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Increased intake of energy-dense diet and negative energy balance in a mouse model of chronic psychosocial defeat

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Abstract

Purpose

Chronic exposure to stress may represent a risk factor for developing metabolic and eating disorders, mostly driven by the overconsumption of easily accessible energy-dense palatable food, although the mechanisms involved remain still unclear. In this study, we used an ethologically oriented murine model of chronic stress caused by chronic psychosocial defeat (CPD) to investigate the effects of unrestricted access to a palatable high fat diet (HFD) on food intake, body weight, energy homeostasis, and expression of different brain neuropeptides. Our aim was to shed light on the mechanisms responsible for body weight and body composition changes due to chronic social stress.

Methods

In our model of subordinate (defeated), mice (CPD) cohabitated in constant sensory contact with dominants, being forced to interact on daily basis, and were offered ad libitum access either to an HFD or to a control diet (CD). Control mice (of the same strain as CPD mice) were housed in pairs and left unstressed in their home cage (UN). In all these mice, we evaluated body weight, different adipose depots, energy metabolism, caloric intake, and neuropeptide expression.

Results

CPD mice increased the intake of HFD and reduced body weight in the presence of enhanced lipid oxidation. Resting energy expenditure and interscapular brown adipose tissue (iBAT) were increased in CPD mice, whereas epididymal adipose tissue increased only in HFD-fed unstressed mice. Propiomelanocortin mRNA levels in hypothalamic arcuate nucleus increased only in HFD-fed unstressed mice. Oxytocin mRNA levels in the paraventricular nucleus and neuropeptide Y mRNA levels within the arcuate were increased only in CD-fed CPD mice. In the arcuate, CART was increased in HFD-fed UN mice and in CD-fed CPD mice, while HFD intake suppressed CART increase in defeated animals. In the basolateral amygdala, CART expression was increased only in CPD animals on HFD.

Conclusions

CPD appears to uncouple the intake of HFD from energy homeostasis causing higher HFD intake, larger iBAT accumulation, increased energy expenditure and lipid oxidation, and lower body weight. Overall, the present study confirms the notion that the chronic activation of the stress response can be associated with metabolic disorders, altered energy homeostasis, and changes of orexigenic and anorexigenic signaling. These changes might be relevant to better understand the etiology of stress-induced obesity and eating disorders and might represent a valid therapeutic approach for the development of new therapies in this field.

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Acknowledgements

This research was supported by the Italian Ministry for Education, University and Research, (PRIN 2009ESX7T3). The authors gratefully acknowledge the C.N.R./E.M.M.A. animal research facility (Monterotondo, Rome, Italy). All authors have read and approved the final manuscript.

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    Authors and Affiliations

    1. Institute of Cell Biology and Neurobiology (IBCN), National Research Council (CNR), Via del Fosso di Fiorano, 64, 00143, Roma, Italy

      Roberto Coccurello, Giacomo Giacovazzo, Marco Fiore & Anna Moles

    2. Fondazione Santa Lucia (FSL-IRCCS), Via del Fosso di Fiorano, 64, 00143, Roma, Italy

      Roberto Coccurello, Giacomo Giacovazzo & Marco Fiore

    3. Department of Physiology and Pharmacology V. Erspamer, Sapienza University of Rome, P.le A. Moro, 5, 00185, Roma, Italy

      Adele Romano, Bianca Tempesta & Silvana Gaetani

    4. Department of Biological and Environmental Sciences and Technologies, University of Salento, Lecce, Italy

      Anna Maria Giudetti

    5. Department of Biochemical Sciences, Sapienza University of Rome, P.le A. Moro, 5, 00185, Roma, Italy

      Ilaria Marrocco & Fabio Altieri

    6. Istituto Pasteur-Fondazione Cenci Bolognetti, Viale Regina Elena, 291, 00161, Roma, Italy

      Ilaria Marrocco & Fabio Altieri

    7. Genomia srl, Via L. Ariosto 21, 20091, Bresso, Milan, Italy

      Anna Moles

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    All the experiments were conducted in accordance with Italian National Laws (DL 116/92), with the European Communities Council Directive of 24 November 1986 (86/609/EEC) and regulations on the use of animals for research, and NIH guidelines on animal care. All the experimental and testing procedures were also in compliance with the recommendations of the European Union concerning animal welfare care and husbandry (2007/526/CE), approved by the internal ethics committee, performed in accordance with the ethical standards as laid down in the 1964 Declaration of Helsinki and its later amendments, and specifically approved by the Italian Ministry of Health by the ministerial decree N 97/2012-B.

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    R. Coccurello and A. Romano equally contributed.

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    Coccurello, R., Romano, A., Giacovazzo, G. et al. Increased intake of energy-dense diet and negative energy balance in a mouse model of chronic psychosocial defeat. Eur J Nutr 57, 1485–1498 (2018). https://doi.org/10.1007/s00394-017-1434-y

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