl Acad Sci U S A 103(14):5478–5483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Buckberry S, Bianco-Miotto T, Bent SJ, Dekker GA, Roberts CT (2014) Integrative transcriptome meta-analysis reveals widespread sex-biased gene expression at the human fetal-maternal interface. Mol Hum Reprod 20(8):810–819

    Article  PubMed  PubMed Central  Google Scholar 

  49. Sedlmeier EM, Brunner S, Much D, Pagel P, Ulbrich SE, Meyer HH et al (2014) Human placental transcriptome shows sexually dimorphic gene expression and responsiveness to maternal dietary n-3 long-chain polyunsaturated fatty acid intervention during pregnancy. BMC Genomics 15:941. https://doi.org/10.1186/1471-2164-15-941

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Cvitic S, Longtine MS, Hackl H, Wagner K, Nelson MD, Desoye G et al (2013) The human placental sexome differs between trophoblast epithelium and villous vessel endothelium. PLoS One 8(10):e79233. https://doi.org/10.1371/journal.pone.0079233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Scott NM, Hodyl NA, Murphy VE, Osei-Kumah A, Wyper H, Hodgson DM et al (2009) Placental cytokine expression covaries with maternal asthma severity and fetal sex. J Immunol 182(3):1411–1420

    Article  CAS  PubMed  Google Scholar 

  52. Osei-Kumah A, Smith R, Jurisica I, Caniggia I, Clifton VL (2011) Sex-specific differences in placental global gene expression in pregnancies complicated by asthma. Placenta 32(8):570–578

    Article  CAS  PubMed  Google Scholar 

  53. 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(12):5557–5562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Yeganegi M, Leung CG, Martins A, Kim SO, Reid G, Challis JR et al (2011) Lactobacillus rhamnosus GR-1 stimulates colony-stimulating factor 3 (granulocyte) (CSF3) output in placental trophoblast cells in a fetal sex-dependent manner. Biol Reprod 84(1):18–25

    Article  CAS  PubMed  Google Scholar 

  55. Baumann MU, Deborde S, Illsley NP (2002) Placental glucose transfer and fetal growth. Endocrine 19(1):13–22

    Article  CAS  PubMed  Google Scholar 

  56. Lager S, Powell TL (2012) Regulation of nutrient transport across the placenta. J Pregnancy 2012:179827. https://doi.org/10.1155/2012/179827

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  57. Cleal JK, Lewis RM (2008) The mechanisms and regulation of placental amino acid transport to the human foetus. J Neuroendocrinol 20(4):419–426

    Article  CAS  PubMed  Google Scholar 

  58. Gaccioli F, Lager S (2016) Placental nutrient transport and intrauterine growth restriction. Front Physiol 7:40. https://doi.org/10.3389/fphys.2016.00040

    Article  PubMed  PubMed Central  Google Scholar 

  59. Herrera E, Ortega-Senovilla H (2014) Lipid metabolism during pregnancy and its implications for fetal growth. Curr Pharm Biotechnol 15(1):24–31

    Article  CAS  PubMed  Google Scholar 

  60. Schaiff WT, Bildirici I, Cheong M, Chern PL, Nelson DM, Sadovsky Y (2005) Peroxisome proliferator-activated receptor-gamma and retinoid X receptor signaling regulate fatty acid uptake by primary human placental trophoblasts. J Clin Endocrinol Metab 90(7):4267–4275

    Article  CAS  PubMed  Google Scholar 

  61. Campbell FM, Bush PG, Veerkamp JH, Dutta-Roy AK (1998) Detection and cellular localization of plasma membrane-associated and cytoplasmic fatty acid-binding proteins in human placenta. Placenta 19(5-6):409–415

    Article  CAS  PubMed  Google Scholar 

  62. Biron-Shental T, Schaiff WT, Ratajczak CK, Bildirici I, Nelson DM, Sadovsky Y (2007) Hypoxia regulates the expression of fatty acid-binding proteins in primary term human trophoblasts. Am J Obstet Gynecol 197(5):516.e1–516.e6

    Article  CAS  Google Scholar 

  63. Stein Z, Susser M (1975) The Dutch famine, 1944-1945, and the reproductive process. II. Interrelations of caloric rations and six indices at birth. Pediatr Res 9(2):76–83

    CAS  PubMed  Google Scholar 

  64. Stein Z, Susser M (1975) The Dutch famine, 1944-1945, and the reproductive process. I. Effects on six indices at birth. Pediatr Res 9(2):70–76

    CAS  PubMed  Google Scholar 

  65. Dowler EA, O'Connor D (2012) Rights-based approaches to addressing food poverty and food insecurity in Ireland and UK. Soc Sci Med 74(1):44–51

    Article  PubMed  Google Scholar 

  66. Hayward CE, Greenwood SL, Sibley CP, Baker PN, Jones RL (2011) Effect of young maternal age and skeletal growth on placental growth and development. Placenta 32(12):990–998

    Article  CAS  PubMed  Google Scholar 

  67. Snell LH, Haughey BP, Buck G, Marecki MA (1998) Metabolic crisis: hyperemesis gravidarum. J Perinat Neonatal Nurs 12(2):26–37

    Article  CAS  PubMed  Google Scholar 

  68. Gaccioli F, Lager S, Powell TL, Jansson T (2013) Placental transport in response to altered maternal nutrition. J Dev Orig Health Dis 4(2):101–115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. 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(Pt 1):3–8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Brawley L, Poston L, Hanson MA (2003) Mechanisms underlying the programming of small artery dysfunction: review of the model using low protein diet in pregnancy in the rat. Arch Physiol Biochem 111(1):23–35

    Article  CAS  PubMed  Google Scholar 

  71. Wallace JM, Aitken RP, Milne JS, Hay WW Jr (2004) Nutritionally mediated placental growth restriction in the growing adolescent: consequences for the fetus. Biol Reprod 71(4):1055–1062

    Article  CAS  PubMed  Google Scholar 

  72. Wallace JM, Luther JS, Milne JS, Aitken RP, Redmer DA, Reynolds LP et al (2006) Nutritional modulation of adolescent pregnancy outcome -- a review. Placenta 27(Suppl A):S61–S68

    Article  PubMed  CAS  Google Scholar 

  73. Redmer DA, Wallace JM, Reynolds LP (2004) Effect of nutrient intake during pregnancy on fetal and placental growth and vascular development. Domest Anim Endocrinol 27(3):199–217

    Article  CAS  PubMed  Google Scholar 

  74. Hayward CE, Greenwood SL, Sibley CP, Baker PN, Challis JR, Jones RL (2012) Effect of maternal age and growth on placental nutrient transport: potential mechanisms for teenagers’ predisposition to small-for-gestational-age birth? Am J Physiol Endocrinol Metab 302(2):E233–E242

    Article  CAS  PubMed  Google Scholar 

  75. Group HSCR, Metzger BE, Lowe LP, Dyer AR, Trimble ER, Chaovarindr U et al (2002) Hyperglycemia and adverse pregnancy outcomes. N Engl J Med 358(19):1991–2002

    Google Scholar 

  76. Jansson T, Wennergren M, Powell TL (1999) Placental glucose transport and GLUT 1 expression in insulin-dependent diabetes. Am J Obstet Gynecol 180(1 Pt 1):163–168

    Article  CAS  PubMed  Google Scholar 

  77. Bibee KP, Illsley NP, Moley KH (2011) Asymmetric syncytial expression of GLUT9 splice variants in human term placenta and alterations in diabetic pregnancies. Reprod Sci 18(1):20–27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Osmond DT, Nolan CJ, King RG, Brennecke SP, Gude NM (2000) Effects of gestational diabetes on human placental glucose uptake, transfer, and utilisation. Diabetologia 43(5):576–582

    Article  CAS  PubMed  Google Scholar 

  79. Jansson T, Ekstrand Y, Wennergren M, Powell TL (2001) Placental glucose transport in gestational diabetes mellitus. Am J Obstet Gynecol 184(2):111–116

    Article  CAS  PubMed  Google Scholar 

  80. Colomiere M, Permezel M, Riley C, Desoye G, Lappas M (2009) Defective insulin signaling in placenta from pregnancies complicated by gestational diabetes mellitus. Eur J Endocrinol 160(4):567–578

    Article  CAS  PubMed  Google Scholar 

  81. Jansson T, Ekstrand Y, Bjorn C, Wennergren M, Powell TL (2002) Alterations in the activity of placental amino acid transporters in pregnancies complicated by diabetes. Diabetes 51(7):2214–2219

    Article  CAS  PubMed  Google Scholar 

  82. Kuruvilla AG, D'Souza SW, Glazier JD, Mahendran D, Maresh MJ, Sibley CP (1994) Altered activity of the system A amino acid transporter in microvillous membrane vesicles from placentas of macrosomic babies born to diabetic women. J Clin Invest 94(2):689–695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Dicke JM, Henderson GI (1988) Placental amino acid uptake in normal and complicated pregnancies. Am J Med Sci 295(3):223–227

    Article  CAS  PubMed  Google Scholar 

  84. Magnusson AL, Waterman IJ, Wennergren M, Jansson T, Powell TL (2004) Triglyceride hydrolase activities and expression of fatty acid binding proteins in the human placenta in pregnancies complicated by intrauterine growth restriction and diabetes. J Clin Endocrinol Metab 89(9):4607–4614

    Article  CAS  PubMed  Google Scholar 

  85. Scifres CM, Chen B, Nelson DM, Sadovsky Y (2011) Fatty acid binding protein 4 regulates intracellular lipid accumulation in human trophoblasts. J Clin Endocrinol Metab 96(7):E1083–E1091

    Article  PubMed  PubMed Central  Google Scholar 

  86. Gauster M, Hiden U, van Poppel M, Frank S, Wadsack C, Hauguel-de Mouzon S et al (2011) Dysregulation of placental endothelial lipase in obese women with gestational diabetes mellitus. Diabetes 60(10):2457–2464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Radaelli T, Lepercq J, Varastehpour A, Basu S, Catalano PM, Hauguel-De Mouzon S (2009) Differential regulation of genes for fetoplacental lipid pathways in pregnancy with gestational and type 1 diabetes mellitus. Am J Obstet Gynecol 201(2):209.e1–209e10

    Article  CAS  Google Scholar 

  88. Stewart FM, Freeman DJ, Ramsay JE, Greer IA, Caslake M, Ferrell WR (2007) Longitudinal assessment of maternal endothelial function and markers of inflammation and placental function throughout pregnancy in lean and obese mothers. J Clin Endocrinol Metab 92(3):969–975

    Article  CAS  PubMed  Google Scholar 

  89. Ghio A, Bertolotto A, Resi V, Volpe L, Di Cianni G (2011) Triglyceride metabolism in pregnancy. Adv Clin Chem 55:133–153

    Article  CAS  PubMed  Google Scholar 

  90. Mazurkiewicz JC, Watts GF, Warburton FG, Slavin BM, Lowy C, Koukkou E (1994) Serum lipids, lipoproteins and apolipoproteins in pregnant non-diabetic patients. J Clin Endocrinol Metab 47(8):728–731

    CAS  Google Scholar 

  91. Okereke NC, Huston-Presley L, Amini SB, Kalhan S, Catalano PM (2004) Longitudinal changes in energy expenditure and body composition in obese women with normal and impaired glucose tolerance. Am J Physiol Endocrinol Metab 287(3):E472–E479

    Article  CAS  PubMed  Google Scholar 

  92. Catalano PM, Huston L, Amini SB, Kalhan SC (1999) Longitudinal changes in glucose metabolism during pregnancy in obese women with normal glucose tolerance and gestational diabetes mellitus. Am J Obstet Gynecol 180(4):903–916

    Article  CAS  PubMed  Google Scholar 

  93. Aviram A, Hod M, Yogev Y (2011) Maternal obesity: implications for pregnancy outcome and long-term risks-a link to maternal nutrition. Int J Gynaecol Obstet 115(Suppl 1):S6–10

    Article  PubMed  Google Scholar 

  94. Jones HN, Jansson T, Powell TL (2009) IL-6 stimulates system A amino acid transporter activity in trophoblast cells through STAT3 and increased expression of SNAT2. Am J Physiol Cell Physiol 297(5):C1228–C1235

    Article  CAS  PubMed  Google Scholar 

  95. Jansson N, Greenwood SL, Johansson BR, Powell TL, Jansson T (2003) Leptin stimulates the activity of the system A amino acid transporter in human placental villous fragments. J Clin Endocrinol Metab 88(3):1205–1211

    Article  CAS  PubMed  Google Scholar 

  96. Johansson M, Karlsson L, Wennergren M, Jansson T, Powell TL (2003) Activity and protein expression of Na+/K+ ATPase are reduced in microvillous syncytiotrophoblast plasma membranes isolated from pregnancies complicated by intrauterine growth restriction. J Clin Endocrinol Metab 88(6):2831–2837

    Article  CAS  PubMed  Google Scholar 

  97. Karl PI, Alpy KL, Fisher SE (1992) Amino acid transport by the cultured human placental trophoblast: effect of insulin on AIB transport. Am J Physiol 262(4 Pt 1):C834–C839

    Article  CAS  PubMed  Google Scholar 

  98. Jones HN, Jansson T, Powell TL (2010) Full-length adiponectin attenuates insulin signaling and inhibits insulin-stimulated amino Acid transport in human primary trophoblast cells. Diabetes 59(5):1161–1170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Jones HN, Woollett LA, Barbour N, Prasad PD, Powell TL, Jansson T (2009) High-fat diet before and during pregnancy causes marked up-regulation of placental nutrient transport and fetal overgrowth in C57/BL6 mice. FASEB J 23(1):271–278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Farley DM, Choi J, Dudley DJ, Li C, Jenkins SL, Myatt L et al (2010) Placental amino acid transport and placental leptin resistance in pregnancies complicated by maternal obesity. Placenta 31(8):718–724

    Article  CAS  PubMed  Google Scholar 

  101. Jansson N, Rosario FJ, Gaccioli F, Lager S, Jones HN, Roos S et al (2013) Activation of placental mTOR signaling and amino acid transporters in obese women giving birth to large babies. J Clin Endocrinol Metab 98(1):105–113

    Article  CAS  PubMed  Google Scholar 

  102. Metzger BE, Persson B, Lowe LP, Dyer AR, Cruickshank JK, Deerochanawong C et al (2010) Hyperglycemia and adverse pregnancy outcome study: neonatal glycemia. Pediatrics 126(6):e1545–e1552

    Article  PubMed  Google Scholar 

  103. Schaefer-Graf UM, Graf K, Kulbacka I, Kjos SL, Dudenhausen J, Vetter K et al (2008) Maternal lipids as strong determinants of fetal environment and growth in pregnancies with gestational diabetes mellitus. Diabetes Care 31(9):1858–1863

    Article  PubMed  PubMed Central  Google Scholar 

  104. Whyte K, Kelly H, O'Dwyer V, Gibbs M, O'Higgins A, Turner MJ (2013) Offspring birth weight and maternal fasting lipids in women screened for gestational diabetes mellitus (GDM). Eur J Obstet Gynecol Reprod Biol 170(1):67–70

    Article  CAS  PubMed  Google Scholar 

  105. Dube E, Gravel A, Martin C, Desparois G, Moussa I, Ethier-Chiasson M et al (2012) Modulation of fatty acid transport and metabolism by maternal obesity in the human full-term placenta. Biol Reprod 87(1):14. 1-11

    Article  PubMed  CAS  Google Scholar 

  106. Brass E, Hanson E, O'Tierney-Ginn PF (2013) Placental oleic acid uptake is lower in male offspring of obese women. Placenta 34(6):503–509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Borengasser SJ, Lau F, Kang P, Blackburn ML, Ronis MJ, Badger TM et al (2011) Maternal obesity during gestation impairs fatty acid oxidation and mitochondrial SIRT3 expression in rat offspring at weaning. PLoS One 6(8):e24068. https://doi.org/10.1371/journal.pone.0024068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Zhu MJ, Ma Y, Long NM, Du M, Ford SP (2010) Maternal obesity markedly increases placental fatty acid transporter expression and fetal blood triglycerides at midgestation in the ewe. Am J Physiol Regul Integr Comp Physiol 299(5):R1224–R1231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Calabuig-Navarro V, Haghiac M, Minium J, Glazebrook P, Ranasinghe GC, Hoppel C et al (2017) Effect of maternal obesity on placental lipid metabolism. Endocrinology. https://doi.org/10.1210/en.2017-00152

  110. Stark MJ, Clifton VL, Wright IM (2009) Neonates born to mothers with preeclampsia exhibit sex-specific alterations in microvascular function. Pediatr Res 65(3):292–295

    Article  PubMed  Google Scholar 

  111. Gheorghe CP, Goyal R, Holweger JD, Longo LD (2009) Placental gene expression responses to maternal protein restriction in the mouse. Placenta 30(5):411–417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Gabory A, Ferry L, Fajardy I, Jouneau L, Gothie JD, Vige A et al (2012) Maternal diets trigger sex-specific divergent trajectories of gene expression and epigenetic systems in mouse placenta. PLoS One 7(11):e47986. https://doi.org/10.1371/journal.pone.0047986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Chen PY, Ganguly A, Rubbi L, Orozco LD, Morselli M, Ashraf D et al (2013) Intrauterine calorie restriction affects placental DNA methylation and gene expression. Physiol Genomics 45(14):565–576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Tarrade A, Rousseau-Ralliard D, Aubriere MC, Peynot N, Dahirel M, Bertrand-Michel J et al (2013) Sexual dimorphism of the feto-placental phenotype in response to a high fat and control maternal diets in a rabbit model. PLoS One 8(12):e83458. https://doi.org/10.1371/journal.pone.0083458

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  115. Cox LA, Li C, Glenn JP, Lange K, Spradling KD, Nathanielsz PW et al (2013) Expression of the placental transcriptome in maternal nutrient reduction in baboons is dependent on fetal sex. J Nutr 143(11):1698–1708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Sferruzzi-Perri AN, Vaughan OR, Haro M, Cooper WN, Musial B, Charalambous M et al (2013) An obesogenic diet during mouse pregnancy modifies maternal nutrient partitioning and the fetal growth trajectory. FASEB J 27(10):3928–3937

    Article  CAS  PubMed  Google Scholar 

  117. Lin Y, Zhuo Y, Fang ZF, Che LQ, Wu D (2012) Effect of maternal dietary energy types on placenta nutrient transporter gene expressions and intrauterine fetal growth in rats. Nutrition 28(10):1037–1043

    Article  CAS  PubMed  Google Scholar 

  118. King V, Hibbert N, Seckl JR, Norman JE, Drake AJ (2013) The effects of an obesogenic diet during pregnancy on fetal growth and placental gene expression are gestation dependent. Placenta 34(11):1087–1090

    Article  CAS  PubMed  Google Scholar 

  119. Choi SW, Friso S (2010) Epigenetics: a new bridge between nutrition and health. Adv Nutr 1(1):8–16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Gut P, Verdin E (2013) The nexus of chromatin regulation and intermediary metabolism. Nature 502(7472):489–498

    Article  CAS  PubMed  Google Scholar 

  121. Heijmans BT, Tobi EW, Lumey LH, Slagboom PE (2009) The epigenome: archive of the prenatal environment. Epigenetics 4(8):526–531

    Article  CAS  PubMed  Google Scholar 

  122. Tobi EW, Lumey LH, Talens RP, Kremer D, Putter H, Stein AD et al (2009) DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum Mol Genet 18(21):4046–4053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Waterland RA, Lin JR, Smith CA, Jirtle RL (2006) Post-weaning diet affects genomic imprinting at the insulin-like growth factor 2 (Igf2) locus. Hum Mol Genet 15(5):705–716

    Article  CAS  PubMed  Google Scholar 

  124. Keyes MK, Jang H, Mason JB, Liu Z, Crott JW, Smith DE et al (2007) Older age and dietary folate are determinants of genomic and p16-specific DNA methylation in mouse colon. J Nutr 137:1713–1717

    Article  CAS  PubMed  Google Scholar 

  125. Hoile SP, Irvine NA, Kelsall CJ, Sibbons C, Feunteun A, Collister A et al (2013) Maternal fat intake in rats alters 20:4n-6 and 22:6n-3 status and the epigenetic regulation of Fads2 in offspring liver. J Nutr Biochem 24(7):1213–1220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Hass BS, Hart RW, MH L, Lyn-Cook BD (1993) Effects of caloric restriction in animals on cellular function, oncogene expression, and DNA methylation in vitro. Mutat Res 295(4-6):281–289

    Article  CAS  PubMed  Google Scholar 

  127. Gallou-Kabani C, Gabory A, Tost J, Karimi M, Mayeur S, Lesage J et al (2010) Sex- and diet-specific changes of imprinted gene expression and DNA methylation in mouse placenta under a high-fat diet. PLoS One 5(12):e14398. https://doi.org/10.1371/journal.pone.0014398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Bouchard L, Hivert MF, Guay SP, St-Pierre J, Perron P, Brisson D (2012) Placental adiponectin gene DNA methylation levels are associated with mothers’ blood glucose concentration. Diabetes 61(5):1272–1280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Bouchard L, Thibault S, Guay SP, Santure M, Monpetit A, St-Pierre J et al (2010) Leptin gene epigenetic adaptation to impaired glucose metabolism during pregnancy. Diabetes Care 33(11):2436–2441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. El Hajj N, Pliushch G, Schneider E, Dittrich M, Muller T, Korenkov M et al (2013) Metabolic programming of MEST DNA methylation by intrauterine exposure to gestational diabetes mellitus. Diabetes 62(4):1320–1328

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  131. Scott JM, Weir DG (1998) Folic acid, homocysteine and one-carbon metabolism: a review of the essential biochemistry. J Cardiovasc Risk 5(4):223–227

    Article  CAS  PubMed  Google Scholar 

  132. Waterland RA, Jirtle RL (2003) Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 23(15):5293–5300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. 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(6):1382–1386

    Article  CAS  PubMed  Google Scholar 

  134. Petrossian TC, Clarke SG (2011) Uncovering the human methyltransferasome. Mol Cell Proteomics 10(1):M110.000976. https://doi.org/10.1074/mcp.M110.000976

    Article  PubMed  CAS  Google Scholar 

  135. Kirkland JB (2009) Niacin status impacts chromatin structure. J Nutr 139(12):2397–2401

    Article  CAS  PubMed  Google Scholar 

  136. Bacalini MG, Friso S, Olivieri F, Pirazzini C, Giuliani C, Capri M et al (2014) Present and future of anti-ageing epigenetic diets. Mech Ageing Dev 136-137:101–115

    Article  CAS  PubMed  Google Scholar 

  137. Reik W, Walter J (2001) Genomic imprinting: parental influence on the genome. Nat Rev Genet 2(1):21–32

    Article  CAS  PubMed  Google Scholar 

  138. Coan PM, Burton GJ, Ferguson-Smith AC (2005) Imprinted genes in the placenta--a review. Placenta 26(Suppl A):S10–S20

    Article  PubMed  CAS  Google Scholar 

  139. Monk D, Arnaud P, Frost J, Hills FA, Stanier P, Feil R et al (2009) Reciprocal imprinting of human GRB10 in placental trophoblast and brain: evolutionary conservation of reversed allelic expression. Hum Mol Genet 18(16):3066–3074

    Article  CAS  PubMed  Google Scholar 

  140. Constancia M, Kelsey G, Reik W (2004) Resourceful imprinting. Nature 432(7013):53–57

    Article  CAS  PubMed  Google Scholar 

  141. Cleaton MA, Edwards CA, Ferguson-Smith AC (2014) Phenotypic outcomes of imprinted gene models in mice: elucidation of pre- and postnatal functions of imprinted genes. Annu Rev Genomics Hum Genet 15:93–126

    Article  CAS  PubMed  Google Scholar 

  142. Reik W, Constancia M, Fowden A, Anderson N, Dean W, Ferguson-Smith A et al (2003) Regulation of supply and demand for maternal nutrients in mammals by imprinted genes. J Physiol 547(Pt 1):35–44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Sferruzzi-Perri AN, Vaughan OR, Coan PM, Suciu MC, Darbyshire R, Constancia M et al (2011) Placental-specific Igf2 deficiency alters developmental adaptations to undernutrition in mice. Endocrinology 152(8):3202–3212

    Article  CAS  PubMed  Google Scholar 

  144. Soubry A, Murphy SK, Wang F, Huang Z, Vidal AC, Fuemmeler BF et al (2013) Newborns of obese parents have altered DNA methylation patterns at imprinted genes. Int J Obes (Lond) 39(4):650–657

    Article  CAS  Google Scholar 

  145. Perkins E, Murphy SK, Murtha AP, Schildkraut J, Jirtle RL, Demark-Wahnefried W et al (2012) Insulin-like growth factor 2/H19 methylation at birth and risk of overweight and obesity in children. J Pediatr 161(1):31–39

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Boyd PA, Scott A, Keeling JW (1986) Quantitative structural studies on placentas from pregnancies complicated by diabetes mellitus. Br J Obstet Gynaecol 93(1):31–35

    Article  CAS  PubMed  Google Scholar 

  147. Nelson SM, Coan PM, Burton GJ, Lindsay RS (2009) Placental structure in type 1 diabetes: relation to fetal insulin, leptin, and IGF-I. Diabetes 58(11):2634–2641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Mayhew TM, Manwani R, Ohadike C, Wijesekara J, Baker PN (2007) The placenta in pre-eclampsia and intrauterine growth restriction: studies on exchange surface areas, diffusion distances and villous membrane diffusive conductances. Placenta 28(2-3):233–238

    Article  CAS  PubMed  Google Scholar 

  149. Alwasel SH, Harrath AH, Aldahmash WM, Abotalib Z, Nyengaard JR, Osmond C et al (2014) Sex differences in regional specialisation across the placental surface. Placenta 35(6):365–369

    Article  CAS  PubMed  Google Scholar 

  150. Roberts CT, Sohlstrom A, Kind KL, Earl RA, Khong TY, Robinson JS et al (2001) Maternal food restriction reduces the exchange surface area and increases the barrier thickness of the placenta in the guinea-pig. Placenta 22(2-3):177–185

    Article  CAS  PubMed  Google Scholar 

  151. Reynolds CM, Vickers MH, Harrison CJ, Segovia SA, Gray C (2015) Maternal high fat and/or salt consumption induces sex-specific inflammatory and nutrient transport in the rat placenta. Physiol Rep 3(5):pii: e12399. 10.14814/phy2.12399

    Article  CAS  Google Scholar 

  152. Kim DW, Young SL, Grattan DR, Jasoni CL (2014) Obesity during pregnancy disrupts placental morphology, cell proliferation, and inflammation in a sex-specific manner across gestation in the mouse. Biol Reprod 90(6):130. https://doi.org/10.1095/biolreprod.113.117259

    Article  PubMed  CAS  Google Scholar 

  153. Muralimanoharan S, Maloyan A, Myatt L (2013) Evidence of sexual dimorphism in the placental function with severe preeclampsia. Placenta 34(12):1183–1189

    Article  CAS  PubMed  Google Scholar 

  154. Coughlan MT, Vervaart PP, Permezel M, Georgiou HM, Rice GE (2004) Altered placental oxidative stress status in gestational diabetes mellitus. Placenta 25(1):78–84

    Article  CAS  PubMed  Google Scholar 

  155. Myatt L, Cui X (2004) Oxidative stress in the placenta. Histochem Cell Biol 122(4):369–382

    Article  CAS  PubMed  Google Scholar 

  156. Roberts VH, Smith J, McLea SA, Heizer AB, Richardson JL, Myatt L (2009) Effect of increasing maternal body mass index on oxidative and nitrative stress in the human placenta. Placenta 30(2):169–175

    Article  CAS  PubMed  Google Scholar 

  157. Evans RW, Powers RW, Ness RB, Cropcho LJ, Daftary AR, Harger GF et al (2003) Maternal and fetal amino acid concentrations and fetal outcomes during pre-eclampsia. Reproduction 125(6):785–790

    Article  CAS  PubMed  Google Scholar 

  158. Alvino G, Cozzi V, Radaelli T, Ortega H, Herrera E, Cetin I (2008) Maternal and fetal fatty acid profile in normal and intrauterine growth restriction pregnancies with and without preeclampsia. Pediatr Res 64(6):615–620

    Article  CAS  PubMed  Google Scholar 

  159. Roy S, Dhobale M, Dangat K, Mehendale S, Wagh G, Lalwani S et al (2014) Differential levels of long chain polyunsaturated fatty acids in women with preeclampsia delivering male and female babies. Prostaglandins Leukot Essent Fatty Acids 91(5):227–232

    Article  CAS  PubMed  Google Scholar 

  160. Desforges M, Ditchfield A, Hirst CR, Pegorie C, Martyn-Smith K, Sibley CP et al (2013) Reduced placental taurine transporter (TauT) activity in pregnancies complicated by pre-eclampsia and maternal obesity. Adv Exp Med Biol 776:81–91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Malina A, Daftary A, Crombleholme W, Markovic N, Roberts JM (2005) Placental system A transporter mRNA is not different in preeclampsia, normal pregnancy, or pregnancies with small-for-gestational-age infants. Hypertens Pregnancy 24(1):65–74

    Article  CAS  PubMed  Google Scholar 

  162. Shibata E, Hubel CA, Powers RW, von Versen-Hoeynck F, Gammill H, Rajakumar A et al (2008) Placental system A amino acid transport is reduced in pregnancies with small for gestational age (SGA) infants but not in preeclampsia with SGA infants. Placenta 29(10):879–882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Speake PF, Glazier JD, Ayuk PT, Reade M, Sibley CP, D'Souza SW (2003) L-Arginine transport across the basal plasma membrane of the syncytiotrophoblast of the human placenta from normal and preeclamptic pregnancies. J Clin Endocrinol Metab 88(9):4287–4292

    Article  CAS  PubMed  Google Scholar 

  164. Wadhwani N, Patil V, Pisal H, Joshi A, Mehendale S, Gupte S et al (2014) Altered maternal proportions of long chain polyunsaturated fatty acids and their transport leads to disturbed fetal stores in preeclampsia. Prostaglandins Leukot Essent Fatty Acids 91(1-2):21–30

    Article  CAS  PubMed  Google Scholar 

  165. Ray PD, Huang BW, Tsuji Y (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24(5):981–990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Muralimanoharan S, Guo C, Myatt L, Maloyan A (2015) Sexual dimorphism in miR-210 expression and mitochondrial dysfunction in the placenta with maternal obesity. Int J Obes (Lond) 39(8):1274–1281

    Article  CAS  Google Scholar 

  167. Sen CK, Packer L (1996) Antioxidant and redox regulation of gene transcription. FASEB J 10(7):709–720

    Article  CAS  PubMed  Google Scholar 

  168. Arner ES, Holmgren A (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267(20):6102–6109

    Article  CAS  PubMed  Google Scholar 

  169. Evans L, Myatt L (2017) Sexual dimorphism in the effect of maternal obesity on antioxidant defense mechanisms in the human placenta. Placenta 51:64–69

    Article  CAS  PubMed  Google Scholar 

  170. Vanderlelie J, Perkins AV (2011) Selenium and preeclampsia: a global perspective. Pregnancy Hypertens 1(3-4):213–224

    Article  CAS  PubMed  Google Scholar 

  171. Blazewicz A, Klatka M, Astel A, Korona-Glowniak I, Dolliver W, Szwerc W et al (2015) Serum and urinary selenium levels in obese children: a cross-sectional study. J Trace Elem Med Biol 29:116–122

    Article  CAS  PubMed  Google Scholar 

  172. Alasfar F, Ben-Nakhi M, Khoursheed M, Kehinde EO, Alsaleh M (2011) Selenium is significantly depleted among morbidly obese female patients seeking bariatric surgery. Obes Surg 21(11):1710–1713

    Article  PubMed  Google Scholar 

  173. Barker D, Osmond C, Grant S, Thornburg KL, Cooper C, Ring S et al (2013) Maternal cotyledons at birth predict blood pressure in childhood. Placenta 34(8):672–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Barker DJ, Hales CN, Fall CH, Osmond C, Phipps K, Clark PM (1993) Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36(1):62–67

    Article  CAS  PubMed  Google Scholar 

  175. Barker DJ, Osmond C, Forsen TJ, Thornburg KL, Kajantie E, Eriksson JG (2013) Foetal and childhood growth and asthma in adult life. Acta Paediatr 102(7):732–738

    Article  PubMed  Google Scholar 

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Myatt, L., Thornburg, K.L. (2018). Effects of Prenatal Nutrition and the Role of the Placenta in Health and Disease. In: Guest, P. (eds) Investigations of Early Nutrition Effects on Long-Term Health. Methods in Molecular Biology, vol 1735. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7614-0_2

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