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“Comfort-foods” chronic intake has different behavioral and neurobiological effects in male rats exposed or not to early-life stress

Published online by Cambridge University Press:  06 June 2019

ACA Cunha
Affiliation:
Programa de Pós-Graduação em Saúde da Criança e do Adolescente, Faculdade de Medicina, Hospital de Clínicas de Porto Alegre, Universidade Federal do Rio Grande do Sul, PoA, RS, Brazil
R Dalle Molle
Affiliation:
Programa de Pós-Graduação em Saúde da Criança e do Adolescente, Faculdade de Medicina, Hospital de Clínicas de Porto Alegre, Universidade Federal do Rio Grande do Sul, PoA, RS, Brazil Faculdade Inedi – Cesuca, Cachoeirinha, RS, Brazil
DP Laureano
Affiliation:
Programa de Pós-Graduação em Neurociências, Universidade Federal do Rio Grande do Sul, PoA, RS, Brazil
AR Reis
Affiliation:
Programa de Pós-Graduação em Saúde da Criança e do Adolescente, Faculdade de Medicina, Hospital de Clínicas de Porto Alegre, Universidade Federal do Rio Grande do Sul, PoA, RS, Brazil
C Corrêa
Affiliation:
Programa de Pós-Graduação em Neurociências, Universidade Federal do Rio Grande do Sul, PoA, RS, Brazil
US Matte
Affiliation:
Programa de Pós-Graduação em Saúde da Criança e do Adolescente, Faculdade de Medicina, Hospital de Clínicas de Porto Alegre, Universidade Federal do Rio Grande do Sul, PoA, RS, Brazil Gene Therapy Center, Hospital de Clínicas de Porto Alegre, BrazilPrograma de Pós Graduação em Genética e Biologia Molecular, Universidade Federal do Rio Grande do Sul, PoA, RS, Brazil
PP Silveira
Affiliation:
Programa de Pós-Graduação em Neurociências, Universidade Federal do Rio Grande do Sul, PoA, RS, Brazil Department of Psychiatry, Faculty of Medicine, McGill University; Ludmer Centre for Neuroinformatics and Mental Health, Douglas Mental Health University Institute and Sackler Program for Epigenetics & Psychobiology at McGill University
TD Machado*
Affiliation:
Programa de Pós-Graduação em Saúde da Criança e do Adolescente, Faculdade de Medicina, Hospital de Clínicas de Porto Alegre, Universidade Federal do Rio Grande do Sul, PoA, RS, Brazil
*
Address for correspondence: Tania Diniz Machado, Programa de Pós-Graduação em Saúde da Criança e do Adolescente – FAMED – Universidade Federal do Rio Grande do Sul. Ramiro Barcelos, Largo Eduardo Zaccaro Faraco. Porto Alegre, RS, Brazil. Email: [email protected]

Abstract

The ability of “comfort-food” (CF) diet to revert long-term effects of early-life stress (ELS) is less well known. The objective of this study was to verify if the chronic exposure to CF diet in animals submitted to ELS could relief the stress response at behavioral, neuroendocrine, and neurobiochemical levels, via differences in glucocorticoid receptors expression in brain areas involved in the stress response. From the second day of life, litters of Wistar rats and their mothers were submitted to the reduced nesting material protocol (ELS). In adult life, ELS and a control group were exposed chronically to two diet schemes: standard rat chow only or both “CF” diet, containing fat (34%) and sugar (20%) and a diet similar to the standard diet. Anxiety-like behavior, neuroendocrine response stress, leptin, GR, SOCS-3, pSTAT3, and the abdominal fat were evaluated. The anxiety-like behavior results showed that ELS group when exposed to comfort food were not different from the others groups. Chronic exposure to CF diet induced an anxiety-like behavior in the control group. Groups chronically exposed to CF diet had lower levels of corticosterone over time independent of the neonatal group. The ELS group exposed to the “CF” diet had higher levels of hippocampal GR, lower levels of hypothalamic SOCS-3 and greater accumulation of abdominal fat. Chronic CF diet consumption is able to reduce corticosterone levels independent of the neonatal history, but is associated with anxiety-like behavior in animals without previous history of trauma. Metabolic disturbances like increased adiposity and altered SOCS-3 seem to be a result of multiple insults (neonatal trauma followed by chronic CF diet). We highlight that the Control-chow and ELS-chow data were previously published, and are included in this study for comparative analysis.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2019 

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References

Dallman, MF, Pecoraro, N, Akana, SF, et al. Chronic stress and obesity: a new view of “comfort food”. Proc Natl Acad Sci U S A. 2003; 100, 1169611701.CrossRefGoogle ScholarPubMed
Adam, TC, Epel, ES. Stress, eating and the reward system. Physiol Behav. 2007; 91, 449458.CrossRefGoogle ScholarPubMed
Pecoraro, N, Reyes, F, Gomez, F, Bhargava, A, Dallman, MF. Chronic stress promotes palatable feeding, which reduces signs of stress: feedforward and feedback effects of chronic stress. Endocrinology. 2004; 145, 37543762.CrossRefGoogle ScholarPubMed
Tomiyama, AJ, Dallman, MF, Epel, ES. Comfort food is comforting to those most stressed: evidence of the chronic stress response network in high stress women. Psychoneuroendocrinology. 2011; 36, 15131519.CrossRefGoogle ScholarPubMed
Dallman, MF. Stress-induced obesity and the emotional nervous system. Trends Endocrinol Metab. 2010; 21, 159165.CrossRefGoogle ScholarPubMed
Tryon, MS, DeCant, R, Laugero, KD. Having your cake and eating it too: a habit of comfort food may link chronic social stress exposure and acute stress-induced cortisol hyporesponsiveness. Physiol Behav. 2013; 114, 115, 3237.CrossRefGoogle ScholarPubMed
Krolow, R, Noschang, CG, Arcego, D, et al. Consumption of a palatable diet by chronically stressed rats prevents effects on anxiety-like behavior but increases oxidative stress in a sex-specific manner. Appetite. 2010; 55, 108116.CrossRefGoogle Scholar
Danese, A, Dove, R, Belsky, DW, et al. Leptin deficiency in maltreated children. Transl Psychiatry. 2014; 4, e446.CrossRefGoogle ScholarPubMed
Lubis, AR, Widia, F, Soegondo, S, Setiawati, A. The role of SOCS-3 protein in leptin resistance and obesity. Acta Med Indones. 2008; 40, 8995.Google ScholarPubMed
Maniam, J, Morris, MJ. Palatable cafeteria diet ameliorates anxiety and depression-like symptoms following an adverse early environment. Psychoneuroendocrinology. 2010; 35, 717728.CrossRefGoogle ScholarPubMed
Krolow, R, Noschang, C, Arcego, DM, et al. Sex-specific effects of isolation stress and consumption of palatable diet during the prepubertal period on metabolic parameters. Metabol Clin Exp. 2013; 62, 12681278.CrossRefGoogle ScholarPubMed
Machado, TD, Dalle Molle, R, Laureano, DP, et al. Early life stress is associated with anxiety, increased stress responsivity and preference for “comfort foods” in adult female rats. Stress. 2013; 16, 549556.CrossRefGoogle Scholar
Silveira, PP, Portella, AK, Assis, SA, et al. Early life experience alters behavioral responses to sweet food and accumbal dopamine metabolism. Int J Dev Neurosci. 2010; 28, 111118.CrossRefGoogle ScholarPubMed
Silveira, PP, Portella, AK, Clemente, Z, et al. Neonatal handling alters feeding behavior of adult rats. Physiol Behav. 2004; 80, 739745.CrossRefGoogle ScholarPubMed
Ivy, AS, Brunson, KL, Sandman, C, Baram, TZ. Dysfunctional nurturing behavior in rat dams with limited access to nesting material: a clinically relevant model for early-life stress. Neuroscience. 2008; 154, 11321142.CrossRefGoogle ScholarPubMed
Dalle Molle, R, Portella, AK, Goldani, MZ, et al. Associations between parenting behavior and anxiety in a rodent model and a clinical sample: relationship to peripheral BDNF levels. Transl Psychiatry. 2012; 2, e195.CrossRefGoogle Scholar
Baram, TZ, Davis, EP, Obenaus, A, et al. Fragmentation and unpredictability of early-life experience in mental disorders. Am J Psychiatry. 2012; 169, 907915.CrossRefGoogle ScholarPubMed
Paxinos, Ge, Watson, Ch. The Rat Brain in Stereotaxic Coordinates. 6th ed. 2007. Amsterdam: Elsevier.Google Scholar
Dalle Molle, R, Laureano, DP, Alves, MB, et al. Intrauterine growth restriction increases the preference for palatable foods and affects sensitivity to food rewards in male and female adult rats. Brain Res. 2015; 1618, 4149.CrossRefGoogle ScholarPubMed
Colman, JB, Laureano, DP, Reis, TM, et al. Variations in the neonatal environment modulate adult behavioral and brain responses to palatable food withdrawal in adult female rats. Int J Dev Neurosci. 2015; 40, 7075.CrossRefGoogle ScholarPubMed
Laureano, DP, Dalle Molle, R, Alves, MB, et al. Intrauterine growth restriction modifies the hedonic response to sweet taste in newborn pups—role of the accumbal µ-opioid receptors. Neuroscience. 2016; 322, 500508.CrossRefGoogle Scholar
Bjorntorp, P. Do stress reactions cause abdominal obesity and comorbidities? Obes Rev. 2001; 2, 7386.CrossRefGoogle ScholarPubMed
Buwalda, B, Blom, WA, Koolhaas, JM, van Dijk, G. Behavioral and physiological responses to stress are affected by high-fat feeding in male rats. Physiol Behav. 2001; 73, 371377.CrossRefGoogle ScholarPubMed
Dalle Molle, R. Estudo translacional sobre a qualidade do cuidado materno em resposta ao estresse neonatal, sua associação com ansiedade na vida adulta e investigação de potenciais mecanismos envolvidos. Dissertação (Mestrado). Faculdade de Medicina. Programa de Pós-Graduação em Saúde da Criança e do Adolescente, Universidade Federal do Rio Grande do Sul; 2011.Google Scholar
Maniam, J, Antoniadis, C, Morris, MJ. Early-life stress, HPA axis adaptation, and mechanisms contributing to later health outcomes. Front Endocrinol (Lausanne). 2014; 5, 7390.CrossRefGoogle ScholarPubMed
Maniam, J, Antoniadis, CP, Le, V, Morris, MJ. A diet high in fat and sugar reverses anxiety-like behaviour induced by limited nesting in male rats: impacts on hippocampal markers. Psychoneuroendocrinology. 2016; 68, 202209.CrossRefGoogle ScholarPubMed
Sivanathan, S, Thavartnam, K, Arif, S, Elegino, T, McGowan, PO. Chronic high fat feeding increases anxiety-like behaviour and reduces transcript abundance of glucocorticoid signalling genes in the hippocampus of female rats. Behav Brain Res. 2015; 286, 265270.CrossRefGoogle ScholarPubMed
Hryhorczuk, C, Decarie-Spain, L, Sharma, S, et al. Saturated high-fat feeding independent of obesity alters hypothalamus-pituitary-adrenal axis function but not anxiety-like behaviour. Psychoneuroendocrinology. 2017; 83, 142149.CrossRefGoogle Scholar
Sasaki, A, de Vega, WC, St-Cyr, S, Pan, P, McGowan, PO. Perinatal high fat diet alters glucocorticoid signaling and anxiety behavior in adulthood. Neuroscience. 2013; 240, 112.CrossRefGoogle ScholarPubMed
Sasaki, A, de Vega, W, Sivanathan, S, St-Cyr, S, McGowan, PO. Maternal high-fat diet alters anxiety behavior and glucocorticoid signaling in adolescent offspring. Neuroscience. 2014; 272, 92101.CrossRefGoogle ScholarPubMed
Corona-Perez, A, Diaz-Munoz, M, Rodriguez, IS, et al. High sucrose intake ameliorates the accumulation of hepatic triacylglycerol promoted by restraint stress in young rats. Lipids. 2015; 50, 11031113.CrossRefGoogle ScholarPubMed
Bell, ME, Bhargava, A, Soriano, L, Laugero, K, Akana, SF, Dallman, MF. Sucrose intake and corticosterone interact with cold to modulate ingestive behaviour, energy balance, autonomic outflow and neuroendocrine responses during chronic stress. J Neuroendocrinol. 2002; 14, 330342.CrossRefGoogle ScholarPubMed
Foster, MT, Warne, JP, Ginsberg, AB, et al. Palatable foods, stress, and energy stores sculpt corticotropin-releasing factor, adrenocorticotropin, and corticosterone concentrations after restraint. Endocrinology. 2009; 150, 23252333.CrossRefGoogle ScholarPubMed
Strack, AM, Akana, SF, Horsley, CJ, Dallman, MF. A hypercaloric load induces thermogenesis but inhibits stress responses in the SNS and HPA system. Am J Physiol. 1997; 272, R840848.Google ScholarPubMed
Matheny, M, Shapiro, A, Tumer, N, Scarpace, PJ. Region-specific diet-induced and leptin-induced cellular leptin resistance includes the ventral tegmental area in rats. Neuropharmacology. 2011; 60, 480487.CrossRefGoogle ScholarPubMed
Souza, CG, Moreira, JD, Siqueira, IR, et al. Highly palatable diet consumption increases protein oxidation in rat frontal cortex and anxiety-like behavior. Life Sci. 2007; 81, 198203.CrossRefGoogle ScholarPubMed
Sharma, S, Fulton, S. Diet-induced obesity promotes depressive-like behaviour that is associated with neural adaptations in brain reward circuitry. Int J Obes (Lond). 2013; 37, 382389.CrossRefGoogle ScholarPubMed
Auvinen, HE, Romijn, JA, Biermasz, NR, et al. The effects of high fat diet on the basal activity of the hypothalamus-pituitary-adrenal axis in mice. J Endocrinol. 2012; 214, 191197.CrossRefGoogle ScholarPubMed
Kim, JY, Lee, JH, Kim, D, Kim, SM, Koo, J, Jahng, JW. Beneficial effects of highly palatable food on the behavioral and neural adversities induced by early life stress experience in female rats. Int J Biol Sci. 2015; 11, 11501159.CrossRefGoogle ScholarPubMed
McNeilly, AD, Stewart, CA, Sutherland, C, Balfour, DJ. High fat feeding is associated with stimulation of the hypothalamic-pituitary-adrenal axis and reduced anxiety in the rat. Psychoneuroendocrinology. 2015; 52, 272280.CrossRefGoogle ScholarPubMed
Prasad, A, Prasad, C. Short-term consumption of a diet rich in fat decreases anxiety response in adult male rats. Physiol Behav. 1996; 60, 10391042.CrossRefGoogle Scholar
Herman, JP, Cullinan, WE. Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci. 1997; 20, 7884.CrossRefGoogle ScholarPubMed
Halasz, I, Rittenhouse, PA, Zorrilla, EP, Redei, E. Sexually dimorphic effects of maternal adrenalectomy on hypothalamic corticotrophin-releasing factor, glucocorticoid receptor and anterior pituitary POMC mRNA levels in rat neonates. Brain Res Dev Brain Res. 1997; 100, 198204.CrossRefGoogle ScholarPubMed