1932

Abstract

The placenta is the gatekeeper between the mother and the fetus. Over the first trimester of pregnancy, the fetus is nourished by uterine gland secretions in a process known as histiotrophic nutrition. During the second trimester of pregnancy, placentation has evolved to the point at which nutrients are delivered to the placenta via maternal blood (hemotrophic nutrition). Over gestation, the placenta must adapt to these variable nutrient supplies, to alterations in maternal physiology and blood flow, and to dynamic changes in fetal growth rates. Numerous questions remain about the mechanisms used to transport nutrients to the fetus and the maternal and fetal determinants of this process. Growing data highlight the ability of the placenta to regulate this process. As new technologies and omics approaches are utilized to study this maternofetal interface, greater insight into this unique organ and its impact on fetal development and long-term health has been obtained.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-nutr-061121-085246
2023-08-21
2024-04-29
Loading full text...

Full text loading...

/deliver/fulltext/nutr/43/1/annurev-nutr-061121-085246.html?itemId=/content/journals/10.1146/annurev-nutr-061121-085246&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    ACOG 2015. Practice bulletin no. 150: early pregnancy loss. Obstet. Gynecol. 125:1258–67
    [Google Scholar]
  2. 2.
    Ahern DT, Bansal P, Armillei MK, Faustino IV, Kondaveeti Y et al. 2022. Monosomy X in isogenic human iPSC-derived trophoblast model impacts expression modules preserved in human placenta. PNAS 119:e2211073119
    [Google Scholar]
  3. 3.
    Akison LK, Nitert MD, Clifton VL, Moritz KM, Simmons DG. 2017. Review: alterations in placental glycogen deposition in complicated pregnancies: current preclinical and clinical evidence. Placenta 54:52–58
    [Google Scholar]
  4. 4.
    Aplin JD, Myers JE, Timms K, Westwood M. 2020. Tracking placental development in health and disease. Nat. Rev. Endocrinol. 16:479–94
    [Google Scholar]
  5. 5.
    Avila Cobos F, Alquicira-Hernandez J, Powell JE, Mestdagh P, De Preter K. 2020. Benchmarking of cell type deconvolution pipelines for transcriptomics data. Nat. Commun. 11:5650
    [Google Scholar]
  6. 6.
    Aye I, Gong S, Avellino G, Barbagallo R, Gaccioli F et al. 2022. Placental sex-dependent spermine synthesis regulates trophoblast gene expression through acetyl-coA metabolism and histone acetylation. Commun. Biol 5:586
    [Google Scholar]
  7. 7.
    Baergen RN. 2005. Manual of Benirschke and Kaufmann's Pathology of the Human Placenta New York: Springer
  8. 8.
    Bahr TM, Ward DM, Jia X, Ohls RK, German KR, Christensen RD. 2021. Is the erythropoietin-erythroferrone-hepcidin axis intact in human neonates?. Blood Cells Mol. Dis. 88:102536
    [Google Scholar]
  9. 9.
    Barker DJ, Gluckman PD, Godfrey KM, Harding JE, Owens JA et al. 1979. Placental hypertrophy in severe pregnancy anemia. Br. J. Obstet. Gynaecol. 77:398–409
    [Google Scholar]
  10. 10.
    Barker DJP. 2012. Sir Richard Doll Lecture. Developmental origins of chronic disease. Public Health 126:185–89
    [Google Scholar]
  11. 11.
    Bastian TW, Rao R, Tran PV, Georgieff MK. 2020. The effects of early-life iron deficiency on brain energy metabolism. Neurosci. Insights 15:2633105520935104
    [Google Scholar]
  12. 12.
    Battaglia FC, Regnault TR. 2001. Placental transport and metabolism of amino acids. Placenta 22:145–61
    [Google Scholar]
  13. 13.
    Beckert RH, Baer RJ, Anderson JG, Jelliffe-Pawlowski LL, Rogers EE. 2019. Maternal anemia and pregnancy outcomes: a population-based study. J. Perinatol. 39:911–19
    [Google Scholar]
  14. 14.
    Benson AE, Shatzel JJ, Ryan KS, Hedges MA, Martens K et al. 2022. The incidence, complications, and treatment of iron deficiency in pregnancy. Eur. J. Haematol. 109:633–42
    [Google Scholar]
  15. 15.
    Best CM, Pressman EK, Chang C, Cooper E, Guillet R et al. 2016. Maternal iron status during pregnancy compared to neonatal iron status better predicts placental iron transporter expression in humans. FASEB J. 30:3541–50
    [Google Scholar]
  16. 16.
    Bhattacharya A, Freedman AN, Avula V, Harris R, Liu W et al. 2022. Placental genomics mediates genetic associations with complex health traits and disease. Nat. Commun. 13:706
    [Google Scholar]
  17. 17.
    Block LN, Bowman BD, Schmidt JK, Keding LT, Stanic AK, Golos TG. 2021. The promise of placental extracellular vesicles: models and challenges for diagnosing placental dysfunction in uterodagger. Biol. Reprod. 104:27–57
    [Google Scholar]
  18. 18.
    Bobinski R, Mikulska M. 2015. The ins and outs of maternal-fetal fatty acid metabolism. Acta Biochim. Pol. 62:499–507
    [Google Scholar]
  19. 19.
    Braun AE, Mitchel OR, Gonzalez TL, Sun T, Flowers AE et al. 2022. Sex at the interface: the origin and impact of sex differences in the developing human placenta. Biol. Sex Differ. 13:50
    [Google Scholar]
  20. 20.
    Brown K, Heller DS, Zamudio S, Illsley NP. 2011. Glucose transporter 3 (GLUT3) protein expression in human placenta across gestation. Placenta 32:1041–49
    [Google Scholar]
  21. 21.
    Brunst KJ, Sanchez Guerra M, Gennings C, Hacker M, Jara C et al. 2017. Maternal lifetime stress and prenatal psychological functioning and decreased placental mitochondrial DNA copy number in the PRISM study. Am. J. Epidemiol. 186:1227–36
    [Google Scholar]
  22. 22.
    Brunst KJ, Zhang L, Zhang X, Baccarelli AA, Bloomquist T, Wright RJ. 2021. Associations between maternal lifetime stress and placental mitochondrial DNA mutations in an urban multiethnic cohort. Biol. Psychiatry 89:570–78
    [Google Scholar]
  23. 23.
    Burton GJ, Jauniaux E. 1995. Sonographic, stereological and Doppler flow velocimetric assessments of placental maturity. Br. J. Obstet. Gynaecol. 102:818–25
    [Google Scholar]
  24. 24.
    Burton GJ, Jauniaux E. 2018. Development of the human placenta and fetal heart: synergic or independent?. Front. Physiol. 9:373
    [Google Scholar]
  25. 25.
    Burton GJ, Woods AW, Jauniaux E, Kingdom JC. 2009. Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy. Placenta 30:473–82
    [Google Scholar]
  26. 26.
    Calabuig-Navarro V, Haghiac M, Minium J, Glazebrook P, Ranasinghe GC et al. 2017. Effect of maternal obesity on placental lipid metabolism. Endocrinology 158:2543–55
    [Google Scholar]
  27. 27.
    Carroll A, Desforges M, Jones CJP, Heazell AEP. 2022. Morphological and functional changes in placentas from prolonged pregnancies. Placenta 125:29–35
    [Google Scholar]
  28. 28.
    Carter RC, Georgieff MK, Ennis KM, Dodge NC, Wainwright H et al. 2021. Prenatal alcohol-related alterations in maternal, placental, neonatal, and infant iron homeostasis. Am. J. Clin. Nutr. 114:1107–22
    [Google Scholar]
  29. 29.
    Cetin I, Marconi AM, Baggiani AM, Buscaglia M, Pardi G et al. 1995. In vivo placental transport of glycine and leucine in human pregnancies. Pediatr. Res. 37:571–75
    [Google Scholar]
  30. 30.
    Cetin I, Ronzoni S, Marconi AM, Perugino G, Corbetta C et al. 1996. Maternal concentrations and fetal-maternal concentration differences of plasma amino acids in normal and intrauterine growth-restricted pregnancies. Am. J. Obstet. Gynecol. 174:1575–83
    [Google Scholar]
  31. 31.
    Chatterjee S, Ouidir M, Tekola-Ayele F. 2021. Genetic and in utero environmental contributions to DNA methylation variation in placenta. Hum. Mol. Genet. 30:1968–76
    [Google Scholar]
  32. 32.
    Chen HJ, Attieh ZK, Syed BA, Kuo YM, Stevens V et al. 2010. Identification of Zyklopen, a new member of the vertebrate multicopper ferroxidase family, and characterization in rodents and human cells. J. Nutr. 140:1728–35
    [Google Scholar]
  33. 33.
    Cindrova-Davies T, Fogarty NME, Jones CJP, Kingdom J, Burton GJ. 2018. Evidence of oxidative stress-induced senescence in mature, post-mature and pathological human placentas. Placenta 68:15–22
    [Google Scholar]
  34. 34.
    Cindrova-Davies T, Sferruzzi-Perri AN. 2022. Human placental development and function. Semin. Cell Dev. Biol. 131:66–77
    [Google Scholar]
  35. 35.
    Cleal JK, Glazier JD, Ntani G, Crozier SR, Day PE et al. 2011. Facilitated transporters mediate net efflux of amino acids to the fetus across the basal membrane of the placental syncytiotrophoblast. J. Physiol. 589:987–97
    [Google Scholar]
  36. 36.
    Cleal JK, Lofthouse EM, Sengers BG, Lewis RM. 2018. A systems perspective on placental amino acid transport. J. Physiol. 596:5511–22
    [Google Scholar]
  37. 37.
    Coorens THH, Oliver TRW, Sanghvi R, Sovio U, Cook E et al. 2021. Inherent mosaicism and extensive mutation of human placentas. Nature 592:80–85
    [Google Scholar]
  38. 38.
    de Angelis P, Miller RK, Darrah TH, Katzman PJ, Pressman EK et al. 2017. Elemental content of the placenta: a comparison between two high-risk obstetrical populations, adult women carrying multiples and adolescents carrying singletons. Environ. Res. 158:553–65
    [Google Scholar]
  39. 39.
    Delaney KM, Guillet R, Pressman EK, Ganz T, Nemeth E, O'Brien KO 2021. Umbilical cord erythroferrone is inversely associated with hepcidin, but does not capture the most variability in iron status of neonates born to teens carrying singletons and women carrying multiples. J. Nutr. 151:2590–600
    [Google Scholar]
  40. 40.
    Demir R, Kayisli UA, Celik-Ozenci C, Korgun ET, Demir-Weusten AY, Arici A. 2002. Structural differentiation of human uterine luminal and glandular epithelium during early pregnancy: an ultrastructural and immunohistochemical study. Placenta 23:672–84
    [Google Scholar]
  41. 41.
    Deyssenroth MA, Peng S, Hao K, Lambertini L, Marsit CJ, Chen J 2017. Whole-transcriptome analysis delineates the human placenta gene network and its associations with fetal growth. BMC Genom. 18:520
    [Google Scholar]
  42. 42.
    Duttaroy AK, Basak S. 2020. Maternal dietary fatty acids and their roles in human placental development. Prostaglandins Leukot. Essent. Fatty Acids 155:102080
    [Google Scholar]
  43. 43.
    Eisenberg T, Abdellatif M, Schroeder S, Primessnig U, Stekovic S et al. 2016. Cardioprotection and lifespan extension by the natural polyamine spermidine. Nat. Med. 22:1428–38
    [Google Scholar]
  44. 44.
    Fallingborg J. 1999. Intraluminal pH of the human gastrointestinal tract. Dan. Med. Bull. 46:183–96
    [Google Scholar]
  45. 45.
    Figueras F, Gardosi J. 2011. Intrauterine growth restriction: new concepts in antenatal surveillance, diagnosis, and management. Am. J. Obstet. Gynecol. 204:288–300
    [Google Scholar]
  46. 46.
    Fisher AL, Nemeth E. 2017. Iron homeostasis during pregnancy. Am. J. Clin. Nutr. 106:1567S–74S
    [Google Scholar]
  47. 47.
    Fowden AL, Sferruzzi-Perri AN, Coan PM, Constancia M, Burton GJ 2009. Placental efficiency and adaptation: endocrine regulation. J. Physiol. 587:3459–72
    [Google Scholar]
  48. 48.
    Frank H-G. 2017. Placental development. Fetal and Neonatal Physiology101–13. Amsterdam: Elsevier
    [Google Scholar]
  49. 49.
    Gaccioli F, Lager S. 2016. Placental nutrient transport and intrauterine growth restriction. Front. Physiol. 7:40
    [Google Scholar]
  50. 50.
    Galan HL, Marconi AM, Paolini CL, Cheung A, Battaglia FC. 2009. The transplacental transport of essential amino acids in uncomplicated human pregnancies. Am. J. Obstet. Gynecol. 200:91.e1–7
    [Google Scholar]
  51. 51.
    Gauster M, Moser G, Wernitznig S, Kupper N, Huppertz B. 2022. Early human trophoblast development: from morphology to function. Cell. Mol. Life Sci. 79:345
    [Google Scholar]
  52. 52.
    Gazquez A, Prieto-Sanchez MT, Blanco-Carnero JE, Ruiz-Palacios M, Nieto A et al. 2020. Altered materno-fetal transfer of 13C-polyunsaturated fatty acids in obese pregnant women. Clin. Nutr. 39:1101–7
    [Google Scholar]
  53. 53.
    Gazquez A, Prieto-Sanchez MT, Blanco-Carnero JE, van Harskamp D, Perazzolo S et al. 2019. In vivo kinetic study of materno-fetal fatty acid transfer in obese and normal weight pregnant women. J. Physiol. 597:4959–73
    [Google Scholar]
  54. 54.
    Gil-Sanchez A, Demmelmair H, Parrilla JJ, Koletzko B, Larque E. 2011. Mechanisms involved in the selective transfer of long chain polyunsaturated fatty acids to the fetus. Front. Genet. 2:57
    [Google Scholar]
  55. 55.
    Giordano C, Iommarini L, Giordano L, Maresca A, Pisano A et al. 2014. Efficient mitochondrial biogenesis drives incomplete penetrance in Leber's hereditary optic neuropathy. Brain 137:335–53
    [Google Scholar]
  56. 56.
    Gong S, Gaccioli F, Dopierala J, Sovio U, Cook E et al. 2021. The RNA landscape of the human placenta in health and disease. Nat. Commun. 12:2639
    [Google Scholar]
  57. 57.
    Gong S, Sovio U, Aye IL, Gaccioli F, Dopierala J et al. 2018. Placental polyamine metabolism differs by fetal sex, fetal growth restriction, and preeclampsia. JCI Insight 3:e120723
    [Google Scholar]
  58. 58.
    Henriksen T, Roland MCP, Sajjad MU, Haugen G, Michelsen TM. 2022. Uteroplacental versus fetal use of glucose in healthy pregnancies at term. A human in vivo study. Placenta 128:116–22
    [Google Scholar]
  59. 59.
    Herrera E, Desoye G. 2016. Maternal and fetal lipid metabolism under normal and gestational diabetic conditions. Horm. Mol. Biol. Clin. Investig. 26:109–27
    [Google Scholar]
  60. 60.
    Hirschmugl B, Perazzolo S, Sengers BG, Lewis RM, Gruber M et al. 2021. Placental mobilization of free fatty acids contributes to altered materno-fetal transfer in obesity. Int. J. Obes. 45:1114–23
    [Google Scholar]
  61. 61.
    Illsley NP. 2000. Glucose transporters in the human placenta. Placenta 21:14–22
    [Google Scholar]
  62. 62.
    Jaacks LM, Young MF, Essley BV, McNanley TJ, Cooper EM et al. 2011. Placental expression of the heme transporter, feline leukemia virus subgroup C receptor, is related to maternal iron status in pregnant adolescents. J. Nutr. 141:1267–72
    [Google Scholar]
  63. 63.
    James-Allan LB, Arbet J, Teal SB, Powell TL, Jansson T. 2019. Insulin stimulates GLUT4 trafficking to the syncytiotrophoblast basal plasma membrane in the human placenta. J. Clin. Endocrinol. Metab. 104:4255–38
    [Google Scholar]
  64. 64.
    James JL, Boss AL, Sun C, Allerkamp HH, Clark AR. 2021. From stem cells to spiral arteries: a journey through early placental development. Placenta 125:68–77
    [Google Scholar]
  65. 65.
    James JL, Chamley LW, Clark AR. 2017. Feeding your baby in utero: how the uteroplacental circulation impacts pregnancy. Physiology 32:234–45
    [Google Scholar]
  66. 66.
    James WH. 1975. Sex ratio in twin births. Ann. Hum. Biol. 2:365–78
    [Google Scholar]
  67. 67.
    Janssen AB, Tunster SJ, Savory N, Holmes A, Beasley J et al. 2015. Placental expression of imprinted genes varies with sampling site and mode of delivery. Placenta 36:790–95
    [Google Scholar]
  68. 68.
    Jaskolka D, Retnakaran R, Zinman B, Kramer CK. 2015. Sex of the baby and risk of gestational diabetes mellitus in the mother: a systematic review and meta-analysis. Diabetologia 58:2469–75
    [Google Scholar]
  69. 69.
    Jauniaux E, Gulbis B, Gerloo E. 1999. Free amino acids in human fetal liver and fluids at 12–17 weeks of gestation. Hum. Reprod. 14:1638–41
    [Google Scholar]
  70. 70.
    Jauniaux E, Watson AL, Hempstock J, Bao YP, Skepper JN, Burton GJ. 2000. Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. Am. J. Pathol. 157:2111–22
    [Google Scholar]
  71. 71.
    Jensen OE, Chernyavsky IE. 2019. Blood flow and transport in the human placenta. Annu. Rev. Fluid Mech. 51:25–47
    [Google Scholar]
  72. 72.
    Jiang S, Teague AM, Tryggestad JB, Aston CE, Lyons T, Chernausek SD. 2017. Effects of maternal diabetes and fetal sex on human placenta mitochondrial biogenesis. Placenta 57:26–32
    [Google Scholar]
  73. 73.
    Jones CJ, Choudhury RH, Aplin JD. 2015. Tracking nutrient transfer at the human maternofetal interface from 4 weeks to term. Placenta 36:372–80
    [Google Scholar]
  74. 74.
    Karahoda R, Zaugg J, Fuenzalida B, Kallol S, Moser-Haessig R et al. 2022. Trophoblast differentiation affects crucial nutritive functions of placental membrane transporters. Front. Cell Dev. Biol. 10:820286
    [Google Scholar]
  75. 75.
    Kertschanska S, Kosanke G, Kaufmann P. 1997. Pressure dependence of so-called transtrophoblastic channels during fetal perfusion of human placental villi. Microsc. Res. Tech. 38:52–62
    [Google Scholar]
  76. 76.
    Kuzawa CW. 1998. Adipose tissue in human infancy and childhood: an evolutionary perspective. Am. J. Phys. Anthropol. 107:Suppl. 27177–209
    [Google Scholar]
  77. 77.
    Lager S, Powell TL. 2012. Regulation of nutrient transport across the placenta. J. Pregnancy 2012:179827
    [Google Scholar]
  78. 78.
    Larque E, Pagan A, Prieto MT, Blanco JE, Gil-Sanchez A et al. 2014. Placental fatty acid transfer: a key factor in fetal growth. Ann. Nutr. Metab. 64:247–53
    [Google Scholar]
  79. 79.
    Liu D, Chen Y, Ren Y, Yuan P, Wang N et al. 2022. Primary specification of blastocyst trophectoderm by scRNA-seq: new insights into embryo implantation. Sci. Adv. 8:eabj3725
    [Google Scholar]
  80. 80.
    Liu X, Fei H, Yang C, Wang J, Zhu X et al. 2022. Trophoblast-derived extracellular vesicles promote preeclampsia by regulating macrophage polarization. Hypertension 79:2274–87
    [Google Scholar]
  81. 81.
    Liu Y, Fan X, Wang R, Lu X, Dang YL et al. 2018. Single-cell RNA-seq reveals the diversity of trophoblast subtypes and patterns of differentiation in the human placenta. Cell Res. 28:819–32
    [Google Scholar]
  82. 82.
    Lofthouse EM, Perazzolo S, Brooks S, Crocker IP, Glazier JD et al. 2016. Phenylalanine transfer across the isolated perfused human placenta: an experimental and modeling investigation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 310:R828–36
    [Google Scholar]
  83. 83.
    Lu M, Sferruzzi-Perri AN. 2021. Placental mitochondrial function in response to gestational exposures. Placenta 104:124–37
    [Google Scholar]
  84. 84.
    Ma Q, Beal JR, Bhurke A, Kannan A, Yu J et al. 2022. Extracellular vesicles secreted by human uterine stromal cells regulate decidualization, angiogenesis, and trophoblast differentiation. PNAS 119:e2200252119
    [Google Scholar]
  85. 85.
    Macklon NS, Pieters MH, Hassan MA, Jeucken PH, Eijkemans MJ, Fauser BC. 2002. A prospective randomized comparison of sequential versus monoculture systems for in-vitro human blastocyst development. Hum. Reprod. 17:2700–5
    [Google Scholar]
  86. 86.
    Martin-Estal I, Castorena-Torres F. 2022. Gestational diabetes mellitus and energy-dense diet: What is the role of the insulin/IGF axis?. Front. Endocrinol. 13:916042
    [Google Scholar]
  87. 87.
    Meier PR, Peterson RG, Bonds DR, Meschia G, Battaglia FC. 1981. Rates of protein synthesis and turnover in fetal life. Am. J. Physiol. 240:E320–24
    [Google Scholar]
  88. 88.
    Melchiorre K, Thilaganathan B, Giorgione V, Ridder A, Memmo A, Khalil A. 2020. Hypertensive disorders of pregnancy and future cardiovascular health. Front. Cardiovasc. Med. 7:59
    [Google Scholar]
  89. 89.
    Middleton P, Shepherd E, Morris J, Crowther CA, Gomersall JC. 2020. Induction of labour at or beyond 37 weeks' gestation. Cochrane Database Syst. Rev. 7:CD004945
    [Google Scholar]
  90. 90.
    Mitsuda N, Eitoku M, Yamasaki K, NA J-P, Fujieda M et al. 2022. Association between the ratio of placental weight to birthweight and the risk of neurodevelopmental delay in 3-year-olds: the Japan Environment and Children's Study. Placenta 128:49–56
    [Google Scholar]
  91. 91.
    Negre-Salvayre A, Swiader A, Salvayre R, Guerby P. 2022. Oxidative stress, lipid peroxidation and premature placental senescence in preeclampsia. Arch. Biochem. Biophys. 730:109416
    [Google Scholar]
  92. 92.
    Novakovic B, Yuen RK, Gordon L, Penaherrera MS, Sharkey A et al. 2011. Evidence for widespread changes in promoter methylation profile in human placenta in response to increasing gestational age and environmental/stochastic factors. BMC Genom. 12:529
    [Google Scholar]
  93. 93.
    O'Brien KO 2022. Maternal, fetal and placental regulation of placental iron trafficking. Placenta 125:47–53
    [Google Scholar]
  94. 94.
    Paolini CL, Marconi AM, Pike AW, Fennessey PV, Pardi G, Battaglia FC. 2001. A multiple infusion start time (MIST) protocol for stable isotope studies of fetal blood. Placenta 22:171–76
    [Google Scholar]
  95. 95.
    Paolini CL, Marconi AM, Ronzoni S, Di Noio M, Fennessey PV et al. 2001. Placental transport of leucine, phenylalanine, glycine, and proline in intrauterine growth-restricted pregnancies. J. Clin. Endocrinol. Metab. 86:5427–32
    [Google Scholar]
  96. 96.
    Pavlicev M, Wagner GP, Chavan AR, Owens K, Maziarz J et al. 2017. Single-cell transcriptomics of the human placenta: inferring the cell communication network of the maternal-fetal interface. Genome Res. 27:349–61
    [Google Scholar]
  97. 97.
    Petry CJ, Olga L, Hughes IA, Ong KK. 2022. Associations between maternal iron supplementation in pregnancy and offspring growth and cardiometabolic risk outcomes in infancy and childhood. PLOS ONE 17:e0263148
    [Google Scholar]
  98. 98.
    Phung TN, Olney KC, Pinto BJ, Silasi M, Perley L et al. 2022. X chromosome inactivation in the human placenta is patchy and distinct from adult tissues. HGG Adv. 3:100121
    [Google Scholar]
  99. 99.
    Popovic M, Chuva de Sousa Lopes SM. 2022. Emerging in vitro platforms and omics technologies for studying the endometrium and early embryo-maternal interface in humans. Placenta 125:36–46
    [Google Scholar]
  100. 100.
    Prater M, Hamilton RS, Wa Yung H, Sharkey AM, Robson P et al. 2021. RNA-Seq reveals changes in human placental metabolism, transport and endocrinology across the first-second trimester transition. Biol. Open 10:bio058222
    [Google Scholar]
  101. 101.
    Redline RW, Roberts DJ, Parast MM, Ernst LM, Morgan TK et al. 2022. Placental pathology is necessary to understand common pregnancy complications and achieve an improved taxonomy of obstetric disease. Am. J. Obstet. Gynecol. 228:187–202
    [Google Scholar]
  102. 102.
    Regnault TR, de Vrijer B, Battaglia FC. 2002. Transport and metabolism of amino acids in placenta. Endocrine 19:23–41
    [Google Scholar]
  103. 103.
    Retnakaran R, Kramer CK, Ye C, Kew S, Hanley AJ et al. 2015. Fetal sex and maternal risk of gestational diabetes mellitus: the impact of having a boy. Diabetes Care 38:844–51
    [Google Scholar]
  104. 104.
    Roland MC, Friis CM, Godang K, Bollerslev J, Haugen G, Henriksen T. 2014. Maternal factors associated with fetal growth and birthweight are independent determinants of placental weight and exhibit differential effects by fetal sex. PLOS ONE 9:e87303
    [Google Scholar]
  105. 105.
    Ru Y, Pressman E, Guillet R, Cooper B, Katzman P et al. 2014. Variable iron status among twins and triplets at birth. FASEB J. 28:636.3
    [Google Scholar]
  106. 106.
    Sangkhae V, Fisher AL, Wong S, Koenig MD, Tussing-Humphreys L et al. 2020. Effects of maternal iron status on placental and fetal iron homeostasis. J. Clin. Investig. 130:625–40
    [Google Scholar]
  107. 107.
    Sferruzzi-Perri AN, Lopez-Tello J, Napso T, Yong HEJ. 2020. Exploring the causes and consequences of maternal metabolic maladaptations during pregnancy: lessons from animal models. Placenta 98:43–51
    [Google Scholar]
  108. 108.
    Sibao L, Yufeng W, Peihong Q, Diao W. 2015. The role of serum hepcidin and ferroportin 1 in placenta on iron transfer from mother to fetus. Zhonghua Xueyexue Zazhi 36:307–11
    [Google Scholar]
  109. 109.
    Sibiak R, Ozegowska K, Wender-Ozegowska E, Gutaj P, Mozdziak P, Kempisty B. 2022. Fetomaternal expression of glucose transporters (GLUTs)—biochemical, cellular and clinical aspects. Nutrients 14:2025
    [Google Scholar]
  110. 110.
    Simpson S, Smith L, Bowe J. 2018. Placental peptides regulating islet adaptation to pregnancy: clinical potential in gestational diabetes mellitus. Curr. Opin. Pharmacol. 43:59–65
    [Google Scholar]
  111. 111.
    Smith MD, Pillman K, Jankovic-Karasoulos T, McAninch D, Wan Q et al. 2021. Large-scale transcriptome-wide profiling of microRNAs in human placenta and maternal plasma at early to mid gestation. RNA Biol. 18:507–20
    [Google Scholar]
  112. 112.
    Sood R, Zehnder JL, Druzin ML, Brown PO. 2006. Gene expression patterns in human placenta. PNAS 103:5478–83
    [Google Scholar]
  113. 113.
    Sparks JW. 1984. Human intrauterine growth and nutrient accretion. Semin. Perinatol. 8:74–93
    [Google Scholar]
  114. 114.
    Staff AC, Redman CW, Williams D, Leeson P, Moe K et al. 2016. Pregnancy and long-term maternal cardiovascular health: progress through harmonization of research cohorts and biobanks. Hypertension 67:251–60
    [Google Scholar]
  115. 115.
    Stanirowski PJ, Lipa M, Bomba-Opon D, Wielgos M. 2021. Expression of placental glucose transporter proteins in pregnancies complicated by fetal growth disorders. Adv. Protein. Chem. Struct. Biol. 123:95–131
    [Google Scholar]
  116. 116.
    Stewart MD, Johnson GA, Gray CA, Burghardt RC, Schuler LA et al. 2000. Prolactin receptor and uterine milk protein expression in the ovine endometrium during the estrous cycle and pregnancy. Biol. Reprod. 62:1779–89
    [Google Scholar]
  117. 117.
    Surekha MV, Sujatha T, Gadhiraju S, Uday Kumar P, Kotturu SK et al. 2022. Impact of maternal iron deficiency anaemia on the expression of the newly discovered multi-copper ferroxidase, Zyklopen, in term placentas. J. Obstet. Gynaecol. 42:74–82
    [Google Scholar]
  118. 118.
    Suryawanshi H, Max K, Bogardus KA, Sopeyin A, Chang MS et al. 2022. Dynamic genome-wide gene expression and immune cell composition in the developing human placenta. J. Reprod. Immunol. 151:103624
    [Google Scholar]
  119. 119.
    Suryawanshi H, Morozov P, Straus A, Sahasrabudhe N, Max KEA et al. 2018. A single-cell survey of the human first-trimester placenta and decidua. Sci. Adv. 4:eaau4788
    [Google Scholar]
  120. 120.
    Szuszkiewicz J, Myszczynski K, Reliszko ZP, Heifetz Y, Kaczmarek MM. 2022. Early steps of embryo implantation are regulated by exchange of extracellular vesicles between the embryo and the endometrium. FASEB J. 36:e22450
    [Google Scholar]
  121. 121.
    Tekola-Ayele F, Zeng X, Chatterjee S, Ouidir M, Lesseur C et al. 2022. Placental multi-omics integration identifies candidate functional genes for birthweight. Nat. Commun. 13:2384
    [Google Scholar]
  122. 122.
    Thursby E, Juge N. 2017. Introduction to the human gut microbiota. Biochem. J. 474:1823–36
    [Google Scholar]
  123. 123.
    Tint MT, Sadananthan SA, Soh SE, Aris IM, Michael N et al. 2020. Maternal glycemia during pregnancy and offspring abdominal adiposity measured by MRI in the neonatal period and preschool years: the Growing Up in Singapore Towards Healthy Outcomes (GUSTO) prospective mother–offspring birth cohort study. Am. J. Clin. Nutr. 112:39–47
    [Google Scholar]
  124. 124.
    Tsang JCH, Vong JSL, Ji L, Poon LCY, Jiang P et al. 2017. Integrative single-cell and cell-free plasma RNA transcriptomics elucidates placental cellular dynamics. PNAS 114:E7786–95
    [Google Scholar]
  125. 125.
    Tukiainen T, Villani AC, Yen A, Rivas MA, Marshall JL et al. 2017. Landscape of X chromosome inactivation across human tissues. Nature 550:244–48
    [Google Scholar]
  126. 126.
    Tunster SJ, Watson ED, Fowden AL, Burton GJ. 2020. Placental glycogen stores and fetal growth: insights from genetic mouse models. Reproduction 159:R213–35
    [Google Scholar]
  127. 127.
    Tussing-Humphreys L, LaBomascus B, O'Brien K, Nemeth E, Sangkhae V et al. 2021. Prepregnancy obesity does not impact placental iron trafficking. J. Nutr. 151:2646–54
    [Google Scholar]
  128. 128.
    Tuuli MG, Longtine MS, Nelson DM. 2011. Review: oxygen and trophoblast biology—a source of controversy. Placenta 32:Suppl. 2S109–18
    [Google Scholar]
  129. 129.
    Tyrmi JS, Kaartokallio T, Lokki I, Jääskeläinen T, Kortelainen E et al. 2022. GWAS of preeclampsia and hypertensive disorders of pregnancy uncovers genes related to cardiometabolic, endothelial and placental function. medRxiv 2022.05.19.22275002. https://www.medrxiv.org/content/10.1101/2022.05.19.22275002v2
  130. 130.
    Ursini G, Punzi G, Chen Q, Marenco S, Robinson JF et al. 2018. Convergence of placenta biology and genetic risk for schizophrenia. Nat. Med. 24:792–801
    [Google Scholar]
  131. 131.
    Ursini G, Punzi G, Langworthy BW, Chen Q, Xia K et al. 2021. Placental genomic risk scores and early neurodevelopmental outcomes. PNAS 118:e2019789118
    [Google Scholar]
  132. 132.
    Vento-Tormo R, Efremova M, Botting RA, Turco MY, Vento-Tormo M et al. 2018. Single-cell reconstruction of the early maternal-fetal interface in humans. Nature 563:347–53
    [Google Scholar]
  133. 133.
    Wander PL, Boyko EJ, Hevner K, Parikh VJ, Tadesse MG et al. 2017. Circulating early- and mid-pregnancy microRNAs and risk of gestational diabetes. Diabetes Res. Clin. Pract. 132:1–9
    [Google Scholar]
  134. 134.
    Wang Q, Li J, Wang S, Deng Q, An Y et al. 2022. Single-cell transcriptional profiling reveals cellular and molecular divergence in human maternal–fetal interface. Sci. Rep. 12:10892
    [Google Scholar]
  135. 135.
    Wang X, Chen C, Wang L, Chen D, Guang W, French J. 2003. Conception, early pregnancy loss, and time to clinical pregnancy: a population-based prospective study. Fertil. Steril. 79:577–84
    [Google Scholar]
  136. 136.
    Wang Y, Guo X, Hong X, Wang G, Pearson C et al. 2022. Association of mitochondrial DNA content, heteroplasmies and inter-generational transmission with autism. Nat. Commun. 13:3790
    [Google Scholar]
  137. 137.
    Widdowson EM. 1968. Growth and composition of the foetus and newborn. The Biology of Gestation N Assali 1–49. New York: Academic
    [Google Scholar]
  138. 138.
    Widdowson EM, Spray CM. 1951. Chemical development in utero. Arch. Dis. Child. 26:205–14
    [Google Scholar]
  139. 139.
    Xiang L, Yin Y, Zheng Y, Ma Y, Li Y et al. 2020. A developmental landscape of 3D-cultured human pre-gastrulation embryos. Nature 577:537–42
    [Google Scholar]
  140. 140.
    Xu P, Ma Y, Wu H, Wang YL. 2021. Placenta-derived microRNAs in the pathophysiology of human pregnancy. Front. Cell Dev. Biol. 9:646326
    [Google Scholar]
  141. 141.
    Yajnik CS, Yajnik PC. 2020. Fetal adiposity epidemic in the modern world: a thrifty phenotype aggravated by maternal obesity and diabetes. Am. J. Clin. Nutr. 112:8–10
    [Google Scholar]
  142. 142.
    Yampolsky M, Salafia CM, Shlakhter O, Haas D, Eucker B, Thorp J. 2009. Centrality of the umbilical cord insertion in a human placenta influences the placental efficiency. Placenta 30:1058–64
    [Google Scholar]
  143. 143.
    Yang Y, Guo F, Peng Y, Chen R, Zhou W et al. 2021. Transcriptomic profiling of human placenta in gestational diabetes mellitus at the single-cell level. Front. Endocrinol. 12:679582
    [Google Scholar]
  144. 144.
    Young MF, Griffin I, Pressman E, McIntyre AW, Cooper E et al. 2012. Maternal hepcidin is associated with placental transfer of iron derived from dietary heme and nonheme sources. J. Nutr. 142:33–39
    [Google Scholar]
  145. 145.
    Young MF, Pressman E, Foehr ML, McNanley T, Cooper E et al. 2010. Impact of maternal and neonatal iron status on placental transferrin receptor expression in pregnant adolescents. Placenta 31:1010–14
    [Google Scholar]
  146. 146.
    Yuan V, Hui D, Yin Y, Penaherrera MS, Beristain AG, Robinson WP. 2021. Cell-specific characterization of the placental methylome. BMC Genom. 22:6
    [Google Scholar]
  147. 147.
    Kennedy KM, de Goffau MC, Perez-Muñoz ME, Arrieta M-C, Bäckhed F et al. 2023. Questioning the fetal microbiome illustrates pitfalls of low-biomass microbial studies. Nature 613:639–49
    [Google Scholar]
  148. 148.
    Zaugg J, Solenthaler F, Albrecht C. 2022. Materno-fetal iron transfer and the emerging role of ferroptosis pathways. Biochem. Pharmacol. 202:115141
    [Google Scholar]
  149. 149.
    Zhang H, Alsaleh G, Feltham J, Sun Y, Napolitano G et al. 2019. Polyamines control eIF5A hypusination, TFEB translation, and autophagy to reverse B cell senescence. Mol. Cell 76:110–25.e9
    [Google Scholar]
/content/journals/10.1146/annurev-nutr-061121-085246
Loading
/content/journals/10.1146/annurev-nutr-061121-085246
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error