Placental adaptations to the maternal–fetal environment: implications for fetal growth and developmental programming
Abstract
The placenta is a transient organ found in eutherian mammals that evolved primarily to provide nutrients for the developing fetus. The placenta exchanges a wide array of nutrients, endocrine signals, cytokines and growth factors with the mother and the fetus, thereby regulating intrauterine development. Recent studies show that the placenta is not just a passive organ mediating maternal-fetal exchange. It can adapt its capacity to supply nutrients in response to intrinsic and extrinsic variations in the maternal-fetal environment. These dynamic adaptations are thought to occur to maximize fetal growth and viability at birth in the prevailing conditions in utero. However, some of these adaptations may also affect the development of individual fetal tissues, with patho-physiological consequences long after birth. Here, this review summarizes current knowledge on the causes, possible mechanisms and consequences of placental adaptive responses, with a focus on the regulation of transporter-mediated processes for nutrients. This review also highlights the emerging roles that imprinted genes and epigenetic mechanisms of gene regulation may play in placental adaptations to the maternal-fetal environment.
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The mouse is favored for developmental programming research because of the ease of genetic manipulations, which enable imbalances to be created among maternal supply, placental size and fetal demands.
“The mouse is favored because of the ease of genetic manipulations, which enable, for example, imbalances to be created among maternal supply, placental size and fetal demands (482).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [482]
Changes in nutritional state and food intake during pregnancy often accompany, and are confounding factors in studying, other environmental challenges such as hypoxia, heat stress, exercise and alterations in housing, lighting and noise levels.
“In addition, changes in nutritional state and food intake during pregnancy often accompany, and are confounding factors in studying, other environmental challenges such as hypoxia, heat stress, exercise and alterations in housing, lighting and noise levels (482).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [482]
Cites
mTOR: from growth signal integration to cancer, diabetes and ageing
Zoncu, R., Efeyan, A., & Sabatini, D. M. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3025 · Cited by 3,941 · see citing works
Effect of In Utero and Early-Life Conditions on Adult Health and Disease
Gluckman, P. D., Hanson, M. A., Cooper, C., & Thornburg, K. L. (2008) · New England Journal of Medicine · doi:10.1056/nejmra0708473 · Cited by 3,898 · see citing works
Placental development: Lessons from mouse mutants
Rossant, J., & Cross, J. C. (2001) · Nature Reviews Genetics · doi:10.1038/35080570 · Cited by 1,273 · see citing works
Genetic conflicts in human pregnancy
Haig, D. (1993) · The Quarterly Review of Biology · doi:10.1086/418300 · Cited by 1,253 · 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-citationGlucocorticoids, prenatal stress and the programming of disease
Harris, A., & Seckl, J. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.06.007 · Cited by 871 · see citing works
Child Health, Developmental Plasticity, and Epigenetic Programming
Hochberg, Z., Feil, R., Constância, M., Fraga, M. F., Junien, C., Carel, J., Boileau, P., Bouc, Y. L., Deal, C., Lillycrop, K. A., et al. (2010) · Endocrine Reviews · doi:10.1210/er.2009-0039 · Cited by 631 · see citing works
Self-citationA transient placental source of serotonin for the fetal forebrain
Bonnin, A., Goeden, N., Chen, K., Wilson, M. L., King, J., Shih, J. C., Blakely, R. D., Deneris, E. S., & Levitt, P. (2011) · Nature · doi:10.1038/nature09972 · Cited by 608 · see citing works
ATF4-dependent transcription mediates signaling of amino acid limitation
Kilberg, M. S., Shan, J., & Su, N. Y. (2009) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2009.05.008 · Cited by 595 · see citing works
DNA methylation and gene expression differences in children conceived in vitro or in vivo
Katari, S., Turan, N., Bibikova, M. V., Erinle, O., Chalian, R. A., Foster, M., Gaughan, J. P., Coutifaris, C., & Sapienza, C. (2009) · Human Molecular Genetics · doi:10.1093/hmg/ddp319 · Cited by 470 · see citing works
Utero-placental vascular development and placental function
Reynolds, L. P., & Redmer, D. A. (1995) · Journal of Animal Science · doi:10.2527/1995.7361839x · Cited by 418 · see citing works
Regulation of supply and demand for maternal nutrients in mammals by imprinted genes
Reik, W., Constância, M., Fowden, A. L., Anderson, N. F., Dean, W., Ferguson‐Smith, A. C., Tycko, B., & Sibley, C. P. (2003) · The Journal of Physiology · doi:10.1111/j.1469-7793.2003.00035.x · Cited by 409 · see citing works
Self-citationYung, H.-W., Calabrese, S., Hynx, D., Hemmings, B. A., Cetin, I., Charnock-Jones, D. S., & Burton, G. J. (2008) · The American Journal of Pathology · doi:10.2353/ajpath.2008.071193 · Cited by 388 · see citing works
Bertram, C. E., Trowern, A. R., Copin, N., Jackson, A. A., & Whorwood, C. B. (2001) · Endocrinology · doi:10.1210/endo.142.7.8238 · Cited by 385 · see citing works
Nelissen, E. C. M., van Montfoort, A. P. A., Dumoulin, J. C. M., & Evers, J. L. H. (2010) · Human Reproduction Update · doi:10.1093/humupd/dmq052 · Cited by 385 · see citing works
Regulation of vascular growth and function in the human placenta
Burton, G. J., Jones, D. S., & Jauniaux, E. (2009) · Reproduction · doi:10.1530/rep-09-0092 · Cited by 362 · see citing works
Placental efficiency and adaptation: endocrine regulation
Fowden, A. L., Sferruzzi-Perri, A. N., Coan, P. M., Constância, M., & Burton, G. J. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.173013 · Cited by 359 · see citing works
Self-citationExpansion of β-cell mass in response to pregnancy
Rieck, S., & Kaestner, K. H. (2010) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2009.11.001 · Cited by 358 · see citing works
Transport of fatty acids across the human placenta: A review
Duttaroy, A. K. (2008) · Progress in Lipid Research · doi:10.1016/j.plipres.2008.11.001 · Cited by 349 · see citing works
Diagnostic Value of Blood Sampling in Fetuses with Growth Retardation
Pardi, G., Cetin, I., Marconi, A. M., Lanfranchi, A., Bozzetti, P., Farrazzi, E., Buscaglia, M., & Battaglia, F. C. (1993) · New England Journal of Medicine · doi:10.1056/nejm199303113281004 · Cited by 345 · see citing works
Fatty Acid Supply to the Human Fetus
Haggarty, P. (2010) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.012809.104742 · Cited by 336 · 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-citationSoares, M. J. (2004) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-2-51 · Cited by 320 · see citing works
Mechanisms involved in the developmental programming of adulthood disease
Warner, M. J., & Ozanne, S. E. (2010) · Biochemical Journal · doi:10.1042/bj20091861 · Cited by 316 · see citing works
Regulation of supply and demand for maternal nutrients in mammals by imprinted genes
Reik, W., Constância, M., Fowden, A. L., et al. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.033274 · Cited by 315 · see citing works
Self-citationJones, H. N., Woollett, L. A., Barbour, N., Prasad, P. D., Powell, T. L., & Jansson, T. (2008) · The FASEB Journal · doi:10.1096/fj.08-116889 · Cited by 310 · see citing works
Development and function of trophoblast giant cells in the rodent placenta
Hu, D., & Cross, J. C. (2009) · The International Journal of Developmental Biology · doi:10.1387/ijdb.082768dh · Cited by 307 · see citing works
Sibley, C. P., Coan, P. M., Ferguson‐Smith, A. C., Dean, W., Hughes, J., Smith, P., Reik, W., Burton, G. J., Fowden, A. L., & Constância, M. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402508101 · Cited by 299 · see citing works
Self-citationDevelopmental 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
Glazier, J. D., Cetin, I., Perugino, G., Ronzoni, S., Grey, A. M., Mahendran, D., Marconi, A. M., Pardi, G., & Sibley, C. P. (1997) · Pediatric Research · doi:10.1203/00006450-199710000-00016 · Cited by 287 · see citing works
Roos, S., Jansson, N., Palmberg, I., Säljö, K., Powell, T. L., & Jansson, T. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.129676 · Cited by 283 · see citing works
Lindsay, R. S., Lindsay, R. M., Waddell, B. J., & Seckl, J. R. (1996) · Diabetologia · doi:10.1007/s001250050573 · Cited by 282 · see citing works
Imprinted Genes, Placental Development and Fetal Growth
Fowden, A. L., Sibley, C. P., Reik, W., & Constância, M. (2006) · Hormone Research in Paediatrics · doi:10.1159/000091506 · Cited by 273 · see citing works
Self-citationThe Placenta and Intrauterine Programming
Fowden, A. L., Forhead, A. J., Coan, P. M., & Burton, G. J. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01663.x · Cited by 267 · see citing works
Jansson, N., Pettersson, J., Haafiz, A., Ericsson, A., Palmberg, I., Tranberg, M., Ganapathy, V., Powell, T. L., & Jansson, T. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.550004 · Cited by 265 · see citing works
Jansson, T., & Powell, T. L. (2006) · Placenta · doi:10.1016/j.placenta.2005.11.010 · Cited by 257 · 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
Maiiendran, D., Donnai, P., Glazier, J. D., D'Souza, S. W., Boyd, R. D., & Sibley, C. P. (1993) · Pediatric Research · doi:10.1203/00006450-199311000-00019 · Cited by 247 · 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
Amino Acid Transporters in the Human Placenta
Jansson, T. (2001) · Pediatric Research · doi:10.1203/00006450-200102000-00003 · Cited by 245 · see citing works
Constância, M., Kelsey, G., & Reik, W. (2004) · Nature · doi:10.1038/432053a · Cited by 242 · see citing works
Self-citationPlacenta-specific Methylation of the Vitamin D 24-Hydroxylase Gene
Novakovic, B., Sibson, M., Ng, H. K., Manuelpillai, U., Rakyan, V. K., Down, T. A., Beck, S., Fournier, T., Evain-Brion, D., Dimitriadis, E., et al. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m809542200 · Cited by 238 · see citing works
Jansson, T., Ekstrand, Y., Björn, C., Wennergren, M., & Powell, T. L. (2002) · Diabetes · doi:10.2337/diabetes.51.7.2214 · Cited by 238 · see citing works
Mechanisms of disease: the developmental origins of disease and the role of the epigenotype
Ozanne, S. E., & Constância, M. (2007) · Nature Clinical Practice Endocrinology & Metabolism · doi:10.1038/ncpendmet0531 · Cited by 232 · see citing works
Self-citationImprinted genes in the placenta – A review
Coan, P. M., Burton, G. J., & Ferguson‐Smith, A. C. (2005) · Placenta · doi:10.1016/j.placenta.2004.12.009 · Cited by 231 · see citing works
Gallou-Kabani, C., Gabory, A., Tost, J., Karimi, M., Mayeur, S., Lesage, J., Boudadi, E., Gross, M.-S., Taurelle, J., Vigé, A., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0014398 · Cited by 229 · see citing works
Placental-fetal glucose exchange and fetal glucose metabolism.
(2006) · Europe PMC (PubMed Central) · Cited by 226 · see citing works
Coadaptation 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
Kulkarni, A. V., Dangat, K. D., Kale, A. A., Sable, P., Chavan, P., & Joshi, S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017706 · Cited by 216 · 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
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-citationNovakovic, B., Yuen, R. K. C., Gordon, L., Peñaherrera, M. S., Sharkey, A., Moffett, A., Craig, J. M., Robinson, W. P., & Saffery, R. (2011) · BMC Genomics · doi:10.1186/1471-2164-12-529 · Cited by 192 · see citing works
In utero tobacco exposure epigenetically modifies placental CYP1A1 expression
Suter, M., Abramovici, A., Showalter, L., Hu, M., Shope, C. D., Varner, M., & Aagaard-Tillery, K. (2010) · Metabolism · doi:10.1016/j.metabol.2010.01.013 · Cited by 188 · see citing works
Placental nutrient supply and fetal growth
Desforges, M., & Sibley, C. P. (2009) · The International Journal of Developmental Biology · doi:10.1387/ijdb.082765md · Cited by 182 · see citing works
Expression of folate transporters in human placenta and implications for homocysteine metabolism
Solanky, N., Jimenez, A. R., D'Souza, S. W., Sibley, C. P., & Glazier, J. D. (2009) · Placenta · doi:10.1016/j.placenta.2009.11.017 · Cited by 182 · see citing works
Gambling, L., Danzeisen, R., Susan, G. A. I. R., Lea, R. G., CHARANIA, Z., Solanky, N., JOORY, K. D., Srai, S. K., & McArdle, H. J. (2001) · Biochemical Journal · doi:10.1042/0264-6021:3560883 · Cited by 179 · 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-citationHan, V. K. M., & Carter, A. M. (2000) · Placenta · doi:10.1053/plac.1999.0498 · Cited by 176 · see citing works
Rosario, F. J., Jansson, N., Kanai, Y., Prasad, P. D., Powell, T. L., & Jansson, T. (2011) · Endocrinology · doi:10.1210/en.2010-1153 · Cited by 176 · see citing works
Identification of Novel Imprinted Genes in a Genome-Wide Screen for Maternal MethylationPreprint
Smith, R. J., Dean, W., Konfortova, G., & Kelsey, G. (2003) · Genome Research · doi:10.1101/gr.781503 · Cited by 176 · see citing works
Altered Placental Function of 11β-Hydroxysteroid Dehydrogenase 2 Knockout Mice
Wyrwoll, C. S., Seckl, J. R., & Holmes, M. C. (2009) · Endocrinology · doi:10.1210/en.2008-1100 · Cited by 169 · see citing works
Placental glucose transport and GLUT 1 expression in insulin-dependent diabetes
Jansson, T., Wennergren, M., & Powell, T. L. (1999) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(99)70169-9 · Cited by 166 · see citing works
Compensatory placental growth after restricted maternal nutrition in early pregnancy
Lunney, L. H. (1998) · Placenta · doi:10.1016/s0143-4004(98)90105-9 · Cited by 164 · see citing works
The prolactin family: effectors of pregnancy-dependent adaptations
Soares, M. J., Konno, T., & Alam, S. M. K. (2007) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2007.02.005 · Cited by 158 · see citing works
The Mechanisms and Regulation of Placental Amino Acid Transport to the Human Foetus
Cleal, J. K., & Lewis, R. M. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01662.x · Cited by 157 · see citing works
Cetin, I., Giovannini, N., Alvino, G., Agostoni, C. V., Riva, E., Giovannini, M., & Pardi, G. (2002) · Pediatric Research · doi:10.1203/00006450-200211000-00023 · Cited by 155 · see citing works
Haycock, P., & Ramsay, M. (2009) · Biology of Reproduction · doi:10.1095/biolreprod.108.074682 · Cited by 155 · see citing works
Larqué, E., Krauss‐Etschmann, S., Campoy, C., Hartl, D., Linde, J., Klingler, M., Demmelmair, H., Caño, Á., Gil, Á., Bondy, B., et al. (2006) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/84.4.853 · Cited by 154 · see citing works
Farley, D. M., Choi, J., Dudley, D. J., Li, C., Jenkins, S. L., Myatt, L., & Nathanielsz, P. W. (2010) · Placenta · doi:10.1016/j.placenta.2010.06.006 · Cited by 150 · see citing works
Regulation of placental amino acid transporter activity by mammalian target of rapamycin
Roos, S., Kanai, Y., Prasad, P. D., Powell, T. L., & Jansson, T. (2009) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00330.2008 · Cited by 150 · see citing works
Malandro, M. S., Beveridge, M. J., Kilberg, M. S., & Novak, D. (1996) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1996.271.1.c295 · Cited by 150 · see citing works
Burton, G. J., Reshetnikova, O. S., Milovanov, A. P., & Teleshova, O. V. (1996) · Placenta · doi:10.1016/s0143-4004(05)80643-5 · Cited by 149 · cited 2× · see citing works
“Human Pre-eclampsia Burton et al. (1996)”
BackgroundGaither, K., Quraishi, A. N., & Illsley, N. P. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.2.5438 · Cited by 149 · see citing works
Deficiency in p57Kip2 expression induces preeclampsia-like symptoms in mice
Kanayama, N. (2002) · Molecular Human Reproduction · doi:10.1093/molehr/8.12.1129 · Cited by 147 · see citing works
Infant growth restriction is associated with distinct patterns of DNA methylation in human placentas
Banister, C. E., Koestler, D. C., Maccani, M. A., Padbury, J. F., Houseman, E. A., & Marsit, C. J. (2011) · Epigenetics · doi:10.4161/epi.6.7.16079 · Cited by 144 · see citing works
Monk, D., Sanches, R. H. D. S., Arnaúd, P., Apostolidou, S., Hills, F. A., Abu-Amero, S. N., Murrell, A., Friess, H., Reik, W., Stanier, P., et al. (2006) · Human Molecular Genetics · doi:10.1093/hmg/ddl041 · Cited by 144 · see citing works
Self-citationImprinted 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-citationHypoglycemia and the Origin of Hypoxia-Induced Reduction in Human Fetal Growth
Zamudio, S., Torricos, T., Fik, E., Oyala, M., Echalar, L., Pullockaran, J., Tutino, E., Martin, B., Belliappa, S., Balanza, E., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008551 · Cited by 141 · see citing works
The maternal endocrine environment in the low-protein model of intra-uterine growth restriction
Fernandez‐Twinn, D. S., Ozanne, S. E., Ekizoglou, S., Doherty, C., James, L. A., Gusterson, B. A., & Hales, C. N. (2003) · British Journal Of Nutrition · doi:10.1079/bjn2003967 · Cited by 140 · see citing works
Calcium channels, transporters and exchangers in placenta: a review
Belkacemi, L., Bédard, I., Simoneau, L., & Lafond, J. (2004) · Cell Calcium · doi:10.1016/j.ceca.2004.06.010 · Cited by 133 · see citing works
Reshetnikova, O. S., Burton, G. J., & Milovanov, A. P. (1994) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(94)90402-2 · Cited by 127 · 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 glucose transporter gene expression and metabolism in the rat.
Zhou, J., & Bondy, C. (1993) · Journal of Clinical Investigation · doi:10.1172/jci116305 · Cited by 125 · see citing works
Dissecting the role of glucocorticoids on pancreas development.
Gésina, E., Tronche, F., Herrera, P., Duchêne, B., Tales, W., Czernichow, P., & Bréant, B. (2004) · Diabetes · doi:10.2337/diabetes.53.9.2322 · Cited by 124 · see citing works
Roberts, C. T., Sohlström, A., Kind, K. L., Earl, R., Khong, T. Y., Robinson, J. S., Owens, P. C., & Owens, J. A. (2001) · Placenta · doi:10.1053/plac.2000.0602 · Cited by 124 · see citing works
Prematurity Is Related to High Placental Cortisol in Preeclampsia
Aufdenblatten, M., Baumann, M. U., Raio, L., Dick, B., Frey, B. M., Schneider, H., Surbek, D., Hocher, B., & Mohaupt, M. G. (2009) · Pediatric Research · doi:10.1203/pdr.0b013e31818d6c24 · Cited by 124 · see citing works
Hormones as epigenetic signals in developmental programming
Fowden, A. L., & Forhead, A. J. (2009) · Experimental Physiology · doi:10.1113/expphysiol.2008.046359 · Cited by 123 · see citing works
Copper and Iron Transport Across the Placenta: Regulation and Interactions
McArdle, H. J., Andersen, H. S., Jones, H. N., & Gambling, L. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01658.x · Cited by 120 · 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
Lopez, M. F., Dikkes, P., Zurakowski, D., & Villa‐Komaroff, L. (1996) · Endocrinology · doi:10.1210/endo.137.5.8612553 · Cited by 115 · see citing works
SNAT4 isoform of system A amino acid transporter is expressed in human placenta
Desforges, M., Lacey, H. A., Glazier, J. D., Greenwood, S. L., Mynett, K. J., Speake, P. F., & Sibley, C. P. (2005) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00258.2005 · Cited by 114 · see citing works
Effects of chronic hypoxia in vivo on the expression of human placental glucose transporters
Zamudio, S., Baumann, M. U., & Illsley, N. P. (2006) · Placenta · doi:10.1016/j.placenta.2004.12.010 · Cited by 114 · see citing works
Placental 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
Ayuk, P. T.-Y., Sibley, C. P., Donnai, P., et al. (2000) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2000.278.6.c1162 · Cited by 109 · see citing works
Wijendran, V., Bendel, R., Couch, S., Philipson, E., Cheruku, S., & Lammi-Keefe, C. (2000) · Lipids · doi:10.1007/s11745-000-0602-2 · Cited by 107 · see citing works
The Placenta and Human Developmental Programming
(2010) · Cambridge University Press eBooks · doi:10.1017/cbo9780511933806 · Cited by 105 · see citing works
Maternally-inherited Grb10 reduces placental size and efficiency
Charalambous, M., Cowley, M., Geoghegan, F., Smith, F. M., Radford, E. J., Marlow, B. P., Graham, C. F., Hurst, L. D., & Ward, A. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2009.10.011 · Cited by 101 · see citing works
Coan, P. M., Fowden, A. L., Constância, M., Ferguson‐Smith, A. C., Burton, G. J., & Sibley, C. P. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.157313 · Cited by 100 · see citing works
Self-citationPlacental anatomy and diffusing capacity in guinea pigs following long-term maternal hypoxia
Bacon, B. J., Gilbert, R. D., Kaufmann, P., Smith, A. D., Trevino, F. T., & Longo, L. D. (1984) · Placenta · doi:10.1016/s0143-4004(84)80002-8 · Cited by 96 · see citing works
Preeclampsia and the anti-angiogenic state
Agarwal, I., & Karumanchi, S. A. (2010) · Pregnancy Hypertension · doi:10.1016/j.preghy.2010.10.007 · Cited by 94 · see citing works
Fetal overgrowth in the Cdkn1c mouse model of Beckwith-Wiedemann syndrome
Tunster, S. J., de Pette, M. V., & John, R. M. (2011) · Disease Models & Mechanisms · doi:10.1242/dmm.007328 · Cited by 94 · see citing works
Coan, P. M., Ferguson‐Smith, A. C., & Burton, G. J. (2005) · Journal of Anatomy · doi:10.1111/j.1469-7580.2005.00488.x · Cited by 94 · see citing works
Enhanced placental GLUT1 and GLUT3 expression in dexamethasone-induced fetal growth retardation
LANGDOWN, M. L., & Sugden, M. C. (2001) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(01)00629-3 · Cited by 92 · see citing works
Understanding placental nutrient transfer – why bother? New biomarkers of fetal growth
Sibley, C. P. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.172403 · Cited by 92 · see citing works
Stereology of the placenta in type 1 and type 2 diabetes
Higgins, M., Felle, P., Mooney, E. E., Bannigan, J., & McAuliffe, F. M. (2011) · Placenta · doi:10.1016/j.placenta.2011.04.015 · Cited by 89 · see citing works
Desforges, M., Mynett, K. J., Jones, R. L., Greenwood, S. L., Westwood, M., Sibley, C. P., & Glazier, J. D. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.161331 · Cited by 88 · 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
Self-citationEricsson, A., Säljö, K., Sjöstrand, E., Jansson, N., Prasad, P. D., Powell, T. L., & Jansson, T. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.131185 · Cited by 83 · see citing works
Haché, S., Takser, L., Bellego, F. L., Weiler, H., Leduc, L., Forest, J., Giguère, Y., Masse, A., Barbeau, B., & Lafond, J. (2010) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2010.01039.x · Cited by 82 · see citing works
Reshetnikova, O. S., Burton, G. J., & Васильевна, Т. О. (1995) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(95)90330-5 · Cited by 82 · see citing works
Placental Vascular Dysfunction in Diabetic Pregnancies: Intimations of Fetal Cardiovascular Disease?
Leach, L. (2011) · Microcirculation · doi:10.1111/j.1549-8719.2011.00091.x · Cited by 81 · see citing works
Gestational changes in Ca2+ transport across rat placenta and mRNA for calbindin9K and Ca(2+)-ATPase
Glazier, J. D., Atkinson, D. E., Thornburg, K. L. R., et al. (1992) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1992.263.4.r930 · Cited by 80 · 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
Does the fetal genotype affect maternal physiology during pregnancy?
Petry, C. J., Ong, K. K., & Dunger, D. B. (2007) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2007.07.007 · Cited by 79 · see citing works
John, R. M., & Hemberger, M. (2012) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2012.03.018 · Cited by 77 · see citing works
Bitsanis, D., Ghebremeskel, K., Moodley, T., Crawford, M. A., & Djahanbakhch, O. (2006) · Lipids · doi:10.1007/s11745-006-5104-8 · Cited by 76 · see citing works
Human placental amino acid transporter genes: expression and function
Kudo, Y., & Boyd, C. A. R. (2002) · Reproduction · doi:10.1530/rep.0.1240593 · Cited by 71 · see citing works
Paternal monoallelic expression of PEG3 in the human placenta
Hiby, S. E. (2001) · Human Molecular Genetics · doi:10.1093/hmg/10.10.1093 · Cited by 67 · see citing works
Dietary composition programmes placental phenotype in mice
Coan, P. M., Vaughan, O. R., McCarthy, J., Mactier, C., Burton, G. J., Constância, M., & Fowden, A. L. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.208629 · Cited by 67 · see citing works
Self-citationYuen, R. K. C., & Robinson, W. P. (2011) · Placenta · doi:10.1016/j.placenta.2011.01.003 · Cited by 65 · see citing works
Fetal regulation of iron transport during pregnancy
Gambling, L., Lang, C., & McArdle, H. J. (2011) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.110.000885 · Cited by 65 · see citing works
Sferruzzi-Perri, A. N., Owens, J. A., Standen, P., Taylor, R. L., Heinemann, G. K., Robinson, J. S., & Roberts, C. T. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00320.2006 · Cited by 65 · 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-citationMagnetic resonance imaging of hypoxic injury to the murine placenta
Tomlinson, T. M., Garbow, J. R., Anderson, J., Engelbach, J. A., Nelson, D. M., & Sadovsky, Y. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00425.2009 · Cited by 61 · see citing works
Increased maternofetal calcium flux in parathyroid hormone‐related protein‐null mice
Bond, H., Dilworth, M. R., Baker, B., Cowley, E. J., Jimenez, A. R., Boyd, R. D. H., Husain, S. M., Ward, B. S., Sibley, C. P., & Glazier, J. D. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2007.149104 · Cited by 60 · see citing works
Strid, H., Bucht, E., Jansson, T., Wennergren, M., & Powell, T. L. (2003) · Placenta · doi:10.1053/plac.2002.0941 · Cited by 60 · see citing works
Lewis, R. M., James, L. A., Zhang, J., Byrne, C. D., & Hales, C. N. (2001) · British Journal Of Nutrition · doi:10.1079/bjn2000247 · Cited by 59 · see citing works
Effect of Gestational Nutrition on Vascular Integrity in the Murine Placenta
Rutland, C. S., Latunde‐Dada, A. O., Thorpe, A., Plant, R., Langley‐Evans, S. C., & Leach, L. (2006) · Placenta · doi:10.1016/j.placenta.2006.07.001 · Cited by 56 · see citing works
Esquiliano, D. R., Guo, W., Li, L., Dikkes, P., & Lopez, M. F. (2009) · Placenta · doi:10.1016/j.placenta.2009.05.004 · Cited by 53 · see citing works
Strid, H., & Powell, T. L. (2000) · Pediatric Research · doi:10.1203/00006450-200007000-00012 · Cited by 51 · see citing works
Transfer of folic acid inside the first-trimester gestational sac and the effect of maternal smoking
Jauniaux, E. R. M., Johns, J., Gulbis, B., Spasić-Bošković, O., & Burton, G. J. (2007) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2007.02.009 · Cited by 48 · see citing works
Gardner, R. L., Squire, S. E., Zaina, S., Hills, S., & Graham, C. F. (1999) · Biology of Reproduction · doi:10.1095/biolreprod60.1.190 · Cited by 45 · see citing works
Petry, C. J., Evans, M. L., Wingate, D. L., Ong, K. K., Reik, W., Constância, M., & Dunger, D. B. (2010) · Diabetes · doi:10.2337/db09-0757 · Cited by 44 · see citing works
Self-citationMandò, C., Tabano, S. M., Colapietro, P., Pileri, P., Colleoni, F., Avagliano, L., Doi, P., Bulfamante, G., Miozzo, M. R., & Cetin, I. (2010) · Placenta · doi:10.1016/j.placenta.2010.10.009 · Cited by 43 · see citing works
Keating, E., Gonçalves, P., Campos, I., Costa, F., & Martel, F. (2009) · Reproductive Toxicology · doi:10.1016/j.reprotox.2009.07.001 · Cited by 42 · see citing works
Kusinski, L. C., Jones, C. J. P., Baker, P. N., Sibley, C. P., & Glazier, J. D. (2009) · Placenta · doi:10.1016/j.placenta.2009.11.006 · Cited by 40 · see citing works
Review: Parent-offspring conflict and the control of placental function
Moore, T. (2011) · Placenta · doi:10.1016/j.placenta.2011.11.016 · Cited by 40 · see citing works
Liebner, S., Gerhardt, H., & Wolburg, H. (2000) · Developmental Dynamics · doi:10.1002/(sici)1097-0177(200001)217:1 · Cited by 40 · see citing works
Change in iron transporter expression in human term placenta with different maternal iron status
Li, Y., Yan, H., & Bai, B. (2008) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2008.02.012 · Cited by 40 · see citing works
The placental imprintome and imprinted gene function in the trophoblast glycogen cell lineage
Lefebvre, L. (2012) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2012.03.019 · Cited by 40 · see citing works
Strakovsky, R. S., Zhou, D., & Pan, Y. (2010) · Journal of Nutrition · doi:10.3945/jn.110.127803 · Cited by 39 · see citing works
Speake, P. F., Glazier, J. D., Ayuk, P. T.-Y., et al. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-030067 · Cited by 39 · see citing works
Maternal muscle mass may influence system A activity in human placenta
Lewis, R. M., Greenwood, S. L., Cleal, J. K., Crozier, S. R., Verrall, L., Inskip, H. M., Cameron, I. T., Cooper, C., Sibley, C. P., Hanson, M. A., et al. (2010) · Placenta · doi:10.1016/j.placenta.2010.02.001 · Cited by 33 · see citing works
Genome-wide expression profiling of placentas in the p57Kip2 model of pre-eclampsia
Knox, K. S., & Baker, J. C. (2007) · MHR: Basic science of reproductive medicine · doi:10.1093/molehr/gal116 · Cited by 33 · see citing works
Lee, B., Lee, G., Jung, E., et al. (2009) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-7-49 · Cited by 32 · see citing works
Genomic imprinting of a placental lactogen gene in Peromyscus
Vrana, P. B., Matteson, P. G., Schmidt, J. V., Ingram, R. S., Joyce, A., Prince, K. L., Dewey, M. J., & Tilghman, S. M. (2001) · Development Genes and Evolution · doi:10.1007/s00427-001-0188-x · Cited by 30 · see citing works
Maternal smoking is associated with decreased 5-methyltetrahydrofolate in cord plasma
Stark, K. D., Pawlosky, R. J., Sokol, R. J., et al. (2007) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/85.3.796 · Cited by 24 · see citing works
Hypoxia Regulates the Expression of PHLDA2 in Primary Term Human Trophoblasts
Kim, H.-S., Roh, C., Chen, B., Tycko, B., Nelson, D. M., & Sadovsky, Y. (2006) · Placenta · doi:10.1016/j.placenta.2006.01.025 · Cited by 24 · see citing works
Khatun, R., Wu, Y., Kanenishi, K., Ueno, M., Tanaka, S., Hata, T., & Sakamoto, H. (2003) · Placenta · doi:10.1016/s0143-4004(03)00138-3 · Cited by 24 · see citing works
ISHIDA, M., Ohashi, S., KIZAKI, Y., NAITO, J.-I., Horiguchi, K., & Harigaya, T. (2007) · Journal of Reproduction and Development · doi:10.1262/jrd.18002 · Cited by 20 · see citing works
Sugden, M. C., & LANGDOWN, M. L. (2001) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(01)00630-x · Cited by 19 · see citing works
Dissecting the Role of Glucocorticoids on Pancreas
Herrera, P. L., Duchêne, B., Czernichow, P., & Bréant, B. (2004) · Cited by 19 · see citing works
Glucocorticoids and placental programming
Vaughan, O. R., Forhead, A. J., & Fowden, A. L. (2010) · Cambridge University Press eBooks · doi:10.1017/cbo9780511933806.015 · Cited by 12 · 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
Maltepe, E., & Fisher, S. J. (2015) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100814-125620 · Cited by 592 · see citing works
Air pollution during pregnancy and placental adaptation in the levels of global DNA methylation
Maghbooli, Z., Hossein-nezhad, A., Adabi, E., Asadollah-pour, E., Sadeghi, M., Mohammad-nabi, S., Zakeri Rad, L., Malek Hosseini, A.-A., Radmehr, M., Faghihi, F., et al. (2018) · PLOS ONE · doi:10.1371/journal.pone.0199772 · Cited by 113 · see citing works
- Authors
- Sandovici, I., Hoelle, K., Angiolini, E., & Constância, M.
- Affiliations
- University of Cambridge (GB)
- Corresponding author
- Sandovici, Ionel
- Constância, Miguel
- Venue
- Reproductive BioMedicine Online
- Publisher
- Elsevier BV
- Published
- 2012-07
- Volume
- 25
- Issue
- 1
- Pages
- 68-89
- ISSN
- 1472-6483 (ISSN-L)
- OpenAlex
- W2047911553
- Cited by
- 224
- References
- 153
- Citations by year
- 2026: 19 · 2025: 9 · 2024: 22 · 2023: 22 · 2022: 12 · 2021: 21 · 2020: 15 · 2019: 17 · 2018: 12 · 2017: 13 · 2016: 22 · 2015: 15 · 2014: 8 · 2013: 11 · 2012: 6
- FWCI
- 1.99
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Reproductive BioMedicine Online (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Biotechnology and Biological Sciences Research Council (BB/I014594/1, BBS/E/T/000PR6193)
- 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
- placental adaptation, fetal growth, developmental programming, nutrient transporters, nutrient exchange, imprinted genes, epigenetic regulation, placenta, fetal viability, placental mammals
- MeSH terms
- Adaptation, Physiological, Amino Acids, Animals, Calcium, Female, Fetus, Folic Acid, Gestational Age, Glucose, Humans, Maternal-Fetal Exchange, Placenta, Pregnancy, Signal Transduction, Genomic Imprinting, Gene Expression Regulation, Developmental, Prenatal Nutritional Physiological Phenomena, Epigenesis, Genetic, Fetal Development
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