Hypothalamic-pituitary-adrenal axis hypersensitivity in female rats on a post-weaning high-fat diet after chronic mild stress

Liu,Lian; Yang,Junqiang; Qian,Feng; Lu,Chengbiao

doi:10.3892/etm.2017.4498

Hypothalamic-pituitary-adrenal axis hypersensitivity in female rats on a post-weaning high-fat diet after chronic mild stress

Authors:
- Lian Liu
- Junqiang Yang
- Feng Qian
- Chengbiao Lu
View Affiliations

Affiliations: Department of Pharmacology, Medical School of Yangtze University, Jingzhou, Hubei 434023, P.R. China, Laboratory of Neuronal and Brain Disease Modulation, Yangtze University, Jingzhou, Hubei 434023, P.R. China
Published online on: May 23, 2017 https://doi.org/10.3892/etm.2017.4498
Pages: 439-446

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

A high-fat diet (HFD) is highly correlated to obesity, metabolic diseases and certain behavioral changes. However, the effects of post‑weaning HFD in rats during puberty and the role of the hypothalamic-pituitary-adrenal (HPA) axis in this process have remained elusive. The present study hypothesized that the HPA axis mediates the behavioral alterations induced by a post‑weaning HFD. To investigate this, female rats were divided into two groups, one of which was fed a HFD from postnatal weeks (PWs) 4‑12, while the other group received standard chow. Rats in each group were then subdivided into two subgroups each, and from PW 9‑12, animals from one of the two subgroups were subjected to chronic mild stress (CMS), while the other subgroup received no stress. At PW 12, the body weight of rats receiving a HFD but no DMS was significantly higher than that in the control group. The frequency of crossing and rearing in the open field test and the time in the center of the Y‑maze were decreased following CMS. Total time to escape was decreased in rats receiving HFD and after CMS. The serum levels of adrenocorticotropic hormone and corticosterone were increased in rats receiving an HFD and after CMS, and the mRNA levels of corticotropin‑releasing hormone and arginine vasopressin in the hypothalamus were increased in the HFD + CMS group compared to that in the control group. The mRNA expression of glucocorticoid receptor (GR) in the hippocampi of rats in the HFD + CMS group was significantly decreased and the mineralocorticoid receptor/GR ratio was increased compared to that in the groups receiving either CMS or a HFD. In conclusion, these results indicated that female rats fed a post‑weaning HFD showed HPA axis hypersensitivity under CMS, which may mediate behavioral alterations.

View Figures

View References

1	Peleg-Raibstein D, Luca E and Wolfrum C: Maternal high-fat diet in mice programs emotional behavior in adulthood. Behav Brain Res. 233:398–404. 2012. View Article : Google Scholar : PubMed/NCBI
2	Auvinen HE, Romijn JA, Biermasz NR, Pijl H, Havekes LM, Smit JW, Rensen PC and Pereira AM: The effects of high fat diet on the basal activity of the hypothalamus-pituitary-adrenal axis in mice. J Endocrinol. 214:191–197. 2012. View Article : Google Scholar : PubMed/NCBI
3	Rofey DL, Kolko RP, Iosif AM, Silk JS, Bost JE, Feng W, Szigethy EM, Noll RB, Ryan ND and Dahl RE: A longitudinal study of childhood depression and anxiety in relation to weight gain. Child Psychiatry Hum Dev. 40:517–526. 2009. View Article : Google Scholar : PubMed/NCBI
4	O'Connor TG: Prenatal and postnatal exposure to an unhealthy diet is associated with behavioural and emotional problems in children. Evid Based Ment Health. 17:382014. View Article : Google Scholar : PubMed/NCBI
5	Soulis G, Papalexi E, Kittas C and Kitraki E: Early impact of a fat-enriched diet on behavioral responses of male and female rats. Behav Neurosci. 121:483–490. 2007. View Article : Google Scholar : PubMed/NCBI
6	Boukouvalas G, Antoniou K, Papalexi E and Kitraki E: Post weaning high fat feeding affects rats' behavior and hypothalamic pituitary adrenal axis at the onset of puberty in a sexually dimorphic manner. Neuroscience. 153:373–382. 2008. View Article : Google Scholar : PubMed/NCBI
7	Boukouvalas G, Gerozissis K and Kitraki E: Adult consequences of post-weaning high fat feeding on the limbic-HPA axis of female rats. Cell Mol Neurobiol. 30:521–530. 2010. View Article : Google Scholar : PubMed/NCBI
8	Verma R, Balhara YP and Gupta CS: Gender differences in stress response: Role of developmental and biological determinants. Ind Psychiatry J. 20:4–10. 2011.PubMed/NCBI
9	Szabo K and Hennerici MG: The Hippocampus in Clinical Neuroscience. Front Neurol Neurosci Basel Karger. 2014. View Article : Google Scholar
10	Li SX, Yan SY, Bao YP, Lian Z, Qu Z, Wu YP and Liu ZM: Depression and alterations in hypothalamic-pituitary-adrenal and hypothalamic-pituitary-thyroid axis function in male abstinent methamphetamine abusers. Hum Psychopharmacol. 28:477–483. 2013. View Article : Google Scholar : PubMed/NCBI
11	Moreno-Ramos OA, Lattig MC and González Barrios AF: Modeling of the hypothalamic-pituitary-adrenal axis-mediated interaction between the serotonin regulation pathway and the stress response using a Boolean approximation: A novel study of depression. Theor Biol Med Model. 10:592013. View Article : Google Scholar : PubMed/NCBI
12	Holsboer F and Ising M: Central CRH system in depression and anxiety-evidence from clinical studies with CRH1 receptor antagonists. Eur J Pharmacol. 583:350–357. 2008. View Article : Google Scholar : PubMed/NCBI
13	Sasaki A, De Vega WC, St-Cyr S, Pan P and McGowan PO: Perinatal high fat diet alters glucocorticoid signaling and anxiety behavior in adulthood. Neuroscience. 240:1–12. 2013. View Article : Google Scholar : PubMed/NCBI
14	García-Díaz DF, Campion J, Milagro FI, Lomba A, Marzo F and Martínez JA: Chronic mild stress induces variations in locomotive behavior and metabolic rates in high fat fed rats. J Physiol Biochem. 63:337–346. 2007. View Article : Google Scholar : PubMed/NCBI
15	Stöhr T, Szuran T, Welzl H, Pliska V, Feldon J and Pryce CR: Lewis/Fischer rat strain differences in endocrine and behavioural responses to environmental challenge. Pharmacol Biochem Behav. 67:809–819. 2000. View Article : Google Scholar : PubMed/NCBI
16	Willner P: Validity, reliability and utility of the chronic mild stress model of depression: A 10-year review and evaluation. Psychopharmacology (Berl). 134:319–329. 1997. View Article : Google Scholar : PubMed/NCBI
17	Willner P, Muscat R and Papp M: Chronic mild stress-induced anhedonia: A realistic animal model of depression. Neurosci Biobehav Rev. 16:525–534. 1992. View Article : Google Scholar : PubMed/NCBI
18	Muscat R and Willner P: Suppression of sucrose drinking by chronic mild unpredictable stress: A methodological analysis. Neurosci Biobehav Rev. 16:507–517. 1992. View Article : Google Scholar : PubMed/NCBI
19	Patterson ZR, Ducharme R, Anisman H and Abizaid A: Altered metabolic and neurochemical responses to chronic unpredictable stressors in ghrelin receptor-deficient mice. Eur J Neurosci. 32:632–639. 2010. View Article : Google Scholar : PubMed/NCBI
20	Westenbroek C, Ter Horst GJ, Roos MH, Kuipers SD, Trentani A and den Boer JA: Gender-specific effects of social housing in rats after chronic mild stress exposure. Prog Neuropsychopharmacol Biol Psychiatry. 27:21–30. 2003. View Article : Google Scholar : PubMed/NCBI
21	Patterson ZR and Abizaid A: Stress induced obesity: Lessons from rodent models of stress. Front Neurosci. 7:1302013. View Article : Google Scholar : PubMed/NCBI
22	Hou DR, Wang Y, Zhou L, Chen K, Tian Y, Song Z, Bao J and Yang QD: Altered angiotensin-converting enzyme and its effects on the brain in a rat model of Alzheimer disease. Chin Med J (Engl). 121:2320–2323. 2008.PubMed/NCBI
23	Zhang L, Xu D, Zhang B, Liu Y, Chu F, Guo Y, Gong J, Zheng X, Chen L and Wang H: Prenatal food restriction induces a hypothalamic-pituitary-adrenocortical axis-associated neuroendocrine metabolic programmed alteration in adult offspring rats. Arch Med Res. 44:335–345. 2013. View Article : Google Scholar : PubMed/NCBI
24	Xinxing W, Wei L, Lei W, Rui Z, Baoying J and Lingjia Q: A neuroendocrine mechanism of co-morbidity of depression-like behavior and myocardial injury in rats. PLoS One. 9:e884272014. View Article : Google Scholar : PubMed/NCBI
25	Liu L, Liu F, Kou H, Zhang BJ, Xu D, Chen B, Chen LB, Magdalou J and Wang H: Prenatal nicotine exposure induced a hypothalamic-pituitary-adrenal axis-associated neuroendocrine metabolic programmed alteration in intrauterine growth retardation offspring rats. Toxicol Lett. 214:307–313. 2012. View Article : Google Scholar : PubMed/NCBI
26	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI
27	Bao AM, Meynen G and Swaab DF: The stress system in depression and neurodegeneration: Focus on the human hypothalamus. Brain Res Rev. 57:531–553. 2008. View Article : Google Scholar : PubMed/NCBI
28	Woods SC, Seeley RJ, Rushing PA, D'Alessio D and Tso P: A controlled high-fat diet induces an obese syndrome in rats. J Nutr. 133:1081–1087. 2003.PubMed/NCBI
29	McAllan L, Keane D, Schellekens H, Roche HM, Korpela R, Cryan JF and Nilaweera KN: Whey protein isolate counteracts the effects of a high-fat diet on energy intake and hypothalamic and adipose tissue expression of energy balance-related genes. Br J Nutr. 110:2114–2126. 2013. View Article : Google Scholar : PubMed/NCBI
30	Nelovkov A, Philips MA, Kõks S and Vasar E: Rats with low exploratory activity in the elevated plus-maze have the increased expression of limbic system-associated membrane protein gene in the periaqueductal grey. Neurosci Lett. 352:179–182. 2003. View Article : Google Scholar : PubMed/NCBI
31	Hoogenboom WS, Perlis RH, Smoller JW, Zeng-Treitler Q, Gainer VS, Murphy SN, Churchill SE, Kohane IS, Shenton ME and Iosifescu DV: Limbic system white matter microstructure and long-term treatment outcome in major depressive disorder: A diffusion tensor imaging study using legacy data. World J Biol Psychiatry. 15:122–134. 2014. View Article : Google Scholar : PubMed/NCBI
32	Winter SS, Köppen JR, Ebert TB and Wallace DG: Limbic system structures differentially contribute to exploratory trip organization of the rat. Hippocampus. 23:139–152. 2013. View Article : Google Scholar : PubMed/NCBI
33	Sasaki A, De Vega W, Sivanathan S, St-Cyr S and McGowan PO: Maternal high-fat diet alters anxiety behavior and glucocorticoid signaling in adolescent offspring. Neuroscience. 272:92–101. 2014. View Article : Google Scholar : PubMed/NCBI
34	Knight EM, Martins IV, Gümüsgöz S, Allan SM and Lawrence CB: High-fat diet-induced memory impairment in triple-transgenic Alzheimer's disease (3xTgAD) mice is independent of changes in amyloid and tau pathology. Neurobiol Aging. 35:1821–1832. 2014. View Article : Google Scholar : PubMed/NCBI
35	Sahin TD, Karson A, Balci F, Yazir Y, Bayramgurler D and Utkan T: TNF-alpha inhibition prevents cognitive decline and maintains hippocampal BDNF levels in the unpredictable chronic mild stress rat model of depression. Behav Brain Res. 292:233–240. 2015. View Article : Google Scholar : PubMed/NCBI
36	Belda X, Ons S, Carrasco J and Armario A: The effects of chronic food restriction on hypothalamic-pituitary-adrenal activity depend on morning versus evening availability of food. Pharmacol Biochem Behav. 81:41–46. 2005. View Article : Google Scholar : PubMed/NCBI
37	Kokavec A, Lindner AJ, Ryan JE and Crowe SF: Ingesting alcohol prior to food can alter the activity of the hypothalamic-pituitary-adrenal axis. Pharmacol Biochem Behav. 93:170–176. 2009. View Article : Google Scholar : PubMed/NCBI
38	Naert G, Ixart G, Maurice T, Tapia-Arancibia L and Givalois L: Brain-derived neurotrophic factor and hypothalamic-pituitary-adrenal axis adaptation processes in a depressive-like state induced by chronic restraint stress. Mol Cell Neurosci. 46:55–66. 2011. View Article : Google Scholar : PubMed/NCBI
39	Lawson EA, Holsen LM, Desanti R, Santin M, Meenaghan E, Herzog DB, Goldstein JM and Klibanski A: Increased hypothalamic-pituitary-adrenal drive is associated with decreased appetite and hypoactivation of food-motivation neurocircuitry in anorexia nervosa. Eur J Endocrinol. 169:639–647. 2013. View Article : Google Scholar : PubMed/NCBI
40	Shalev U, Tylor A, Schuster K, Frate C, Tobin S and Woodside B: Long-term physiological and behavioral effects of exposure to a highly palatable diet during the perinatal and post-weaning periods. Physiol Behav. 101:494–502. 2010. View Article : Google Scholar : PubMed/NCBI
41	Csabafi K, Jászberènyi M, Bagosi Z, Liptàk N and Telegdy G: Effects of kisspeptin-13 on the hypothalamic-pituitary-adrenal axis, thermoregulation, anxiety and locomotor activity in rats. Behav Brain Res. 241:56–61. 2013. View Article : Google Scholar : PubMed/NCBI
42	Kenny R, Dinan T, Cai G and Spencer SJ: Effects of mild calorie restriction on anxiety and hypothalamic-pituitary-adrenal axis responses to stress in the male rat. Physiol Rep. 2:e002652014. View Article : Google Scholar : PubMed/NCBI
43	Sarubin N, Nothdurfter C, Schüle C, Lieb M, Uhr M, Born C, Zimmermannc R, Bühner M, Konopka K, Rupprecht R and Baghai TC: The influence of Hatha yoga as an add-on treatment in major depression on hypothalamic-pituitary-adrenal-axis activity: A randomized trial. J Psychiatr Res. 53:76–83. 2014. View Article : Google Scholar : PubMed/NCBI
44	McElroy SL, Kotwal R, Malhotra S, Nelson EB, Keck PE and Nemeroff CB: Are mood disorders and obesity related? A review for the mental health professional. J Clin Psychiatry. 65:634–651. 2004. View Article : Google Scholar : PubMed/NCBI
45	de Kloet ER, Vreugdenhil E, Oitzl MS and Joëls M: Brain corticosteroid receptor balance in health and disease. Endocr Rev. 19:269–301. 1998. View Article : Google Scholar : PubMed/NCBI
46	de Kloet ER, Sutanto W, van den Berg DT, Carey MP, van Haarst AD, Hornsby CD, Meijer OC, Rots NY and Oitzl MS: Brain mineralocorticoid receptor diversity: Functional implications. J Steroid Biochem Mol Biol. 47:183–190. 1993. View Article : Google Scholar : PubMed/NCBI
47	de Quervain DJ, Aerni A, Schelling G and Roozendaal B: Glucocorticoids and the regulation of memory in health and disease. Front Neuroendocrinol. 30:358–370. 2009. View Article : Google Scholar : PubMed/NCBI
48	Zhe D, Fang H and Yuxiu S: Expressions of hippocampal mineralocorticoid receptor (MR) and glucocorticoid receptor (GR) in the single-prolonged stress-rats. Acta Histochem Cytochem. 41:89–95. 2008. View Article : Google Scholar : PubMed/NCBI
49	de Kloet ER, Oitzl MS and Joëls M: Functional implications of brain corticosteroid receptor diversity. Cell Mol Neurobiol. 13:433–455. 1993. View Article : Google Scholar : PubMed/NCBI