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

Published online by Cambridge University Press:  04 January 2017

S. Lecoutre
Affiliation:
EA4489, Équipe Malnutrition Maternelle et Programmation des Maladies Métaboliques, Univ. Lille, Lille, France
L. Marousez
Affiliation:
EA4489, Équipe Malnutrition Maternelle et Programmation des Maladies Métaboliques, Univ. Lille, Lille, France
A. Drougard
Affiliation:
European Associated Laboratory NeuroMicrobiota (INSERM/UCL), Team 3, IRSD, INSERM U1220, Toulouse, France
C. Knauf
Affiliation:
European Associated Laboratory NeuroMicrobiota (INSERM/UCL), Team 3, IRSD, INSERM U1220, Toulouse, France
C. Guinez
Affiliation:
EA4489, Équipe Malnutrition Maternelle et Programmation des Maladies Métaboliques, Univ. Lille, Lille, France
D. Eberlé
Affiliation:
EA4489, Équipe Malnutrition Maternelle et Programmation des Maladies Métaboliques, Univ. Lille, Lille, France
C. Laborie
Affiliation:
EA4489, Équipe Malnutrition Maternelle et Programmation des Maladies Métaboliques, Univ. Lille, Lille, France
D. Vieau
Affiliation:
EA4489, Équipe Malnutrition Maternelle et Programmation des Maladies Métaboliques, Univ. Lille, Lille, France
J. Lesage
Affiliation:
EA4489, Équipe Malnutrition Maternelle et Programmation des Maladies Métaboliques, Univ. Lille, Lille, France
C. Breton*
Affiliation:
EA4489, Équipe Malnutrition Maternelle et Programmation des Maladies Métaboliques, Univ. Lille, Lille, France
*
*Address for correspondence: C. Breton, EA4489, Équipe Malnutrition Maternelle et Programmation des Maladies Métaboliques, Univ. Lille, F59000 Lille, France. (Email [email protected])

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.

Type
Rapid Communication
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2017 

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References

1. Barker, DJP. Developmental origins of adult health and disease. J Epidemiol Community Health. 2004; 58, 114115.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
6. Breton, C. The hypothalamus–adipose axis is a key target of developmental programming by maternal nutritional manipulation. J Endocrinol. 2013; 216, R19R31.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
13. Boucher, J, Masri, B, Daviaud, D, et al. Apelin, a newly identified adipokine up-regulated by insulin and obesity. Endocrinology. 2005; 146, 17641771.Google Scholar
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.Google Scholar
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.Google Scholar
16. Than, A, Cheng, Y, Foh, LC, et al. Apelin inhibits adipogenesis and lipolysis through distinct molecular pathways. Mol Cell Endocrinol. 2012; 362, 227241.CrossRefGoogle ScholarPubMed
17. Zhu, S, Cheng, G, Zhu, H, Guan, G. A study of genes involved in adipocyte differentiation. J Pediatr Endocrinol Metab. 2015; 28, 9399.Google Scholar
18. Than, A, He, HL, Chua, SH, et al. Apelin enhances brown adipogenesis and browning of white adipocytes. J Biol Chem. 2015; 290, 1467914691.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed