Age-Dependent Control of Energy Homeostasis by Brown Adipose Tissue in Progeny Subjected to Maternal Diet–Induced Fetal Programming
Abstract
Epidemiological and animal studies show that deleterious maternal environments predispose aging offspring to metabolic disorders and type 2 diabetes. Young progenies in a rat model of maternal low-protein (LP) diet are normoglycemic despite collapsed insulin secretion. However, without further worsening of the insulin secretion defect, glucose homeostasis deteriorates in aging LP descendants. Here we report that normoglycemic and insulinopenic 3-month-old LP progeny shows increased body temperature and energy dissipation in association with enhanced brown adipose tissue (BAT) activity. In addition, it is protected against a cold challenge and high-fat diet (HFD)–induced obesity with associated insulin resistance and hyperglycemia. Surgical BAT ablation in 3-month-old LP offspring normalizes body temperature and causes postprandial hyperglycemia. At 10 months, BAT activity declines in LP progeny with the appearance of reduced protection to HFD-induced obesity; at 18 months, LP progeny displays a BAT activity comparable to control offspring and insulin resistance and hyperglycemia occur. Together our findings identify BAT as a decisive physiological determinant of the onset of metabolic dysregulation in offspring predisposed to altered β-cell function and hyperglycemia and place it as a critical regulator of fetal programming of adult metabolic disease.
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As offspring from protein restricted mothers get older, they have a greater sensitivity to the obesogenic effect and metabolic dysfunction induced by chronic exposure to high-fat diet.
“Furthermore, as they get older, offspring from protein restricted mothers have a greater sensitivity to the obesogenic effect and metabolic dysfunction induced by chronic exposure to high-fat diet [79].”
From Developmental programming of offspring adipose tissue biology and obesity risk (2021) · cites this paper as [79]
Offspring of low protein diet-fed mothers show increased BAT thermogenic activity and UCP1 expression, which may provide some explanation for their initial protection against high-fat-diet-induced obesity as young adults.
“Finally, although less explored, offspring of low protein diet-fed mothers show increased BAT thermogenic activity and UCP1 expression [79], which may provide some explanation for their initial protection against high-fat-diet-induced obesity as young adults.”
From Developmental programming of offspring adipose tissue biology and obesity risk (2021) · cites this paper as [79]
Cites
Brown adipose tissue activity controls triglyceride clearance
Bartelt, A., Bruns, O. T., Reimer, R., Hohenberg, H., Ittrich, H., Peldschus, K., Kaul, M. G., Tromsdorf, U. I., Weller, H., Waurisch, C., et al. (2011) · Nature Medicine · doi:10.1038/nm.2297 · Cited by 1,608 · cited 1× · see citing works
“Cold-activated BAT has been shown to contribute to the regulation of energy balance in mice by burning a considerable amount of ingested triglycerides and glucose (21,22).”
BackgroundType 2 diabetes across generations: from pathophysiology to prevention and management
Nolan, C. J., Damm, P., & Prentki, M. (2011) · The Lancet · doi:10.1016/s0140-6736(11)60614-4 · Cited by 923 · see citing works
Self-citationNonshivering thermogenesis and its adequate measurement in metabolic studies
Cannon, B., & Nedergaard, J. (2011) · Journal of Experimental Biology · doi:10.1242/jeb.050989 · Cited by 677 · cited 2× · see citing works
“Indeed, thermoneutrality for mice lies around 30°C, whereas for rats, it is close to 22°C (28).”
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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
Kim, J., Choi, A., & Kwon, Y. H. (2020) · Nutrients · doi:10.3390/nu12041103 · Cited by 18 · see citing works
- Authors
- Dumortier, O., Roger, E., Pisani, D. F., Casamento, V., Gautier, N., Lebrun, P., Johnston, H., Lopez, P., Amri, E.-Z., Jousse, C., Fafournoux, P., Prentki, M., Hinault, C., & Van Obberghen, E.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Unité de Nutrition Humaine (FR)
- Université de Montréal (CA)
- Université Côte d’Azur, CHU, INSERM, CNRS, IRCAN, Nice, France
- ORCID
- Venue
- Diabetes
- Publisher
- American Diabetes Association
- Published
- 2016-12-07
- Volume
- 66
- Issue
- 3
- Pages
- 627-639
- ISSN
- 0012-1797 (ISSN-L)
- 1939-327X
- OpenAlex
- W2560145611
- Cited by
- 22
- References
- 3
- Citations by year
- 2025: 2 · 2024: 1 · 2023: 1 · 2022: 2 · 2021: 2 · 2020: 4 · 2019: 4 · 2018: 5 · 2017: 1
- FWCI
- 2.69
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Diabetes (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- EU FP7 (HEALTH-F2-2011-278373)
- INSERM
- Agence Nationale de la Recherche (ANR-RPV12004AAA)
- European Foundation for the Study of Diabetes
- Topics
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
- Keywords
- brown adipose tissue, fetal programming, maternal low-protein diet, energy homeostasis, insulin deficiency, beta-cell dysfunction, hyperglycemia, insulin resistance, high-fat diet-induced obesity, cold tolerance, aging, type 2 diabetes, glucose homeostasis, body temperature
- MeSH terms
- Age Factors, Animals, Blood Glucose, Body Temperature Regulation, Adipose Tissue, Brown, Diabetes Mellitus, Type 2, Energy Metabolism, Female, Glucose Tolerance Test, Homeostasis, Hyperglycemia, Immunohistochemistry, Insulin, Insulin Resistance, Lipolysis, Male, Obesity, Pregnancy, Prenatal Exposure Delayed Effects, Triglycerides, Blotting, Western, Rats, Wistar, Diet, Protein-Restricted, Postprandial Period, Fetal Development, Rats, Diet, High-Fat, Real-Time Polymerase Chain Reaction
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