Skip to main content Accessibility help
×
Home

Maternal undernutrition programs the apelinergic system of adipose tissue in adult male rat offspring

  • S. Lecoutre (a1), L. Marousez (a1), A. Drougard (a2), C. Knauf (a2), C. Guinez (a1), D. Eberlé (a1), C. Laborie (a1), D. Vieau (a1), J. Lesage (a1) and C. Breton (a1)...

Abstract

Based on the Developmental Origin of Health and Disease concept, maternal undernutrition has been shown to sensitize adult offspring to metabolic pathologies such as obesity. Using a model of maternal 70% food restriction in pregnant female rats throughout gestation (called FR30), we previously reported that obesity-prone adult male rat offspring displayed hyperleptinemia with modifications in leptin and leptin receptor messenger RNA (mRNA) levels in white adipose tissue (WAT). Apelin is a member of the adipokine family that regulates various aspects of energy metabolism and WAT functionality. We investigated whether apelin and its receptor APJ could be a target of maternal undernutrition. Adult male rat offspring from FR30 dams showed increased plasma apelin levels and apelin gene expression in WAT. Post-weaning high-fat diet led to marked increase in APJ mRNA and protein levels in offspring’s WAT. We demonstrate that maternal undernutrition and post-weaning diet have long-term consequences on the apelinergic system of adult male rat offspring.

Copyright

Corresponding author

*Address for correspondence: C. Breton, EA4489, Équipe Malnutrition Maternelle et Programmation des Maladies Métaboliques, Univ. Lille, F59000 Lille, France. (Email christophe.breton@univ-lille1.fr)

References

Hide All
1. Barker, DJP. Developmental origins of adult health and disease. J Epidemiol Community Health. 2004; 58, 114115.
2. Ravelli, AC, van Der Meulen, JH, Osmond, C, Barker, DJ, Bleker, OP. Obesity at the age of 50 y in men and women exposed to famine prenatally. Am J Clin Nutr. 1999; 70, 811816.
3. Rivière, G, Michaud, A, Breton, C, et al. Angiotensin-converting enzyme 2 (ACE2) and ACE activities display tissue-specific sensitivity to undernutrition-programmed hypertension in the adult rat. Hypertension. 2005; 46, 11691174.
4. Breton, C, Lukaszewski, M-A, Risold, P-Y, et al. Maternal prenatal undernutrition alters the response of POMC neurons to energy status variation in adult male rat offspring. Am J Physiol Endocrinol Metab. 2009; 296, E462E472.
5. Lukaszewski, M-A, Mayeur, S, Fajardy, I, et al. Maternal prenatal undernutrition programs adipose tissue gene expression in adult male rat offspring under high-fat diet. Am J Physiol Endocrinol Metab. 2011; 301, E548E559.
6. Breton, C. The hypothalamus–adipose axis is a key target of developmental programming by maternal nutritional manipulation. J Endocrinol. 2013; 216, R19R31.
7. Lukaszewski, M-A, Eberlé, D, Vieau, D, Breton, C. Nutritional manipulations in the perinatal period program adipose tissue in offspring. Am J Physiol Endocrinol Metab. 2013; 305, E1195E1207.
8. Tatemoto, K, Hosoya, M, Habata, Y, et al. Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochem Biophys Res Commun. 1998; 251, 471476.
9. Hosoya, M, Kawamata, Y, Fukusumi, S, et al. Molecular and functional characteristics of APJ. Tissue distribution of mRNA and interaction with the endogenous ligand apelin. J Biol Chem. 2000; 275, 2106121067.
10. Heinonen, MV, Purhonen, AK, Miettinen, P, et al. Apelin, orexin-A and leptin plasma levels in morbid obesity and effect of gastric banding. Regul Pept. 2005; 130, 713.
11. Soriguer, F, Garrido-Sanchez, L, Garcia-Serrano, S, et al. Apelin levels are increased in morbidly obese subjects with type 2 diabetes mellitus. Obes Surg. 2009; 19, 15741580.
12. Dray, C, Debard, C, Jager, J, et al. Apelin and APJ regulation in adipose tissue and skeletal muscle of type 2 diabetic mice and humans. Am J Physiol Endocrinol Metab. 2010; 298, E1161E1169.
13. Boucher, J, Masri, B, Daviaud, D, et al. Apelin, a newly identified adipokine up-regulated by insulin and obesity. Endocrinology. 2005; 146, 17641771.
14. Castan-Laurell, I, Dray, C, Knauf, C, Kunduzova, O, Valet, P. Apelin, a promising target for type 2 diabetes treatment? Trends Endocrinol Metab. 2012; 23, 234241.
15. Yue, P, Jin, H, Xu, S, et al. Apelin decreases lipolysis via G(q), G(i), and AMPK-dependent mechanisms. Endocrinology. 2011; 152, 5968.
16. Than, A, Cheng, Y, Foh, LC, et al. Apelin inhibits adipogenesis and lipolysis through distinct molecular pathways. Mol Cell Endocrinol. 2012; 362, 227241.
17. Zhu, S, Cheng, G, Zhu, H, Guan, G. A study of genes involved in adipocyte differentiation. J Pediatr Endocrinol Metab. 2015; 28, 9399.
18. Than, A, He, HL, Chua, SH, et al. Apelin enhances brown adipogenesis and browning of white adipocytes. J Biol Chem. 2015; 290, 1467914691.
19. Chen, H, Zheng, C, Zhang, X, et al. Apelin alleviates diabetes-associated endoplasmic reticulum stress in the pancreas of Akita mice. Peptides. 2011; 32, 16341639.
20. Dray, C, Knauf, C, Daviaud, D, et al. Apelin stimulates glucose utilization in normal and obese insulin-resistant mice. Cell Metab. 2008; 8, 437445.
21. Butruille, L, Drougard, A, Knauf, C, et al. The apelinergic system: sexual dimorphism and tissue-specific modulations by obesity and insulin resistance in female mice. Peptides. 2013; 46, 94101.
22. Sörhede Winzell, M, Magnusson, C, Ahrén, B. The apj receptor is expressed in pancreatic islets and its ligand, apelin, inhibits insulin secretion in mice. Regul Pept. 2005; 131, 1217.
23. Higuchi, K, Masaki, T, Gotoh, K, et al. Apelin, an APJ receptor ligand, regulates body adiposity and favors the messenger ribonucleic acid expression of uncoupling proteins in mice. Endocrinology. 2007; 148, 26902697.
24. Jousse, C, Parry, L, Lambert-Langlais, S, et al. Perinatal undernutrition affects the methylation and expression of the leptin gene in adults: implication for the understanding of metabolic syndrome. FASEB J. 2011; 25, 32713278.
25. Mishra, A, Kohli, S, Dua, S, et al. Genetic differences and aberrant methylation in the apelin system predict the risk of high-altitude pulmonary edema. Proc Natl Acad Sci U S A. 2015; 112, 61346139.

Keywords

Maternal undernutrition programs the apelinergic system of adipose tissue in adult male rat offspring

  • S. Lecoutre (a1), L. Marousez (a1), A. Drougard (a2), C. Knauf (a2), C. Guinez (a1), D. Eberlé (a1), C. Laborie (a1), D. Vieau (a1), J. Lesage (a1) and C. Breton (a1)...

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed