Molecular mechanisms governing offspring metabolic programming in rodent models of in utero stress
Open accessAbstract
The results of different human epidemiological datasets provided the impetus to introduce the now commonly accepted theory coined as ‘developmental programming’, whereby the presence of a stressor during gestation predisposes the growing fetus to develop diseases, such as metabolic dysfunction in later postnatal life. However, in a clinical setting, human lifespan and inaccessibility to tissue for analysis are major limitations to study the molecular mechanisms governing developmental programming. Subsequently, studies using animal models have proved indispensable to the identification of key molecular pathways and epigenetic mechanisms that are dysregulated in metabolic organs of the fetus and adult programmed due to an adverse gestational environment. Rodents such as mice and rats are the most used experimental animals in the study of developmental programming. This review summarises the molecular pathways and epigenetic mechanisms influencing alterations in metabolic tissues of rodent offspring exposed to in utero stress and subsequently programmed for metabolic dysfunction. By comparing molecular mechanisms in a variety of rodent models of in utero stress, we hope to summarise common themes and pathways governing later metabolic dysfunction in the offspring whilst identifying reasons for incongruencies between models so to inform future work. With the continued use and refinement of such models of developmental programming, the scientific community may gain the knowledge required for the targeted treatment of metabolic diseases that have intrauterine origins.
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Exposure to a diverse array of suboptimal maternal environments, including nutritionally unbalanced diets, low oxygen availability, and high body mass index (BMI) during gestation, modifies the risk of the offspring developing obesity.
“Extensions of this work using human population and experimental animal data have shown that exposure to a diverse array of suboptimal maternal environments, including nutritionally unbalanced diets, low oxygen availability, and high body mass index (BMI) during gestation, modifies the risk of the offspring developing obesity [9, 10].”
From Developmental programming of offspring adipose tissue biology and obesity risk (2021) · cites this paper as [10]
The ‘Adipose lipid metabolism and morphology’ section links maternal undernutrition, protein restriction and high-fat diets to increased offspring body adiposity. The ‘Rodent models of developmental programming’ and ‘Alterations in DNA methylation in response to in utero stressors’ sections also discuss maternal obesity and gestational hypoxia, but link them to offspring metabolic disease or metabolic syndrome rather than specifically to obesity risk. The source therefore supports the broader metabolic-programming claim, but not the obesity-specific outcome for every exposure listed. (LLM, conf=0.84)
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Cites
Histone methylation: a dynamic mark in health, disease and inheritance
Greer, E. L., & Shi, Y. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3173 · Cited by 2,241 · see citing works
Pathogenesis of type 2 diabetes mellitus
DeFronzo, R. A. (2004) · Medical Clinics of North America · doi:10.1016/j.mcna.2004.04.013 · Cited by 1,342 · see citing works
Circulating microRNAs as novel biomarkers for diabetes mellitus
Guay, C., & Regazzi, R. (2013) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2013.86 · Cited by 563 · see citing works
Orchestrating liver development
Gordillo, M., Evans, T., & Gouon-Evans, V. (2015) · Development · doi:10.1242/dev.114215 · Cited by 375 · see citing works
Taylor, P. D., McConnell, J., Khan, I. Y., Holemans, K., Lawrence, K. M., Asare-Anane, H., Persaud, S. J., Jones, P. M., Petrie, L., Hanson, M. A., et al. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00355.2004 · Cited by 297 · see citing works
Daddy Issues: Paternal Effects on Phenotype
Rando, O. J. (2012) · Cell · doi:10.1016/j.cell.2012.10.020 · Cited by 292 · see citing works
Humans at high altitude: Hypoxia and fetal growth
Moore, L. G., Charles, S. M., & Julian, C. G. (2011) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2011.04.017 · Cited by 251 · see citing works
Lee, H.-S. (2015) · Nutrients · doi:10.3390/nu7115467 · Cited by 236 · see citing works
The Programming Power of the Placenta
Sferruzzi-Perri, A. N., & Camm, E. J. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00033 · Cited by 223 · see citing works
Self-citationReynolds, L. P., Borowicz, P. P., Caton, J. S., Vonnahme, K. A., Luther, J. S., Hammer, C. J., Maddock Carlin, K. R., Grazul-Bilska, A. T., & Redmer, D. A. (2010) · Journal of Animal Science · doi:10.2527/jas.2009-2359 · Cited by 191 · see citing works
Agarwal, P., Brar, N., Morriseau, T. S., Kereliuk, S. M., Fonseca, M. A., Cole, L. K., Jha, A., Xiang, B., Hunt, K. L., Seshadri, N., et al. (2019) · Endocrinology · doi:10.1210/en.2019-00232 · Cited by 34 · see citing works
Mark, P. J., Wyrwoll, C. S., Zulkafli, I. S., Mori, T. A., & Waddell, B. J. (2014) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-12-39 · Cited by 19 · see citing works
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Research works printed but not linked: 276
- [1]Alberti KG, Zimmet PZ (1998) Definition, diagnosis and classification of diabetes mellitus and its complications Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med 15(7):539–553. 10.1002/(sici)1096-9136(199807)15:7<539::Aid-dia668>3.0.Co;2-s 9686693 · DOI
- [2]Saklayen MG The global epidemic of the metabolic syndrome Curr Hypertens Rep 2018 20 2 12 10.1007/s11906-018-0812-z 29480368 PMC5866840 · DOI · Paper page
- [3]O'Neill S O'Driscoll L Metabolic syndrome: a closer look at the growing epidemic and its associated pathologies Obes Rev 2015 16 1 1 12 10.1111/obr.12229 25407540 · DOI
- [4]Kolb H Martin S Environmental/lifestyle factors in the pathogenesis and prevention of type 2 diabetes BMC Med 2017 15 1 131 10.1186/s12916-017-0901-x 28720102 PMC5516328 · DOI
- [5]Povel CM Boer JM Reiling E Feskens EJ Genetic variants and the metabolic syndrome: a systematic review Obes Rev 2011 12 11 952 967 10.1111/j.1467-789X.2011.00907.x 21749608 · DOI
- [6]Pollex RL Hegele RA Genetic determinants of the metabolic syndrome Nat Clin Pract Cardiovasc Med 2006 3 9 482 489 10.1038/ncpcardio0638 16932765 · DOI
- [7]Barouki R Gluckman PD Grandjean P Hanson M Heindel JJ Developmental origins of non-communicable disease: implications for research and public health Environ Health 2012 11 42 10.1186/1476-069x-11-42 22715989 PMC3384466 · DOI
- [8]Hoffman DJ Reynolds RM Hardy DB Developmental origins of health and disease: current knowledge and potential mechanisms Nutr Rev 2017 75 12 951 970 10.1093/nutrit/nux053 29186623 · DOI
- [10]Wadhwa PD Buss C Entringer S Swanson JM Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms Semin Reprod Med 2009 27 5 358 368 10.1055/s-0029-1237424 19711246 PMC2862635 · DOI
- [11]Barker DJ Osmond C Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales Lancet 1986 1 8489 1077 1081 10.1016/S0140-6736(86)91340-1 2871345 · DOI · Paper page
- [12]Hales CN Barker DJ Clark PM Cox LJ Fall C Osmond C Winter PD Fetal and infant growth and impaired glucose tolerance at age 64 BMJ 1991 303 6809 1019 1022 10.1136/bmj.303.6809.1019 1954451 PMC1671766 · DOI · Paper page
- [13]Tan HC Roberts J Catov J Krishnamurthy R Shypailo R Bacha F Mother's pre-pregnancy BMI is an important determinant of adverse cardiometabolic risk in childhood Pediatr Diabetes 2015 16 6 419 426 10.1111/pedi.12273 25800542 PMC4534350 · DOI · Paper page
- [14]Plagemann A Harder T Kohlhoff R Rohde W Dorner G Glucose tolerance and insulin secretion in children of mothers with pregestational IDDM or gestational diabetes Diabetologia 1997 40 9 1094 1100 10.1007/s001250050792 9300247 · DOI
- [15]Fuglestad AJ Boys CJ Chang PN Miller BS Eckerle JK Deling L Fink BA Hoecker HL Hickey MK Jimenez-Vega JM Wozniak JR Overweight and obesity among children and adolescents with fetal alcohol spectrum disorders Alcohol Clin Exp Res 2014 38 9 2502 2508 10.1111/acer.12516 25159809 PMC4691582 · DOI
- [16]Li Y Ley SH VanderWeele TJ Curhan GC Rich-Edwards JW Willett WC Forman JP Hu FB Qi L Joint association between birth weight at term and later life adherence to a healthy lifestyle with risk of hypertension: a prospective cohort study BMC Med 2015 13 175 10.1186/s12916-015-0409-1 26228391 PMC4521367 · DOI
- [17]Li Y Ley SH Tobias DK Chiuve SE VanderWeele TJ Rich-Edwards JW Curhan GC Willett WC Manson JE Hu FB Qi L Birth weight and later life adherence to unhealthy lifestyles in predicting type 2 diabetes: prospective cohort study BMJ 2015 351 h3672 10.1136/bmj.h3672 26199273 PMC4510778 · DOI
- [18]Lopez-Tello J Arias-Alvarez M Gonzalez-Bulnes A Sferuzzi-Perri AN Models of Intrauterine growth restriction and fetal programming in rabbits Mol Reprod Dev 2019 10.1002/mrd.23271 31538701 · DOI
- [20]Gonzalez-Bulnes A Chavatte-Palmer P Contribution of large animals to translational research on prenatal programming of obesity and associated diseases Curr Pharm Biotechnol 2017 18 7 541 551 10.2174/1389201018666170811150920 28799494 · DOI
- [21]Morrison JL Botting KJ Darby JRT David AL Dyson RM Gatford KL Gray C Herrera EA Hirst JJ Kim B Kind KL Krause BJ Matthews SG Palliser HK Regnault TRH Richardson BS Sasaki A Thompson LP Berry MJ Guinea pig models for translation of the developmental origins of health and disease hypothesis into the clinic J Physiol 2018 596 23 5535 5569 10.1113/jp274948 29633280 PMC6265540 · DOI
- [22]Ailhaud G Grimaldi P Négrel R Cellular and molecular aspects of adipose tissue development Annu Rev Nutr 1992 12 207 233 10.1146/annurev.nu.12.070192.001231 1503804 · DOI
- [23]Burchell A Gibb L Waddell ID Giles M Hume R The ontogeny of human hepatic microsomal glucose-6-phosphatase proteins Clin Chem 1990 36 9 1633 1637 10.1093/clinchem/36.9.1633 2170061 · DOI
- [24]Matsumoto M Pocai A Rossetti L Depinho RA Accili D Impaired regulation of hepatic glucose production in mice lacking the forkhead transcription factor Foxo1 in liver Cell Metab 2007 6 3 208 216 10.1016/j.cmet.2007.08.006 17767907 · DOI
- [26]Romer AI Sussel L Pancreatic islet cell development and regeneration Curr Opin Endocrinol Diabetes Obes 2015 22 4 255 264 10.1097/med.0000000000000174 26087337 PMC4660868 · DOI
- [27]Fowden AL Hill DJ Intra-uterine programming of the endocrine pancreas Br Med Bull 2001 60 123 142 10.1093/bmb/60.1.123 11809622 · DOI
- [28]Pan FC Wright C Pancreas organogenesis: from bud to plexus to gland Dev Dyn 2011 240 3 530 565 10.1002/dvdy.22584 21337462 · DOI
- [29]Sadava D Frykman P Harris E Majerus D Mustard J Bernard B Development of enzymes of glycolysis and gluconeogenesis in human fetal liver Biol Neonate 1992 62 2–3 89 95 10.1159/000243859 1330004 · DOI
- [30]Clausen TD Mathiesen ER Hansen T Pedersen O Jensen DM Lauenborg J Schmidt L Damm P Overweight and the metabolic syndrome in adult offspring of women with diet-treated gestational diabetes mellitus or type 1 diabetes J Clin Endocrinol Metab 2009 94 7 2464 2470 10.1210/jc.2009-0305 19417040 · DOI · Paper page
- [31]Roseboom TJ Painter RC van Abeelen AF Veenendaal MV de Rooij SR Hungry in the womb: what are the consequences? Lessons from the Dutch famine Maturitas 2011 70 2 141 145 10.1016/j.maturitas.2011.06.017 21802226 · DOI · Paper page
- [32]Roseboom T de Rooij S Painter R The Dutch famine and its long-term consequences for adult health Early Hum Dev 2006 82 8 485 491 10.1016/j.earlhumdev.2006.07.001 16876341 · DOI · Paper page
- [33]Chandler-Laney PC Bush NC Granger WM Rouse DJ Mancuso MS Gower BA Overweight status and intrauterine exposure to gestational diabetes are associated with children's metabolic health Pediatr Obes 2012 7 1 44 52 10.1111/j.2047-6310.2011.00009.x 22308218 PMC3269827 · DOI
- [35]Micheli K Komninos I Bagkeris E Roumeliotaki T Koutis A Kogevinas M Chatzi L Sleep patterns in late pregnancy and risk of preterm birth and fetal growth restriction Epidemiology 2011 22 5 738 744 10.1097/EDE.0b013e31822546fd 21734587 · DOI · Paper page
- [36]Rich DQ Demissie K Lu SE Kamat L Wartenberg D Rhoads GG Ambient air pollutant concentrations during pregnancy and the risk of fetal growth restriction J Epidemiol Community Health 2009 63 6 488 496 10.1136/jech.2008.082792 19359274 PMC4019072 · DOI
- [37]Jauniaux E Burton GJ Morphological and biological effects of maternal exposure to tobacco smoke on the feto-placental unit Early Hum Dev 2007 83 11 699 706 10.1016/j.earlhumdev.2007.07.016 17900829 · DOI
- [38]Popova S Lange S Probst C Gmel G Rehm J Estimation of national, regional, and global prevalence of alcohol use during pregnancy and fetal alcohol syndrome: a systematic review and meta-analysis Lancet Glob Health 2017 5 3 e290 e299 10.1016/s2214-109x(17)30021-9 28089487 · DOI · Paper page
- [39]Arduini D Rizzo G Romanini C Mancuso S Utero-placental blood flow velocity waveforms as predictors of pregnancy-induced hypertension Eur J Obstet Gynecol Reprod Biol 1987 26 4 335 341 10.1016/0028-2243(87)90131-6 2961632 · DOI
- [40]Roberts D Brown J Medley N Dalziel SR Antenatal corticosteroids for accelerating fetal lung maturation for women at risk of preterm birth Cochrane Database Syst Rev 2017 3 Cd004454 10.1002/14651858.CD004454.pub3 28321847 PMC6464568 · DOI · Paper page
- [41]Blais L Beauchesne MF Rey E Malo JL Forget A Use of inhaled corticosteroids during the first trimester of pregnancy and the risk of congenital malformations among women with asthma Thorax 2007 62 4 320 328 10.1136/thx.2006.062950 17121872 PMC2092465 · DOI
- [42]Takahashi LK Turner JG Kalin NH Prolonged stress-induced elevation in plasma corticosterone during pregnancy in the rat: implications for prenatal stress studies Psychoneuroendocrinology 1998 23 6 571 581 10.1016/s0306-4530(98)00024-9 9802128 · DOI
- [43]Chen HE Lin YJ Lin IC Yu HR Sheen JM Tsai CC Huang LT Tain YL Resveratrol prevents combined prenatal N(G)-nitro-l-arginine-methyl ester (L-NAME) treatment plus postnatal high-fat diet induced programmed hypertension in adult rat offspring: interplay between nutrient-sensing signals, oxidative stress and gut microbiota J Nutr Biochem 2019 70 28 37 10.1016/j.jnutbio.2019.04.002 31108332 · DOI
- [44]Tain YL Huang LT Lee CT Chan JY Hsu CN Maternal citrulline supplementation prevents prenatal N(G)-nitro-l-arginine-methyl ester (L-NAME)-induced programmed hypertension in rats Biol Reprod 2015 92 1 7 10.1095/biolreprod.114.121384 25395680 · DOI
- [45]Hao XQ Du JX Li Y Li M Zhang SY Prenatal exposure to lipopolysaccharide combined with pre- and postnatal high-fat diet result in lowered blood pressure and insulin resistance in offspring rats PLoS ONE 2014 9 2 e88127 10.1371/journal.pone.0088127 24498431 PMC3912172 · DOI
- [46]Chen H Iglesias MA Caruso V Morris MJ Maternal cigarette smoke exposure contributes to glucose intolerance and decreased brain insulin action in mice offspring independent of maternal diet PLoS ONE 2011 6 11 e27260 10.1371/journal.pone.0027260 22076142 PMC3208635 · DOI
- [47]Holloway AC Lim GE Petrik JJ Foster WG Morrison KM Gerstein HC Fetal and neonatal exposure to nicotine in Wistar rats results in increased beta cell apoptosis at birth and postnatal endocrine and metabolic changes associated with type 2 diabetes Diabetologia 2005 48 12 2661 2666 10.1007/s00125-005-0022-5 16270195 · DOI
- [48]Bolton JL Auten RL Bilbo SD Prenatal air pollution exposure induces sexually dimorphic fetal programming of metabolic and neuroinflammatory outcomes in adult offspring Brain Behav Immun 2014 37 30 44 10.1016/j.bbi.2013.10.029 24184474 · DOI
- [49]Bolton JL Smith SH Huff NC Gilmour MI Foster WM Auten RL Bilbo SD Prenatal air pollution exposure induces neuroinflammation and predisposes offspring to weight gain in adulthood in a sex-specific manner Faseb J 2012 26 11 4743 4754 10.1096/fj.12-210989 22815382 · DOI
- [50]Wei J Lin Y Li Y Ying C Chen J Song L Zhou Z Lv Z Xia W Chen X Xu S Perinatal exposure to bisphenol A at reference dose predisposes offspring to metabolic syndrome in adult rats on a high-fat diet Endocrinology 2011 152 8 3049 3061 10.1210/en.2011-0045 21586551 · DOI
- [51]Angle BM Do RP Ponzi D Stahlhut RW Drury BE Nagel SC Welshons WV Besch-Williford CL Palanza P Parmigiani S vom Saal FS Taylor JA Metabolic disruption in male mice due to fetal exposure to low but not high doses of bisphenol A (BPA): evidence for effects on body weight, food intake, adipocytes, leptin, adiponectin, insulin and glucose regulation Reprod Toxicol 2013 42 256 268 10.1016/j.reprotox.2013.07.017 23892310 PMC3886819 · DOI
- [52]Lejonklou MH Dunder L Bladin E Pettersson V Rönn M Lind L Waldén TB Lind PM Effects of low-dose developmental bisphenol a exposure on metabolic parameters and gene expression in male and female fischer 344 rat offspring Environ Health Perspect 2017 125 6 067018 10.1289/ehp505 28657538 PMC5743697 · DOI
- [53]Pei LG Yuan C Guo YT Kou H Xia LP Zhang L Yan YE Xu D Wang H Prenatal caffeine exposure induced high susceptibility to metabolic syndrome in adult female offspring rats and its underlying mechanisms Reprod Toxicol 2017 71 150 158 10.1016/j.reprotox.2017.06.045 28625926 · DOI
- [54]Zhang H Chu X Huang Y Li G Wang Y Li Y Sun C Maternal vitamin D deficiency during pregnancy results in insulin resistance in rat offspring, which is associated with inflammation and Iκbα methylation Diabetologia 2014 57 10 2165 2172 10.1007/s00125-014-3316-7 24985146 · DOI · Paper page
- [55]Lewis RM Forhead AJ Petry CJ Ozanne SE Hales CN Long-term programming of blood pressure by maternal dietary iron restriction in the rat Br J Nutr 2002 88 3 283 290 10.1079/bjn2002656 12207838 · DOI
- [56]Crowe C Dandekar P Fox M Dhingra K Bennet L Hanson M The effects of anaemia on heart, placenta and body weight, and blood pressure in fetal and neonatal rats J Physiol 1995 488 2 515 519 10.1113/jphysiol.1995.sp020986 8568690 PMC1156690 · DOI
- [57]Bonaventura MM Bourguignon NS Bizzozzero M Rodriguez D Ventura C Cocca C Libertun C Lux-Lantos VA Arsenite in drinking water produces glucose intolerance in pregnant rats and their female offspring Food Chem Toxicol 2017 100 207 216 10.1016/j.fct.2016.12.025 28017702 · DOI
- [58]Kimura I Miyamoto J Ohue-Kitano R Watanabe K Yamada T Onuki M Aoki R Isobe Y Kashihara D Inoue D Inaba A Takamura Y Taira S Kumaki S Watanabe M Ito M Nakagawa F Irie J Kakuta H Shinohara M Iwatsuki K Tsujimoto G Ohno H Arita M Itoh H Hase K Maternal gut microbiota in pregnancy influences offspring metabolic phenotype in mice Science 2020 10.1126/science.aaw8429 32108090 · DOI
- [59]Varcoe TJ Wight N Voultsios A Salkeld MD Kennaway DJ Chronic phase shifts of the photoperiod throughout pregnancy programs glucose intolerance and insulin resistance in the rat PLoS ONE 2011 6 4 e18504 10.1371/journal.pone.0018504 21494686 PMC3071829 · DOI · Paper page
- [60]Agote M Goya L Ramos S Alvarez C Gavete ML Pascual-Leone AM Escriva F Glucose uptake and glucose transporter proteins in skeletal muscle from undernourished rats Am J Physiol Endocrinol Metab 2001 281 5 E1101 1109 10.1152/ajpendo.2001.281.5.E1101 11595669 · DOI
- [61]Norman AM Miles-Chan JL Thompson NM Breier BH Huber K Postnatal development of metabolic flexibility and enhanced oxidative capacity after prenatal undernutrition Reprod Sci 2012 19 6 607 614 10.1177/1933719111428519 22138545 · DOI
- [62]Somm E Vauthay DM Guerardel A Toulotte A Cettour-Rose P Klee P Meda P Aubert ML Huppi PS Schwitzgebel VM Early metabolic defects in dexamethasone-exposed and undernourished intrauterine growth restricted rats PLoS ONE 2012 7 11 e50131 10.1371/journal.pone.0050131 23166830 PMC3500352 · DOI
- [63]Thompson N Huber K Bedurftig M Hansen K Miles-Chan J Breier BH Metabolic programming of adipose tissue structure and function in male rat offspring by prenatal undernutrition Nutr Metab (Lond) 2014 11 1 50 10.1186/1743-7075-11-50 25352910 PMC4210519 · DOI
- [64]Lecoutre S Marousez L Drougard A Knauf C Guinez C Eberle D Laborie C Vieau D Lesage J Breton C Maternal undernutrition programs the apelinergic system of adipose tissue in adult male rat offspring J Dev Orig Health Dis 2017 8 1 3 7 10.1017/s2040174416000702 28051763 · DOI
- [65]Lecoutre S Montel V Vallez E Pourpe C Delmont A Eury E Verbanck M Dickes-Coopman A Daubersies P Lesage J Laborie C Tailleux A Staels B Froguel P Breton C Vieau D Transcription profiling in the liver of undernourished male rat offspring reveals altered lipid metabolism pathways and predisposition to hepatic steatosis Am J Physiol Endocrinol Metab 2019 10.1152/ajpendo.00291.2019 31638854 · DOI
- [66]Xu YP Liang L Wang XM The levels of Pdx1/insulin, Cacna1c and Cacna1d, and beta-cell mass in a rat model of intrauterine undernutrition J Matern Fetal Neonatal Med 2011 24 3 437 443 10.3109/14767058.2010.497571 20873977 · DOI
- [67]Theys N Ahn MT Bouckenooghe T Reusens B Remacle C Maternal malnutrition programs pancreatic islet mitochondrial dysfunction in the adult offspring J Nutr Biochem 2011 22 10 985 994 10.1016/j.jnutbio.2010.08.015 21190832 · DOI
- [68]Smith T Sloboda DM Saffery R Joo E Vickers MH Maternal nutritional history modulates the hepatic IGF-IGFBP axis in adult male rat offspring Endocrine 2014 46 1 70 82 10.1007/s12020-013-0034-8 23963811 · DOI
- [69]Zhu WF Zhu JF Liang L Shen Z Wang YM Maternal undernutrition leads to elevated hepatic triglycerides in male rat offspring due to increased expression of lipoprotein lipase Mol Med Rep 2016 13 5 4487 4493 10.3892/mmr.2016.5040 27035287 · DOI
- [70]Wang X Liang L Du L The effects of intrauterine undernutrition on pancreas ghrelin and insulin expression in neonate rats J Endocrinol 2007 194 1 121 129 10.1677/joe-07-0057 17592026 · DOI
- [71]Reynolds CM Li M Gray C Vickers MH Preweaning growth hormone treatment ameliorates adipose tissue insulin resistance and inflammation in adult male offspring following maternal undernutrition Endocrinology 2013 154 8 2676 2686 10.1210/en.2013-1146 23715866 · DOI
- [72]Raychaudhuri N Raychaudhuri S Thamotharan M Devaskar SU Histone code modifications repress glucose transporter 4 expression in the intrauterine growth-restricted offspring J Biol Chem 2008 283 20 13611 13626 10.1074/jbc.M800128200 18326493 PMC2376250 · DOI
- [73]Magee TR Han G Cherian B Khorram O Ross MG Desai M Down-regulation of transcription factor peroxisome proliferator-activated receptor in programmed hepatic lipid dysregulation and inflammation in intrauterine growth-restricted offspring Am J Obstet Gynecol 2008 199 3 271.e271 275 10.1016/j.ajog.2008.05.022 PMC2597035 18667178 · DOI
- [74]Yamada M Wolfe D Han G French SW Ross MG Desai M Early onset of fatty liver in growth-restricted rat fetuses and newborns Congenit Anom (Kyoto) 2011 51 4 167 173 10.1111/j.1741-4520.2011.00336.x 22103455 PMC3244689 · DOI
- [75]Delahaye F Lukaszewski MA Wattez JS Cisse O Dutriez-Casteloot I Fajardy I Montel V Dickes-Coopman A Laborie C Lesage J Breton C Vieau D Maternal perinatal undernutrition programs a "brown-like" phenotype of gonadal white fat in male rat at weaning Am J Physiol Regul Integr Comp Physiol 2010 299 1 R101 110 10.1152/ajpregu.00604.2009 20463183 · DOI
- [76]Campisano SE Echarte SM Podaza E Chisari AN Protein malnutrition during fetal programming induces fatty liver in adult male offspring rats J Physiol Biochem 2017 73 2 275 285 10.1007/s13105-017-0549-1 28160259 · DOI
- [77]Desai M Byrne CD Zhang J Petry CJ Lucas A Hales CN Programming of hepatic insulin-sensitive enzymes in offspring of rat dams fed a protein-restricted diet Am J Physiol 1997 272 5 Pt 1 G1083 1090 10.1152/ajpgi.1997.272.5.G1083 9176217 · DOI
- [78]Desai M Byrne CD Meeran K Martenz ND Bloom SR Hales CN Regulation of hepatic enzymes and insulin levels in offspring of rat dams fed a reduced-protein diet Am J Physiol 1997 273 4 G899 904 10.1152/ajpgi.1997.273.4.G899 9357833 · DOI
- [79]Zheng J Xiao X Zhang Q Yu M Xu J Wang Z Maternal protein restriction induces early-onset glucose intolerance and alters hepatic genes expression in the peroxisome proliferator-activated receptor pathway in offspring J Diabetes Investig 2015 6 3 269 279 10.1111/jdi.12303 25969711 PMC4420558 · DOI
- [80]Fernandez-Twinn DS Wayman A Ekizoglou S Martin MS Hales CN Ozanne SE Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21-mo-old female rat offspring Am J Physiol Regul Integr Comp Physiol 2005 288 2 R368 373 10.1152/ajpregu.00206.2004 15514105 · DOI
- [81]Claycombe KJ Roemmich JN Johnson L Vomhof-DeKrey EE Johnson WT Skeletal muscle Sirt3 expression and mitochondrial respiration are regulated by a prenatal low-protein diet J Nutr Biochem 2015 26 2 184 189 10.1016/j.jnutbio.2014.10.003 25483313 · DOI
- [82]Gosby AK Stanton LM Maloney CA Thompson M Briody J Baxter RC Bryson JM Denyer GS Caterson ID Postnatal nutrition alters body composition in adult offspring exposed to maternal protein restriction Br J Nutr 2009 101 12 1878 1884 10.1017/S0007114508135851 19055852 · DOI
- [83]Shepherd PR Crowther NJ Desai M Hales CN Ozanne SE Altered adipocyte properties in the offspring of protein malnourished rats Br J Nutr 1997 78 1 121 129 10.1079/bjn19970124 9292765 · DOI
- [84]Guan H Arany E van Beek JP Chamson-Reig A Thyssen S Hill DJ Yang K Adipose tissue gene expression profiling reveals distinct molecular pathways that define visceral adiposity in offspring of maternal protein-restricted rats Am J Physiol Endocrinol Metab 2005 288 4 E663 673 10.1152/ajpendo.00461.2004 15562247 · DOI
- [85]Theys N Bouckenooghe T Ahn MT Remacle C Reusens B Maternal low-protein diet alters pancreatic islet mitochondrial function in a sex-specific manner in the adult rat Am J Physiol Regul Integr Comp Physiol 2009 297 5 R1516 1525 10.1152/ajpregu.00280.2009 19759337 · DOI
- [86]Sohi G Marchand K Revesz A Arany E Hardy DB Maternal protein restriction elevates cholesterol in adult rat offspring due to repressive changes in histone modifications at the cholesterol 7alpha-hydroxylase promoter Mol Endocrinol 2011 25 5 785 798 10.1210/me.2010-0395 21372147 PMC5417260 · DOI
- [87]Tarry-Adkins JL Chen JH Smith NS Jones RH Cherif H Ozanne SE Poor maternal nutrition followed by accelerated postnatal growth leads to telomere shortening and increased markers of cell senescence in rat islets Faseb j 2009 23 5 1521 1528 10.1096/fj.08-122796 19126595 · DOI
- [88]Vo TX Revesz A Sohi G Ma N Hardy DB Maternal protein restriction leads to enhanced hepatic gluconeogenic gene expression in adult male rat offspring due to impaired expression of the liver X receptor J Endocrinol 2013 218 1 85 97 10.1530/JOE-13-0055 23633563 · DOI
- [89]Liu X Qi Y Tian B Chen D Gao H Xi C Xing Y Yuan Z Maternal protein restriction induces alterations in hepatic tumor necrosis factor-alpha/CYP7A1 signaling and disorders regulation of cholesterol metabolism in the adult rat offspring J Clin Biochem Nutr 2014 55 1 40 47 10.3164/jcbn.13-100 25120278 PMC4078062 · DOI
- [90]Abuzgaia AM Hardy DB Arany E Regulation of postnatal pancreatic Pdx1 and downstream target genes after gestational exposure to protein restriction in rats Reproduction 2015 149 3 293 303 10.1530/REP-14-0245 25667428 · DOI
- [91]Alejandro EU Gregg B Wallen T Kumusoglu D Meister D Chen A Merrins MJ Satin LS Liu M Arvan P Bernal-Mizrachi E Maternal diet-induced microRNAs and mTOR underlie beta cell dysfunction in offspring J Clin Invest 2014 124 10 4395 4410 10.1172/JCI74237 25180600 PMC4191023 · DOI
- [92]Lillycrop KA Phillips ES Jackson AA Hanson MA Burdge GC Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring J Nutr 2005 135 6 1382 1386 10.1093/jn/135.6.1382 15930441 · DOI
- [93]Lillycrop KA Slater-Jefferies JL Hanson MA Godfrey KM Jackson AA Burdge GC 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 Br J Nutr 2007 97 6 1064 1073 10.1017/S000711450769196X 17433129 PMC2211425 · DOI
- [94]Zheng S Rollet M Pan YX Protein restriction during gestation alters histone modifications at the glucose transporter 4 (GLUT4) promoter region and induces GLUT4 expression in skeletal muscle of female rat offspring J Nutr Biochem 2012 23 9 1064 1071 10.1016/j.jnutbio.2011.05.013 22079207 · DOI
- [95]Erhuma A Bellinger L Langley-Evans SC Bennett AJ Prenatal exposure to undernutrition and programming of responses to high-fat feeding in the rat Br J Nutr 2007 98 3 517 524 10.1017/s0007114507721505 17442129 PMC3861785 · DOI
- [96]Nusken KD Schneider H Plank C Trollmann R Nusken E Rascher W Dotsch J Fetal programming of gene expression in growth-restricted rats depends on the cause of low birth weight Endocrinology 2011 152 4 1327 1335 10.1210/en.2010-1116 21266509 · DOI
- [97]da Silva AR Guzman-Quevedo O Perez-Garcia G Toscano AE Gois Leandro C Manhaes-de-Castro R Bolanos-Jimenez F Differential developmental programming by early protein restriction of rat skeletal muscle according to its fibre-type composition Acta Physiol (Oxf) 2014 210 1 70 83 10.1111/apha.12073 23362831 · DOI
- [98]Latouche C Heywood SE Henry SL Ziemann M Lazarus R El-Osta A Armitage JA Kingwell BA Maternal overnutrition programs changes in the expression of skeletal muscle genes that are associated with insulin resistance and defects of oxidative phosphorylation in adult male rat offspring J Nutr 2014 144 3 237 244 10.3945/jn.113.186775 24381224 · DOI
- [99]Zhang X Strakovsky R Zhou D Zhang Y Pan YX A maternal high-fat diet represses the expression of antioxidant defense genes and induces the cellular senescence pathway in the liver of male offspring rats J Nutr 2011 141 7 1254 1259 10.3945/jn.111.139576 21562236 · DOI
- [100]Dudley KJ Sloboda DM Connor KL Beltrand J Vickers MH Offspring of mothers fed a high fat diet display hepatic cell cycle inhibition and associated changes in gene expression and DNA methylation PLoS ONE 2011 6 7 e21662 10.1371/journal.pone.0021662 21779332 PMC3133558 · DOI
- [101]Yang KF Cai W Xu JL Shi W Maternal high-fat diet programs Wnt genes through histone modification in the liver of neonatal rats J Mol Endocrinol 2012 49 2 107 114 10.1530/jme-12-0046 22696509 · DOI
- [102]Yang QY Liang JF Rogers CJ Zhao JX Zhu MJ Du M Maternal obesity induces epigenetic modifications to facilitate Zfp423 expression and enhance adipogenic differentiation in fetal mice Diabetes 2013 62 11 3727 3735 10.2337/db13-0433 23884886 PMC3806589 · DOI · Paper page
- [103]Bringhenti I Ornellas F Mandarim-de-Lacerda CA Aguila MB The insulin-signaling pathway of the pancreatic islet is impaired in adult mice offspring of mothers fed a high-fat diet Nutrition 2016 32 10 1138 1143 10.1016/j.nut.2016.03.001 27155954 · DOI
- [104]Pereira TJ Fonseca MA Campbell KE Moyce BL Cole LK Hatch GM Doucette CA Klein J Aliani M Dolinsky VW Maternal obesity characterized by gestational diabetes increases the susceptibility of rat offspring to hepatic steatosis via a disrupted liver metabolome J Physiol 2015 593 14 3181 3197 10.1113/jp270429 25922055 PMC4532536 · DOI · Paper page
- [106]Fante T Simino LA Reginato A Payolla TB Vitoreli DC Souza M Torsoni MA Milanski M Torsoni AS Diet-induced maternal obesity alters insulin signalling in male mice offspring rechallenged with a high-fat diet in adulthood PLoS ONE 2016 11 8 e0160184 10.1371/journal.pone.0160184 27479001 PMC4968809 · DOI
- [107]Payolla TB Lemes SF de Fante T Reginato A Mendes da Silva C de Oliveira MT Rodrigues HG Torsoni AS Milanski M Torsoni MA High-fat diet during pregnancy and lactation impairs the cholinergic anti-inflammatory pathway in the liver and white adipose tissue of mouse offspring Mol Cell Endocrinol 2016 422 192 202 10.1016/j.mce.2015.12.004 26687064 · DOI
- [108]Zheng J Xiao X Zhang Q Yu M Xu J Wang Z Maternal high-fat diet modulates hepatic glucose, lipid homeostasis and gene expression in the PPAR pathway in the early life of offspring Int J Mol Sci 2014 15 9 14967 14983 10.3390/ijms150914967 25158235 PMC4200747 · DOI
- [109]Buckley AJ Keseru B Briody J Thompson M Ozanne SE Thompson CH Altered body composition and metabolism in the male offspring of high fat-fed rats Metabolism 2005 54 4 500 507 10.1016/j.metabol.2004.11.003 15798958 · DOI
- [110]Khalyfa A Carreras A Hakim F Cunningham JM Wang Y Gozal D Effects of late gestational high-fat diet on body weight, metabolic regulation and adipokine expression in offspring Int J Obes (Lond) 2013 37 11 1481 1489 10.1038/ijo.2013.12 23399773 PMC3701742 · DOI
- [111]Seet EL Yee JK Jellyman JK Han G Ross MG Desai M Maternal high-fat-diet programs rat offspring liver fatty acid metabolism Lipids 2015 50 6 565 573 10.1007/s11745-015-4018-8 25899040 PMC4451084 · DOI
- [112]Lecoutre S Deracinois B Laborie C Eberle D Guinez C Panchenko PE Lesage J Vieau D Junien C Gabory A Breton C Depot- and sex-specific effects of maternal obesity in offspring's adipose tissue J Endocrinol 2016 230 1 39 53 10.1530/JOE-16-0037 27122310 · DOI
- [113]Lecoutre S Pourpe C Butruille L Marousez L Laborie C Guinez C Lesage J Vieau D Eeckhoute J Gabory A Oger F Eberle D Breton C Reduced PPARgamma2 expression in adipose tissue of male rat offspring from obese dams is associated with epigenetic modifications Faseb J 2018 32 5 2768 2778 10.1096/fj.201700997R 29295860 · DOI
- [114]Desai M Jellyman JK Han G Lane RH Ross MG Programmed regulation of rat offspring adipogenic transcription factor (PPARgamma) by maternal nutrition J Dev Orig Health Dis 2015 6 6 530 538 10.1017/s2040174415001440 26286138 PMC4630004 · DOI
- [115]Yokomizo H Inoguchi T Sonoda N Sakaki Y Maeda Y Inoue T Hirata E Takei R Ikeda N Fujii M Fukuda K Sasaki H Takayanagi R Maternal high-fat diet induces insulin resistance and deterioration of pancreatic beta-cell function in adult offspring with sex differences in mice Am J Physiol Endocrinol Metab 2014 306 10 E1163 1175 10.1152/ajpendo.00688.2013 24691028 · DOI
- [116]Simmons RA Suponitsky-Kroyter I Selak MA Progressive accumulation of mitochondrial DNA mutations and decline in mitochondrial function lead to beta-cell failure J Biol Chem 2005 280 31 28785 28791 10.1074/jbc.M505695200 15946949 · DOI · Paper page
- [117]Park JH Stoffers DA Nicholls RD Simmons RA Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1 J Clin Invest 2008 118 6 2316 2324 10.1172/jci33655 18464933 PMC2373422 · DOI · Paper page
- [118]Sadiq HF Das UG Tracy TF Devaskar SU Intra-uterine growth restriction differentially regulates perinatal brain and skeletal muscle glucose transporters Brain Res 1999 823 1–2 96 103 10.1016/s0006-8993(99)01145-2 10095016 · DOI
- [119]Stoffers DA Desai BM DeLeon DD Simmons RA Neonatal exendin-4 prevents the development of diabetes in the intrauterine growth retarded rat Diabetes 2003 52 3 734 740 10.2337/diabetes.52.3.734 12606515 · DOI
- [120]Germani D Puglianiello A Cianfarani S Uteroplacental insufficiency down regulates insulin receptor and affects expression of key enzymes of long-chain fatty acid (LCFA) metabolism in skeletal muscle at birth Cardiovasc Diabetol 2008 7 14 10.1186/1475-2840-7-14 18485240 PMC2396605 · DOI
- [121]Fu Q Yu X Callaway CW Lane RH McKnight RA Epigenetics: intrauterine growth retardation (IUGR) modifies the histone code along the rat hepatic IGF-1 gene Faseb J 2009 23 8 2438 2449 10.1096/fj.08-124768 19364764 PMC2717764 · DOI
- [122]Camm EJ Martin-Gronert MS Wright NL Hansell JA Ozanne SE Giussani DA Prenatal hypoxia independent of undernutrition promotes molecular markers of insulin resistance in adult offspring FASEB J 2011 25 1 420 427 10.1096/fj.10-158188 20923964 · DOI
- [123]Osumek JE Revesz A Morton JS Davidge ST Hardy DB Enhanced trimethylation of histone h3 mediates impaired expression of hepatic glucose 6-phosphatase expression in offspring from rat dams exposed to hypoxia during pregnancy Reprod Sci 2014 21 1 112 121 10.1177/1933719113492212 23744881 PMC3857770 · DOI
- [124]Rueda-Clausen CF Dolinsky VW Morton JS Proctor SD Dyck JR Davidge ST Hypoxia-induced intrauterine growth restriction increases the susceptibility of rats to high-fat diet-induced metabolic syndrome Diabetes 2011 60 2 507 516 10.2337/db10-1239 21270262 PMC3028350 · DOI
- [125]Badran M Yassin BA Lin DTS Kobor MS Ayas N Laher I Gestational intermittent hypoxia induces endothelial dysfunction, reduces perivascular adiponectin and causes epigenetic changes in adult male offspring J Physiol 2019 597 22 5349 5364 10.1113/jp277936 31441069 · DOI · Paper page
- [126]Nyirenda MJ Lindsay RS Kenyon CJ Burchell A Seckl JR Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring J Clin Invest 1998 101 10 2174 2181 10.1172/jci1567 9593773 PMC508805 · DOI
- [127]Drake AJ Walker BR Seckl JR Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats Am J Physiol Regul Integr Comp Physiol 2005 288 1 R34 38 10.1152/ajpregu.00106.2004 15178540 · DOI
- [128]Sheen JM Hsieh CS Tain YL Li SW Yu HR Chen CC Tiao MM Chen YC Huang LT Programming effects of prenatal glucocorticoid exposure with a postnatal high-fat diet in diabetes mellitus Int J Mol Sci 2016 17 4 533 10.3390/ijms17040533 27070590 PMC4848989 · DOI
- [129]Chen YC Huang YH Sheen JM Tain YL Yu HR Chen CC Tiao MM Kuo HC Huang LT Prenatal dexamethasone exposure programs the development of the pancreas and the secretion of insulin in rats Pediatr Neonatol 2017 58 2 135 144 10.1016/j.pedneo.2016.02.008 27531015 · DOI
- [130]Cleasby ME Kelly PA Walker BR Seckl JR Programming of rat muscle and fat metabolism by in utero overexposure to glucocorticoids Endocrinology 2003 144 3 999 1007 10.1210/en.2002-220559 12586777 · DOI
- [131]O'Regan D Kenyon CJ Seckl JR Holmes MC Glucocorticoid exposure in late gestation in the rat permanently programs gender-specific differences in adult cardiovascular and metabolic physiology Am J Physiol Endocrinol Metab 2004 287 5 E863 870 10.1152/ajpendo.00137.2004 15238353 · DOI
- [132]Franko KL Forhead AJ Fowden AL Differential effects of prenatal stress and glucocorticoid administration on postnatal growth and glucose metabolism in rats J Endocrinol 2010 204 3 319 329 10.1677/JOE-09-0390 20016055 · DOI
- [133]Carbone DL Zuloaga DG Hiroi R Foradori CD Legare ME Handa RJ Prenatal dexamethasone exposure potentiates diet-induced hepatosteatosis and decreases plasma IGF-I in a sex-specific fashion Endocrinology 2012 153 1 295 306 10.1210/en.2011-1601 22067322 PMC3249671 · DOI
- [135]Brunton PJ Sullivan KM Kerrigan D Russell JA Seckl JR Drake AJ Sex-specific effects of prenatal stress on glucose homoeostasis and peripheral metabolism in rats J Endocrinol 2013 217 2 161 173 10.1530/joe-12-0540 23428582 · DOI
- [136]Paternain L de la Garza AL Batlle MA Milagro FI Martínez JA Campión J Prenatal stress increases the obesogenic effects of a high-fat-sucrose diet in adult rats in a sex-specific manner Stress 2013 16 2 220 232 10.3109/10253890.2012.707708 22738222 · DOI
- [137]Franko KL Forhead AJ Fowden AL Effects of stress during pregnancy on hepatic glucogenic capacity in rat dams and their fetuses Physiol Rep 2017 10.14814/phy2.13293 28611150 PMC5471435 · DOI
- [138]Maeyama H Hirasawa T Tahara Y Obata C Kasai H Moriishi K Mochizuki K Kubota T Maternal restraint stress during pregnancy in mice induces 11β-HSD1-associated metabolic changes in the livers of the offspring J Dev Orig Health Dis 2015 6 2 105 114 10.1017/s2040174415000100 25708481 · DOI
- [139]Kamel MA Helmy MH Hanafi MY Mahmoud SA Abo Elfetooh H Impaired peripheral glucose sensing in F1 offspring of diabetic pregnancy J Physiol Biochem 2014 70 3 685 699 10.1007/s13105-014-0338-z 24895245 · DOI
- [140]Inoguchi Y Ichiyanagi K Ohishi H Maeda Y Sonoda N Ogawa Y Inoguchi T Sasaki H Poorly controlled diabetes during pregnancy and lactation activates the Foxo1 pathway and causes glucose intolerance in adult offspring Sci Rep 2019 9 1 10181 10.1038/s41598-019-46638-2 31308441 PMC6629688 · DOI
- [141]Oliveira AC Andreotti S Chimin P Sertie RA Farias Tda S Torres-Leal FL de Proenca AR Campana AB D'Avila LS Oliveira KA Lima FB Neonatal streptozotocin-induced diabetes in mothers promotes metabolic programming of adipose tissue in male rat offspring Life Sci 2015 136 151 156 10.1016/j.lfs.2015.06.024 26144624 · DOI
- [142]Dong HP Tan MZ Liu QJ Wang J Zhong SB The study on the effect of hyperglycemia on offspring fatty tissue metabolism during pregnancy Eur Rev Med Pharmacol Sci 2017 21 16 3658 3664 28925477
- [143]Nazari Z Nabiuni M Saeidi M Golalipour MJ Gestational diabetes leads to down-regulation of CDK4-pRB-E2F1 pathway genes in pancreatic islets of rat offspring Iran J Basic Med Sci 2017 20 2 150 154 10.22038/ijbms.2017.8240 28293391 PMC5339655 · DOI
- [144]Su R Yan J Yang H Transgenerational glucose intolerance of tumor necrosis factor with epigenetic alteration in rat perirenal adipose tissue induced by intrauterine hyperglycemia J Diabetes Res 2016 2016 4952801 10.1155/2016/4952801 26881249 PMC4735892 · DOI
- [145]Zhu H Chen B Cheng Y Zhou Y Yan YS Luo Q Jiang Y Sheng JZ Ding GL Huang HF Insulin therapy for gestational diabetes mellitus does not fully protect offspring from diet-induced metabolic disorders Diabetes 2019 68 4 696 708 10.2337/db18-1151 30696708 · DOI
- [146]Chen L Nyomba BL Effects of prenatal alcohol exposure on glucose tolerance in the rat offspring Metabolism 2003 52 4 454 462 10.1053/meta.2003.50073 12701058 · DOI
- [147]Yao XH Gregoire Nyomba BL Abnormal glucose homeostasis in adult female rat offspring after intrauterine ethanol exposure Am J Physiol Regul Integr Comp Physiol 2007 292 5 R1926 1933 10.1152/ajpregu.00822.2006 17218436 · DOI
- [148]Chen L Yao XH Nyomba BL In vivo insulin signaling through PI3-kinase is impaired in skeletal muscle of adult rat offspring exposed to ethanol in utero J Appl Physiol (1985) 2005 99 2 528 534 10.1152/japplphysiol.01098.2004 15790685 · DOI
- [149]Yao XH Chen L Nyomba BL Adult rats prenatally exposed to ethanol have increased gluconeogenesis and impaired insulin response of hepatic gluconeogenic genes J Appl Physiol (1985) 2006 100 2 642 648 10.1152/japplphysiol.01115.2005 16239604 · DOI
- [150]Yao XH Nyomba BL Hepatic insulin resistance induced by prenatal alcohol exposure is associated with reduced PTEN and TRB3 acetylation in adult rat offspring Am J Physiol Regul Integr Comp Physiol 2008 294 6 R1797 1806 10.1152/ajpregu.00804.2007 18385463 · DOI
- [151]Gardebjer EM Anderson ST Pantaleon M Wlodek ME Moritz KM Maternal alcohol intake around the time of conception causes glucose intolerance and insulin insensitivity in rat offspring, which is exacerbated by a postnatal high-fat diet FASEB J 2015 29 7 2690 2701 10.1096/fj.14-268979 25733565 · DOI
- [152]Yao XH Nguyen HK Nyomba BL Prenatal ethanol exposure causes glucose intolerance with increased hepatic gluconeogenesis and histone deacetylases in adult rat offspring: reversal by tauroursodeoxycholic acid PLoS ONE 2013 8 3 e59680 10.1371/journal.pone.0059680 23544086 PMC3609812 · DOI
- [153]Nguyen TMT Steane SE Moritz KM Akison LK Prenatal alcohol exposure programmes offspring disease: insulin resistance in adult males in a rat model of acute exposure J Physiol 2019 10.1113/jp278531 31595508 · DOI
- [154]Shen L Liu Z Gong J Zhang L Wang L Magdalou J Chen L Wang H Prenatal ethanol exposure programs an increased susceptibility of non-alcoholic fatty liver disease in female adult offspring rats Toxicol Appl Pharmacol 2014 274 2 263 273 10.1016/j.taap.2013.11.009 24275070 · DOI
- [155]Wierup N Yang S McEvilly RJ Mulder H Sundler F Ghrelin is expressed in a novel endocrine cell type in developing rat islets and inhibits insulin secretion from INS-1 (832/13) cells J Histochem Cytochem 2004 52 3 301 310 10.1177/002215540405200301 14966197 · DOI
- [156]Ellis-Hutchings RG Zucker RM Grey BE Norwood J Jr Richards JH Lau C Rogers JM Altered health outcomes in adult offspring of Sprague Dawley and Wistar rats undernourished during early or late pregnancy Birth Defects Res B Dev Reprod Toxicol 2010 89 5 396 407 10.1002/bdrb.20265 20973054 · DOI
- [157]Sampaio de Freitas M Garcia De Souza EP Vargas da Silva S da Rocha KA da Silva VR Sanchez Moura A Barja-Fidalgo C Up-regulation of phosphatidylinositol 3-kinase and glucose transporter 4 in muscle of rats subjected to maternal undernutrition BBA Mol Basis Dis 2003 1639 1 8 16 10.1016/s0925-4439(03)00096-6 12943963 · DOI
- [158]Holemans K Van Bree R Verhaeghe J Meurrens K Van Assche FA Maternal semistarvation and streptozotocin-diabetes in rats have different effects on the in vivo glucose uptake by peripheral tissues in their female adult offspring J Nutr 1997 127 7 1371 1376 10.1093/jn/127.7.1371 9202093 · DOI
- [160]Srinivasan M Katewa SD Palaniyappan A Pandya JD Patel MS Maternal high-fat diet consumption results in fetal malprogramming predisposing to the onset of metabolic syndrome-like phenotype in adulthood Am J Physiol Endocrinol Metab 2006 291 4 E792 799 10.1152/ajpendo.00078.2006 16720630 · DOI
- [161]Zambrano E Martinez-Samayoa PM Rodriguez-Gonzalez GL Nathanielsz PW Dietary intervention prior to pregnancy reverses metabolic programming in male offspring of obese rats J Physiol 2010 588 Pt 10 1791 1799 10.1113/jphysiol.2010.190033 20351043 PMC2887995 · DOI
- [162]Volpato AM Schultz A Magalhaes-da-Costa E Correia ML Aguila MB Mandarim-de-Lacerda CA Maternal high-fat diet programs for metabolic disturbances in offspring despite leptin sensitivity Neuroendocrinology 2012 96 4 272 284 10.1159/000336377 22456428 · DOI
- [163]Desai M Jellyman JK Han G Beall M Lane RH Ross MG Maternal obesity and high-fat diet program offspring metabolic syndrome Am J Obstet Gynecol 2014 211 3 237 10.1016/j.ajog.2014.03.025 24631702 PMC4149836 · DOI · Paper page
- [164]Bergman RN Ader M Huecking K Van Citters G Accurate assessment of beta-cell function: the hyperbolic correction Diabetes 2002 51 Suppl 1 S212 220 10.2337/diabetes.51.2007.s212 11815482 · DOI
- [165]Poy MN Yang Y Rezaei K Fernstrom MA Lee AD Kido Y Erickson SK Najjar SM CEACAM1 regulates insulin clearance in liver Nat Genet 2002 30 3 270 276 10.1038/ng840 11850617 · DOI
- [166]Dumortier O Blondeau B Duvillie B Reusens B Breant B Remacle C Different mechanisms operating during different critical time-windows reduce rat fetal beta cell mass due to a maternal low-protein or low-energy diet Diabetologia 2007 50 12 2495 2503 10.1007/s00125-007-0811-0 17882398 · DOI · Paper page
- [167]Petersen MC Vatner DF Shulman GI Regulation of hepatic glucose metabolism in health and disease Nat Rev Endocrinol 2017 13 10 572 587 10.1038/nrendo.2017.80 28731034 PMC5777172 · DOI
- [169]Barthel A Schmoll D Novel concepts in insulin regulation of hepatic gluconeogenesis Am J Physiol Endocrinol Metab 2003 285 4 E685 692 10.1152/ajpendo.00253.2003 12959935 · DOI
- [170]Tsuru M Katagiri H Asano T Yamada T Ohno S Ogihara T Oka Y Role of PKC isoforms in glucose transport in 3T3-L1 adipocytes: insignificance of atypical PKC Am J Physiol Endocrinol Metab 2002 283 2 E338 345 10.1152/ajpendo.00457.2001 12110540 · DOI
- [171]Leto D Saltiel AR Regulation of glucose transport by insulin: traffic control of GLUT4 Nat Rev Mol Cell Biol 2012 13 6 383 396 10.1038/nrm3351 22617471 · DOI · Paper page
- [172]He W Barak Y Hevener A Olson P Liao D Le J Nelson M Ong E Olefsky JM Evans RM Adipose-specific peroxisome proliferator-activated receptor gamma knockout causes insulin resistance in fat and liver but not in muscle Proc Natl Acad Sci USA 2003 100 26 15712 15717 10.1073/pnas.2536828100 14660788 PMC307633 · DOI
- [173]Mooradian AD Chehade J Thurman JE The role of thiazolidinediones in the treatment of patients with type 2 diabetes mellitus Treat Endocrinol 2002 1 1 13 20 10.2165/00024677-200201010-00002 15765617 · DOI
- [174]Repa JJ Liang G Ou J Bashmakov Y Lobaccaro JM Shimomura I Shan B Brown MS Goldstein JL Mangelsdorf DJ Regulation of mouse sterol regulatory element-binding protein-1c gene (SREBP-1c) by oxysterol receptors, LXRalpha and LXRbeta Genes Dev 2000 14 22 2819 2830 10.1101/gad.844900 11090130 PMC317055 · DOI
- [175]Cao G Liang Y Broderick CL Oldham BA Beyer TP Schmidt RJ Zhang Y Stayrook KR Suen C Otto KA Miller AR Dai J Foxworthy P Gao H Ryan TP Jiang XC Burris TP Eacho PI Etgen GJ Antidiabetic action of a liver x receptor agonist mediated by inhibition of hepatic gluconeogenesis J Biol Chem 2003 278 2 1131 1136 10.1074/jbc.M210208200 12414791 · DOI
- [176]Westwick JK Weitzel C Minden A Karin M Brenner DA Tumor necrosis factor alpha stimulates AP-1 activity through prolonged activation of the c-Jun kinase J Biol Chem 1994 269 42 26396 26401 7929360
- [177]Sluss HK Barrett T Derijard B Davis RJ Signal transduction by tumor necrosis factor mediated by JNK protein kinases Mol Cell Biol 1994 14 12 8376 8384 10.1128/mcb.14.12.8376 7969172 PMC359376 · DOI
- [178]Peng K Pan Y Li J Khan Z Fan M Yin H Tong C Zhao Y Liang G Zheng C 11beta-hydroxysteroid dehydrogenase type 1(11beta-HSD1) mediates insulin resistance through JNK activation in adipocytes Sci Rep 2016 6 37160 10.1038/srep37160 27841334 PMC5107914 · DOI
- [179]Saegusa H Nakagawa Y Liu Y-J Ohzeki T Influence of placental 11β-hydroxysteroid dehydrogenase (11β-HSD) inhibition on glucose metabolism and 11β-HSD regulation in adult offspring of rats Metabol Clin Exp 1999 48 12 1584 1588 10.1016/S0026-0495(99)90249-4 10599992 · DOI
- [180]Lindsay R Lindsay R Waddell B Seckl J Prenatal glucocorticoid exposure leads to offspring hyperglycaemia in the rat: studies with the 11 b-hydroxysteroid dehydrogenase inhibitor carbenoxolone Diabetologia 1996 39 11 1299 1305 10.1007/s001250050573 8932995 · DOI
- [181]Thompson MD Cismowski MJ Trask AJ Lallier SW Graf AE Rogers LK Lucchesi PA Brigstock DR Enhanced steatosis and fibrosis in liver of adult offspring exposed to maternal high-fat diet Gene Expr 2016 17 1 47 59 10.3727/105221616x692135 27342733 PMC5611859 · DOI
- [182]Qasem RJ Cherala G D'Mello AP Maternal protein restriction during pregnancy and lactation in rats imprints long-term reduction in hepatic lipid content selectively in the male offspring Nutr Res 2010 30 6 410 417 10.1016/j.nutres.2010.05.008 20650349 · DOI
- [183]Wattez JS Delahaye F Barella LF Dickes-Coopman A Montel V Breton C Mathias P Foligne B Lesage J Vieau D Short- and long-term effects of maternal perinatal undernutrition are lowered by cross-fostering during lactation in the male rat J Dev Orig Health Dis 2014 5 2 109 120 10.1017/S2040174413000548 24847697 · DOI
- [184]Tapanainen PJ Bang P Wilson K Unterman TG Vreman HJ Rosenfeld RG Maternal hypoxia as a model for intrauterine growth retardation: effects on insulin-like growth factors and their binding proteins Pediatr Res 1994 36 2 152 158 10.1203/00006450-199408000-00004 7526325 · DOI
- [185]Yakar S Liu JL Stannard B Butler A Accili D Sauer B LeRoith D Normal growth and development in the absence of hepatic insulin-like growth factor I Proc Natl Acad Sci USA 1999 96 13 7324 7329 10.1073/pnas.96.13.7324 10377413 PMC22084 · DOI
- [186]Sferruzzi-Perri AN Vaughan OR Forhead AJ Fowden AL Hormonal and nutritional drivers of intrauterine growth Curr Opin Clin Nutr Metab Care 2013 16 3 298 309 10.1097/MCO.0b013e32835e3643 23340010 · DOI
- [187]Aguirre GA De Ita JR de la Garza RG Castilla-Cortazar I Insulin-like growth factor-1 deficiency and metabolic syndrome J Transl Med 2016 14 3 10.1186/s12967-015-0762-z 26733412 PMC4702316 · DOI
- [188]Lewitt MS Dent MS Hall K The insulin-like growth factor system in obesity, insulin resistance and type 2 diabetes mellitus J Clin Med 2014 3 4 1561 1574 10.3390/jcm3041561 26237614 PMC4470198 · DOI
- [189]Rosen ED Hsu CH Wang X Sakai S Freeman MW Gonzalez FJ Spiegelman BM C/EBPalpha induces adipogenesis through PPARgamma: a unified pathway Genes Dev 2002 16 1 22 26 10.1101/gad.948702 11782441 PMC155311 · DOI
- [190]Rosen ED Walkey CJ Puigserver P Spiegelman BM Transcriptional regulation of adipogenesis Genes Dev 2000 14 11 1293 1307 10837022
- [191]Ouchi N Parker JL Lugus JJ Walsh K Adipokines in inflammation and metabolic disease Nat Rev Immunol 2011 11 2 85 97 10.1038/nri2921 21252989 PMC3518031 · DOI · Paper page
- [192]Bird A Perceptions of epigenetics Nature 2007 447 7143 396 398 10.1038/nature05913 17522671 · DOI · Paper page
- [193]Claycombe KJ Uthus EO Roemmich JN Johnson LK Johnson WT Prenatal low-protein and postnatal high-fat diets induce rapid adipose tissue growth by inducing Igf2 expression in Sprague Dawley rat offspring J Nutr 2013 143 10 1533 1539 10.3945/jn.113.178038 23946348 · DOI · Paper page
- [194]Zeng Y Gu P Liu K Huang P Maternal protein restriction in rats leads to reduced PGC-1alpha expression via altered DNA methylation in skeletal muscle Mol Med Rep 2013 7 1 306 312 10.3892/mmr.2012.1134 23117952 · DOI
- [195]Lillycrop KA Phillips ES Torrens C Hanson MA Jackson AA Burdge GC Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPAR alpha promoter of the offspring Br J Nutr 2008 100 2 278 282 10.1017/s0007114507894438 18186951 PMC2564112 · DOI
- [196]Gong L Pan YX Chen H Gestational low protein diet in the rat mediates Igf2 gene expression in male offspring via altered hepatic DNA methylation Epigenetics 2010 5 7 619 626 10.4161/epi.5.7.12882 20671425 · DOI
- [197]van Straten EM Bloks VW Huijkman NC Baller JF van Meer H Lutjohann D Kuipers F Plosch T The liver X-receptor gene promoter is hypermethylated in a mouse model of prenatal protein restriction Am J Physiol Regul Integr Comp Physiol 2010 298 2 R275 282 10.1152/ajpregu.00413.2009 19889862 · DOI
- [198]Jousse C Parry L Lambert-Langlais S Maurin AC Averous J Bruhat A Carraro V Tost J Letteron P Chen P Jockers R Launay JM Mallet J Fafournoux P Perinatal undernutrition affects the methylation and expression of the leptin gene in adults: implication for the understanding of metabolic syndrome Faseb J 2011 25 9 3271 3278 10.1096/fj.11-181792 21670064 · DOI · Paper page
- [199]Yu HL Dong S Gao LF Li L Xi YD Ma WW Yuan LH Xiao R Global DNA methylation was changed by a maternal high-lipid, high-energy diet during gestation and lactation in male adult mice liver Br J Nutr 2015 113 7 1032 1039 10.1017/s0007114515000252 25778733 · DOI
- [200]Liang X Yang Q Fu X Rogers CJ Wang B Pan H Zhu MJ Nathanielsz PW Du M Maternal obesity epigenetically alters visceral fat progenitor cell properties in male offspring mice J Physiol 2016 594 15 4453 4466 10.1113/jp272123 27060371 PMC4967739 · DOI
- [201]Jiao F Yan X Yu Y Zhu X Ma Y Yue Z Ou H Yan Z Protective effects of maternal methyl donor supplementation on adult offspring of high fat diet-fed dams J Nutr Biochem 2016 34 42 51 10.1016/j.jnutbio.2016.04.005 27183114 · DOI
- [202]Moody L Wang H Jung PM Chen H Pan YX Maternal and post-weaning high-fat diets produce distinct DNA methylation patterns in hepatic metabolic pathways within specific genomic contexts Int J Mol Sci 2019 10.3390/ijms20133229 31262088 PMC6651091 · DOI
- [203]Simmons RA Templeton LJ Gertz SJ Intrauterine growth retardation leads to the development of type 2 diabetes in the rat Diabetes 2001 50 10 2279 2286 10.2337/diabetes.50.10.2279 11574409 · DOI · Paper page
- [204]Thompson RF Fazzari MJ Niu H Barzilai N Simmons RA Greally JM Experimental intrauterine growth restriction induces alterations in DNA methylation and gene expression in pancreatic islets of rats J Biol Chem 2010 285 20 15111 15118 10.1074/jbc.M109.095133 20194508 PMC2865297 · DOI · Paper page
- [205]Keshet I Lieman-Hurwitz J Cedar H DNA methylation affects the formation of active chromatin Cell 1986 44 4 535 543 10.1016/0092-8674(86)90263-1 3456276 · DOI
- [206]Lister R Pelizzola M Dowen RH Hawkins RD Hon G Tonti-Filippini J Nery JR Lee L Ye Z Ngo QM Edsall L Antosiewicz-Bourget J Stewart R Ruotti V Millar AH Thomson JA Ren B Ecker JR Human DNA methylomes at base resolution show widespread epigenomic differences Nature 2009 462 7271 315 322 10.1038/nature08514 19829295 PMC2857523 · DOI · Paper page
- [207]Bestor T Laudano A Mattaliano R Ingram V Cloning and sequencing of a cDNA encoding DNA methyltransferase of mouse cells. The carboxyl-terminal domain of the mammalian enzymes is related to bacterial restriction methyltransferases J Mol Biol 1988 203 4 971 983 10.1016/0022-2836(88)90122-2 3210246 · DOI
- [208]Okano M Xie S Li E Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases Nat Genet 1998 19 3 219 220 10.1038/890 9662389 · DOI
200 of 276 shown
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Sorted by citations
Developmental programming of offspring adipose tissue biology and obesity risk
Rodgers, A., & Sferruzzi-Perri, A. N. (2021) · International Journal of Obesity · doi:10.1038/s41366-021-00790-w · Cited by 57 · see citing works
Self-citation
- Authors
- Christoforou, E. R., & Sferruzzi-Perri, A. N.
- Affiliations
- University of Cambridge (GB)
- Corresponding author
- Sferruzzi-Perri, Amanda N.
- Venue
- Cellular and Molecular Life Sciences
- Published
- 2020-06-03
- Volume
- 77
- Issue
- 23
- Pages
- 4861-4898
- ISSN
- 1420-682X (ISSN-L)
- 1420-9071
- PMC
- PMC7658077
- OpenAlex
- W3030004809
- Cited by
- 44
- References
- 12
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 4 · 2023: 13 · 2022: 4 · 2021: 10 · 2020: 2
- FWCI
- 1.60
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Cellular and Molecular Life Sciences (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Apollo (University of Cambridge) (submittedVersion, cc-by)
- Apollo (cc-by)
- Apollo
- Funders
- Royal Society (RG74249)
- Lister Institute of Preventive Medicine (RG93692)
- Medical Research Council (RG93186)
- 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
- developmental programming, fetal programming, metabolic dysfunction, epigenetic mechanisms, rodent models, metabolic tissues, metabolic disorders, molecular pathways
- MeSH terms
- Animals, Disease Models, Animal, Insulin, Liver, Metabolism, Rodentia, Stress, Physiological, Epigenesis, Genetic
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