Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-03T08:31:49.445Z Has data issue: false hasContentIssue false
  • English
  • Français

Chronic high-fat diet increases acute neuroendocrine stress response independently of prenatal dexamethasone treatment in male rats

Published online by Cambridge University Press:  14 June 2013

Anders Abildgaard ,
Sten Lund  and
Karin S Hougaard
Anders Abildgaard*
Affiliation:
Translational Neuropsychiatry Unit, Aarhus University, Risskov, Denmark
Sten Lund
Affiliation:
Medical Department MEA (endocrinology), Aarhus University Hospital, Aarhus, Denmark
Karin S Hougaard
Affiliation:
National Research Centre for the Working Environment, Copenhagen, Denmark
*
Anders Abildgaard, Translational Neuropsychiatry Unit, Aarhus University Hospital, Risskov, Skovagervej 2, 8240 Risskov, Denmark. Tel: +45 7847 1291;Fax: +45 7847 1108; E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective

Intrauterine growth restriction (IUGR) has been associated with metabolic disorders later in life such as obesity and diabetes as well as psychiatric disorders such as depression and schizophrenia. Therefore, we wanted to investigate whether behavioural, metabolic or neuroendocrine abnormalities could be provoked or exacerbated by a high-fat diet (HFD) in an experimental model of IUGR.

Methods

Pregnant dams were exposed to dexamethasone (DEX) in the third gestational week to induce IUGR. Late adolescent male offspring of DEX- and vehicle-treated dams were then fed a HFD or standard chow for 8 weeks and subjected to a variety of assessments.

Results

Only diet affected the hypothalamus-pituitary-adrenal (HPA) axis stress response, as HFD doubled the observed corticosterone levels following acute restraint. HFD and prenatal DEX exposure concomitantly exacerbated depressive-like behaviour in the forced swim test, even though no interaction was seen. Prenatal DEX treatment tended to increase the basal acoustic startle response (ASR), while an interaction between HFD and DEX was present in the ASR pre-pulse inhibition suggestive of fundamental changes in neuronal gating mechanisms. Metabolic parameters were only affected by diet, as HFD increased fasting glucose and insulin levels.

Conclusion

We conclude that chronic HFD may be more important in programming of the HPA axis stress responsiveness than an adverse foetal environment and therefore potentially implies an increased risk for developing psychiatric and metabolic disease.

Keywords

depressive disorderdiethigh-fatIUGRmodelanimalsstressphysiological
Type
Original Articles
Information
Acta Neuropsychiatrica , Volume 26 , Issue 1 , February 2014 , pp. 8 - 18
Copyright
Copyright © Scandinavian College of Neuropsychopharmacology 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1.McMillen, IC, Robinson, JS. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 2005;85:571–633.CrossRefGoogle ScholarPubMed
2.Kingston, D, Tough, S, Whitfield, H. Prenatal and postpartum maternal psychological distress and infant development: a systematic review. Child Psychiatry Hum Dev 2012;43:683–714.CrossRefGoogle ScholarPubMed
3.Godfrey, KM, Inskip, HM, Hanson, MA. The long-term effects of prenatal development on growth and metabolism. Semin Reprod Med 2011;29:257–265.CrossRefGoogle ScholarPubMed
4.Hales, CN, Barker, DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diab tologia 1992;35:595–601.CrossRefGoogle ScholarPubMed
5.Desai, M, Ross, MG. Fetal programming of adipose tissue: effects of intrauterine growth restriction and maternal obesity/high-fat diet. Semin Reprod Med 2011;29:237–245.CrossRefGoogle ScholarPubMed
6.Cannon, M, Jones, PB, Murray, RM. Obstetric complications and schizophrenia: historical and meta-analytic review. Am J Psychiatry 2002;159:1080–1092.CrossRefGoogle ScholarPubMed
7.Gale, CR, Martyn, CN. Birth weight and later risk of depression in a national birth cohort. Br J Psychiatry 2004;184:28–33.CrossRefGoogle Scholar
8.Wojcik, W, Lee, W, Colman, I, Hardy, R, Hotopf, M. Foetal origins of depression? A systematic review and meta-analysis of low birth weight and later depression. Psychol Med 2013;43:1–12.CrossRefGoogle ScholarPubMed
9.Rees, S, Harding, R, Walker, D. An adverse intrauterine environment: implications for injury and altered development of the brain. Int J Dev Neurosci 2008;26:3–11.CrossRefGoogle ScholarPubMed
10.Phillips, DI. Programming of the stress response: a fundamental mechanism underlying the long-term effects of the fetal environment? J Intern Med 2007;261:453–460.CrossRefGoogle ScholarPubMed
11.Mezuk, B, Eaton, WW, Albrecht, S, Golden, SH. Depression and type 2 diabetes over the lifespan: a meta-analysis. Diabetes Care 2008;31:2383–2390.CrossRefGoogle ScholarPubMed
12.Ali, S, Stone, MA, Peters, JL, Davies, MJ, Khunti, K. The prevalence of co-morbid depression in adults with type 2 diabetes: a systematic review and meta-analysis. Diabet Med 2006;23:1165–1173.CrossRefGoogle ScholarPubMed
13.Pan, A, Keum, N, Okereke, OIet al. Bidirectional association between depression and metabolic syndrome: a systematic review and meta-analysis of epidemiological studies. Diabetes Care 2012;35:1171–1180.CrossRefGoogle ScholarPubMed
14.Reinisch, JM, Simon, NG, Karow, WG, Gandelman, R. Prenatal exposure to prednisone in humans and animals retards intrauterine growth. Science 1978;202:436–438.CrossRefGoogle ScholarPubMed
15.Nyirenda, MJ, Lindsay, RS, Kenyon, CJ, Burchell, A, Seckl, JR. Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. J Clin Invest 1998;101:2174–2181.CrossRefGoogle ScholarPubMed
16.Buhl, ES, Neschen, S, Yonemitsu, Set al. Increased hypothalamic–pituitary–adrenal axis activity and hepatic insulin resistance in low-birth-weight rats. Am J Physiol Endocrinol Metab 2007;293:E1451–E1458.CrossRefGoogle ScholarPubMed
17.Hauser, J, Feldon, J, Pryce, CR. Direct and dam-mediated effects of prenatal dexamethasone on emotionality, cognition and HPA axis in adult Wistar rats. Horm Behav 2009;56:364–375.CrossRefGoogle ScholarPubMed
18.Welberg, LA, Seckl, JR, Holmes, MC. Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: possible implications for behaviour. Neuroscience 2001;104:71–79.CrossRefGoogle ScholarPubMed
19.Brabham, T, Phelka, A, Zimmer, C, Nash, A, Lopez, JF, Vazquez, DM. Effects of prenatal dexamethasone on spatial learning and response to stress is influenced by maternal factors. Am J Physiol Regul Integr Comp Physiol 2000;279:R1899–R1909.CrossRefGoogle ScholarPubMed
20.Shoener, JA, Baig, R, Page, KC. Prenatal exposure to dexamethasone alters hippocampal drive on hypothalamic–pituitary–adrenal axis activity in adult male rats. Am J Physiol Regul Integr Comp Physiol 2006;290:R1366–R1373.CrossRefGoogle ScholarPubMed
21.O'Regan, D, Kenyon, CJ, Seckl, JR, Holmes, MC. Glucocorticoid exposure in late gestation in the rat permanently programs gender-specific differences in adult cardiovascular and metabolic physiology. Am J Physiol Endocrinol Metab 2004;287:E863–E870.CrossRefGoogle ScholarPubMed
22.Oliveira, M, Bessa, JM, Mesquita, Aet al. Induction of a hyperanxious state by antenatal dexamethasone: a case for less detrimental natural corticosteroids. Biol Psychiatry 2006;59:844–852.CrossRefGoogle ScholarPubMed
23.Kjaer, SL, Wegener, G, Rosenberg, R, Hougaard, KS. Reduced mobility but unaffected startle response in female rats exposed to prenatal dexamethasone: different sides to a phenotype. Dev Neurosci 2010;32:208–216.CrossRefGoogle ScholarPubMed
24.Nagano, M, Ozawa, H, Suzuki, H. Prenatal dexamethasone exposure affects anxiety-like behaviour and neuroendocrine systems in an age-dependent manner. Neurosci Res 2008;60:364–371.CrossRefGoogle Scholar
25.Drake, AJ, Raubenheimer, PJ, Kerrigan, D, McInnes, KJ, Seckl, JR, Walker, BR. Prenatal dexamethasone programs expression of genes in liver and adipose tissue and increased hepatic lipid accumulation but not obesity on a high-fat diet. Endocrinology 2010;151:1581–1587.CrossRefGoogle Scholar
26.Shahkhalili, Y, Moulin, J, Zbinden, I, Aprikian, O, Mace, K. Comparison of two models of intrauterine growth restriction for early catch-up growth and later development of glucose intolerance and obesity in rats. Am J Physiol Regul Integr Comp Physiol 2010;298:R141–R146.CrossRefGoogle ScholarPubMed
27.Koch, M. The neurobiology of startle. Prog Neurobiol 1999;59:107–128.CrossRefGoogle ScholarPubMed
28.Hougaard, KS, Andersen, MB, Kjaer, SL, Hansen, AM, Werge, T, Lund, SP. Prenatal stress may increase vulnerability to life events: comparison with the effects of prenatal dexamethasone. Brain Res Dev Brain Res 2005;159:55–63.CrossRefGoogle ScholarPubMed
29.O'Regan, D, Kenyon, CJ, Seckl, JR, Holmes, MC. Prenatal dexamethasone ‘programmes’ hypotension, but stress-induced hypertension in adult offspring. J Endocrinol 2008;196:343–352.CrossRefGoogle ScholarPubMed
30.Buettner, R, Scholmerich, J, Bollheimer, LC. High-fat diets: modeling the metabolic disorders of human obesity in rodents. Obesity (Silver Spring) 2007;15:798–808.CrossRefGoogle ScholarPubMed
31.Winocur, G, Greenwood, CE. Studies of the effects of high fat diets on cognitive function in a rat model. Neurobiol Aging 2005;26(Suppl. 1):46–49.CrossRefGoogle ScholarPubMed
32.Pathan, AR, Gaikwad, AB, Viswanad, B, Ramarao, P. Rosiglitazone attenuates the cognitive deficits induced by high fat diet feeding in rats. Eur J Pharmacol 2008;589:176–179.CrossRefGoogle ScholarPubMed
33.Abildgaard, A, Solskov, L, Volke, V, Harvey, BH, Lund, S, Wegener, G. A high-fat diet exacerbates depressive-like behavior in the Flinders Sensitive Line (FSL) rat, a genetic model of depression. Psychoneuroendocrinology 2011;36:623–633.CrossRefGoogle Scholar
34.Porsolt, RD, Le, PM, Jalfre, M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977;266:730–732.CrossRefGoogle ScholarPubMed
35.Cryan, JF, Markou, A, Lucki, I. Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci 2002;23:238–245.CrossRefGoogle ScholarPubMed
36.Detke, MJ, Rickels, M, Lucki, I. Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacology (Berl) 1995;121:66–72.CrossRefGoogle ScholarPubMed
37.Grillon, C. Models and mechanisms of anxiety: evidence from startle studies. Psychopharmacology (Berl) 2008;199:421–437.CrossRefGoogle ScholarPubMed
38.Swerdlow, NR, Weber, M, Qu, Y, Light, GA, Braff, DL. Realistic expectations of prepulse inhibition in translational models for schizophrenia research. Psychopharmacology (Berl) 2008;199:331–388.CrossRefGoogle ScholarPubMed
39.Hougaard, KS, Andersen, MB, Hansen, AM, Hass, U, Werge, T, Lund, SP. Effects of prenatal exposure to chronic mild stress and toluene in rats. Neurotoxicol Teratol 2005;27:153–167.CrossRefGoogle ScholarPubMed
40.Wallace, TM, Levy, JC, Matthews, DR. Use and abuse of HOMA modeling. Diabetes Care 2004;27:1487–1495.CrossRefGoogle ScholarPubMed
41.Tannenbaum, BM, Brindley, DN, Tannenbaum, GS, Dallman, MF, McArthur, MD, Meaney, MJ. High-fat feeding alters both basal and stress-induced hypothalamic–pituitary–adrenal activity in the rat. Am J Physiol 1997;273(Pt 1):E1168–E1177.Google ScholarPubMed
42.Kamara, K, Eskay, R, Castonguay, T. High-fat diets and stress responsivity. Physiol Behav 1998;64:1–6.CrossRefGoogle ScholarPubMed
43.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;37:382–389.CrossRefGoogle ScholarPubMed
44.Maniam, J, Morris, MJ. Voluntary exercise and palatable high-fat diet both improve behavioural profile and stress responses in male rats exposed to early life stress: role of hippocampus. Psychoneuroendocrinology 2010;35(10):1553–1564.CrossRefGoogle ScholarPubMed
45.la Fleur, SE, Houshyar, H, Roy, M, Dallman, MF. Choice of lard, but not total lard calories, damps adrenocorticotropin responses to restraint. Endocrinology 2005;146:2193–2199.CrossRefGoogle Scholar
46.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;145:3754–3762.CrossRefGoogle ScholarPubMed
47.Ulrich-Lai, YM, Ostrander, MM, Herman, JP. HPA axis dampening by limited sucrose intake: reward frequency vs. caloric consumption. Physiol Behav 2011;103:104–110.CrossRefGoogle ScholarPubMed
48.Pasquali, R, Vicennati, V, Cacciari, M, Pagotto, U. The hypothalamic–pituitary–adrenal axis activity in obesity and the metabolic syndrome. Ann N Y Acad Sci 2006;1083:111–128.CrossRefGoogle ScholarPubMed
49.Champaneri, S, Xu, X, Carnethon, MRet al. Diurnal salivary cortisol is associated with body mass index and waist circumference: the multiethnic study of atherosclerosis. Obesity (Silver Spring) 2013;21:E56–E63.CrossRefGoogle ScholarPubMed
50.Hougaard, KS, Mandrup, KR, Kjaer, SL, Bogh, IB, Rosenberg, R, Wegener, G. Gestational chronic mild stress: effects on acoustic startle in male offspring of rats. Int J Dev Neurosci 2011;29:495–500.CrossRefGoogle ScholarPubMed
51.Kjaer, SL, Wegener, G, Rosenberg, R, Lund, SP, Hougaard, KS. Prenatal and adult stress interplay – behavioral implications. Brain Res 2010;1320:106–113.CrossRefGoogle ScholarPubMed
52.Skripuletz, T, Kruschinski, C, Pabst, R, von Horsten, S, Stephan, M. Postnatal experiences influence the behavior in adult male and female Fischer and Lewis rats. Int J Dev Neurosci 2010;28:561–571.CrossRefGoogle ScholarPubMed
53.Akbaraly, TN, Brunner, EJ, Ferrie, JE, Marmot, MG, Kivimaki, M, Singh-Manoux, A. Dietary pattern and depressive symptoms in middle age. Br J Psychiatry 2009;195:408–413.CrossRefGoogle ScholarPubMed
54.Brinkworth, GD, Buckley, JD, Noakes, M, Clifton, PM, Wilson, CJ. Long-term effects of a very low-carbohydrate diet and a low-fat diet on mood and cognitive function. Arch Intern Med 2009;169:1873–1880.CrossRefGoogle Scholar
55.Jacka, FN, Pasco, JA, Mykletun, Aet al. Association of Western and traditional diets with depression and anxiety in women. Am J Psychiatry 2010;167:305–311.CrossRefGoogle ScholarPubMed
56.Hauser, J, Feldon, J, Pryce, CR. Prenatal dexamethasone exposure, postnatal development, and adulthood prepulse inhibition and latent inhibition in Wistar rats. Behav Brain Res 2006;175:51–61.CrossRefGoogle ScholarPubMed
57.Claessens, SE, Daskalakis, NP, Oitzl, MS, de Kloet, ER. Early handling modulates outcome of neonatal dexamethasone exposure. Horm Behav 2012;62:433–441.CrossRefGoogle ScholarPubMed
58.Morrison, JL, Duffield, JA, Muhlhausler, BS, Gentili, S, McMillen, IC. Fetal growth restriction, catch-up growth and the early origins of insulin resistance and visceral obesity. Pediatr Nephrol 2010;25:669–677.CrossRefGoogle ScholarPubMed
59. WHO. Diet, nutrition and the prevention of chronic diseases: WHO2003. Report No.: 0512-3054 (Print).Google Scholar
60. WHO. WHO Fact Sheet 311: Obesity and overweight: WHO2006.Google Scholar