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Citations to this article

Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1
Jun H. Park, … , Robert D. Nicholls, Rebecca A. Simmons
Jun H. Park, … , Robert D. Nicholls, Rebecca A. Simmons
Published May 8, 2008
Citation Information: J Clin Invest. 2008;118(6):2316-2324. https://doi.org/10.1172/JCI33655.
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Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1

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Abstract

Intrauterine growth retardation (IUGR) has been linked to the onset of diseases in adulthood, including type 2 diabetes, and has been proposed to result from altered gene regulation patterns due to epigenetic modifications of developmental genes. To determine whether epigenetic modifications may play a role in the development of adult diabetes following IUGR, we used a rodent model of IUGR that expresses lower levels of Pdx1, a pancreatic and duodenal homeobox 1 transcription factor critical for β cell function and development, which develops diabetes in adulthood. We found that expression of Pdx1 was permanently reduced in IUGR β cells and underwent epigenetic modifications throughout development. The fetal IUGR state was characterized by loss of USF-1 binding at the proximal promoter of Pdx1, recruitment of the histone deacetylase 1 (HDAC1) and the corepressor Sin3A, and deacetylation of histones H3 and H4. Following birth, histone 3 lysine 4 (H3K4) was demethylated and histone 3 lysine 9 (H3K9) was methylated. During the neonatal period, these epigenetic changes and the reduction in Pdx1 expression could be reversed by HDAC inhibition. After the onset of diabetes in adulthood, the CpG island in the proximal promoter was methylated, resulting in permanent silencing of the Pdx1 locus. These results provide insight into the development of type 2 diabetes following IUGR and we believe they are the first to describe the ontogeny of chromatin remodeling in vivo from the fetus to the onset of disease in adulthood.

Authors

Jun H. Park, Doris A. Stoffers, Robert D. Nicholls, Rebecca A. Simmons

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Nature Communications 2016
Brief neonatal nutritional supplementation has sex-specific effects on glucose tolerance and insulin regulating genes in juvenile lambs
AL Jaquiery, SS Park, HH Phua, MJ Berry, D Meijler, JE Harding, MH Oliver, FH Bloomfield
Pediatric Research 2016
Dopamine–prolactin pathway potentially contributes to the schizophrenia and type 2 diabetes comorbidity
C Gragnoli, GM Reeves, J Reazer, TT Postolache
Translational Psychiatry 2016
Recent progress in genetic and epigenetic research on type 2 diabetes
SH Kwak, KS Park
Experimental & molecular medicine 2016
Expression of epigenetic machinery genes is sensitive to maternal obesity and weight loss in relation to fetal growth in mice
PE Panchenko, S Voisin, M Jouin, L Jouneau, A Prézelin, S Lecoutre, C Breton, H Jammes, C Junien, A Gabory
Clinical Epigenetics 2016
Developmental Programming, a Pathway to Disease
V Padmanabhan, RC Cardoso, M Puttabyatappa
Endocrinology 2016
Gene–environment interaction in type 2 diabetes
Y Kido
Diabetology International 2016
Developmental programming: State-of-the-science and future directions-Summary from a Pennington Biomedical symposium: Nutritional Developmental Programming
EF Sutton, LA Gilmore, DB Dunger, BT Heijmans, MF Hivert, C Ling, JA Martinez, SE Ozanne, RA Simmons, M Szyf, RA Waterland, LM Redman, E Ravussin
Obesity 2016
Transgenerational Glucose Intolerance of Tumor Necrosis Factor with Epigenetic Alteration in Rat Perirenal Adipose Tissue Induced by Intrauterine Hyperglycemia
R Su, J Yan, H Yang
Journal of Diabetes Research 2016
E2F1 Orchestrates Transcriptomics and Oxidative Metabolism in Wharton’s Jelly-Derived Mesenchymal Stem Cells from Growth-Restricted Infants
PY Tan, CW Chang, K Duan, M Poidinger, KL Ng, YS Chong, PD Gluckman, W Stünkel, J Sun
PloS one 2016
Intrauterine Growth Restriction: Hungry for an Answer
SU Devaskar, A Chu
Physiology (Bethesda, Md.) 2016
Growth hormone actions during development influence adult phenotype and longevity
A Bartke, L Sun, Y Fang, C Hill
Experimental Gerontology 2016
Epigenetic changes in peripheral leucocytes as biomarkers in intrauterine growth retardation rat
XF Xu, SS Xu, LC Fu, QY Hu, Y Lv, LZ Du
Biomedical Reports 2016
Paternal allelic mutation at the Kcnq1 locus reduces pancreatic β-cell mass by epigenetic modification of Cdkn1c
S Asahara, H Etoh, H Inoue, K Teruyama, Y Shibutani, Y Ihara, Y Kawada, A Bartolome, N Hashimoto, T Matsuda, M Koyanagi-Kimura, A Kanno, Y Hirota, T Hosooka, K Nagashima, W Nishimura, H Inoue, M Matsumoto, MJ Higgins, K Yasuda, N Inagaki, S Seino, M Kasuga, Y Kido
Proceedings of the National Academy of Sciences 2015
Role of placental insufficiency and intrauterine growth restriction on the activation of fetal hepatic glucose production
SR Wesolowski, WW Hay
Molecular and Cellular Endocrinology 2015
Obesity-induced DNA hypermethylation of the adiponectin gene mediates insulin resistance
AY Kim, YJ Park, X Pan, KC Shin, SH Kwak, AF Bassas, RM Sallam, KS Park, AA Alfadda, A Xu, JB Kim
Nature Communications 2015
A systems view of epigenetic networks regulating pancreas development and β-cell function: Epigenetic networks in pancreas development and function
R Xie, AC Carrano, M Sander
Wiley Interdisciplinary Reviews Systems Biology and Medicine 2015
Recent developments in epigenetics of acute and chronic kidney diseases
MA Reddy, R Natarajan
Kidney International 2015
Intraplacental Gene Therapy with Ad-IGF-1 Corrects Naturally Occurring Rabbit Model of Intrauterine Growth Restriction
SG Keswani, S Balaji, AB Katz, A King, K Omar, M Habli, C Klanke, TM Crombleholme
Human Gene Therapy 2015
Epigenetic Regulation of Placenta-Specific 8 Contributes to Altered Function of Endothelial Colony-Forming Cells Exposed to Intrauterine Gestational Diabetes Mellitus
EK Blue, BA Sheehan, ZV Nuss, FA Boyle, CM Hocutt, CR Gohn, KM Varberg, JN McClintick, LS Haneline
Diabetes 2015
Long-Term Pancreatic Beta Cell Exposure to High Levels of Glucose but Not Palmitate Induces DNA Methylation within the Insulin Gene Promoter and Represses Transcriptional Activity
K Ishikawa, S Tsunekawa, M Ikeniwa, T Izumoto, A Iida, H Ogata, E Uenishi, Y Seino, N Ozaki, Y Sugimura, Y Hamada, A Kuroda, K Shinjo, Y Kondo, Y Oiso, E Ayuso
PloS one 2015
Epigenetic modifications and long noncoding RNAs influence pancreas development and function
L Arnes, L Sussel
Trends in Genetics 2015
Fetal, Neonatal, Infant, and Child International Growth Standards: An Unprecedented Opportunity for an Integrated Approach to Assess Growth and Development
C Garza
Advances in nutrition (Bethesda, Md.) 2015
I’m Eating for Two: Parental Dietary Effects on Offspring Metabolism
OJ Rando, RA Simmons
Cell 2015
Heritable IUGR and adult metabolic syndrome are reversible and associated with alterations in the metabolome following dietary supplementation of 1-carbon intermediates
MD Seferovic, DM Goodspeed, DM Chu, LA Krannich, PJ Gonzalez-Rodriguez, JE Cox, KM Aagaard
The FASEB Journal 2015
Chromatin deregulation in disease
AC Mirabella, BM Foster, T Bartke
Chromosoma 2015
Reversing Fetal Undernutrition by Kick-Starting Early Growth
K Shankar
Endocrinology 2015
Early Life Nutrition and Energy Balance Disorders in Offspring in Later Life
C Reynolds, C Gray, M Li, S Segovia, M Vickers
Nutrients 2015
Intergenerational epigenetic inheritance in models of developmental programming of adult disease
DS Fernandez-Twinn, M Constância, SE Ozanne
Seminars in Cell & Developmental Biology 2015
MicroRNAs and mTOR levels contribute to developmental programming of β-cells
Emilyn Alejandro, Brigid Gregg, Taylor Wallen, Doga Kumusoglu, Daniel Meister, Angela Chen, Matthew Merrins, Leslie Satin, Ming Liu, Peter Arvan, Ernesto Bernal-Mizrachi
Journal of Clinical Investigation 2014
Natural history of β-cell adaptation and failure in type 2 diabetes
EU Alejandro, B Gregg, M Blandino-Rosano, C Cras-Méneur, E Bernal-Mizrachi
Molecular Aspects of Medicine 2014
Gene-Environment Interactions Controlling Energy and Glucose Homeostasis and the Developmental Origins of Obesity
S Bouret, BE Levin, SE Ozanne
Physiological reviews 2014
New Insights Into Molecular Mechanisms of Diabetic Kidney Disease
SS Badal, FR Danesh
American Journal of Kidney Diseases 2014
Fetal hyperglycemia and a high-fat diet contribute to aberrant glucose tolerance and hematopoiesis in adult rats
EK Blue, K Ballman, F Boyle, E Oh, T Kono, SK Quinney, DC Thurmond, C Evans-Molina, LS Haneline
Pediatric Research 2014
Effects of genetics and in utero diet on murine pancreatic development
CL Lin, L Williams, Y Seki, H Kaur, K Hartil, A Fiallo, AS Glenn, EB Katz, MJ Charron, PM Vuguin
Journal of Endocrinology 2014
Genome-wide DNA methylation analysis of human pancreatic islets from type 2 diabetic and non-diabetic donors identifies candidate genes that influence insulin secretion
T Dayeh, P Volkov, S Salö, E Hall, E Nilsson, AH Olsson, CL Kirkpatrick, CB Wollheim, L Eliasson, T Rönn, K Bacos, C Ling
PLoS genetics 2014
Translational implications of the β-cell epigenome in diabetes mellitus
JS Johnson, C Evans-Molina
Translational Research 2014
Early Developmental Conditioning of Later Health and Disease: Physiology or Pathophysiology?
MA Hanson, PD Gluckman
Physiological reviews 2014
Effects of palmitate on genome-wide mRNA expression and DNA methylation patterns in human pancreatic islets
E Hall, P Volkov, T Dayeh, K Bacos, T Rönn, MD Nitert, C Ling
BMC Medicine 2014
11p15 DNA-methylation analysis in monozygotic twins with discordant intrauterine development due to severe twin-to-twin transfusion syndrome
F Schreiner, B Gohlke, S Stutte, P Bartmann, K Hecher, J Oldenburg, O El-Maarri, J Woelfle
Clinical Epigenetics 2014
Non-referenced genome assembly from epigenomic short-read data
A Kaspi, M Ziemann, ST Keating, I Khurana, T Connor, B Spolding, A Cooper, R Lazarus, K Walder, P Zimmet, A El-Osta
Epigenetics : official journal of the DNA Methylation Society 2014
Novel DNA methylation profiles associated with key gene regulation and transcription pathways in blood and placenta of growth-restricted neonates
SL Hillman, S Finer, MC Smart, C Mathews, R Lowe, VK Rakyan, GA Hitman, DJ Williams
Epigenetics : official journal of the DNA Methylation Society 2014
Epigenetics of hyper-responsiveness to allergen challenge following intrauterine growth retardation rat
XF Xu, QY Hu, LF Liang, L Wu, WZ Gu, LL Tang, LC Fu, LZ Du
Respiratory Research 2014
Exercise Prevents Maternal High-Fat Diet–Induced Hypermethylation of the Pgc-1α Gene and Age-Dependent Metabolic Dysfunction in the Offspring
RC Laker, TS Lillard, M Okutsu, M Zhang, KL Hoehn, JJ Connelly, Z Yan
Diabetes 2014
Epigenetics across the human lifespan
RR Kanherkar, N Bhatia-Dey, AB Csoka
Frontiers in Cell and Developmental Biology 2014
Down-regulation of pancreatic and duodenal homeobox-1 by somatostatin receptor subtype 5: a novel mechanism for inhibition of cellular proliferation and insulin secretion by somatostatin
G Zhou, J Sinnett-Smith, SH Liu, J Yu, J Wu, R Sanchez, SJ Pandol, R Abrol, J Nemunaitis, E Rozengurt, FC Brunicardi
Frontiers in physiology 2014
The Missing lnc(RNA) between the pancreatic β-cell and diabetes
V Kameswaran, KH Kaestner
Frontiers in Genetics 2014
Early life nutrition, epigenetics and programming of later life disease
MH Vickers
Nutrients 2014
Detection of type 2 diabetes related modules and genes based on epigenetic networks
H Liu, T Wang, H Liu, Y Wei, G Zhao, J Su, Q Wu, H Qiao, Y Zhang
BMC Systems Biology 2014
Childhood bone mineral content is associated with methylation status of the RXRA promoter at birth
NC Harvey, A Sheppard, KM Godfrey, C McLean, E Garratt, G Ntani, L Davies, R Murray, HM Inskip, PD Gluckman, MA Hanson, KA Lillycrop, C Cooper
Journal of Bone and Mineral Research 2014
Mammalian Non-CpG Methylation: Stem Cells and Beyond
S Pinney
Biology : open access journal 2014
Epigenetic contributions to the developmental origins of adult lung disease
LA Joss-Moore, RH Lane, KH Albertine
Biochemistry and Cell Biology 2014
Epigenetics and type II diabetes mellitus: underlying mechanisms of prenatal predisposition
JD Sterns, CB Smith, JR Steele, KL Stevenson, GI Gallicano
Frontiers in Cell and Developmental Biology 2014
Epigenome: Biosensor of Cumulative Exposure to Chemical and Nonchemical Stressors Related to Environmental Justice
K Olden, YS Lin, D Gruber, B Sonawane
American journal of public health 2014
Persistent Apparent Pancreatic β-Cell Defects in Premenarchal PCOS Relatives
LC Torchen, NR Fogel, WJ Brickman, R Paparodis, A Dunaif
The Journal of clinical endocrinology and metabolism 2014
Essential nutrient supplementation prevents heritable metabolic disease in multigenerational intrauterine growth-restricted rats
D Goodspeed, MD Seferovic, W Holland, RA Mcknight, SA Summers, DW Branch, RH Lane, KM Aagaard
The FASEB Journal 2014
 -Cell Failure in Type 2 Diabetes: Postulated Mechanisms and Prospects for Prevention and Treatment
PA Halban, KS Polonsky, DW Bowden, MA Hawkins, C Ling, KJ Mather, AC Powers, CJ Rhodes, L Sussel, GC Weir
Diabetes care 2014
 -Cell Failure in Type 2 Diabetes: Postulated Mechanisms and Prospects for Prevention and Treatment
PA Halban, KS Polonsky, DW Bowden, MA Hawkins, C Ling, KJ Mather, AC Powers, CJ Rhodes, L Sussel, GC Weir
Diabetes care 2014
MafA, MafB, Nkx6.1 and Pdx1 inactivation in Type 2 diabetes
Shuangli Guo, Chunhua Dai, Min Guo, Brandon Taylor, Jamie Harmon, Maike Sander, R. Paul Robertson, Alvin Powers, Roland Stein
Journal of Clinical Investigation 2013
Epigenetics of hypoxic pulmonary arterial hypertension following intrauterine growth retardation rat: epigenetics in PAH following IUGR
XF Xu, Y Lv, WZ Gu, LL Tang, JK Wei, LY Zhang, LZ Du
Respiratory Research 2013
The transcriptional co-regulator HCF-1 is required for INS-1 β-cell glucose-stimulated insulin secretion
TN Iwata, TJ Cowley, M Sloma, Y Ji, H Kim, L Qi, SS Lee
PloS one 2013
Developmental and environmental epigenetic programming of the endocrine pancreas: consequences for type 2 diabetes
I Sandovici, CM Hammerle, SE Ozanne, M Constância
Cellular and Molecular Life Sciences 2013
Microarray analysis of novel candidate genes responsible for glucose-stimulated insulin secretion in mouse pancreatic β cell line MIN6
E Yamato, F Tashiro, J Miyazaki
PloS one 2013
Neonatal exendin-4 reduces growth, fat deposition and glucose tolerance during treatment in the intrauterine growth-restricted lamb
KL Gatford, SA Sulaiman, SN Mohammad, MJ de Blasio, ML Harland, RA Simmons, JA Owens
PloS one 2013
Epigenetic Regulation of Pancreatic Islets
C Haumaitre
Current Diabetes Reports 2013
Developmental origins of obesity and type 2 diabetes: molecular aspects and role of chemicals
H Inadera
Environmental Health and Preventive Medicine 2013
Towards identification of molecular mechanisms of short stature
LA Waldman, DJ Chia
International Journal of Pediatric Endocrinology 2013
Global differences in specific histone H3 methylation are associated with overweight and type 2 diabetes
A Jufvas, S Sjödin, K Lundqvist, R Amin, AV Vener, P Strålfors
Clinical Epigenetics 2013
Current Thoughts on Maternal Nutrition and Fetal Programming of the Metabolic Syndrome
B Brenseke, MR Prater, J Bahamonde, JC Gutierrez
Journal of Pregnancy 2013
Maternal Obesity Enhances White Adipose Tissue Differentiation and Alters Genome-Scale DNA Methylation in Male Rat Offspring
SJ Borengasser, Y Zhong, P Kang, F Lindsey, MJ Ronis, TM Badger, H Gomez-Acevedo, K Shankar
Endocrinology 2013
Intrauterine growth retardation – a developmental model of type 2 diabetes
SE Pinney
Drug Discovery Today: Disease Models 2013
Paternal transgenerational glucose intolerance with epigenetic alterations in second generation offspring of GDM
GL Ding, HF Huang
Asian Journal of Andrology 2013
Reducing maternal weight improves offspring metabolism and alters (or modulates) methylation
ME Patti
Proceedings of the National Academy of Sciences 2013
Maternal Exercise Improves Insulin Sensitivity in Mature Rat Offspring:
LG Carter, NR Qi, RD Cabo, KJ Pearson
Medicine and Science in Sports and Exercise 2013
Genetic effects on DNA methylation and its potential relevance for obesity in Mexican Americans
MA Carless, H Kulkarni, MZ Kos, J Charlesworth, JM Peralta, HH Göring, JE Curran, L Almasy, TD Dyer, AG Comuzzie, MC Mahaney, J Blangero
PloS one 2013
Endocrine pancreatic development: impact of obesity and diet
JF O'Dowd, CJ Stocker
Frontiers in physiology 2013
Mutations in Mll2, an H3K4 methyltransferase, result in insulin resistance and impaired glucose tolerance in mice
M Goldsworthy, NL Absalom, D Schröter, HC Matthews, D Bogani, L Moir, A Long, C Church, A Hugill, QM Anstee, R Goldin, M Thursz, F Hollfelder, RD Cox
PloS one 2013
Maternal obesity and diabetes induces latent metabolic defects and widespread epigenetic changes in isogenic mice
CC Li, PE Young, CA Maloney, SA Eaton, MJ Cowley, ME Buckland, T Preiss, DC Henstridge, GJ Cooney, MA Febbraio, DI Martin, JE Cropley, CM Suter
Epigenetics : official journal of the DNA Methylation Society 2013
Enhanced Trimethylation of Histone H3 Mediates Impaired Expression of Hepatic Glucose 6-Phosphatase Expression in Offspring From Rat Dams Exposed to Hypoxia During Pregnancy
JE Osumek, A Revesz, JS Morton, ST Davidge, DB Hardy
Reproductive sciences (Thousand Oaks, Calif.) 2013
Role of endogenous IL-6 in the neonatal expansion and functionality of Wistar rat pancreatic alpha cells
E Fernández-Millán, J de Toro-Martín, E Lizárraga-Mollinedo, F Escrivá, C Álvarez
Diabetologia 2013
Metabolic syndrome: Role of maternal undernutrition and fetal programming
R Lakshmy
Reviews in Endocrine and Metabolic Disorders 2013
Impact of an exercise intervention on DNA methylation in skeletal muscle from first-degree relatives of patients with type 2 diabetes
MD Nitert, T Dayeh, P Volkov, T Elgzyri, E Hall, E Nilsson, BT Yang, S Lang, H Parikh, Y Wessman, H Weishaupt, J Attema, M Abels, N Wierup, P Almgren, PA Jansson, T Rönn, O Hansson, KF Eriksson, L Groop, C Ling
Diabetes 2012
Transgenerational glucose intolerance with Igf2/H19 epigenetic alterations in mouse islet induced by intrauterine hyperglycemia
GL Ding, FF Wang, J Shu, S Tian, Y Jiang, D Zhang, N Wang, Q Luo, Y Zhang, F Jin, PC Leung, JZ Sheng, HF Huang
Diabetes 2012
Epigenetics and diabetes treatment: an unrealized promise?
NC Bramswig, KH Kaestner
Trends in Endocrinology & Metabolism 2012
Mechanisms underlying the developmental origins of disease
MS Martin-Gronert, SE Ozanne
Reviews in Endocrine and Metabolic Disorders 2012
DNA methylation at differentially methylated regions of imprinted genes is resistant to developmental programming by maternal nutrition
E Ivanova, JH Chen, A Segonds-Pichon, SE Ozanne, G Kelsey
Epigenetics : official journal of the DNA Methylation Society 2012
Increased DNA methylation and decreased expression of PDX-1 in pancreatic islets from patients with type 2 diabetes
BT Yang, TA Dayeh, PA Volkov, CL Kirkpatrick, S Malmgren, X Jing, E Renström, CB Wollheim, MD Nitert, C Ling
Molecular Endocrinology 2012
Nutrition, Epigenetics, and Metabolic Syndrome
J Wang, Z Wu, D Li, N Li, SV Dindot, MC Satterfield, FW Bazer, G Wu
Antioxidants & Redox Signaling 2012
DNA methylation profiling identifies epigenetic dysregulation in pancreatic islets from type 2 diabetic patients
M Volkmar, S Dedeurwaerder, DA Cunha, MN Ndlovu, M Defrance, R Deplus, E Calonne, U Volkmar, M Igoillo-Esteve, N Naamane, SD Guerra, M Masini, M Bugliani, P Marchetti, M Cnop, DL Eizirik, F Fuks
The EMBO Journal 2012
Epigenetic Inheritance of Disease and Disease Risk
J Bohacek, IM Mansuy
Neuropsychopharmacology 2012
Early postnatal low-protein nutrition, metabolic programming and the autonomic nervous system in adult life
JC de Oliveira, S Grassiolli, C Gravena, PC de Mathias
Nutrition & Metabolism 2012
Developmental origins of adult diseases
V Mathew, SV Ayyar
Indian journal of endocrinology and metabolism 2012
Mechanisms affecting neuroendocrine and epigenetic regulation of body weight and onset of puberty: Potential implications in the child born small for gestational age (SGA)
CL Roth, S Sathyanarayana
Reviews in Endocrine and Metabolic Disorders 2012
Gestational Diabetes and the Offspring: Implications in the Development of the Cardiorenal Metabolic Syndrome in Offspring
L Garcia-Vargas, SS Addison, R Nistala, D Kurukulasuriya, JR Sowers
Cardiorenal Medicine 2012
The thrifty phenotype hypothesis revisited
AA Vaag, LG Grunnet, GP Arora, C Brøns
Diabetologia 2012
An Unbiased Assessment of the Role of Imprinted Genes in an Intergenerational Model of Developmental Programming
EJ Radford, E Isganaitis, J Jimenez-Chillaron, J Schroeder, M Molla, S Andrews, N Didier, M Charalambous, K McEwen, G Marazzi, D Sassoon, ME Patti, AC Ferguson-Smith
PLoS genetics 2012
Strategies for Reversing the Effects of Metabolic Disorders Induced as a Consequence of Developmental Programming
MH Vickers, DM Sloboda
Frontiers in physiology 2012
Impact of Oxidative Stress in Fetal Programming
LP Thompson, Y Al-Hasan
Journal of Pregnancy 2012
Epigenetic mechanisms and therapeutic perspectives for neurodevelopmental disorders
T Kubota, H Takae, K Miyake
Pharmaceuticals (Basel, Switzerland) 2012
Frontiers in research on maternal diabetes-induced neural tube defects: Past, present and future
S Sukanya, BH Bay, SS Tay, ST Dheen
World journal of diabetes 2012
Early childhood growth failure and the developmental origins of adult disease: do enteric infections and malnutrition increase risk for the metabolic syndrome?
MD DeBoer, AA Lima, RB Oría, RJ Scharf, SR Moore, MA Luna, RL Guerrant
Nutrition Reviews 2012
Increased hepatic glucose production in fetal sheep with intrauterine growth restriction is not suppressed by insulin
SR Thorn, LD Brown, PJ Rozance, WW Hay, JE Friedman
Diabetes 2012
Epigenetics: the missing link to understanding β-cell dysfunction in the pathogenesis of type 2 diabetes
ER Gilbert, D Liu
Epigenetics : official journal of the DNA Methylation Society 2012
Metabolic memory and chronic diabetes complications: potential role for epigenetic mechanisms
RV Intine, MP Sarras
Current Diabetes Reports 2012
Minireview: Epigenetic programming of diabetes and obesity: animal models
Y Seki, L Williams, PM Vuguin, MJ Charron
Endocrinology 2012
Update: consequences of abnormal fetal growth
SD Chernausek
The Journal of clinical endocrinology and metabolism 2012
Epigenetics and developmental programming of adult onset diseases
L OSullivan, MH Little, AN Combes, KM Moritz
Pediatric Nephrology 2012
The Epigenome and Its Role in Diabetes
H Waki, T Yamauchi, T Kadowaki
Current Diabetes Reports 2012
Who Should We Target for Diabetes Prevention and Diabetes Risk Reduction?
S Blüher, J Markert, S Herget, T Yates, M Davis, G Müller, T Waldow, PE Schwarz
Current Diabetes Reports 2012
Maternal protein restriction elevates cholesterol in adult rat offspring due to repressive changes in histone modifications at the cholesterol 7alpha-hydroxylase promoter
G Sohi, K Marchand, A Revesz, E Arany, DB Hardy
Molecular Endocrinology 2011
Epigenetics: deciphering its role in diabetes and its chronic complications: Chronic kidney disease
LM Villeneuve, MA Reddy, R Natarajan
Clinical and Experimental Pharmacology and Physiology 2011
Knockouts of SOD1 and GPX1 Exert Different Impacts on Murine Islet Function and Pancreatic Integrity
X Wang, MZ Vatamaniuk, CA Roneker, MP Pepper, LG Hu, RA Simmons, XG Lei
Antioxidants & Redox Signaling 2011
Histone deacetylase (HDAC) inhibition as a novel treatment for diabetes mellitus
DP Christensen, M Dahllöf, M Lundh, DN Rasmussen, MD Nielsen, N Billestrup, LG Grunnet, T Mandrup-Poulsen
Molecular Medicine 2011
Epigenetic mechanisms in developmental programming of adult disease
M Chen, L Zhang
Drug Discovery Today 2011
Two Tales of Antioxidant Enzymes on β Cells and Diabetes
XG Lei, MZ Vatamaniuk
Antioxidants & Redox Signaling 2011
Multiparity leads to obesity and inflammation in mothers and obesity in male offspring
SL Rebholz, T Jones, KT Burke, A Jaeschke, P Tso, DA D'Alessio, LA Woollett
American journal of physiology. Endocrinology and metabolism 2011
Early-Life Origins of Type 2 Diabetes: Fetal Programming of the Beta-Cell Mass
B Portha, A Chavey, J Movassat
Experimental Diabetes Research 2011
Exendin-4 increases histone acetylase activity and reverses epigenetic modifications that silence Pdx1 in the intrauterine growth retarded rat
SE Pinney, LJ Santos, Y Han, DA Stoffers, RA Simmons
Diabetologia 2011
Maternal diet and aging alter the epigenetic control of a promoter-enhancer interaction at the Hnf4a gene in rat pancreatic islets
I Sandovici, NH Smith, MD Nitert, M Ackers-Johnson, S Uribe-Lewis, Y Ito, RH Jones, VE Marquez, W Cairns, M Tadayyon, LP O'Neill, A Murrell, C Ling, M Constância, SE Ozanne
Proceedings of the National Academy of Sciences 2011
Fetal programming and metabolic syndrome
P Rinaudo, E Wang
Annual Review of Physiology 2011
Association of COMT genotypes with S-COMT promoter methylation in growth-discordant monozygotic twins and healthy adults
F Schreiner, O El-Maarri, B Gohlke, S Stutte, N Nuesgen, M Mattheisen, R Fimmers, P Bartmann, J Oldenburg, J Woelfle
BMC Medical Genetics 2011
A sustained dietary change increases epigenetic variation in isogenic mice
CC Li, JE Cropley, MJ Cowley, T Preiss, DI Martin, CM Suter
PLoS genetics 2011
Epigenetic mechanisms in diabetic vascular complications
MA Reddy, R Natarajan
Cardiovascular Research 2011
Epigenetic mechanisms involved in developmental nutritional programming
A Gabory, L Attig, C Junien
World journal of diabetes 2011
Developmental programming of the metabolic syndrome - critical windows for intervention
MH Vickers
World journal of diabetes 2011
Metabolic Programming in the Immediate Postnatal Life
MS Patel, M Srinivasan
Annals of nutrition & metabolism 2011
DNA methylation of IGF2, GNASAS, INSIGF and LEP and being born small for gestational age
EW Tobi, BT Heijmans, D Kremer, H Putter, HA de Waal, MJ Finken, JM Wit, PE Slagboom
Epigenetics : official journal of the DNA Methylation Society 2011
Inhibition of TGF-β Signaling and Decreased Apoptosis in IUGR-Associated Lung Disease in Rats
MA Alcázar, RE Morty, L Lendzian, C Vohlen, I Oestreicher, C Plank, H Schneider, J Dötsch
PloS one 2011
Humans at high altitude: hypoxia and fetal growth
LG Moore, SM Charles, CG Julian
Respiratory Physiology & Neurobiology 2011
Evaluation of methylation status of the eNOS promoter at birth in relation to childhood bone mineral content
NC Harvey, KA Lillycrop, E Garratt, A Sheppard, C McLean, G Burdge, J Slater-Jefferies, J Rodford, S Crozier, H Inskip, BS Emerald, CR Gale, M Hanson, P Gluckman, K Godfrey, C Cooper
Calcified Tissue International 2011
Maternal nicotine exposure and fetal programming of vascular oxidative stress in adult offspring
R Lim, CG Sobey
British Journal of Pharmacology 2011
Metabolic Programming, Epigenetics, and Gestational Diabetes Mellitus
SE Pinney, RA Simmons
Current Diabetes Reports 2011
Glial cell line-derived neurotrophic factor enhances neurogenin3 gene expression and beta-cell proliferation in the developing mouse pancreas
SM Mwangi, Y Usta, SM Raja, M Anitha, B Chandrasekharan, A Parsadanian, SV Sitaraman, S Srinivasan
American journal of physiology. Gastrointestinal and liver physiology 2010
Maternal obesity and fetal metabolic programming: a fertile epigenetic soil
MJ Heerwagen, MR Miller, LA Barbour, JE Friedman
American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2010
Differential Effects of Prenatal and Postnatal Nutritional Environment on β-Cell Mass Development and Turnover in Male and Female Rats
AV Matveyenko, I Singh, BC Shin, S Georgia, SU Devaskar
Endocrinology 2010
Hepatocyte nuclear factor (HNF)-4α-driven epigenetic silencing of the human PED gene
P Ungaro, R Teperino, P Mirra, M Longo, M Ciccarelli, GA Raciti, C Nigro, C Miele, P Formisano, F Beguinot
Diabetologia 2010
The role of epigenetics in the pathology of diabetic complications
LM Villeneuve, R Natarajan
American journal of physiology. Renal physiology 2010
Experimental intrauterine growth restriction induces alterations in DNA methylation and gene expression in pancreatic islets of rats
RF Thompson, MJ Fazzari, H Niu, N Barzilai, RA Simmons, JM Greally
The Journal of biological chemistry 2010
Epigenetics of diabetic complications
LM Villeneuve, R Natarajan
Expert Review of Endocrinology & Metabolism 2010
The Possible Role of Epigenetics in Gestational Diabetes: Cause, Consequence, or Both
JL Fernández-Morera, S Rodríguez-Rodero, E Menéndez-Torre, MF Fraga
Obstetrics and Gynecology International 2010
Insulin resistance is not conserved in myotubes established from women with PCOS
M Eriksen, AD Pørneki, V Skov, JS Burns, H Beck-Nielsen, D Glintborg, M Gaster
PloS one 2010
Regulation of homocysteine metabolism and methylation in human and mouse tissues
NC Chen, F Yang, LM Capecci, Z Gu, AI Schafer, W Durante, XF Yang, H Wang
The FASEB Journal 2010
Stress and the epigenetic landscape: a link to the pathobiology of human diseases?
SE Johnstone, SB Baylin
Nature reviews. Genetics 2010
Developmental origins of health and disease: reducing the burden of chronic disease in the next generation
PD Gluckman, MA Hanson, MD Mitchell
Genome Medicine 2010
Child Health, Developmental Plasticity, and Epigenetic Programming
Z Hochberg, R Feil, M Constancia, M Fraga, C Junien, JC Carel, P Boileau, YL Bouc, CL Deal, K Lillycrop, R Scharfmann, A Sheppard, M Skinner, M Szyf, RA Waterland, DJ Waxman, E Whitelaw, K Ong, K Albertsson-Wikland
Endocrine reviews 2010
Epigenetic Changes Predisposing to Type 2 Diabetes in Intrauterine Growth Retardation
A Liguori, A Puglianiello, D Germani, A Deodati, E Peschiaroli, S Cianfarani
Frontiers in Endocrinology 2010
Consequences of a compromised intrauterine environment on islet function
AS Green, PJ Rozance, SW Limesand
Journal of Endocrinology 2010
Review: Placental Programming of Postnatal Diabetes and Impaired Insulin Action after IUGR
KL Gatford, RA Simmons, MJ Blasio, JS Robinson, JA Owens
Placenta 2010
Obstetrical and Neonatal Outcomes of Pregnancies following Gastric Bypass Surgery: A Retrospective Cohort Study in a French Referral Centre
P Santulli, L Mandelbrot, E Facchiano, C Dussaux, PF Ceccaldi, S Ledoux, S Msika
Obesity Surgery 2010
Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd
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Pdx1 and other factors that regulate pancreatic β-cell survival
K Fujimoto, KS Polonsky
Diabetes, Obesity and Metabolism 2009
Epigenetics and fetal adaptation to perinatal events: Diversity through fidelity
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Journal of animal science 2009
Nutritional programming of the metabolic syndrome
ME Symonds, SP Sebert, MA Hyatt, H Budge
Nature Reviews Endocrinology 2009
Epigenetics: A Molecular Link Between Environmental Factors and Type 2 Diabetes
C Ling, L Groop
Diabetes 2009
Expansion of beta-cell mass in response to pregnancy
S Rieck, KH Kaestner
Trends in endocrinology and metabolism: TEM 2009
Epigenetic mechanisms that underpin metabolic and cardiovascular diseases
PD Gluckman, MA Hanson, T Buklijas, FM Low, AS Beedle
Nature Reviews Endocrinology 2009
Accelerated postnatal growth increases lipogenic gene expression and adipocyte size in low-birth weight mice
E Isganaitis, J Jimenez-Chillaron, M Woo, A Chow, J DeCoste, M Vokes, M Liu, S Kasif, AM Zavacki, RL Leshan, MG Myers, ME Patti
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Epigenetic mechanisms in the development of type 2 diabetes
SE Pinney, RA Simmons
Trends in endocrinology and metabolism: TEM 2009
Hypothalamic proopiomelanocortin promoter methylation becomes altered by early overfeeding: an epigenetic model of obesity and the metabolic syndrome
A Plagemann, T Harder, M Brunn, A Harder, K Roepke, M Wittrock-Staar, T Ziska, K Schellong, E Rodekamp, K Melchior, JW Dudenhausen
The Journal of Physiology 2009
Dissection of genetic factors modulating fetal growth in cattle indicates a substantial role of the non-SMC condensin I complex, subunit G (NCAPG) gene
A Eberlein, A Takasuga, K Setoguchi, R Pfuhl, K Flisikowski, R Fries, N Klopp, R Fürbass, R Weikard, C Kühn
Genetics 2009
Consequences of perinatal treatment with L-arginine and antioxidants for the renal transcriptome in spontaneously hypertensive rats
S Wesseling, MP Koeners, F Kantouh, JA Joles, B Braam
Pflügers Archiv : European journal of physiology 2009
Sleeping Beauty, awake! Regulation of insulin gene expression by methylation of histone H3
DR Cavener
Diabetes 2009
Developmental Origins of Adult Disease
RA Simmons
Pediatric Clinics of North America 2009
The developmental origins of adult disease.
Joss-Moore LA, Lane RH
Current Opinion in Pediatrics 2009
Intergenerational Transmission of Glucose Intolerance and Obesity by In Utero Undernutrition in Mice
JC Jimenez-Chillaron, E Isganaitis, M Charalambous, S Gesta, T Pentinat-Pelegrin, RR Faucette, JP Otis, A Chow, R Diaz, A Ferguson-Smith, ME Patti
Diabetes 2008
Metabolic syndrome: from epidemiology to systems biology
AJ Lusis, AD Attie, K Reue
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The Emerging Genetic Architecture of Type 2 Diabetes
A Doria, ME Patti, CR Kahn
Cell Metabolism 2008
Highly individual methylation patterns of alternative glucocorticoid receptor promoters suggest individualized epigenetic regulatory mechanisms
JD Turner, LP Pelascini, JA Macedo, CP Muller
Nucleic Acids Research 2008
A fingerprint marker from early gestation associated with diabetes in middle age: the Dutch Hunger Winter Families Study
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International Journal of Epidemiology 2008

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