Cited by 629Birth, Development, and HealthEpigenetics and DNA MethylationGenetic Syndromes and Imprinting

The DOI matches its Crossref record; 94 of the 94 references it cites were found in a registry or an index.

Epigenetic mechanisms that underpin metabolic and cardiovascular diseases

Gluckman, Peter D., Hanson, Mark A., Buklijas, Tatjana, Low, Felicia M., Beedle, Alan S.·2009·Nature Reviews Endocrinology

DOI 10.1038/nrendo.2009.102

Open this paper in CoChat — free account

Abstract

Cellular commitment to a specific lineage is controlled by differential silencing of genes, which in turn depends on epigenetic processes such as DNA methylation and histone modification. During early embryogenesis, the mammalian genome is 'wiped clean' of most epigenetic modifications, which are progressively re-established during embryonic development. Thus, the epigenome of each mature cellular lineage carries the record of its developmental history. The subsequent trajectory and pattern of development are also responsive to environmental influences, and such plasticity is likely to have an epigenetic basis. Epigenetic marks may be transmitted across generations, either directly by persisting through meiosis or indirectly through replication in the next generation of the conditions in which the epigenetic change occurred. Developmental plasticity evolved to match an organism to its environment, and a mismatch between the phenotypic outcome of adaptive plasticity and the current environment increases the risk of metabolic and cardiovascular disease. These considerations point to epigenetic processes as a key mechanism that underpins the developmental origins of chronic noncommunicable disease. Here, we review the evidence that environmental influences during mammalian development lead to stable changes in the epigenome that alter the individual's susceptibility to chronic metabolic and cardiovascular disease, and discuss the clinical implications.

Integrity signals

Registry

Crossref · 10.1038/nrendo.2009.102

Cites

94 of 94 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls
The Wellcome Trust Case Control Consortium, Management Committee, Burton, P. R., Clayton, D. G., Cardon, L. R., Craddock, N., Deloukas, P., Duncanson, A., Kwiatkowski, D. P., McCarthy, M. I., et al. (2007) · Nature · doi:10.1038/nature05911 · Cited by 9,442
Epigenetic programming by maternal behavior
Weaver, I. C. G., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., Dymov, S., Szyf, M., & Meaney, M. J. (2004) · Nature Neuroscience · doi:10.1038/nn1276 · Cited by 6,177
Developmental Plasticity and Evolution
West-Eberhard, M. J. (2003) · doi:10.1093/oso/9780195122343.001.0001 · Cited by 6,115
Epigenetic differences arise during the lifetime of monozygotic twins
Fraga, M. F., Ballestar, E., Paz, M. F., Ropero, S., Setien, F., Ballestar, M. L., Heine-Suñer, D., Cigudosa, J. C., Urioste, M., Benitez, J., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500398102 · Cited by 3,602
Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis
Hales, C. N., & Barker, D. J. P. (1992) · Diabetologia · doi:10.1007/bf00400248 · Cited by 3,294
Persistent epigenetic differences associated with prenatal exposure to famine in humans
Heijmans, B. T., Tobi, E. W., Stein, A. D., Putter, H., Blauw, G. J., Susser, E. S., Slagboom, P. E., & Lumey, L. H. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806560105 · Cited by 3,082
The Wellcome Trust Case Control Consortium, U.K.
Mossman, K. (2008) · Scientific American · doi:10.1038/scientificamerican0108-42a · Cited by 2,714
Genome-scale DNA methylation maps of pluripotent and differentiated cells
Meissner, A., Mikkelsen, T. S., Gu, H., Wernig, M., Hanna, J., Sivachenko, A., Zhang, X., Bernstein, B. E., Nusbaum, C., Jaffe, D. B., et al. (2008) · Nature · doi:10.1038/nature07107 · Cited by 2,536
Epigenetics: A landscape takes shape
Goldberg, A. D., Allis, C. D., & Bernstein, E. (2007) · Cell · doi:10.1016/j.cell.2007.02.006 · Cited by 2,466
Metabolic Syndrome in Childhood: Association With Birth Weight, Maternal Obesity, and Gestational Diabetes Mellitus
Boney, C. M., Verma, A., Tucker, R., & Vohr, B. R. (2005) · Pediatrics · doi:10.1542/peds.2004-1808 · Cited by 2,303
Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome
Weber, M., Hellmann, I., Stadler, M. B., Ramos, L., Pääbo, S., Rebhan, M., & Schübeler, D. (2007) · Nature Genetics · doi:10.1038/ng1990 · Cited by 2,297
Stability and flexibility of epigenetic gene regulation in mammalian development
Reik, W. (2007) · Nature · doi:10.1038/nature05918 · Cited by 1,963 · cited 1×
“In general, DNA methylation seems to be involved in long-term silencing of gene expression, whereas histone modifications have a short-term and flexible effect, but substantial crosstalk exists between these different mechanisms”
Background
The Strategy of the Genes: A Discussion of Some Aspects of Theoretical Biology
(1958) · The Medical Journal of Australia · doi:10.5694/j.1326-5377.1958.tb86500.x · Cited by 1,238
Dietary Protein Restriction of Pregnant Rats Induces and Folic Acid Supplementation Prevents Epigenetic Modification of Hepatic Gene Expression in the Offspring
Lillycrop, K. A., Phillips, E. S., Jackson, A. A., Hanson, M. A., & Burdge, G. C. (2005) · Journal of Nutrition · doi:10.1093/jn/135.6.1382 · Cited by 1,139
Self-citation
Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia
El-Osta, A., Brasacchio, D., Yao, D., Pocai, A., Jones, P. L., Roeder, R. G., Cooper, M. E., & Brownlee, M. (2008) · The Journal of Experimental Medicine · doi:10.1084/jem.20081188 · Cited by 1,115
Early life events and their consequences for later disease: a life history and evolutionary perspective
Gluckman, P. D., Hanson, M. A., & Beedle, A. S. (2007) · American Journal of Human Biology · doi:10.1002/ajhb.20590 · Cited by 1,006
Self-citation
Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition
Vickers, M. H., Breier, B. H., Cutfield, W. S., Hofman, P. L., & Gluckman, P. D. (2000) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2000.279.1.e83 · Cited by 999
Self-citation
Maternal Genistein Alters Coat Color and Protects Avy Mouse Offspring from Obesity by Modifying the Fetal Epigenome
Dolinoy, D. C., Weidman, J. R., Waterland, R. A., & Jirtle, R. L. (2006) · Environmental Health Perspectives · doi:10.1289/ehp.8700 · Cited by 943
RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse
Rassoulzadegan, M., Grandjean, V., Gounon, P., Vincent, S. D., Gillot, I., & Cuzin, F. (2006) · Nature · doi:10.1038/nature04674 · Cited by 940
Clinical risk factors, DNA variants, and the development of type 2 diabetes
Lyssenko, V., Jonsson, A., Almgren, P., Pulizzi, N., Isomaa, B., Tuomi, T., Berglund, G., Altshuler, D., Nilsson, P., & Groop, L. (2008) · New England Journal of Medicine · doi:10.1056/nejmoa0801869 · Cited by 938
Early growth and death from cardiovascular disease in women.
Osmond, C., BARKER, D. J. P., Winter, P. D., Fall, C. H. D., & Simmonds, S. J. (1993) · BMJ · doi:10.1136/bmj.307.6918.1519 · Cited by 821
DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status
Sinclair, K. D., Allegrucci, C., Singh, R., Gardner, D. S., Sebastian, S., Bispham, J., Thurston, A., Huntley, J. F., Rees, W. D., Maloney, C. A., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707258104 · Cited by 812
Early nutrition, epigenetic changes at transposons and imprinted genes, and enhanced susceptibility to adult chronic diseases
Waterland, R. A., & Jirtle, R. L. (2003) · Nutrition · doi:10.1016/j.nut.2003.09.011 · Cited by 790
Vitamin B12 and folate concentrations during pregnancy and insulin resistance in the offspring: the Pune Maternal Nutrition Study
Yajnik, C. S., Deshpande, S. S., Jackson, A. A., Refsum, H., Rao, S., Fisher, D. J., Bhat, D., Naik, S. S., Coyaji, K., Joglekar, C. V., et al. (2007) · Diabetologia · doi:10.1007/s00125-007-0793-y · Cited by 789
Prenatal exposure to the Dutch famine and disease in later life: An overview
Painter, R. C., Roseboom, T. J., & Bleker, O. P. (2005) · Reproductive Toxicology · doi:10.1016/j.reprotox.2005.04.005 · Cited by 784
Genotype score in addition to common risk factors for prediction of type 2 diabetes
Meigs, J. B., Shrader, P., Sullivan, L. M., McAteer, J. B., Fox, C. S., Dupuis, J., Manning, A. K., Florez, J. C., Wilson, P. W. F., D'Agostino, R. B., et al. (2008) · New England Journal of Medicine · doi:10.1056/nejmoa0804742 · Cited by 759 · cited 1×
“First, although genomic information has added little to clinical risk factors in the prediction of the onset of type 2 diabetes mellitus”
Background
Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life
Painter, R., Osmond, C., Gluckman, P., Hanson, M., Phillips, D., & Roseboom, T. (2008) · BJOG: An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2008.01822.x · Cited by 733
Self-citation
Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis
Hales, C., & Barker, D. (2013) · International Journal of Epidemiology · doi:10.1093/ije/dyt133 · Cited by 711
Neonatal anthropometry: the thin–fat Indian baby. The Pune Maternal Nutrition Study
Yajnik, C. S., Fall, C. H. D., Coyaji, K., Hirve, S. S., Rao, S. R., Barker, D. J. P., Joglekar, C. V., & Kellingray, S. (2003) · International Journal of Obesity · doi:10.1038/sj.ijo.802219 · Cited by 709
Transgenerational inheritance of epigenetic states at the murine Axin Fu allele occurs after maternal and paternal transmission
Rakyan, V. K., Chong, S., Blewitt, M. E., Cuthbert, P. C., Morgan, H. D., Luu, K. V. K., & Whitelaw, E. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0436776100 · Cited by 642
Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1
Park, J. H., Stoffers, D. A., Nicholls, R. D., & Simmons, R. A. (2008) · Journal of Clinical Investigation · doi:10.1172/jci33655 · Cited by 640
Neonatal Leptin Treatment Reverses Developmental Programming
Vickers, M. H., Gluckman, P. D., Coveny, A. H., Hofman, P. L., Cutfield, W. S., Gertler, A., Breier, B. H., & Harris, M. A. (2005) · Endocrinology · doi:10.1210/en.2005-0581 · Cited by 616
Self-citation
Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications
Lillycrop, K. A., Slater-Jefferies, J. L., Hanson, M. A., Godfrey, K. M., Jackson, A. A., & Burdge, G. C. (2007) · British Journal Of Nutrition · doi:10.1017/s000711450769196x · Cited by 569
Self-citation
Epigenetic Regulation of Foxp3 Expression in Regulatory T Cells by DNA Methylation
Lal, G., Zhang, N., van der Touw, W., Ding, Y., Ju, W., Böttinger, E. P., Reid, S. P., Levy, D. E., & Bromberg, J. S. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.182.1.259 · Cited by 564
Noncoding RNA in development
Amaral, P., & Mattick, J. S. (2008) · Mammalian Genome · doi:10.1007/s00335-008-9136-7 · Cited by 492
Early Life Origins of Insulin Resistance and Type 2 Diabetes in India and Other Asian Countries
Yajnik, C. S. (2004) · Journal of Nutrition · doi:10.1093/jn/134.1.205 · Cited by 491
Epigenetic Modification of the Renin-Angiotensin System in the Fetal Programming of Hypertension
Bogdarina, I. G., Welham, S. J. M., King, P., BURNS, S. P., & Clark, A. J. L. (2007) · Circulation Research · doi:10.1161/01.res.0000258855.60637.58 · Cited by 486
Maternal methyl supplements increase offspring DNA methylation at Axin fused
Waterland, R. A., Dolinoy, D. C., Lin, J., Smith, C. A., Shi, X., & Tahiliani, K. G. (2006) · genesis · doi:10.1002/dvg.20230 · Cited by 480
Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPARα promoter of the offspring
Lillycrop, K. A., Phillips, E. S., Torrens, C., Hanson, M. A., Jackson, A. A., & Burdge, G. C. (2008) · British Journal Of Nutrition · doi:10.1017/s0007114507894438 · Cited by 466
Self-citation
Developmental origins of disease and determinants of chromatin structure: maternal diet modifies the primate fetal epigenome
Aagaard-Tillery, K. M., Grove, K. L., Bishop, J. M., Ke, X., Fu, Q., McKnight, R. A., & Lane, R. H. (2008) · Journal of Molecular Endocrinology · doi:10.1677/jme-08-0025 · Cited by 449
Dietary protein restriction of pregnant rats in the F 0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F 1 and F 2 generations
Burdge, G. C., Slater-Jefferies, J. L., Torrens, C., Phillips, E. S., Hanson, M. A., & Lillycrop, K. A. (2007) · British Journal Of Nutrition · doi:10.1017/s0007114507352392 · Cited by 431
Self-citation
Methyl donor supplementation prevents transgenerational amplification of obesity
Waterland, R. A., Travisano, M., Tahiliani, K. G., Rached, M.-T., & Mirza, S. (2008) · International Journal of Obesity · doi:10.1038/ijo.2008.100 · Cited by 418
Epigenetic histone H3 lysine 9 methylation in metabolic memory and inflammatory phenotype of vascular smooth muscle cells in diabetes
Villeneuve, L. M., Reddy, M. A., Lanting, L. L., Wang, M., Li, M., & Natarajan, R. D. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803623105 · Cited by 411
Early evidence of ethnic differences in cardiovascular risk: cross sectional comparison of British South Asian and white children
Whincup, P. H. (2002) · BMJ · doi:10.1136/bmj.324.7338.635 · Cited by 410
Inheritance of a Cancer-Associated MLH1 Germ-Line Epimutation
Hitchins, M. P., Wong, J. J. L., Suthers, G., Suter, C. M., Martin, D. I. K., Hawkins, N. J., & Ward, R. L. (2007) · New England Journal of Medicine · doi:10.1056/nejmoa064522 · Cited by 409
Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats
Drake, A. J., Walker, B. R., & Seckl, J. R. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00106.2004 · Cited by 407
Non‐genomic transgenerational inheritance of disease risk
Gluckman, P. D., Hanson, M. A., & Beedle, A. S. (2007) · BioEssays · doi:10.1002/bies.20522 · Cited by 384
Self-citation
Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5
Ng, R. K., Dean, W., Dawson, C., Lucifero, D., Madeja, Z. E., Reik, W., & Hemberger, M. (2008) · Nature Cell Biology · doi:10.1038/ncb1786 · Cited by 374
Global Mapping of DNA Methylation in Mouse Promoters Reveals Epigenetic Reprogramming of Pluripotency Genes
Farthing, C. R., Ficz, G., Ng, R. K., Chan, C.-F., Andrews, S., Dean, W., Hemberger, M., & Reik, W. (2008) · PLoS Genetics · doi:10.1371/journal.pgen.1000116 · Cited by 365
Post-weaning diet affects genomic imprinting at the insulin-like growth factor 2 (Igf2) locus
Waterland, R. A., Lin, J.-R., Smith, C. A., & Jirtle, R. L. (2006) · Human Molecular Genetics · doi:10.1093/hmg/ddi484 · Cited by 341
Maternal constraint of fetal growth and its consequences
Gluckman, P. D., & Hanson, M. A. (2004) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2004.03.001 · Cited by 336
Self-citation
Discordant KCNQ1OT1 imprinting in sets of monozygotic twins discordant for Beckwith-Wiedemann syndrome
Weksberg, R. (2002) · Human Molecular Genetics · doi:10.1093/hmg/11.11.1317 · Cited by 329
Histone modifications: signalling receptors and potential elements of a heritable epigenetic code
Nightingale, K. P., O’Neill, L. P., & Turner, B. M. (2006) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2006.02.015 · Cited by 318
A review of known imprinting syndromes and their association with assisted reproduction technologies
Amor, D. J., & Halliday, J. L. (2008) · Human Reproduction · doi:10.1093/humrep/den310 · Cited by 311
Metabolic plasticity during mammalian development is directionally dependent on early nutritional status
Gluckman, P. D., Lillycrop, K. A., Vickers, M. H., Pleasants, A. B., Phillips, E. S., Beedle, A. S., Burdge, G. C., & Hanson, M. A. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705667104 · Cited by 309
Self-citation
Intergenerational Transmission of Glucose Intolerance and Obesity by In Utero Undernutrition in Mice
Jiménez‐Chillarón, J. C., ISGANAITIS, E. M., Charalambous, M., Gesta, S., Pentinat, T., Faucette, R., Otis, J. P., Chow, A., Díaz, R., Ferguson‐Smith, A. C., et al. (2008) · Diabetes · doi:10.2337/db08-0490 · Cited by 306
A common MYBPC3 (cardiac myosin binding protein C) variant associated with cardiomyopathies in South Asia
Dhandapany, P. S., Sadayappan, S., Xue, Y., Powell, G. T., Rani, D. S., Nallari, P., Singh, T., Khullar, M., Soares, P. A., Bahl, A., et al. (2009) · Nature Genetics · doi:10.1038/ng.309 · Cited by 286
Uteroplacental insufficiency increases apoptosis and alters p53 gene methylation in the full-term IUGR rat kidney
Pham, T. D., MacLennan, N. K., Chiu, C. T., Laksana, G. S., Hsu, J. L., & Lane, R. H. (2003) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00201.2003 · Cited by 280
Epidemiologic evidence for the fetal overnutrition hypothesis: findings from the mater-university study of pregnancy and its outcomes.
Lawlor, D., Smith, G., O'callaghan, M., Alati, R., Mamun, A. A., Williams, G., & Najman, J. (2006) · American Journal of Epidemiology · doi:10.1093/aje/kwk030 · Cited by 280
Histone Code Modifications Repress Glucose Transporter 4 Expression in the Intrauterine Growth-restricted Offspring
Raychaudhuri, N., Raychaudhuri, S., Thamotharan, M., & Devaskar, S. U. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m800128200 · Cited by 232
Metabolic reconfiguration is a regulated response to oxidative stress
Grant, C. M. (2008) · Journal of Biology · doi:10.1186/jbiol63 · Cited by 225
Review article: Epigenetic control of fetal gene expression
Nafee, T. M., Farrell, W., Carroll, W. D., Fryer, A. A., & Ismail, K. (2007) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2007.01528.x · Cited by 224
Birth Weight and Parental BMI Predict Overweight in Children From Mothers With Gestational Diabetes
Schaefer-Graf, U. M., Pawliczak, J., Passow, D., Hartmann, R., Rossi, R., Bührer, C., Harder, T., Plagemann, A., Vetter, K., & Kordonouri, O. (2005) · Diabetes Care · doi:10.2337/diacare.28.7.1745 · Cited by 219
Transgene silencing by the host genome defense: implications for the evolution of epigenetic control mechanisms in plants and vertebrates
Matzke, M. A., Mette, M. F., & Matzke, A. J. M. (2000) · Plant Molecular Biology · doi:10.1023/a:1006484806925 · Cited by 214
Developmental Origins of Health and Disease
Rass, E. (2017) · Routledge eBooks · doi:10.4324/9781315445564-6 · Cited by 200
Diet‐induced hypermethylation at agouti viable yellow is not inherited transgenerationally through the female
Waterland, R. A., Travisano, M., & Tahiliani, K. G. (2007) · The FASEB Journal · doi:10.1096/fj.07-8229com · Cited by 199
Genetic and epigenetic factors are associated with expression of respiratory chain component NDUFB6 in human skeletal muscle
Ling, C., Poulsen, P., Simonsson, S., Rönn, T., Holmkvist, J., Almgren, P., Hagert, P., Nilsson, E., Mabey, A. G., Nilsson, P. M., et al. (2007) · Journal of Clinical Investigation · doi:10.1172/jci30938 · Cited by 195
Low protein diet fed exclusively during mouse oocyte maturation leads to behavioural and cardiovascular abnormalities in offspring
Watkins, A. J., Wilkins, A., Cunningham, C. M., Perry, V. H., Seet, M. J., Osmond, C., Eckert, J. J., Torrens, C., Cagampang, F. R. A., Cleal, J. K., et al. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2007.149229 · Cited by 190
Self-citation
Age influences DNA methylation and gene expression of COX7A1 in human skeletal muscle.
Rönn, T., Poulsen, P., Hansson, O., Holmkvist, J., Almgren, P., Nilsson, P., Tuomi, T., Isomaa, B., Groop, L., Vaag, A., et al. (2008) · Diabetologia · doi:10.1007/s00125-008-1018-8 · Cited by 175
Impact of educational attainment on the quality of young women's diets
Robinson, S. M., Crozier, S., Borland, S. E., Hammond, J., Barker, D. J. P., & Inskip, H. M. (2004) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1601946 · Cited by 174
Parasympathetic response in chick myocytes and mouse heart is controlled by SREBP
Park, H., Georgescu, S. P., Du, C., Madias, C. A., Aronovitz, M. J., Welzig, C. M., Wang, B., Begley, U., Zhang, Y., Blaustein, R. O., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci32011 · Cited by 171
DNA methylation profile of tissue-dependent and differentially methylated regions (T-DMRs) in mouse promoter regions demonstrating tissue-specific gene expressionPreprint
Yagi, S., Hirabayashi, K., Sato, S., Li, W., Takahashi, Y., Hirakawa, T., Wu, G., Hattori, N., Hattori, N., Ohgane, J., et al. (2008) · Genome Research · doi:10.1101/gr.074070.107 · Cited by 162
Developmental Origins of Health and Disease: List of contributors
Gluckman, P., & Hanson, M. (2006) · Cambridge University Press eBooks · doi:10.1017/cbo9780511544699 · Cited by 142
Self-citation
Hypergonadotrophinaemia with reduced uterine and ovarian size in women born small-for-gestational-age
Ibáñez, L. (2003) · Human Reproduction · doi:10.1093/humrep/deg351 · Cited by 130
Tissue specific differentially methylated regions (TDMR): Changes in DNA methylation during development
Song, F., Mahmood, S., Ghosh, S., Liang, P., Smiraglia, D. J., Nagase, H., & Held, W. A. (2008) · Genomics · doi:10.1016/j.ygeno.2008.09.003 · Cited by 126
Lipid profiles in adolescent Filipinos: relation to birth weight and maternal energy status during pregnancy
Kuzawa, C. W., & Adair, L. S. (2003) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/77.4.960 · Cited by 126
Imprinted gene expression in the rat embryo–fetal axis is altered in response to periconceptional maternal low protein diet
Kwong, W. Y., Miller, D. J., Ursell, E., Wild, A. E., Wilkins, A., Osmond, C., Anthony, F. W., & Fleming, T. P. (2006) · Reproduction · doi:10.1530/rep.1.01038 · Cited by 123
Uteroplacental insufficiency induces site-specific changes in histone H3 covalent modifications and affects DNA-histone H3 positioning in day 0 IUGR rat liver.
Fu, Q., McKnight, R., Yu, X., Wang, L., Callaway, C., & Lane, R. (2004) · Physiological Genomics · doi:10.1152/physiolgenomics.00175.2004 · Cited by 120
Intrauterine Growth Retardation and Development of Endocrine Pancreas in the Experimental Rat
Prins, F. A. D., & Assche, F. A. V. (2009) · Biology of the Neonate · doi:10.1159/000241511 · Cited by 98
Hypermethylation of hepatic Gck promoter in ageing rats contributes to diabetogenic potential
Jiang, M., Fei, J., Lan, M. S., Lu, Z., Liu, M., Fan, W., Gao, X., & Lu, D. (2008) · Diabetologia · doi:10.1007/s00125-008-1034-8 · Cited by 87
The ‘developmental origins’ hypothesis: epidemiology
Godfrey, K. M. (2006) · Cambridge University Press eBooks · doi:10.1017/cbo9780511544699.003 · Cited by 86
Differential methylation of the X‐chromosome is a possible source of discordance for bipolar disorder female monozygotic twins
Rosa, A., Picchioni, M., Kalidindi, S., Loat, C. S., Knight, J., Toulopoulou, T., Vonk, R., van der Schot, A. C., Nolen, W. A., Kahn, R. S., et al. (2007) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30616 · Cited by 85
Analysis of Histones in Xenopus laevis
Shechter, D., Nicklay, J. J., Chitta, R. K., Shabanowitz, J., Hunt, D. F., & Allis, C. D. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m807273200 · Cited by 78
Safeguarding parental identity: Dnmt1 maintains imprints during epigenetic reprogramming in early embryogenesis: Figure 1.Preprint
Branco, M. R., Oda, M., & Reik, W. (2008) · Genes & Development · doi:10.1101/gad.1690508 · Cited by 72
Early Nutrition and Long-Term Cardiovascular Health
Singhal, A. (2006) · Nutrition Reviews · doi:10.1301/nr.2006.may.s44-s49 · Cited by 70
Origins of differentiation via phenotypic plasticity
Schlichting, C. D. (2002) · Evolution & Development · doi:10.1046/j.1525-142x.2003.03015.x · Cited by 68
Genomic imprinting in marsupial placentation
Renfree, M. B., Ager, E. I., Shaw, G., & Pask, A. J. (2008) · Reproduction · doi:10.1530/rep-08-0264 · Cited by 63
Maternal regulation of estrogen receptor α methylation
Champagne, F. A., & Curley, J. P. (2008) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2008.06.018 · Cited by 63
Metabolic Consequences of Obesity and Body Fat Pattern: Lessons from Migrant Studies
McKeigue, P. (2007) · Novartis Foundation symposium · doi:10.1002/9780470514962.ch4 · Cited by 62
X-chromosome inactivation: the molecular basis of silencing
Panning, B. (2008) · Journal of Biology · doi:10.1186/jbiol95 · Cited by 60
Analysis of Histones in Xenopus laevis
Nicklay, J. J., Shechter, D., Chitta, R. K., Garcia, B. A., Shabanowitz, J., Allis, C. D., & Hunt, D. F. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m807274200 · Cited by 46
Neurobiology of disease: new therapeutical perspectives
Annunziato, L., & Simon, R. P. (2008) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2007.12.014 · Cited by 39
Evolution, developmental plasticity, and metabolic disease
Kuzawa, C. W., Gluckman, P. D., Hanson, M. A., & Beedle, A. S. (2007) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199207466.003.0019 · Cited by 27
Self-citation
Untitled work
Leguizamon (2000) · doi:10.1002/(sici)1520-6661(200001/02)9:1

Sorted by citations

Epigenetics and the environment: emerging patterns and implications
Feil, R., & Fraga, M. F. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3142 · Cited by 1,929
Epigenetic Modifications
Handy, D. E., Castro, R., & Loscalzo, J. (2011) · Circulation · doi:10.1161/circulationaha.110.956839 · Cited by 1,123
Diabetes: a 21st century challenge
Zimmet, P. Z., Magliano, D. J., Herman, W. H., & Shaw, J. E. (2014) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(13)70112-8 · Cited by 1,062
Type 2 diabetes in East Asians: similarities and differences with populations in Europe and the United States
Ronald, C. W., & Chan, J. C. N. (2013) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12098 · Cited by 841
The importance of nutrition in pregnancy and lactation: lifelong consequences
Marshall, N. E., Abrams, B., Barbour, L. A., Catalano, P., Christian, P., Friedman, J. E., Hay, W. W., Hernandez, T. L., Krebs, N. F., Oken, E., et al. (2022) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2021.12.035 · Cited by 709

See all 629

Authors: Gluckman, P. D., Hanson, M. A., Buklijas, T., Low, F. M., & Beedle, A. S.
Affiliations: University of Auckland (NZ)
University of Southampton (GB)
Corresponding author: Gluckman, Peter D.
ORCID: Gluckman, Peter D.
Hanson, Mark A.
Low, Felicia M.
Venue: Nature Reviews Endocrinology
Publisher: Springer Science and Business Media LLC
Published: 2009-06-02
Volume: 5
Issue: 7
Pages: 401-408
ISSN: 1759-5029 (ISSN-L)
1759-5037
DOI: 10.1038/nrendo.2009.102
OpenAlex: W2134682046
Cited by: 627
References: 94
Citations by year: 2026: 14 · 2025: 14 · 2024: 13 · 2023: 26 · 2022: 29 · 2021: 31 · 2020: 37 · 2019: 38 · 2018: 41 · 2017: 43 · 2016: 42 · 2015: 44 · 2014: 49 · 2013: 57 · 2012: 43
FWCI: 6.59
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature Reviews Endocrinology (publishedVersion)
PubMed (publishedVersion)
ePrints Soton (University of Southampton) (submittedVersion)
ResearchSpace (University of Auckland) (submittedVersion)
Funders: British Heart Foundation
Topics: Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
Keywords: epigenetics, metabolic disorders, cardiovascular disease, developmental origins of health and disease, DNA methylation, histone modifications, developmental plasticity, transgenerational epigenetic inheritance, gene silencing, non-communicable diseases, disease prevention
MeSH terms: Animals, Cardiovascular Diseases, Humans, Metabolic Diseases, Epigenesis, Genetic

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

Epigenetic mechanisms that underpin metabolic and cardiovascular diseases

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks