Mechanisms involved in the developmental programming of adulthood disease

Warner, Matthew J.; Ozanne, Susan E.

doi:10.1042/bj20091861

Cited by 316Birth, Development, and HealthPrenatal Substance Exposure EffectsPregnancy and preeclampsia studies

Mechanisms involved in the developmental programming of adulthood disease

Warner, Matthew J., Ozanne, Susan E.·2010·Biochemical Journal

DOI 10.1042/bj20091861

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Abstract

There are many instances in life when the environment plays a critical role in the health outcomes of an individual, yet none more so than those experienced in fetal and neonatal life. One of the most detrimental environmental problems encountered during this critical growth period are changes in nutrition to the growing fetus and newborn. Disturbances in the supply of nutrients and oxygen to the fetus can not only lead to adverse fetal growth patterns, but they have also been associated with the development of features of metabolic syndrome in adult life. This fetal response has been termed developmental programming or the developmental origins of health and disease. The present review focuses on the epidemiological studies that identified this association and the importance that animal models have played in studying this concept. We also address the potential mechanisms that may underpin the developmental programming of future disease. It also highlights (i) how developmental plasticity, although beneficial for short-term survival, can subsequently programme glucose intolerance and insulin resistance in adult life by eliciting changes in key organ structures and the epigenome, and (ii) how aberrant mitochondrial function can potentially lead to the development of Type 2 diabetes and other features of metabolic syndrome.

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Perturbation of gene expression or cell proliferation and differentiation during vulnerable periods by nutritional and other environmental influences can alter the structure and functional capacity of major organ systems for life, a process known as developmental programming.
“Perturbation of gene expression or cell proliferation and differentiation during vulnerable periods by nutritional and other environmental influences can alter the structure and functional capacity of major organ systems for life, a process known as developmental programming.”
From Placental Origins of Chronic Disease (2016) · cites this paper as [565]
The end result of deficient remodeling will be altered development of the fetal organs, as seen in cases of severe maternal undernutrition.
“The end result will be altered development of the fetal organs, as seen in cases of severe maternal undernutrition (215, 374, 565).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [565]

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Placental Origins of Chronic Disease
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International Federation of Gynecology and Obstetrics opinion on reproductive health impacts of exposure to toxic environmental chemicals
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Nutrition, Epigenetics, and Metabolic Syndrome
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Placental adaptations to the maternal–fetal environment: implications for fetal growth and developmental programming
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Nutritionally Mediated Programming of the Developing Immune System
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Pre-eclampsia and offspring cardiovascular health: mechanistic insights from experimental studies
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Maternal methyl-donor supplementation induces prolonged murine offspring colitis susceptibility in association with mucosal epigenetic and microbiomic changes
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Programming of maternal and offspring disease: impact of growth restriction, fetal sex and transmission across generations
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DNA Methylation Patterns in Cord Blood DNA and Body Size in Childhood
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Methionine, homocysteine, one carbon metabolism and fetal growth
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Fetal Programming and the Risk of Noncommunicable Disease
Fall, C. H. D. (2012) · The Indian Journal of Pediatrics · doi:10.1007/s12098-012-0834-5 · Cited by 136 · see citing works
One carbon metabolism in pregnancy: Impact on maternal, fetal and neonatal health
Kalhan, S. C. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.06.006 · Cited by 135 · see citing works
An obesogenic diet during mouse pregnancy modifies maternal nutrient partitioning and the fetal growth trajectory
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Endocrine regulation of fetal skeletal muscle growth: impact on future metabolic health
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Fetal stress and programming of hypoxic/ischemic-sensitive phenotype in the neonatal brain: Mechanisms and possible interventions
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Rationale and cross-sectional study design of the Research on Obesity and type 2 Diabetes among African Migrants: the RODAM study
Agyemang, C. O., Beune, E., Meeks, K. A. C., Owusu‐Dabo, E., Agyei‐Baffour, P., Aikins, A. D., Dodoo, F., Smeeth, L. L., Addo, J., Mockenhaupt, F. P., et al. (2014) · BMJ Open · doi:10.1136/bmjopen-2014-004877 · Cited by 126 · see citing works
Evidence for the intra-uterine programming of adiposity in later life
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Gestational Diabetes Mellitus Impairs Nrf2-Mediated Adaptive Antioxidant Defenses and Redox Signaling in Fetal Endothelial Cells In Utero
Cheng, X., Chapple, S. J., Patel, B., Puszyk, W. M., Sugden, D., Yin, X., Mayr, M., Siow, R. C. M., & Mann, G. E. (2013) · Diabetes · doi:10.2337/db13-0169 · 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
Developmental Origins of Health and Disease – from a small body size at birth to epigenetics
Eriksson, J. G. (2016) · Annals of Medicine · doi:10.1080/07853890.2016.1193786 · Cited by 115 · see citing works
MATERNAL DEPRESSIVE, ANXIOUS, AND STRESS SYMPTOMS DURING PREGNANCY PREDICT INTERNALIZING PROBLEMS IN ADOLESCENCE
Betts, K. S., Williams, G. M., Najman, J. M., & Alati, R. (2013) · Depression and Anxiety · doi:10.1002/da.22210 · Cited by 114 · see citing works
Maternal exposure to di-(2-ethylhexyl)phthalate alters kidney development through the renin–angiotensin system in offspring
Wei, Z., Song, L., Wei, J., Chen, T. X., Chen, J., Lin, Y., Xia, W., Xu, B., Li, X., Chen, X., et al. (2012) · Toxicology Letters · doi:10.1016/j.toxlet.2012.05.023 · Cited by 110 · see citing works
Maternal antenatal multiple micronutrient supplementation for long-term health benefits in children: a systematic review and meta-analysis
Devakumar, D., Fall, C. H. D., Sachdev, H. S., Margetts, B., Osmond, C., Wells, J. C. K., Costello, A. M. D. L., & Osrin, D. (2016) · BMC Medicine · doi:10.1186/s12916-016-0633-3 · Cited by 111 · see citing works
Fetal Malnutrition and Long-Term Outcomes
Fall, C. H. D. (2013) · Nestlé Nutrition Institute Workshop series · doi:10.1159/000348384 · Cited by 110 · see citing works
Maternal Periconceptional and Gestational Low Protein Diet Affects Mouse Offspring Growth, Cardiovascular and Adipose Phenotype at 1 Year of Age
Watkins, A. J., Lucas, E. S., Wilkins, A., Cagampang, F. R. A., & Fleming, T. P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028745 · Cited by 108 · see citing works
Evidence for transgenerational metabolic programming inDrosophila
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Risk of metabolic syndrome in adults exposed to the great Chinese famine during the fetal life and early childhood
Zheng, X., Wang, Y., Ren, W., Luo, R., Zhang, S., Zhang, J. H., & Zeng, Q. (2011) · European Journal of Clinical Nutrition · doi:10.1038/ejcn.2011.161 · Cited by 103 · see citing works
Zinc restriction during different periods of life: Influence in renal and cardiovascular diseases
Tomat, A. L., Costa, M. A., & Arranz, C. T. (2010) · Nutrition · doi:10.1016/j.nut.2010.09.010 · Cited by 101 · see citing works
Models of stress in nonhuman primates and their relevance for human psychopathology and endocrine dysfunction
Meyer, J. S., & Hamel, A. F. (2014) · ILAR Journal · doi:10.1093/ilar/ilu023 · Cited by 96 · see citing works
Metabolic Programming in the Immediate Postnatal Life
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Mechanisms underlying the developmental origins of disease
Martin‐Gronert, M. S., & Ozanne, S. E. (2012) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-012-9210-z · Cited by 95 · see citing works
Self-citation
Increased Intake of Foods with High Nutrient Density Can Help to Break the Intergenerational Cycle of Malnutrition and Obesity
Troesch, B., Biesalski, H. K., Bos, R., Buskens, E., Calder, P. C., Saris, W. H. M., Spieldenner, J., Verkade, H. J., Weber, P., & Eggersdorfer, M. L. (2015) · Nutrients · doi:10.3390/nu7075266 · Cited by 90 · see citing works
Exposure to the Chinese Famine in Childhood Increases Type 2 Diabetes Risk in Adults
Wang, J., Li, Y., Han, X., Liu, B., Hu, H., Wang, F., Li, X., YANG, K. Y., Yuan, J., Yao, P., et al. (2016) · Journal of Nutrition · doi:10.3945/jn.116.234575 · Cited by 89 · see citing works
Social determinants of health for Native Hawaiian children and adolescents.
Liu, D. M. K. I., & Alameda, C. K. (2011) · PubMed Central · Cited by 88 · see citing works
Preimplantation Exposure of Mouse Embryos to Palmitic Acid Results in Fetal Growth Restriction Followed by Catch-Up Growth in the Offspring1
Jungheim, E. S., Louden, E. D., Chi, M. M.-Y., Frolova, A. I., Riley, J. K., & Moley, K. H. (2011) · Biology of Reproduction · doi:10.1095/biolreprod.111.092148 · Cited by 86 · see citing works
Analgesic exposure in pregnant rats affects fetal germ cell development with inter-generational reproductive consequences
Dean, A., van den Driesche, S., Wang, Y., McKinnell, C., Macpherson, S., Eddie, S. L., Kinnell, H. L., Hurtado-Gonzalez, P., Chambers, T. J. G., Stevenson, K., et al. (2016) · Scientific Reports · doi:10.1038/srep19789 · Cited by 86 · 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
Metabolic and Genomic Response to Dietary Isocaloric Protein Restriction in the Rat
Kalhan, S. C., Uppal, S. O., Moorman, J. L., Bennett, C. D., Gruca, L. L., Parimi, P. S., Dasarathy, S., Serre, D., & Hanson, R. W. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.185991 · Cited by 80 · see citing works
Maternal obesity in the rat programs male offspring exploratory, learning and motivation behavior: prevention by dietary intervention pre‐gestation or in gestation
Rodriguez, J. S., Rodríguez‐González, G. L., Reyes‐Castro, L. A., Ibáñez, C., Ramírez, A., Chavira, R., Larrea, F., Nathanielsz, P. W., & Zambrano, E. (2012) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2011.12.012 · Cited by 77 · see citing works
Maternal obesity has little effect on the immediate offspring but impacts on the next generation.
King, V., Dakin, R., Liu, L., Hadoke, P., Walker, B., Seckl, J., Norman, J., & Drake, A. (2013) · Endocrinology · doi:10.1210/en.2013-1013 · Cited by 82 · see citing works
Preadult Parental Diet Affects Offspring Development and Metabolism in Drosophila melanogaster
Matzkin, L. M., Johnson, S., Paight, C., & Markow, T. A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0059530 · Cited by 76 · see citing works
Acute supplementation of amino acids increases net protein accretion in IUGR fetal sheep
Brown, L. D., Rozance, P. J., Wesolowski, S. R., Friedman, J. E., & Hay, W. W. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00059.2012 · Cited by 75 · see citing works
Stress, glucocorticoids and liquorice in human pregnancy: Programmers of the offspring brain
Räikkönen, K., Seckl, J. R., Pesonen, A., Simons, A., & den Bergh, B. R. H. V. (2011) · Stress · doi:10.3109/10253890.2011.602147 · Cited by 70 · 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
The Olfactory Receptor OR51E1 Is Present along the Gastrointestinal Tract of Pigs, Co-Localizes with Enteroendocrine Cells and Is Modulated by Intestinal Microbiota
Priori, D., Colombo, M., Clavenzani, P., Jansman, A. J. M., Lallès, J.-P., Trevisi, P., & Bosi, P. (2015) · PLOS ONE · doi:10.1371/journal.pone.0129501 · Cited by 66 · see citing works
Birth Weight, Postnatal Weight Change, and Risk for High Blood Pressure Among Chinese Children
Bowers, K. A., Liu, G., Wang, P., Ye, T., Tian, Z., Liu, E., Yu, Z., Yang, X., Klebanoff, M. A., Yeung, E. H., et al. (2011) · PEDIATRICS · doi:10.1542/peds.2010-2213 · Cited by 65 · see citing works
Guthrie card methylomics identifies temporally stable epialleles that are present at birth in humansPreprint
Beyan, H., Down, T. A., Ramagopalan, S. V., Uvebrant, K., Nilsson, A., Holland, M. L., Gemma, C., Giovannoni, G., Boehm, B. O., Ebers, G. C., et al. (2012) · Genome Research · doi:10.1101/gr.134304.111 · Cited by 64 · see citing works
Prenatal Exposure to BPA and Offspring Outcomes
Alonso‐Magdalena, P., Quesada, I., & Nadal, Á. (2015) · Dose-Response · doi:10.1177/1559325815590395 · Cited by 61 · see citing works
Paternal treadmill exercise enhances spatial learning and memory related to hippocampus among male offspring
Yin, M. M., Wang, W., Sun, J., Liu, S., Liu, X. L., Niu, Y., Yuan, H., Yang, F., & Fu, L. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.07.040 · Cited by 61 · see citing works
Effects of paternal obesity on growth and adiposity of male rat offspring
Lecomte, V., Maloney, C., Wang, K. W., & Morris, M. J. (2016) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00262.2016 · Cited by 59 · see citing works
Long term effects of pre- and early postnatal nutrition and environment on the gut1
Lallès, J. P. (2012) · Journal of Animal Science · doi:10.2527/jas.53904 · Cited by 58 · see citing works
Disorders of placental villous maturation in fetal death
Jaiman, S., Romero, R. J., Pacora, P., Jung, E., Bhatti, G., Yeo, L., Kim, Y. M., Kim, B., Kim, C. J., Kim, J.-S., et al. (2020) · Journal of Perinatal Medicine · doi:10.1515/jpm-2020-0030 · Cited by 57 · see citing works
Maternal and post-weaning high-fat, high-sucrose diet modulates glucose homeostasis and hypothalamic POMC promoter methylation in mouse offspring
Zheng, J., Xiao, X., Zhang, Q., Yu, M., Xu, J., Wang, Z., Qi, C., & Wang, T. (2015) · Metabolic Brain Disease · doi:10.1007/s11011-015-9678-9 · Cited by 56 · see citing works
Early Changes in Microbial Colonization Selectively Modulate Intestinal Enzymes, but Not Inducible Heat Shock Proteins in Young Adult Swine
Arnal, M.-É., Zhang, J., Messori, S., Bosi, P., Smidt, H., & Lallès, J. P. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087967 · Cited by 56 · see citing works
Developmental programming of adult obesity and cardiovascular disease in rodents by maternal nutrition imbalance
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Exercise during pregnancy protects adult mouse offspring from diet-induced obesity
Wasinski, F., Bacurau, R. F. P., Estrela, G. R., Klempin, F., Arakaki, A. M., Batista, R. O., Mafra, F. F. P., do Nascimento, L. F. R., Hiyane, M. I., Velloso, L. A., et al. (2015) · Nutrition & Metabolism · doi:10.1186/s12986-015-0052-z · Cited by 54 · see citing works
Developmental programming of neonatal pancreatic β-cells by a maternal low-protein diet in rats involves a switch from proliferation to differentiation
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Authors: Warner, M. J., & Ozanne, S. E.
Affiliations: University of Cambridge (GB)
ORCID: Ozanne, Susan E.
Venue: Biochemical Journal
Publisher: Portland Press Ltd.
Published: 2010-04-14
Volume: 427
Issue: 3
Pages: 333-347
ISSN: 0264-6021 (ISSN-L)
1470-8728
DOI: 10.1042/bj20091861
OpenAlex: W1983684926
Cited by: 316
References: 226
Citations by year: 2025: 3 · 2024: 5 · 2023: 18 · 2022: 14 · 2021: 13 · 2020: 23 · 2019: 14 · 2018: 13 · 2017: 15 · 2016: 27 · 2015: 30 · 2014: 21 · 2013: 39 · 2012: 37
FWCI: 5.63
Type: journal article
Language: en
Open access: closed
Locations: Biochemical Journal (publishedVersion)
PubMed (publishedVersion)
Funders: British Heart Foundation (FS/09/029/27902)
Biotechnology and Biological Sciences Research Council (BB/F015364/1, BB/E00797X/1)
Topics: Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Keywords: developmental programming, developmental origins of health and disease, fetal nutrition, neonatal nutrition, metabolic syndrome, developmental plasticity, insulin resistance, impaired glucose tolerance, epigenome, mitochondrial dysfunction, type 2 diabetes, fetal growth restriction, animal models
MeSH terms: Adult, Animals, Diabetes Mellitus, Type 2, Disease Models, Animal, Female, Humans, Male, Models, Biological, Pregnancy, Prenatal Exposure Delayed Effects, Metabolic Syndrome, Prenatal Nutritional Physiological Phenomena, Fetal Development

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Mechanisms involved in the developmental programming of adulthood disease

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