Programming placental nutrient transport capacity

Fowden, A. L.; Ward, J. W.; Wooding, F. P. B.; Forhead, A. J.; Constancia, M.

doi:10.1113/jphysiol.2005.104141

Cited by 334Birth, Development, and HealthPregnancy and preeclampsia studiesGrowth Hormone and Insulin-like Growth Factors

Programming placental nutrient transport capacity

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Fowden, A. L., Ward, J. W., Wooding, F. P. B., Forhead, A. J., Constancia, M.·2006·The Journal of Physiology

DOI 10.1113/jphysiol.2005.104141PMC PMC1779642

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Abstract

Many animal studies and human epidemiological findings have shown that impaired growth in utero is associated with physiological abnormalities in later life and have linked this to tissue programming during suboptimal intrauterine conditions at critical periods of development. However, few of these studies have considered the contribution of the placenta to the ensuing adult phenotype. In mammals, the major determinant of intrauterine growth is the placental nutrient supply, which, in turn, depends on the size, morphology, blood supply and transporter abundance of the placenta and on synthesis and metabolism of nutrients and hormones by the uteroplacental tissues. This review examines the regulation of placental nutrient transfer capacity and the potential programming effects of nutrition and glucocorticoid over‐exposure on placental phenotype with particular emphasis on the role of the Igf2 gene in these processes.

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Direct manipulation of the fetal genome by gene deletion or disruption is known to alter resource allocation to fetal growth via alterations in placental phenotype.
“Similarly, direct manipulation of the fetal genome by gene deletion or disruption is known to alter resource allocation to fetal growth via alterations in placental phenotype (198).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [198]
Similar changes in placental growth and efficiency are seen in murine and ovine placentas in response to maternal undernutrition.
“Similar changes in placental growth and efficiency are seen in murine and ovine placentas in response to maternal undernutrition (198,546,550).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [198]
In sheep, undernutrition during the early stages of pregnancy when the placenta is growing most rapidly leads to an increase in term placental weight, whereas nutrient restriction later in pregnancy once the placenta is fully formed leads to reduced placental weight at term.
“In sheep, undernutrition during the early stages of pregnancy when the placenta is growing most rapidly leads to an increase in term placental weight, whereas nutrient restriction later in pregnancy once the placenta is fully formed leads to reduced placental weight at term (198).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [198]

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Restriction of placental size in sheep enhances efficiency of placental transfer of antipyrine, 3-O-methyl-D-glucose but not of urea.
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Effects of dexamethasone on the uterine and umbilical vascular beds during basal and hypoxemic conditions in sheep.
Jellyman, J., Gardner, D., Fowden, A., & Giussani, D. (2004) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2003.09.046 · Cited by 29 · see citing works
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Metabolic Alterations in the Fetal Hepatic and Umbilical Circulations during Glucocorticoid-Induced Parturition in Sheep
Barbera, A., Wilkening, R. B., Teng, C. C., Battaglia, F. C., & Meschia, G. (1997) · Pediatric Research · doi:10.1203/00006450-199702000-00015 · Cited by 26 · see citing works
Na+/K+-ATPase Activity and Expression in Syncytiotrophoblast Plasma Membranes in Pregnancies Complicated by Diabetes
Persson, A., Johansson, M., Jansson, T., & Powell, T. L. (2002) · Placenta · doi:10.1053/plac.2002.0807 · Cited by 25 · see citing works
Effect of dexamethasone on fetal hepatic glutamine-glutamate exchange
Timmerman, M., Teng, C. C., Wilkening, R. B., et al. (2000) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2000.278.5.e839 · Cited by 25 · see citing works
The Effect of a Reversible Period of Adverse Intrauterine Conditions During Late Gestation on Fetal and Placental Weight and Placentome Distribution in Sheep
Gardner, D. S., Ward, J. W., Giussani, D. A., & Fowden, A. L. (2002) · Placenta · doi:10.1053/plac.2002.0830 · Cited by 23 · see citing works
Self-citation
Changes in the maternal body and feto-placental growth following various lengths of feed restriction during mid-pregnancy in sheep
McCrabb, G. J., Hosking, B., & Egan, A. (1992) · Australian Journal of Agricultural Research · doi:10.1071/ar9921429 · Cited by 22 · see citing works
Nutrient transfer across the equine placenta: correlation of structure and function
Wooding, F. B. P., & Fowden, A. L. (2006) · Equine Veterinary Journal · doi:10.2746/042516406776563341 · Cited by 22 · see citing works
Self-citation
Effects of a restricted diet during mid pregnancy of ewes on uterine and fetal growth and lamb birth weight
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Effect of Maternal Fasting on Ovine Fetal and Maternal Branched-Chain Amino Acid Transaminase Activities
Liechty, E. A., Barone, S., & Nutt, M. E. (2009) · Biology of the Neonate · doi:10.1159/000242706 · Cited by 19 · see citing works
COMPARATIVE PLACENTATION
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Microscopic anatomy of the ungulate placenta
Macdonald, A. A., & Fowden, A. L. (1997) · Equine Veterinary Journal · doi:10.1111/j.2042-3306.1997.tb05072.x · Cited by 13 · see citing works
Self-citation
Interrelationships of placental development with nutrition in pregnancy and lamb birth weight
Davis, Rattray, P. V., Me, P., et al. (1981) · Proceedings of the New Zealand Society of Animal Production · Cited by 11 · see citing works
Comparative aspects of prepartum maturation: Provision of nutrients
Fowden, A. L., Ousey, J. C., & Forhead, A. J. (2001) · Pferdeheilkunde Equine Medicine · doi:10.21836/pem20010623 · Cited by 10 · see citing works
Self-citation
Regulation of uterine and umbilical amino acid uptakes by maternal amino acid concentrations
Thureen, P. J., Anderson, S. M., & Hay, W. W. (2000) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2000.279.3.r849 · Cited by 9 · see citing works

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Placental Origins of Chronic Disease
Burton, G. J., Fowden, A. L., & Thornburg, K. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00029.2015 · Cited by 717 · see citing works
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The omniscient placenta: Metabolic and epigenetic regulation of fetal programming
Nugent, B. M., & Bale, T. L. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.09.001 · Cited by 222 · see citing works
The Programming Power of the Placenta
Sferruzzi-Perri, A. N., & Camm, E. J. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00033 · Cited by 223 · see citing works
Factors Affecting the FcRn-Mediated Transplacental Transfer of Antibodies and Implications for Vaccination in Pregnancy
Wilcox, C. R., Holder, B., & Jones, C. E. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01294 · Cited by 200 · see citing works
“One study reported a 14% reduction in antibody transfer among malnourished pregnant women compared to controls (109); however, the reasons for this are unclear and possibly relate to differences in placental size, morphology, and vascular development (110, 111).”
Adaptations in placental phenotype support fetal growth during undernutrition of pregnant mice: Undernutrition and placental phenotype
Coan, P. M., Vaughan, O. R., Sekita, Y., Finn, S. L., Burton, G. J., Constancia, M., & Fowden, A. L. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2009.181214 · Cited by 199 · see citing works
Self-citation
Nutritionally Mediated Programming of the Developing Immune System
Palmer, A. C. (2011) · Advances in Nutrition · doi:10.3945/an.111.000570 · Cited by 198 · see citing works
Adaptations in placental nutrient transfer capacity to meet fetal growth demands depend on placental size in mice
Coan, P. M., Angiolini, E., Sandovici, I., Burton, G. J., Constância, M., & Fowden, A. L. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.156133 · Cited by 194 · see citing works
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Early-life glucocorticoid exposure: the hypothalamic-pituitary-adrenal axis, placental function, and long-term disease risk
Braun, T., Challis, J. R., Newnham, J. P., & Sloboda, D. M. (2013) · Endocrine Reviews · doi:10.1210/er.2013-1012 · Cited by 196 · see citing works
Imprinted genes and the epigenetic regulation of placental phenotype
Fowden, A. L., Coan, P. M., Angiolini, E., Burton, G. J., & Constancia, M. (2011) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2010.11.005 · Cited by 142 · see citing works
Self-citation
An obesogenic diet during mouse pregnancy modifies maternal nutrient partitioning and the fetal growth trajectory
Sferruzzi‐Perri, A. N., Vaughan, O. R., Haro, M., Cooper, W. N., Musial, B., Charalambous, M., Pestana, D., Ayyar, S., Ferguson‐Smith, A. C., Burton, G. J., et al. (2013) · The FASEB Journal · doi:10.1096/fj.13-234823 · Cited by 134 · see citing works
Self-citation
Maternal obesity markedly increases placental fatty acid transporter expression and fetal blood triglycerides at midgestation in the ewe
Zhu, M. J., Ma, Y., Long, N. M., Du, M., & Ford, S. P. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00309.2010 · Cited by 137 · see citing works
Placental-Specific Igf2 Deficiency Alters Developmental Adaptations to Undernutrition in Mice
Sferruzzi-Perri, A. N., Vaughan, O. R., Coan, P. M., Suciu, M. C., Darbyshire, R., Constancia, M., Burton, G. J., & Fowden, A. L. (2011) · Endocrinology · doi:10.1210/en.2011-0240 · Cited by 115 · see citing works
Self-citation
Maternal-fetal resource allocation: Co-operation and conflict
Fowden, A. L., & Moore, T. (2012) · Placenta · doi:10.1016/j.placenta.2012.05.002 · Cited by 114 · see citing works
Self-citation
Developmental adaptations to increased fetal nutrient demand in mouse genetic models of Igf2‐mediated overgrowth
Angiolini, E., Coan, P. M., Sandovici, I., Iwajomo, O. H., Peck, G., Burton, G. J., Sibley, C. P., Reik, W., Fowden, A. L., & Constância, M. (2011) · The FASEB Journal · doi:10.1096/fj.10-175273 · Cited by 64 · see citing works
Self-citation
They are what you eat: Can nutritional factors during gestation and early infancy modulate the neonatal immune response?
Prentice, S. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01641 · Cited by 52 · see citing works

Українсько-Американський проект дослідження наслідків опромінення in utero внаслідок аварії на Чорнобильській АЕС: огляд наукових публікацій
Tronko, M. D., Zamotayeva, G., Pasteur, I. P., et al. (2019) · Endokrynologia · doi:10.31793/1680-1466.2019.24-4.346 · Cited by 3 · see citing works
BIDIRECTIONAL TRANSFER OF SELENIUM ACROSS THE SHEEP PLACENTA IN UTERO
SHARIFF, M. A., Krishnamurti, C. R., Schaefer, A. L., et al. (1984) · Canadian Journal of Animal Science · doi:10.4141/cjas84-248 · Cited by 13 · see citing works
Phase contrast microscopy of the placenta
Coles, R. (1971) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(71)90779-4 · Cited by 4 · see citing works
Fetal and Postnatal Growth and Development
May, L. E. (2012) · SpringerBriefs in physiology · doi:10.1007/978-1-4614-3408-5_3
In Utero Programming of Testicular Cancer
Elad, D., Jaffa, A. J., Grisaru, D., et al. (2021) · Journal of Developmental Biology · doi:10.3390/jdb9030035 · Cited by 5 · see citing works

Authors: Fowden, A. L., Ward, J. W., Wooding, F. P. B., Forhead, A. J., & Constancia, M.
Affiliations: University of Cambridge (GB)
Corresponding author: Fowden, A. L.
ORCID: Fowden, A. L.
Forhead, A. J.
Venue: The Journal of Physiology
Publisher: Wiley
Published: 2006-03-28
Volume: 572
Issue: 1
Pages: 5-15
ISSN: 0022-3751 (ISSN-L)
1469-7793
DOI: 10.1113/jphysiol.2005.104141
PMC: PMC1779642
OpenAlex: W1693014831
Cited by: 334
References: 101
Citations by year: 2026: 9 · 2025: 13 · 2024: 17 · 2023: 11 · 2022: 13 · 2021: 18 · 2020: 13 · 2019: 9 · 2018: 21 · 2017: 22 · 2016: 26 · 2015: 20 · 2014: 14 · 2013: 20 · 2012: 21
FWCI: 2.28
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The Journal of Physiology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Biotechnology and Biological Sciences Research Council (BB/B50118X/1)
Topics: Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Growth Hormone and Insulin-like Growth Factors
Keywords: placental nutrient transport, fetal growth restriction, developmental programming, placenta, insulin-like growth factor II, maternal nutrition, adult phenotype
MeSH terms: Aging, Animals, Biological Transport, Active, Female, Humans, Insulin-Like Growth Factor II, Maternal-Fetal Exchange, Placenta, Pregnancy, Proteins, Placental Circulation, Prenatal Nutritional Physiological Phenomena, Fetal Development

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Programming placental nutrient transport capacity

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