Imprinted genes and the epigenetic regulation of placental phenotype

Fowden, A.L.; Coan, P.M.; Angiolini, E.; Burton, G.J.; Constancia, M.

doi:10.1016/j.pbiomolbio.2010.11.005

Cited by 142Genetic Syndromes and ImprintingBirth, Development, and HealthPregnancy and preeclampsia studies

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

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Abstract

Imprinted genes are expressed in a parent-of-origin manner by epigenetic modifications that silence either the paternal or maternal allele. They are widely expressed in fetal and placental tissues and are essential for normal placental development. In general, paternally expressed genes enhance feto-placental growth while maternally expressed genes limit conceptus growth, consistent with the hypothesis that imprinting evolved in response to the conflict between parental genomes in the allocation of maternal resources to fetal growth. Using targeted deletion, uniparental duplication, loss of imprinting and transgenic approaches, imprinted genes have been shown to determine the transport capacity of the definitive mouse placenta by regulating its growth, morphology and transporter abundance. Imprinted genes in the placenta are also responsive to environmental challenges and adapt placental phenotype to the prevailing nutritional conditions, in part, by varying their epigenetic status. In addition, interplay between placental and fetal imprinted genes is important in regulating resource partitioning via the placenta both developmentally and in response to environmental factors. By balancing the opposing parental drives on resource allocation with the environmental signals of nutrient availability, imprinted genes, like the Igf2-H19 locus, may act as nutrient sensors and optimise the fetal acquisition of nutrients for growth. These genes, therefore, have a major role in the epigenetic regulation of placental phenotype with long term consequences for the developmental programming of adult health and disease.

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Imprinted genes have an important role in the developmental plasticity of the placenta, particularly with respect to resource allocation.
“Imprinted genes, therefore, have an important role in the developmental plasticity of the placenta, particularly with respect to resource allocation (189, 445).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [189]
Imprinted genes are known to have a disproportionately important role in fetal-placental development and are involved in resource allocation more widely.
“These studies have tended to concentrate on the imprinted genes, which are known to have a disproportionately important role in fetal-placental development and are involved in resource allocation more widely (126, 189, 385, 544).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [189]

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Šerman, L., Vlahović, M., Šijan, M., Bulić‐Jakuš, F., Šerman, A., Sinčić, N., Matijević, R., Jurić‐Lekić, G., & Bojanac, A. K. (2007) · Placenta · doi:10.1016/j.placenta.2007.04.001 · Cited by 88 · see citing works
Placental transporter activity and expression in relation to fetal growth
Sibley, C. P., Glazier, J. D., & D’Souza, S. W. (1997) · Experimental Physiology · doi:10.1113/expphysiol.1997.sp004034 · Cited by 86 · see citing works
Placental-specific Igf2 knockout mice exhibit hypocalcemia and adaptive changes in placental calcium transport
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
Disruption of imprinting in cloned mouse fetuses from embryonic stem cells
Ogawa, H., Ono, Y., Shimozawa, N., Sotomaru, Y., Katsuzawa, Y., Hiura, H., Ito, M., & Kono, T. (2003) · Reproduction · doi:10.1530/rep.0.1260549 · Cited by 77 · see citing works
Somatic cell nuclear transfer in the sheep induces placental defects that likely precede fetal demise
Fletcher, C., Roberts, C. T., Hartwich, K. M., Walker, S., & McMillen, I. C. (2007) · Reproduction · doi:10.1530/rep.1.01203 · Cited by 70 · see citing works
Molecular and clinical findings and their correlations in Silver-Russell syndrome: implications for a positive role of IGF2 in growth determination and differential imprinting regulation of the IGF2–H19 domain in bodies and placentas
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
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
Placental Anionic and Cationic Amino Acid Transporter Expression in Growth Hormone Overexpressing and Null IGF-II or Null IGF-I Receptor Mice
Matthews, J. C., Beveridge, M. J., Dialynas, E., Bartke, A., Kilberg, M. S., & Novak, D. (1999) · Placenta · doi:10.1053/plac.1999.0421 · Cited by 53 · see citing works
Placental Glycogen Stores are Increased in Mice with H19 Null Mutations but not in those with Insulin or IGF Type 1 Receptor Mutations
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
Hypomethylation trends in the intergenic region of the imprinted IGF2 and H19 genes in cloned cattle
Curchoe, C. L., Zhang, S., Yang, L., Page, R. L., & Tian, X. (2009) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2009.02.008 · Cited by 52 · see citing works
Epigenetics and Assisted Reproductive Technologies: Human Imprinting Syndromes
Lawrence, L. T., & Moley, K. (2008) · Seminars in Reproductive Medicine · doi:10.1055/s-2008-1042953 · Cited by 47 · see citing works
Genomic loss of imprinting in first-trimester human placenta
Pozharny, Y., Lambertini, L., Ma, Y., Ferrara, L. A., Litton, C. G., Diplas, A. I., Jacobs, A. R., Chen, J., Stone, J. L., Wetmur, J. G., et al. (2010) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2010.01.039 · Cited by 46 · see citing works
Abnormal Expression of the Imprinted Gene Phlda2 in Cloned Bovine Placenta
Guillomot, M., Taghouti, G., Constant, F., Degrelle, S. A., Hue, I., Chavatte‐Palmer, P., & Jammes, H. (2010) · Placenta · doi:10.1016/j.placenta.2010.03.004 · Cited by 45 · see citing works
Raised Late Pregnancy Glucose Concentrations in Mice Carrying Pups With Targeted Disruption of H19Δ13
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
Endothelial Progenitor Cells: Their Potential in the Placental Vasculature and Related Complications
Sipos, P. I., Crocker, I. P., Hubel, C. A., & Baker, P. N. (2009) · Placenta · doi:10.1016/j.placenta.2009.10.006 · Cited by 41 · see citing works
Differential expression of endothelial ?-catenin and plakoglobin during development and maturation of the blood-brain and blood-retina barrier in the chicken
Liebner, S., Gerhardt, H., & Wolburg, H. (2000) · Developmental Dynamics · doi:10.1002/(sici)1097-0177(200001)217:1 · Cited by 40 · see citing works
Genomic imprinting effects in a compromised in utero environment: Implications for a healthy pregnancy
Lim, A. L., & Ferguson‐Smith, A. C. (2009) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2009.10.008 · Cited by 39 · see citing works
Chorioallantoic placenta defects in cloned mice
Wakisaka‐Saito, N., Kohda, T., Inoue, K., Ogonuki, N., Miki, H., Hikichi, T., Mizutani, E., Wakayama, T., Kaneko‐Ishino, T., Ogura, A., et al. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.08.057 · Cited by 38 · see citing works
IS MOM IN CHARGE? IMPLICATIONS OF RESOURCE PROVISIONING ON THE EVOLUTION OF THE PLACENTA
Banet, A. I., Au, A. G., & Reznick, D. N. (2010) · Evolution · doi:10.1111/j.1558-5646.2010.01059.x · Cited by 36 · see citing works
Detection of differentially expressed genes between Erhualian and Large White placentas on day 75 and 90 of gestation
Zhou, Q., Fang, M.-D., Huang, T., Li, C., Yu, M., & Zhao, S. (2009) · BMC Genomics · doi:10.1186/1471-2164-10-337 · Cited by 34 · see citing works
Distinct Patterns of Gene-Specific Methylation in Mammalian Placentas: Implications for Placental Evolution and Function
Ng, H., Novakovic, B., Hiendleder, S., Craig, J. M., Roberts, C. T., & Saffery, R. (2010) · Placenta · doi:10.1016/j.placenta.2010.01.009 · Cited by 33 · see citing works
Effects of food restriction and pregnancy on the expression of insulin-like growth factors-I and -II in tIssues from guinea pigs
Olausson, H., & Sohlström, A. (2003) · Journal of Endocrinology · doi:10.1677/joe.0.1790437 · Cited by 25 · see citing works
Characterization of the Placenta Specific Bovine Mammalian Achaete Scute-like Homologue 2 (Mash2) Gene
Arnold, D. R., Lefebvre, R., & Smith, L. C. (2006) · Placenta · doi:10.1016/j.placenta.2005.12.001 · Cited by 23 · see citing works
Defining Contributions of Paternally Methylated Imprinted Genes at the Igf2-H19 and Dlk1-Gtl2 Domains to Mouse Placentation by Transcriptomic Analysis
Kawahara, M., Morita, S., Takahashi, N., & Kono, T. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.000299 · Cited by 22 · see citing works
Allelic switching of the imprinted IGF2R gene in cloned bovine fetuses and calves
Suteevun, T., Curchoe, C. L., Evans, A. C. O., Boland, E. J., Rizos, D. V., Fair, T., Duffy, P., Sung, L., Du, F., Chaubal, S., et al. (2009) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2009.01.003 · Cited by 22 · see citing works
Quantitative studies on the mechanisms of amino acid supply to rat embryos during organogenesis
Beckman, D. A., Lloyd, J. B., & Brent, R. L. (1998) · Reproductive Toxicology · doi:10.1016/s0890-6238(97)00147-0 · Cited by 18 · see citing works
Placental-specific Igf-2 regulates the diffusional exchange characteristics of the mouse placenta
Sibley, C. P., Coan, P., Ferguson-Smith, A., Dean, W., Hughes, J. P., Smith, P. D., Reik, W., Burton, G. J., Fowden, A., & Constância, M. (2004) · Research Explorer (The University of Manchester) · Cited by 4 · 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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What is fetal programming?: a lifetime health is under the control of in utero health
Kwon, E. J., & Kim, Y. J. (2017) · Obstetrics & Gynecology Science · doi:10.5468/ogs.2017.60.6.506 · Cited by 376 · see citing works
Placental adaptations to the maternal–fetal environment: implications for fetal growth and developmental programming
Sandovici, I., Hoelle, K., Angiolini, E., & Constância, M. (2012) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2012.03.017 · Cited by 224 · see citing works
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New insights into establishment and maintenance of DNA methylation imprints in mammals
Kelsey, G., & Feil, R. (2012) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2011.0336 · Cited by 212 · see citing works
Paternally expressed genes predominate in the placenta
Wang, X., Miller, D. C., Harman, R. M., Antczak, D. F., & Clark, A. G. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1308998110 · Cited by 191 · see citing works
Placentas from pregnancies conceived by IVF/ICSI have a reduced DNA methylation level at the H19 and MEST differentially methylated regions†
Nelissen, E. C. M., Dumoulin, J. C. M., Daunay, A., Evers, J. L. H., Tost, J., & van Montfoort, A. P. A. (2013) · Human Reproduction · doi:10.1093/humrep/des459 · Cited by 147 · see citing works
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
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The ever growing complexity of placental epigenetics – Role in adverse pregnancy outcomes and fetal programming
Novakovic, B., & Saffery, R. (2012) · Placenta · doi:10.1016/j.placenta.2012.10.003 · Cited by 123 · see citing works
Glucocorticoids as regulatory signals during intrauterine development
Fowden, A. L., & Forhead, A. J. (2015) · Experimental Physiology · doi:10.1113/ep085212 · Cited by 118 · see citing works
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Regulation of maternal–fetal metabolic communication
Bowman, C. E., Arany, Z. P., & Wolfgang, M. J. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03674-w · Cited by 116 · 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
The placenta: phenotypic and epigenetic modifications induced by Assisted Reproductive Technologies throughout pregnancy
Choux, C., Carmignac, V., Bruno, C., Sagot, P., Vaiman, D., & Fauque, P. (2015) · Clinical Epigenetics · doi:10.1186/s13148-015-0120-2 · Cited by 110 · see citing works
The 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
Imprinted MicroRNA Gene Clusters in the Evolution, Development, and Functions of Mammalian Placenta
Malnou, C. E., Umlauf, D., Mouysset, M., & Cavaillé, J. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2018.00706 · Cited by 100 · see citing works
Genomic imprinting, growth and maternal–fetal interactions
Cassidy, F. C., & Charalambous, M. (2018) · Journal of Experimental Biology · doi:10.1242/jeb.164517 · Cited by 95 · see citing works
The role of extracellular matrix in normal and pathological pregnancy: Future applications of microphysiological systems in reproductive medicine
O’Connor, B. B., Pope, B. D., Peters, M. M., Ris‐Stalpers, C., & Parker, K. K. (2020) · Experimental Biology and Medicine · doi:10.1177/1535370220938741 · Cited by 94 · see citing works
Assisted reproduction causes placental maldevelopment and dysfunction linked to reduced fetal weight in mice
Chen, S., Sun, F.-Z., Huang, X.-Y., Wang, X., Tang, N., Zhu, B., & Li, B. (2015) · Scientific Reports · doi:10.1038/srep10596 · Cited by 94 · see citing works
Review: Placenta, evolution and lifelong health
Lewis, R. M., Cleal, J. K., & Hanson, M. A. (2011) · Placenta · doi:10.1016/j.placenta.2011.12.003 · Cited by 93 · see citing works
Review: Endocrine regulation of placental phenotype
Fowden, A. L., Forhead, A. J., Sferruzzi-Perri, A. N., Burton, G. J., & Vaughan, O. R. (2014) · Placenta · doi:10.1016/j.placenta.2014.11.018 · Cited by 96 · see citing works
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Impacts of bisphenol A (BPA) and phthalate exposures on epigenetic outcomes in the human placenta
Strakovsky, R. S., & Schantz, S. L. (2018) · Current Zoology · doi:10.1093/eep/dvy022 · Cited by 90 · see citing works
Differences in Gene Expression between First and Third Trimester Human Placenta: A Microarray Study
Sitras, V., Fenton, C. G., Paulssen, R. H., Vårtun, Å., & Acharya, G. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033294 · Cited by 86 · see citing works
Imprinted genes in mouse placental development and the regulation of fetal energy stores
Tunster, S. J., Jensen, A. B., & John, R. M. (2013) · Reproduction · doi:10.1530/rep-12-0511 · Cited by 85 · see citing works
Hormonal and nutritional drivers of intrauterine growth
Sferruzzi-Perri, A. N., Vaughan, O. R., Forhead, A. J., & Fowden, A. L. (2013) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e32835e3643 · Cited by 82 · see citing works
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A Concise Review on Epigenetic Regulation: Insight into Molecular Mechanisms
Golbabapour, S., Abdulla, M. A., & Hajrezaei, M. (2011) · International Journal of Molecular Sciences · doi:10.3390/ijms12128661 · Cited by 68 · see citing works
Interplay of Placental DNA Methylation and Maternal Insulin Sensitivity in Pregnancy
Hivert, M., Cárdenas, A., Allard, C., Doyon, M., Powe, C. E., Catalano, P. M., Perron, P., & Bouchard, L. (2019) · Diabetes · doi:10.2337/db19-0798 · Cited by 65 · see citing works
Loss of DNMT1o Disrupts Imprinted X Chromosome Inactivation and Accentuates Placental Defects in Females
McGraw, S., Oakes, C. C., Martel, J., Cirio, M. C., de Zeeuw, P., Mak, W., Plass, C., Bartolomei, M. S., Chaillet, J. R., & Trasler, J. M. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003873 · Cited by 64 · see citing works
Humans as Superorganisms
Krämer, P., & Bressan, P. (2015) · Perspectives on Psychological Science · doi:10.1177/1745691615583131 · Cited by 66 · see citing works
Predisposing Factors to Abnormal First Trimester Placentation and the Impact on Fetal Outcomes
Kroener, L. L., Wang, E. T., & Pisarska, M. D. (2015) · Seminars in Reproductive Medicine · doi:10.1055/s-0035-1570029 · Cited by 65 · see citing works
Metabolic Disease Programming: From Mitochondria to Epigenetics, Glucocorticoid Signalling and Beyond
Grilo, L. F., Tocantins, C., Diniz, M. S., Gomes, R. M., Oliveira, P. J., Matafome, P. N., & Pereira, S. P. (2021) · European Journal of Clinical Investigation · doi:10.1111/eci.13625 · Cited by 62 · see citing works
Environmental regulation of placental phenotype: implications for fetal growth
Vaughan, O. R., Sferruzzi-Perri, A. N., Coan, P. M., & Fowden, A. L. (2011) · Reproduction Fertility and Development · doi:10.1071/rd11909 · Cited by 55 · see citing works
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Pathology from evolutionary conflict, with a theory of X chromosome versus autosome conflict over sexually antagonistic traits
Frank, S. A., & Crespi, B. J. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100921108 · Cited by 49 · see citing works
Expression of KCNQ1OT1, CDKN1C, H19, and PLAGL1 and the methylation patterns at the KvDMR1 and H19/IGF2 imprinting control regions is conserved between human and bovine
Robbins, K., Chen, Z., Wells, K. D., & Rivera, R. M. (2012) · Journal of Biomedical Science · doi:10.1186/1423-0127-19-95 · Cited by 49 · see citing works
Extensive load of somatic CNVs in the human placenta
Kasak, L., Rull, K., Vaas, P., Teesalu, P., & Laan, M. (2015) · Scientific Reports · doi:10.1038/srep08342 · Cited by 48 · see citing works
Fetal growth factors and fetal nutrition
Bloomfield, F. H., Spiroski, A., & Harding, J. E. (2013) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2013.03.003 · Cited by 50 · see citing works
Prenatal origins of postnatal variation in growth, development and productivity of ruminants
Bell, A. W., & Greenwood, P. L. (2016) · Animal Production Science · doi:10.1071/an15408 · Cited by 45 · see citing works
Placental miR-340 mediates vulnerability to activity based anorexia in mice
Schroeder, M., Jakovcevski, M., Polacheck, T., Drori, Y., Luoni, A., Röh, S., Zaugg, J., Ben‐Dor, S., Albrecht, C., & Chen, A. (2018) · Nature Communications · doi:10.1038/s41467-018-03836-2 · Cited by 44 · see citing works
Genetics of the human placenta: implications for toxicokinetics
Gundacker, C., Neesen, J., Straka, E., Ellinger, I., Dolznig, H., & Hengstschläger, M. (2016) · Archives of Toxicology · doi:10.1007/s00204-016-1816-6 · Cited by 44 · see citing works
Role of genomic imprinting in mammalian development
Thamban, T., Agarwaal, V., & Khosla, S. (2020) · Journal of Biosciences · doi:10.1007/s12038-019-9984-1 · Cited by 43 · see citing works
Imprinted and X-linked non-coding RNAs as potential regulators of human placental function
Buckberry, S., Bianco‐Miotto, T., & Roberts, C. T. (2013) · Epigenetics · doi:10.4161/epi.26197 · Cited by 42 · see citing works
Altered gene expression and spongiotrophoblast differentiation in placenta from a mouse model of diabetes in pregnancy
Salbaum, J. M., Krüger, C., Zhang, X., Delahaye, N. A., Pavlínková, G., Burk, D. H., & Kappen, C. (2011) · Diabetologia · doi:10.1007/s00125-011-2132-6 · Cited by 42 · 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
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
Chorioallantoic and yolk sac placentation in the plains viscacha (Lagostomus maximus) – A caviomorph rodent with natural polyovulation
Flamini, M. A., Portiansky, E. L., Favaron, P. O., Martins, D. D. S., Ambrósio, C. E., Mess, A., Miglino, M. A., & Barbeito, C. G. (2011) · Placenta · doi:10.1016/j.placenta.2011.09.002 · Cited by 40 · see citing works
The genome-defence gene Tex19.1 suppresses LINE-1 retrotransposons in the placenta and prevents intra-uterine growth retardation in mice
Reichmann, J., Reddington, J. P., Best, D., Read, D., Öllinger, R., Meehan, R. R., & Adams, I. R. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt029 · Cited by 39 · see citing works
Epigenetic features of the mouse trophoblast
Rugg‐Gunn, P. J. (2012) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2012.01.012 · Cited by 38 · see citing works
Neurobehavioral Consequences of Fetal Exposure to Gestational Stress
Sandman, C. A., Glynn, L. M., & Davis, E. P. (2016) · Springer eBooks · doi:10.1007/978-3-319-22023-9_13 · Cited by 37 · see citing works
Gene expression and epigenetic aberrations in F1‐placentas fathered by obese males
Mitchell, M., Strick, R., Strissel, P. L., Dittrich, R., McPherson, N. O., Lane, M., Pliushch, G., Potabattula, R., Haaf, T., & Hajj, N. E. (2017) · Molecular Reproduction and Development · doi:10.1002/mrd.22784 · Cited by 35 · see citing works
Unique transcriptomic landscapes identified in idiopathic spontaneous and infection related preterm births compared to normal term births
Brockway, H., Kallapur, S. G., Buhimschi, I. A., Buhimschi, C. S., Ackerman, W. E., Muglia, L. J., & Jones, H. N. (2019) · PLoS ONE · doi:10.1371/journal.pone.0225062 · Cited by 33 · see citing works
Birth weight, umbilical and placental traits in relation to neonatal loss in cloned pigs
Ao, Z., Liu, D., Zhao, C., Yue, Z., Shi, J., Zhou, R., Cai, G., Zheng, E., Li, Z., & Wu, Z. (2017) · Placenta · doi:10.1016/j.placenta.2017.06.010 · Cited by 31 · see citing works
Paternal obesity induces placental hypoxia and sex-specific impairments in placental vascularization and offspring metabolism
Jazwiec, P. A., Patterson, V. S., Ribeiro, T. A., Yeo, E., Kennedy, K. M., Mathias, P. C. D. F., Petrik, J., & Sloboda, D. M. (2022) · Biology of Reproduction · doi:10.1093/biolre/ioac066 · Cited by 31 · see citing works
Aberrant H3K4me3 modification of epiblast genes of extraembryonic tissue causes placental defects and implantation failure in mouse IVF embryos
Bai, D., Sun, J., Chen, C., Jia, Y., Li, Y., Liu, K., Zhang, Y., Yin, J., Liu, Y., Han, X., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110784 · Cited by 31 · see citing works
Placental DNA methylation in pregnancies complicated by maternal diabetes and/or obesity: State of the art and research gaps
Hjort, L., Novakovic, B., Cvitic, S., Saffery, R., Damm, P., & Desoyé, G. (2022) · Epigenetics · doi:10.1080/15592294.2022.2111755 · Cited by 27 · see citing works
Is there a genomically imprinted social brain?
Curley, J. P. (2011) · BioEssays · doi:10.1002/bies.201100060 · 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
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Paternal age, placental weight and placental to birthweight ratio: a population-based study of 590 835 pregnancies
Strøm‐Roum, E. M., Haavaldsen, C., Tanbo, T., & Eskild, A. (2013) · Human Reproduction · doi:10.1093/humrep/det299 · Cited by 27 · see citing works
Brain and placental transcriptional responses as a readout of maternal and paternal preconception stress are fetal sex specific
Cissé, Y. M., Chan, J. C., Nugent, B. M., Banducci, C., & Bale, T. L. (2020) · Placenta · doi:10.1016/j.placenta.2020.06.019 · Cited by 25 · see citing works
Is Placental Mitochondrial Function a Regulator that Matches Fetal and Placental Growth to Maternal Nutrient Intake in the Mouse?
Chiaratti, M. R., Malik, S., Diot, A., Rapa, E., Macleod, L., Morten, K., Vatish, M., Boyd, R., & Poulton, J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0130631 · Cited by 24 · see citing works
Placenta and Placental Transport Function
Sadovsky, Y., & Jansson, T. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00039-9 · Cited by 24 · see citing works
What does genetics tell us about imprinting and the placenta connection?
Varmuza, S., & Miri, K. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1714-0 · Cited by 22 · see citing works
Effect of paternal folate deficiency on placental folate content and folate receptor α expression in rats
Kim, H. W., Choi, Y. J., Kim, K. N., Tamura, T., & Chang, N. (2011) · Nutrition Research and Practice · doi:10.4162/nrp.2011.5.2.112 · Cited by 22 · see citing works
Negative uterine asynchrony retards early equine conceptus development and upregulation of placental imprinted genes
Gibson, C. M. E., de Ruijter‐Villani, M., & Stout, T. A. E. (2017) · Placenta · doi:10.1016/j.placenta.2017.07.007 · Cited by 21 · see citing works
The Consequences of Assisted Reproduction Technologies on the Offspring Health Throughout Life: A Placental Contribution
Schroeder, M., Badini, G., Sferruzzi-Perri, A. N., & Albrecht, C. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.906240 · Cited by 20 · see citing works
The Dysfunctional Placenta Epigenome: Causes and Consequences
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Self-citation

Authors: Fowden, A. L., Coan, P. M., Angiolini, E., Burton, G. J., & Constancia, M.
Affiliations: University of Cambridge (GB)
Corresponding author: Fowden, A.L.
ORCID: Fowden, A.L.
Coan, P.M.
Burton, G.J.
Venue: Progress in Biophysics and Molecular Biology
Publisher: Elsevier BV
Published: 2011-07
Volume: 106
Issue: 1
Pages: 281-288
ISSN: 0079-6107 (ISSN-L)
DOI: 10.1016/j.pbiomolbio.2010.11.005
OpenAlex: W2019362605
Cited by: 142
References: 102
Citations by year: 2026: 3 · 2025: 4 · 2024: 4 · 2023: 7 · 2022: 5 · 2021: 13 · 2020: 8 · 2019: 6 · 2018: 12 · 2017: 9 · 2016: 8 · 2015: 16 · 2014: 5 · 2013: 14 · 2012: 17
FWCI: 1.42
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Progress in Biophysics and Molecular Biology (publishedVersion)
PubMed (publishedVersion)
Funders: Wellcome Trust
Biotechnology and Biological Sciences Research Council (BB/C513626/1)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Keywords: genomic imprinting, imprinted genes, placental development, epigenetic regulation, parent-of-origin gene expression, loss of imprinting, Igf2/H19 locus, placental transporters, fetal growth, developmental programming, maternal nutrition
MeSH terms: Adult, Animals, Female, Humans, Maternal-Fetal Exchange, Phenotype, Placentation, Pregnancy, Genomic Imprinting, Epigenesis, Genetic, Mice

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Imprinted genes and the epigenetic regulation of placental phenotype

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