Review: The placenta and developmental programming: Balancing fetal nutrient demands with maternal resource allocation
Abstract
The placenta evolved to support development of the fetus, and so potentially plays a key role in the aetiology of developmental programming through its impact on nutrient transfer. Placental transport efficiency depends on a variety of parameters, including surface area for exchange, thickness of the interhaemal membrane and density of transporter proteins inserted into the trophoblast membranes. Here, we review recent studies that tested whether adaptations of placental efficiency are induced in the mouse placenta when maternal nutrient supply and fetal demand are manipulated experimentally. Naturally small placentas, and those exposed to maternal undernutrition, displayed structural changes indicative of accelerated maturation at E16, with enlargement of the labyrinth exchange zone at the expense of the endocrine junctional zone. These changes were associated with increased transport of a non-metabolisable amino acid analogue per gram of placenta, and expression of genes encoding specific System A transporters. Up-regulation of transporters was also observed when a mismatch between placental size and fetal demand was generated through genetic manipulation of the Igf2/H19 axis. Conversely, overgrowth of the placenta induced by deletion of H19 resulted in reduced transport capacity and expression of transporter genes. We conclude that under conditions when the maternal nutrient supply or placental size may be limiting for normal fetal growth, the placenta adapts so as to increase its transport capacity. Hence, it ameliorates the effects of environmental cues that would otherwise lead to more extensive developmental programming. The P0 transcript of Igf2 appears to be a strong candidate as a mediator of these adaptations in the mouse.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The placenta has a dynamic role in optimising resource allocation between the fetus and mother during pregnancy.
“It has a dynamic role in optimising resource allocation between the fetus and mother during pregnancy (74).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [74]
The placenta acts as an environmental sensor, integrating signals of the current availability of oxygen and nutrients, maternal stores of nutrient reserves and of the fetal nutrient demands for growth driven by the genes and actual mass of the fetus.
“Thus, the placenta acts as an environmental sensor, integrating signals of the current availability of oxygen and nutrients, maternal stores of nutrient reserves and of the fetal nutrient demands for growth driven by the genes and actual mass of the fetus (74,204).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [74]
The extent to which this strategy is successful in altering maternal-fetal resource allocation in favour of the mouse fetus depends on the actual nutritional and endocrine environment of the mother and on the mass, gestational age and genetic background of her litter.
“However, the extent to which this strategy is successful in altering maternal-fetal resource allocation in favour of the mouse fetus depends on the actual nutritional and endocrine environment of the mother and on the mass, gestational age and genetic background of her litter (74,193,546).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [74]
The responses of the placenta to environmental cues, such as hypoxia and nutrition, indicate that there is significant interaction between maternal nutrient availability and fetal demands for these resources in determining maternal-fetal nutrient allocation at the level of the placenta.
“The responses of the placenta to environmental cues, such as hypoxia and nutrition, indicate that there is significant interaction between maternal nutrient availability and fetal demands for these resources in determining maternal-fetal nutrient allocation at the level of the placenta (74,144).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [74]
Cites
Genomic imprinting in mammalian development: a parental tug-of-war
Moore, T. (1991) · Trends in Genetics · doi:10.1016/0168-9525(91)90230-n · Cited by 1,281 · see citing works
Placental-specific IGF-II is a major modulator of placental and fetal growth
Constância, M., Hemberger, M., Hughes, J., Dean, W., Ferguson-Smith, A., Fundele, R., Stewart, F., Kelsey, G., Fowden, A., Sibley, C., et al. (2002) · Nature · doi:10.1038/nature00819 · Cited by 1,054 · see citing works
Self-citationThorvaldsen, J. L., Duran, K. L., & Bartolomei, M. S. (1998) · Genes & Development · doi:10.1101/gad.12.23.3693 · Cited by 648 · see citing works
A census of mammalian imprinting
Morison, I. M., Ramsay, J. P., & Spencer, H. G. (2005) · Trends in Genetics · doi:10.1016/j.tig.2005.06.008 · Cited by 645 · see citing works
Comparative Developmental Anatomy of the Murine and Human Definitive Placentae
Georgiades, P., Ferguson-Smith, A. C., & Burton, G. J. (2002) · Placenta · doi:10.1053/plac.2001.0738 · Cited by 641 · see citing works
Self-citationA comparison of placental development and endocrine functions between the human and mouse model
Malassine, A., Frendo, J. L., & Evain-Brion, D. (2003) · Human Reproduction Update · doi:10.1093/humupd/dmg043 · Cited by 476 · see citing works
Constância, M., Angiolini, E., Sandovici, I., Smith, P., Smith, R., Kelsey, G., Dean, W., Ferguson-Smith, A., Sibley, C. P., Reik, W., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504468103 · Cited by 323 · see citing works
Self-citationUnbalanced Placental Expression of Imprinted Genes in Human Intrauterine Growth Restriction
McMinn, J. E., Wei, M., Schupf, N., Cusmai, J., Johnson, E., Smith, A. C., Weksberg, R., Thaker, H. M., & Tycko, B. (2005) · Placenta · doi:10.1016/j.placenta.2005.07.004 · Cited by 299 · see citing works
Developmental Dynamics of the Definitive Mouse Placenta Assessed by Stereology1
Coan, P. M., Ferguson-Smith, A. C., & Burton, G. J. (2004) · Biology of Reproduction · doi:10.1095/biolreprod.103.024166 · Cited by 296 · see citing works
Self-citationLimited evolutionary conservation of imprinting in the human placenta
Monk, D., Arnaúd, P., Apostolidou, S., Hills, F. A., Kelsey, G., Stanier, P., Feil, R., & Moore, G. E. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511031103 · Cited by 264 · see citing works
Moore, T., Constância, M., Zubair, M., Bailleul, B., Feil, R., Sasaki, H., & Reik, W. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.23.12509 · Cited by 252 · see citing works
Review: The Placenta is a Programming Agent for Cardiovascular Disease
Thornburg, K. L. R., O'Tierney, P. F., & Louey, S. (2010) · Placenta · doi:10.1016/j.placenta.2010.01.002 · Cited by 248 · see citing works
The Importance of Imprinting in the Human Placenta
Frost, J. M., & Moore, G. E. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001015 · Cited by 247 · see citing works
Comparative Placentation: Structures, Functions and Evolution
Wooding, P., & Burton, G. (2008) · doi:10.1007/978-3-540-78797-6 · Cited by 228 · see citing works
Self-citationCoadaptation in mother and infant regulated by a paternally expressed imprinted gene
Curley, J. P., Barton, S. C., Surani, M. A., & Keverne, E. B. (2004) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2004.2725 · Cited by 223 · see citing works
A Maternal–Offspring Coadaptation Theory for the Evolution of Genomic Imprinting
Wolf, J. B., & Hager, R. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040380 · Cited by 213 · see citing works
The surface area of the placenta and hypertension in the offspring in later life
Barker, D. J. P., Thornburg, K. L., Osmond, C., Kajantie, E., & Eriksson, J. G. (2010) · The International Journal of Developmental Biology · doi:10.1387/ijdb.082760db · Cited by 212 · see citing works
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-citationPlacental Oxygen Consumption. Part I: In Vivo Studies—A Review
Carter, A. M. (2000) · Placenta · doi:10.1053/plac.1999.0513 · Cited by 196 · see citing works
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
Self-citationImplantation. The role of proteinases, and blockage of implantation by proteinase inhibitors.
Denker, H. (1977) · PubMed · Cited by 192 · see citing works
Differential expression of imprinted genes in normal and IUGR human placentas
Diplas, A. I., Lambertini, L., Lee, M., SPERLING, R. S., Lee, Y. L., Wetmur, J. G., & Chen, J. (2009) · Epigenetics · doi:10.4161/epi.9019 · Cited by 186 · see citing works
Regulation of Placental Efficiency for Nutrient Transport by Imprinted Genes
Angiolini, E., Fowden, A., Coan, P., Sandovici, I., Smith, P., Dean, W., Burton, G., Tycko, B., Reik, W., Sibley, C., et al. (2006) · Placenta · doi:10.1016/j.placenta.2005.12.008 · Cited by 179 · see citing works
Self-citationEvolution of Genomic Imprinting: Insights from Marsupials and Monotremes
Renfree, M. B., Hore, T. A., Shaw, G., Graves, J. A. M., & Pask, A. J. (2009) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-082908-150026 · Cited by 178 · see citing works
Han, V. K. M., & Carter, A. M. (2000) · Placenta · doi:10.1053/plac.1999.0498 · Cited by 176 · see citing works
Haig, D. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904111106 · Cited by 139 · see citing works
A stereological perspective on placental morphology in normal and complicated pregnancies
Mayhew, T. M. (2009) · Journal of Anatomy · doi:10.1111/j.1469-7580.2008.00994.x · Cited by 126 · 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-citationPlacental protection of the fetal brain during short-term food deprivation
Broad, K. D., & Keverne, E. B. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1106022108 · Cited by 109 · see citing works
Illsley, N. P., Caniggia, I., & Zamudio, S. (2010) · The International Journal of Developmental Biology · doi:10.1387/ijdb.082798ni · Cited by 107 · see citing works
Dilworth, M. R., Kusinski, L. C., Cowley, E. J., Ward, B. S., Husain, S. M., Constância, M., Sibley, C. P., & Glazier, J. D. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911710107 · Cited by 86 · see citing works
Godfrey, K. M., Matthews, N., Glazier, J. D., Jackson, A. A., Wilman, C., & Sibley, C. P. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.9.5132 · Cited by 85 · see citing works
Oxygenation of the placental–fetal unit in humans
Schneider, H. (2011) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2011.05.009 · Cited by 84 · see citing works
Morphometry of the Placental Exchange Area
Baur, R. (1977) · Springer eBooks · doi:10.1007/978-3-642-66603-2 · Cited by 83 · see citing works
Mayhew, T. M., Jackson, M. R., & Boyd, P. A. (1993) · Placenta · doi:10.1016/s0143-4004(05)80248-6 · Cited by 80 · see citing works
Roberts, C. T., Owens, J. A., & Sferruzzi-Perri, A. N. (2008) · Placenta · doi:10.1016/j.placenta.2007.12.002 · Cited by 74 · see citing works
Godfrey, K. M. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.83.9.3320 · Cited by 72 · see citing works
Yamazawa, K., Kagami, M., Nagai, T., Kondoh, T., Onigata, K., Maeyama, K., Hasegawa, T., Hasegawa, Y., Yamazaki, T., Mizuno, S., et al. (2008) · Journal of Molecular Medicine · doi:10.1007/s00109-008-0377-4 · Cited by 67 · see citing works
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-citationEvolution of Placentation in Primates: Implications of Mammalian Phylogeny
Martin, R. D. (2008) · Evolutionary Biology · doi:10.1007/s11692-008-9016-9 · Cited by 62 · see citing works
Identification of the human homolog of the imprinted mouse Air non-coding RNA
Yotova, I., Vlatkovic, I., Pauler, F. M., Warczok, K. E., Ambros, P. F., Oshimura, M., Theussl, H., Gessler, M., Wagner, E. F., & Barlow, D. P. (2008) · Genomics · doi:10.1016/j.ygeno.2008.08.004 · Cited by 57 · see citing works
Riccio, A., Sparago, A., Verde, G., Crescenzo, A. D., Citro, V., Cubellis, M. V., Ferrero, G. B., Silengo, M., Russo, S., Larizza, L., et al. (2009) · Endocrine development · doi:10.1159/000207461 · Cited by 50 · see citing works
Multiple Paternity and Genomic Imprinting
Haig, D. (1999) · Genetics · doi:10.1093/genetics/151.3.1229 · Cited by 48 · see citing works
Atkinson, D. E., BOYD, R., & Sibley, C. P. (2006) · Elsevier eBooks · doi:10.1016/b978-012515400-0/50057-9 · Cited by 36 · see citing works
System A activity and vascular function in the placental-specific Igf2 knockout mouse
Kusinski, L. C., Dilworth, M. R., Baker, P. N., Sibley, C. P., Wareing, M., & Glazier, J. D. (2011) · Placenta · doi:10.1016/j.placenta.2011.07.086 · Cited by 16 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The Placenta: A Multifaceted, Transient Organ
Burton, G. J., & Fowden, A. L. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0066 · Cited by 833 · see citing works
Self-citationPlacental 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
Self-citationBromfield, J. J., Schjenken, J. E., Chin, P. Y., Care, A. S., Jasper, M. J., & Robertson, S. A. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305609111 · Cited by 374 · see citing works
The risk of maternal obesity to the long‐term health of the offspring
O’Reilly, J. R., & Reynolds, R. M. (2012) · Clinical Endocrinology · doi:10.1111/cen.12055 · Cited by 273 · see citing works
Placenta-on-a-chip: a novel platform to study the biology of the human placenta
Lee, J. S., Romero, R. J., Han, Y. M., Kim, H. C., Kim, C. J., Hong, J., & Huh, D. (2015) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767058.2015.1038518 · Cited by 272 · see citing works
The frequency and type of placental histologic lesions in term pregnancies with normal outcome
Romero, R. J., Kim, Y. M., Pacora, P., Kim, C. J., Benshalom-Tirosh, N., Jaiman, S., Bhatti, G., Kim, J.-S., Qureshi, F., Jacques, S. M., et al. (2018) · Journal of Perinatal Medicine · doi:10.1515/jpm-2018-0055 · Cited by 185 · see citing works
The Role of Placental Nutrient Sensing in Maternal-Fetal Resource Allocation1
Díaz, P., Powell, T. L., & Jansson, T. (2014) · Biology of Reproduction · doi:10.1095/biolreprod.114.121798 · Cited by 158 · see citing works
Huang, Z., Huang, S., Song, T., Yin, Y., & Tan, C. (2021) · Advances in Nutrition · doi:10.1093/advances/nmab070 · Cited by 131 · see citing works
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-citationMuralimanoharan, S., Guo, C. C., Myatt, L., & Maloyan, A. (2015) · International Journal of Obesity · doi:10.1038/ijo.2015.45 · Cited by 113 · see citing works
Albers, R. E., Kaufman, M. R., Natale, B. V., Keoni, C., Kulkarni-Datar, K. S., Min, S., Williams, C. R., Natale, D. R. C., & Brown, T. L. (2019) · Scientific Reports · doi:10.1038/s41598-019-39426-5 · Cited by 110 · see citing works
Mechanisms by which maternal obesity programs offspring for obesity: evidence from animal studies
Zambrano, E., & Nathanielsz, P. W. (2013) · Nutrition Reviews · doi:10.1111/nure.12068 · Cited by 109 · see citing works
A review of fundamental principles for animal models of DOHaD research: an Australian perspective
Dickinson, H., Moss, T. J. M., Gatford, K. L., Moritz, K. M., Akison, L. K., Fullston, T., Hryciw, D. H., Maloney, C., Morris, M. J., Wooldridge, A. L., et al. (2016) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174416000477 · Cited by 105 · see citing works
Higgins, J., Vaughan, O. R., de Liger, E. F., Fowden, A. L., & Sferruzzi-Perri, A. N. (2015) · The Journal of Physiology · doi:10.1113/jp271057 · Cited by 102 · see citing works
Self-citationThe Human Placental MethylomePreprint
Robinson, W. P., & Price, E. M. (2015) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a023044 · Cited by 102 · see citing works
Saben, J. L., Zhong, Y., Gómez-Acevedo, H., Thakali, K. M., Borengasser, S. J., Andres, A., & Shankar, K. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00076.2013 · Cited by 98 · see citing works
LACTATION BIOLOGY SYMPOSIUM: Lactocrine signaling and developmental programming1,2
Bartol, F. F., Wiley, A. A., Miller, D. J., Silva, A. J., Roberts, K. E., Davolt, M. L. P., Chen, J. C., Frankshun, A., Camp, M. E., Rahman, K. M., et al. (2012) · Journal of Animal Science · doi:10.2527/jas.2012-5764 · Cited by 98 · see citing works
Do fatty acids affect fetal programming?
Kabaran, S., & Besler, H. T. (2015) · Journal of Health Population and Nutrition · doi:10.1186/s41043-015-0018-9 · Cited by 97 · see citing works
Drug transport across the human placenta: review of placenta-on-a-chip and previous approaches
Pemathilaka, R. L., Reynolds, D. E., & Hashemi, N. N. (2019) · Interface Focus · doi:10.1098/rsfs.2019.0031 · Cited by 96 · see citing works
Gårdebjer, E. M., Cuffe, J. S. M., Pantaleon, M., Wlodek, M. E., & Moritz, K. M. (2013) · Placenta · doi:10.1016/j.placenta.2013.10.008 · Cited by 89 · see citing works
Sex Differences: A Resultant of an Evolutionary Pressure?
Torre, S. D., & Maggi, A. C. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.01.006 · Cited by 86 · see citing works
Son, J. S., Liu, X., Tian, Q., Zhao, L., Chen, Y., Hu, Y., Chae, S. A., de Avila, J. M., Zhu, M. J., & Du, . (2019) · The Journal of Physiology · doi:10.1113/jp277698 · Cited by 86 · see citing works
Muralimanoharan, S., Gao, X., Weintraub, S. T., Myatt, L., & Maloyan, A. (2016) · Autophagy · doi:10.1080/15548627.2016.1156822 · Cited by 83 · see citing works
Placental Gas Exchange and the Oxygen Supply to the Fetus
Carter, A. M. (2015) · Comprehensive physiology · doi:10.1002/cphy.c140073 · Cited by 77 · see citing works
Mina, T. H., Räikkönen, K., Riley, S. C., Norman, J. E., & Reynolds, R. M. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.05.004 · Cited by 76 · see citing works
Development of an Organ-on-a-Chip-Device for Study of Placental Pathologies
Mosavati, B., Oleinikov, A. V., & Du, E. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228755 · Cited by 75 · see citing works
Placental metabolism: substrate requirements and the response to stress
Vaughan, O. R., & Fowden, A. (2016) · Reproduction in Domestic Animals · doi:10.1111/rda.12797 · Cited by 74 · see citing works
Self-citationPlacental programming of anxiety in adulthood revealed by Igf2-null models
Mikaelsson, M. A., Constância, M., Dent, C. L., Wilkinson, L. S., & Humby, T. (2013) · Nature Communications · doi:10.1038/ncomms3311 · Cited by 72 · see citing works
Thayer, Z. M., Rutherford, J. N., & Kuzawa, C. W. (2020) · Evolution Medicine and Public Health · doi:10.1093/emph/eoz037 · Cited by 72 · see citing works
Targeting Toll‐like receptor‐4 to tackle preterm birth and fetal inflammatory injury
Robertson, S. A., Hutchinson, M. R., Rice, K. C., Chin, P. Y., Moldenhauer, L. M., Stark, M. J., Olson, D. M., & Keelan, J. A. (2020) · Clinical & Translational Immunology · doi:10.1002/cti2.1121 · Cited by 68 · see citing works
The brain-placental axis: Therapeutic and pharmacological relevancy to pregnancy
Behura, S. K., Dhakal, P., Kelleher, A. M., Balboula, A. Z., Patterson, A. L., & Spencer, T. E. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.104468 · Cited by 63 · see citing works
González, P., Gasperowicz, M., Barbeito‐Andrés, J., Klenin, N., Cross, J. C., & Hallgrímsson, B. (2016) · PLoS ONE · doi:10.1371/journal.pone.0152227 · Cited by 62 · see citing works
Alcohol-Induced Developmental Origins of Adult-Onset Diseases
Lunde, E. R., Washburn, S. E., Golding, M. C., Bake, S., Miranda, R. C., & Ramadoss, J. (2016) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.13114 · Cited by 62 · see citing works
Westermeier, F., Sáez, P. J., Villalobos-Labra, R., Sobrevía, L., & Farías, M. (2014) · BioMed Research International · doi:10.1155/2014/917672 · Cited by 59 · see citing works
Physiological function of seminal vesicle secretions on male fecundity
Noda, T., & Ikawa, M. (2019) · Reproductive Medicine and Biology · doi:10.1002/rmb2.12282 · Cited by 57 · see citing works
Vonnahme, K. A., Lemley, C. O., Caton, J. S. S., & Meyer, A. M. (2015) · Nutrients · doi:10.3390/nu7053497 · Cited by 55 · see citing works
Prenatal Endotoxemia and Placental Drug Transport in The Mouse: Placental Size-Specific Effects
Bloise, E., Bhuiyan, M., Audette, M. C., Sophie Petropoulos, A., Javam, M., Gibb, W., & Matthews, S. G. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065728 · Cited by 53 · see citing works
Sexual dimorphism in placental development and its contribution to health and diseases
Yu, P., Chen, Y., Ge, C., & Wang, H. (2021) · Critical Reviews in Toxicology · doi:10.1080/10408444.2021.1977237 · Cited by 50 · see citing works
Dexamethasone and sex regulate placental glucocorticoid receptor isoforms in mice
Cuffe, J. S. M., Saif, Z., Perkins, A. V., Moritz, K. M., & Clifton, V. L. (2017) · Journal of Endocrinology · doi:10.1530/joe-17-0171 · Cited by 50 · see citing works
Wilkinson, L. J., Neal, C. S., Singh, R. R., Sparrow, D. B., Kurniawan, N. D., Ju, A. L., Grieve, S. M., Dunwoodie, S. L., Moritz, K. M., & Little, M. H. (2015) · Kidney International · doi:10.1038/ki.2014.394 · Cited by 47 · see citing works
Zhang, G.-B., Wang, H., Hu, J., Guo, M.-Y., Wang, Y., Zhou, Y., Yu, Z., Fu, L., Chen, Y., & Xu, D. (2016) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2016.07.007 · Cited by 45 · see citing works
Strakovsky, R. S., & Schantz, S. L. (2018) · Toxicological Sciences · doi:10.1093/toxsci/kfy224 · Cited by 44 · see citing works
Reyes-Camacho, D., Vinyeta, E., Pérez, J. F., Aumiller, T., Criado‐Mesas, L., Palade, L. M., Țăranu, I., Folch, J. M., Calvo, M. A., van der Klis, J. D., et al. (2020) · Journal of Animal Science · doi:10.1093/jas/skz390 · Cited by 44 · see citing works
A Review on Microfluidics: An Aid to Assisted Reproductive Technology
Alias, A. B., Huang, H.-Y., & Yao, D. (2021) · Molecules · doi:10.3390/molecules26144354 · Cited by 43 · see citing works
3D microfluidics-assisted modeling of glucose transport in placental malaria
Mosavati, B., Oleinikov, A. V., & Du, E. (2022) · Scientific Reports · doi:10.1038/s41598-022-19422-y · Cited by 42 · see citing works
Yu, P., Zhou, J., Ge, C., Fang, M., Zhang, Y., & Wang, H. (2022) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2022.154396 · Cited by 42 · see citing works
Johns, E. C., Denison, F. C., & Reynolds, R. M. (2019) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.12.025 · Cited by 41 · see citing works
Schjenken, J. E., Moldenhauer, L. M., Sharkey, D. J., Chan, H. Y., Chin, P. Y., Fullston, T., McPherson, N. O., & Robertson, S. A. (2021) · Endocrinology · doi:10.1210/endocr/bqab123 · Cited by 41 · see citing works
Wilson, R. L., Leemaqz, S., Goh, Z., McAninch, D., Jankovic‐Karasoulos, T., Leghi, G. E., Phillips, J. A., Colafella, K. M. M., Tran, C. D., O’Leary, S., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-15085-2 · Cited by 39 · see citing works
Giesbrecht, G. F., Letourneau, N. L., Campbell, T. S., & The Alberta Pregnancy Outcomes and Nutrition Study Team (2016) · Development and Psychopathology · doi:10.1017/s0954579416000493 · Cited by 38 · see citing works
Rawn, S. M., Huang, C., Hughes, M. L., Shaykhutdinov, R. A., Vogel, H. J., & Cross, J. C. (2015) · Biology of Reproduction · doi:10.1095/biolreprod.115.132431 · Cited by 36 · see citing works
Effects of Maternal Obesity On Placental Phenotype
Fowden, A. L., Camm, E. J., & Sferruzzi-Perri, A. N. (2020) · Current Vascular Pharmacology · doi:10.2174/1570161118666200513115316 · Cited by 35 · see citing works
Self-citationMangwiro, Y. T. M., Cuffe, J. S. M., Briffa, J. F., Mahizir, D., Anevska, K., Jefferies, A. J., Hosseini, S., Romano, T., Moritz, K. M., & Wlodek, M. E. (2018) · The Journal of Physiology · doi:10.1113/jp275758 · Cited by 35 · see citing works
Revolutionizing the female reproductive system research using microfluidic chip platform
Yan, J., Wu, T., Zhang, J.-J., Gao, Y.-Y., Wu, J.-M., & Wang, S.-X. (2023) · Journal of Nanobiotechnology · doi:10.1186/s12951-023-02258-7 · Cited by 30 · see citing works
Phillips, E. A., Hendricks, N., Bucher, M., & Maloyan, A. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.893848 · Cited by 34 · see citing works
Findings in Stillbirths Associated with Placental Disease
Gibbins, K. J., Pınar, H., Reddy, U. M., Saade, G. R., Goldenberg, R. L., Dudley, D. J., Drews‐Botsch, C., Freedman, A. A., Daniels, L. M., Parker, C. B., et al. (2019) · American Journal of Perinatology · doi:10.1055/s-0039-1688472 · Cited by 33 · see citing works
Chen, Y., Xia, X., Fang, M., Chen, G., Cao, J., Qu, H., & Wang, H. (2021) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2021.149084 · Cited by 33 · see citing works
Yung, H. W., Zhao, X., Glover, L., Burrin, C., Pang, P., Jones, C. J. P., Gill, C. A., Duhig, K. E., Olovsson, M. H., Chappell, L. C., et al. (2022) · iScience · doi:10.1016/j.isci.2022.105911 · Cited by 32 · see citing works
Self-citationEpidemiological evidence for metabolic programming in dairy cattle
OPSOMER, G., Eetvelde, M. V., Kamal, M. M., & Soom, A. V. (2016) · Reproduction Fertility and Development · doi:10.1071/rd16410 · Cited by 31 · see citing works
Assisted Reproductive Technologies and the Placenta: Clinical, Morphological, and Molecular Outcomes
Riesche, L., & Bartolomei, M. S. (2018) · Seminars in Reproductive Medicine · doi:10.1055/s-0038-1676640 · Cited by 30 · see citing works
Langford, M. B., Outhwaite, J. E., Hughes, M. L., Natale, D. R. C., & Simmons, D. G. (2018) · Scientific Reports · doi:10.1038/s41598-018-22040-2 · Cited by 30 · see citing works
Ogoyama, M., Ohkuchi, A., Takahashi, H., Zhao, D., Matsubara, S., & Takizawa, T. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22031237 · Cited by 29 · see citing works
Robker, R. L., Watson, L. N., Robertson, S. A., Dunning, K. R., McLaughlin, E. A., & Russell, D. L. (2014) · PLoS ONE · doi:10.1371/journal.pone.0101182 · Cited by 28 · see citing works
Post-natal imprinting: evidence from marsupials
Stringer, J. M., Pask, A. J., Shaw, G., & Renfree, M. B. (2014) · Heredity · doi:10.1038/hdy.2014.10 · Cited by 28 · see citing works
Maternal High Linoleic Acid Alters Placental Fatty Acid Composition
Shrestha, N., Holland, O. J., Kent, N. L., Perkins, A. V., McAinch, A. J., Cuffe, J. S. M., & Hryciw, D. H. (2020) · Nutrients · doi:10.3390/nu12082183 · Cited by 28 · see citing works
The Interplay of Molecular Factors and Morphology in Human Placental Development and Implantation
Vornic, I., Buciu, V. B., Furau, C. G., Zara, F., Novacescu, D., Barb, A. C., Cumpănaş, A. A., Latcu, S. C., Sas, I., Șerban, D. M., et al. (2024) · Biomedicines · doi:10.3390/biomedicines12122908 · Cited by 27 · see citing works
Maternal to offspring resource allocation in plants and mammals
Gutièrrez‐Marcos, J. F., Constância, M., & Burton, G. J. (2012) · Placenta · doi:10.1016/j.placenta.2012.08.006 · Cited by 26 · see citing works
Self-citationPsychomotor regression due to vitamin B12 deficiency
Bousselamti, A., Hasbaoui, B. E., Echahdi, H., & Krouile, Y. (2018) · Pan African Medical Journal · doi:10.11604/pamj.2018.30.152.12046 · Cited by 26 · see citing works
Consequences of assisted reproductive technologies for offspring function in cattle
Siqueira, L. G. B., Silva, M. V. G., Panetto, J. C. D. C., & Viana, J. H. M. (2019) · Reproduction Fertility and Development · doi:10.1071/rd19278 · Cited by 25 · see citing works
Guo, H., Yang, Y., Qiao, Y., He, J., Yao, W., & Zheng, W. (2021) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2021.112916 · Cited by 23 · see citing works
Daniel, Z. C. T. R., Swali, A., Emes, R. D., & Langley‐Evans, S. C. (2016) · Genes & Nutrition · doi:10.1186/s12263-016-0541-3 · Cited by 23 · see citing works
Zheng, X., Ma, W., Wang, Y., Wu, C., Wang, J., Ma, Z., Wei, Y., Cui, C., Zhang, S., Guan, W., et al. (2023) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.3c07058 · Cited by 21 · see citing works
Thompson, L. P., Turan, S., & Aberdeen, G. W. (2020) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00249.2019 · Cited by 21 · see citing works
A proteomic profile of the healthy human placenta
Manna, S., Scheel, J., Noone, A., McElwain, C. J., Scaife, C., Gupta, S. K., English, J., McCarthy, C., & McCarthy, F. P. (2023) · Clinical Proteomics · doi:10.1186/s12014-022-09388-4 · Cited by 20 · see citing works
Vonnahme, K. A., Tanner, A. R., & Vasquez-Hidalgo, M. A. (2018) · Animal Reproduction · doi:10.21451/1984-3143-ar2018-0050 · Cited by 20 · see citing works
Chin, P. Y., Dorian, C. L., Sharkey, D. J., Hutchinson, M. R., Rice, K. C., Moldenhauer, L. M., & Robertson, S. A. (2019) · Endocrinology · doi:10.1210/en.2019-00493 · Cited by 20 · see citing works
Iqbal, K., Pierce, S. H., Kozai, K., Dhakal, P., Scott, R. L., Roby, K. F., Vyhlidal, C. A., & Soares, M. J. (2021) · Environmental Health Perspectives · doi:10.1289/ehp9256 · Cited by 20 · see citing works
Monteiro, V. R. D. S., de Andrade, C. B. V., Gomes, H. R., Reginatto, M. W., Império, G. E., Fontes, K. N., Spiess, D. A., Rangel-Junior, W. S., Nascimento, V. M. D. O., Lima, C. O. S., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-14248-0 · Cited by 19 · see citing works
Metabolic control of feto–placental development and pregnancy outcomes
Gao, Y., Yu, X., Wang, Y., Wang, H., Wang, Y., & Shyh‐Chang, N. (2025) · Nature Reviews Endocrinology · doi:10.1038/s41574-025-01206-9 · Cited by 18 · see citing works
Nutritional Programming of Intrauterine Development: A Concept Applicable to the Horse?
Fowden, A. L., Jellyman, J. K., Valenzuela, O. A., & Forhead, A. J. (2013) · Journal of Equine Veterinary Science · doi:10.1016/j.jevs.2013.03.005 · Cited by 18 · see citing works
Self-citationA mouse model of antepartum stillbirth
Rahman, A., Cahill, L. S., Zhou, Y., Hoggarth, J., Rennie, M. Y., Seed, M., Macgowan, C. K., Kingdom, J. C., Adamson, S. L., & Sled, J. G. (2017) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2017.06.009 · Cited by 18 · see citing works
Shanmugam, S., Patel, D., Wolpert, J. M., Keshvani, C., Liu, X., Bergeson, S. E., Kidambi, S., Mahimainathan, L., Henderson, G. I., & Narasimhan, M. (2019) · Biomolecules · doi:10.3390/biom9110669 · Cited by 18 · see citing works
Gestational protein restriction alters cell proliferation in rat placenta
Rebelato, H. J., Esquisatto, M. A. M., Righi, E. F. D. S., & Catisti, R. (2016) · Journal of Molecular Histology · doi:10.1007/s10735-016-9660-9 · Cited by 17 · see citing works
Vitamin B12 and placental expression of transcobalamin in pregnant adolescents
Layden, A. J., O'Brien, K. O., Pressman, E. K., Cooper, E., Kent, T. R., & Finkelstein, J. L. (2016) · Placenta · doi:10.1016/j.placenta.2016.06.011 · Cited by 16 · see citing works
MacGhee, M. E., Bradley, J. S., McCoski, S. R., Reeg, A., Ealy, A. D., & Johnson, S. (2016) · Journal of Animal Physiology and Animal Nutrition · doi:10.1111/jpn.12568 · Cited by 16 · see citing works
dos Santos, T. C., de Oliveira, M. F., Papa, P. D. C., Dantzer, V., & Miglino, M. A. (2014) · Theriogenology · doi:10.1016/j.theriogenology.2014.06.016 · Cited by 16 · see citing works
Analytical model of the feto-placental vascular system: consideration of placental oxygen transport
Mirbod, P. (2018) · Royal Society Open Science · doi:10.1098/rsos.180219 · Cited by 15 · see citing works
Liu, X., Lin, J., Chen, Y., Jiang, M., Liu, Q., Zhang, J., Lu, X., Hong, J., Sun, W., Sun, Y., et al. (2022) · Food and Chemical Toxicology · doi:10.1016/j.fct.2022.113579 · Cited by 15 · see citing works
Zhu, C., Li, X., Bazer, F. W., Johnson, G. A., Burghardt, R. C., Jiang, Z., & Wu, G. (2021) · Amino Acids · doi:10.1007/s00726-021-03038-z · Cited by 14 · see citing works
Foyle, K. L., & Robertson, S. A. (2024) · Discovery Immunology · doi:10.1093/discim/kyae004 · Cited by 14 · see citing works
Cross, J. C. (2015) · Reproduction Fertility and Development · doi:10.1071/rd15342 · Cited by 14 · see citing works
Gupta, R. K., & Gupta, R. C. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-804239-7.00068-8 · Cited by 13 · see citing works
Dimas, A., Politi, A., Papaioannou, G., Barber, T. M., Weickert, M. O., Grammatopoulos, D. K., Kumar, S., Kalantaridou, S., & Valsamakis, G. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23020695 · Cited by 13 · see citing works
3D organoid formation and EVT differentiation of various trophoblastic cell lines
Dietrich, B., Kunihs, V., Pollheimer, J., Knöfler, M., & Haider, S. (2023) · Placenta · doi:10.1016/j.placenta.2023.01.005 · Cited by 13 · see citing works
Yan, Q., Xu, J., Wu, X., Su, D., & Tan, Z. (2018) · British Journal Of Nutrition · doi:10.1017/s0007114518000727 · Cited by 13 · see citing works
Jeong, S., Fuwad, A., Yoon, S., Jeon, T., & Kim, S. M. (2024) · Biomimetics · doi:10.3390/biomimetics9050289 · Cited by 12 · see citing works
Zhao, Y., Yin, N., Yang, R., & Faiola, F. (2024) · Food and Chemical Toxicology · doi:10.1016/j.fct.2024.115022 · Cited by 12 · see citing works
Environmental and maternal factors associated with gross placental morphology in dairy cattle
Kamal, M. M., Eetvelde, M. V., Vandaele, L., & OPSOMER, G. (2016) · Reproduction in Domestic Animals · doi:10.1111/rda.12887 · Cited by 12 · see citing works
Morphometric study of the porcine placental vascularization
Cristofolini, A., Fiorimanti, M. R., Campos, M., Sanchis, E. G., Diaz, T., Moschetti, E., & Merkis, C. I. (2017) · Reproduction in Domestic Animals · doi:10.1111/rda.13095 · Cited by 12 · see citing works
Narapareddy, L., Wildman, D. E., Armstrong, D. L., Weckle, A. L., Bell, A. F., Patil, C. L., Tardif, S. D., Ross, C. N., & Rutherford, J. N. (2020) · American Journal of Primatology · doi:10.1002/ajp.23101 · Cited by 12 · see citing works
- Authors
- Burton, G. J., & Fowden, A. L.
- Affiliations
- University of Cambridge (GB)
- Corresponding author
- Burton, G.J.
- Venue
- Placenta
- Publisher
- Elsevier BV
- Published
- 2012-02
- Volume
- 33
- Pages
- S23-S27
- ISSN
- 0143-4004 (ISSN-L)
- OpenAlex
- W1964036070
- Cited by
- 177
- References
- 45
- Citations by year
- 2026: 8 · 2025: 13 · 2024: 10 · 2023: 14 · 2022: 12 · 2021: 15 · 2020: 8 · 2019: 13 · 2018: 12 · 2017: 8 · 2016: 19 · 2015: 21 · 2014: 11 · 2013: 8 · 2012: 5
- FWCI
- 1.13
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Placenta (publishedVersion)
- PubMed (publishedVersion)
- Funders
- MRC
- BBSRC
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
- Keywords
- developmental programming, placental maturation, labyrinth zone, system A amino acid transporter, H19, insulin-like growth factor II, maternal undernutrition, fetal growth
- MeSH terms
- Animals, Female, Humans, Male, Maternal-Fetal Exchange, Nutritional Requirements, Placenta, Placentation, Pregnancy, Maternal Nutritional Physiological Phenomena, Malnutrition, Fetal Development, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review