Increased Hepatic Glucose Production in Fetal Sheep With Intrauterine Growth Restriction Is Not Suppressed by Insulin

Thorn, Stephanie R.; Brown, Laura D.; Rozance, Paul J.; Hay, William W.; Friedman, Jacob E.

doi:10.2337/db11-1727

Cited by 89Birth, Development, and HealthPregnancy and preeclampsia studiesPancreatic function and diabetes

Increased Hepatic Glucose Production in Fetal Sheep With Intrauterine Growth Restriction Is Not Suppressed by Insulin

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Thorn, Stephanie R., Brown, Laura D., Rozance, Paul J., Hay, William W., Friedman, Jacob E.·2013·Diabetes

DOI 10.2337/db11-1727PMC PMC3526037

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Abstract

Intrauterine growth restriction (IUGR) increases the risk for metabolic disease and diabetes, although the developmental origins of this remain unclear. We measured glucose metabolism during basal and insulin clamp periods in a fetal sheep model of placental insufficiency and IUGR. Compared with control fetuses (CON), fetuses with IUGR had increased basal glucose production rates and hepatic PEPCK and glucose-6-phosphatase expression, which were not suppressed by insulin. In contrast, insulin significantly increased peripheral glucose utilization rates in CON and IUGR fetuses. Insulin robustly activated AKT, GSK3β, and forkhead box class O (FOXO)1 in CON and IUGR fetal livers. IUGR livers, however, had increased basal FOXO1 phosphorylation, nuclear FOXO1 expression, and Jun NH2-terminal kinase activation during hyperinsulinemia. Expression of peroxisome proliferator–activated receptor γ coactivator 1α and hepatocyte nuclear factor-4α were increased in IUGR livers during basal and insulin periods. Cortisol and norepinephrine concentrations were positively correlated with glucose production rates. Isolated IUGR hepatocytes maintained increased glucose production in culture. In summary, fetal sheep with IUGR have increased hepatic glucose production, which is not suppressed by insulin despite insulin sensitivity for peripheral glucose utilization. These data are consistent with a novel mechanism involving persistent transcriptional activation in the liver that seems to be unique in the fetus with IUGR.

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Maternal undernutrition may lead to foetal growth restriction, characterised by reduced pancreatic growth, impaired insulin secretion, and hepatic insulin resistance.
“Maternal undernutrition may lead to foetal growth restriction (FGR), characterised by reduced pancreatic growth, impaired insulin secretion, and hepatic insulin resistance [28,29,30].”
From Medical Nutrition Therapy for Women with Gestational Diabetes: Current Practice and Future Perspectives (2025) · cites this paper as [30]
The Discussion (page unavailable) reports that insulin did not suppress hepatic glucose production in growth-restricted fetal sheep, and the introductory text reports decreased pancreatic insulin secretion in animal models of growth restriction. But the Methods (page unavailable) describe growth restriction induced by maternal heat exposure, not maternal undernutrition; our copy also does not establish reduced pancreatic growth. (LLM, conf=0.88)
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Authors: Thorn, S. R., Brown, L. D., Rozance, P. J., Hay, W. W., & Friedman, J. E.
Affiliations: Perinatal Research Center, Department of Pediatrics, University of Colorado School of Medicine, Aurora, Colorado
University of Colorado Anschutz (US)
ORCID: Brown, Laura D.
Rozance, Paul J.
Hay, William W.
Friedman, Jacob E.
Venue: Diabetes
Publisher: American Diabetes Association
Published: 2012-12-13
Volume: 62
Issue: 1
Pages: 65-73
ISSN: 0012-1797 (ISSN-L)
1939-327X
DOI: 10.2337/db11-1727
PMC: PMC3526037
OpenAlex: W2162533346
Cited by: 89
References: 51
Citations by year: 2026: 5 · 2025: 8 · 2024: 6 · 2023: 6 · 2022: 5 · 2021: 9 · 2020: 5 · 2019: 7 · 2018: 8 · 2017: 6 · 2016: 12 · 2015: 3 · 2014: 7 · 2013: 1 · 2012: 1
FWCI: 3.37
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-nd
creativecommons.org/licenses/by-nc-nd/3.0/ (vor, 3179 d)
Locations: Diabetes (publishedVersion, cc-by-nc-nd)
PubMed Central (publishedVersion, cc-by-nc-nd)
PubMed (publishedVersion)
Funders: National Institute of Diabetes and Digestive and Kidney Diseases (F32-DK-08220, R01DK088139, P50-DK-048520, K01DK090199, P30DK048520)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (K08HD060688, K12-HD-04332, T32HD007186)
Topics: Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
Keywords: fetal growth restriction, hepatic glucose production, insulin resistance, fetal liver, placental insufficiency, fetal sheep, phosphoenolpyruvate carboxykinase, glucose-6-phosphatase, FOXO1, JNK, Akt/GSK-3β signaling, PPARγ coactivator-1α, HNF4α, cortisol, norepinephrine, hyperinsulinemia, developmental origins of health and disease, diabetes risk
MeSH terms: Animals, Female, Fetal Growth Retardation, Fetus, Gluconeogenesis, Glucose, Hydrocortisone, Insulin, Liver, Sheep, Hepatocytes, JNK Mitogen-Activated Protein Kinases, Proto-Oncogene Proteins c-akt, Forkhead Transcription Factors

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Increased Hepatic Glucose Production in Fetal Sheep With Intrauterine Growth Restriction Is Not Suppressed by Insulin

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