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Maternal high fat diet during critical windows of development alters adrenal cortical and medullary enzyme expression in adult male rat offspring

Published online by Cambridge University Press:  18 May 2010

K. L. Connor ,
M. H. Vickers ,
C. Cupido ,
E. Sirimanne  and
D. M. Sloboda
K. L. Connor
Affiliation:
Liggins Institute and the National Research Centre for Growth and Development, University of Auckland, Auckland, New Zealand
M. H. Vickers
Affiliation:
Liggins Institute and the National Research Centre for Growth and Development, University of Auckland, Auckland, New Zealand
C. Cupido
Affiliation:
Liggins Institute and the National Research Centre for Growth and Development, University of Auckland, Auckland, New Zealand
E. Sirimanne
Affiliation:
Liggins Institute and the National Research Centre for Growth and Development, University of Auckland, Auckland, New Zealand
D. M. Sloboda*
Affiliation:
Liggins Institute and the National Research Centre for Growth and Development, University of Auckland, Auckland, New Zealand
*
*Address for correspondence: Dr D. M. Sloboda, Liggins Institute and the National Research Centre for Growth and Development, University of Auckland, Auckland, New Zealand. (Email [email protected])
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Abstract

We previously reported that a maternal high fat (HF) diet resulted in adult offspring with increased adiposity and hyperleptinemia. As leptin has an inhibitory effect on adrenal steroidogenesis and a stimulatory effect on epinephrine synthesis, we hypothesized that key adrenal steroidogenic and catecholaminergic enzymes would be altered in these offspring. Wistar rats were randomized into three groups at weaning: (1) control dams fed a standard control chow diet from weaning and throughout pregnancy and lactation (CON), (2) dams fed a HF diet from weaning and throughout pregnancy and lactation (MHF) and (3) dams fed standard control chow diet throughout life until conception, then fed a HF diet in pregnancy and lactation (PLHF). Dams were mated at day 100 (P100). After birth at P22 (weaning), male offspring were fed a standard control chow (con) or high fat (hf) diet. At P160, plasma samples and adrenal tissues were collected. Postweaning hf diet significantly elevated plasma corticosterone concentrations in PLHF-hf offspring compared to PLHF-con. MHF nutrition increased adrenal adrenocorticotrophic hormone receptor (ACTH-R) mRNA levels compared to CON-con. 3β-hydroxysteroid dehydrogenase (3βHSD) mRNA levels were decreased in MHF compared to PLHF offspring. Phenylethanolamine N-methyltransferase (PNMT) mRNA levels were increased in MHF-hf offspring compared to MHF-con. Plasma homocysteine (HCY) concentrations were significantly elevated in CON-hf and MHF-hf offspring compared to chow-fed offspring, associated with elevated intakes of methionine and reduced intakes of pyridoxine. Immunoreactive leptin receptor (ObRb) and PNMT were colocalized in medullary chromaffin cells. This study suggests that a postweaning HF diet in offspring induced changes in adrenal gene expression levels that are dependent upon the level of maternal nutrition.

Keywords

adrenalhigh fatpregnancyobesity
Type
Original Articles
Information
Journal of Developmental Origins of Health and Disease , Volume 1 , Issue 4 , August 2010 , pp. 245 - 254
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2010

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References

1.Barker, DJP, Winter, PD, Osmond, C, Margetts, B, Simmonds, SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989; 2, 577–580.CrossRefGoogle ScholarPubMed
2.Barker, DJ, Eriksson, JG, Forsen, T, Osmond, C. Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol. 2002; 31, 1235–1239.CrossRefGoogle ScholarPubMed
3.Yajnik, CS, Deshmukh, US. Maternal nutrition, intrauterine programming and consequential risks in the offspring. Rev Endocr Metab Disord. 2008; 9, 203–211.CrossRefGoogle ScholarPubMed
4.Ehrenberg, HM, Dierker, L, Milluzzi, C, Mercer, BM. Prevalence of maternal obesity in an urban center. Am J Obstet Gynecol. 2002; 187, 1189–1193.CrossRefGoogle Scholar
5.Catalano, PM, Ehrenberg, HM. The short- and long-term implications of maternal obesity on the mother and her offspring. BJOG. 2006; 113, 1126–1133.CrossRefGoogle Scholar
6.Guo, F, Jen, KLC. High-fat feeding during pregnancy and lactation affects offspring metabolism in rats. Physiol Behav. 1995; 57, 681–686.CrossRefGoogle ScholarPubMed
7.Khan, IY, Taylor, PD, Dekou, V, et al. Gender-linked hypertension in offspring of lard-fed pregnant rats. Hypertension. 2003; 41, 168–175.CrossRefGoogle ScholarPubMed
8.Khan, I, Dekou, V, Hanson, M, Poston, L, Taylor, P. Predictive adaptive responses to maternal high-fat diet prevent endothelial dysfunction but not hypertension in adult rat offspring. Circulation. 2004; 110, 1097–1102.CrossRefGoogle Scholar
9.Samuelsson, A-M, Matthews, PA, Argenton, M, et al. Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension. 2008; 51, 383–392.CrossRefGoogle ScholarPubMed
10.Howie, GJ, Sloboda, DM, Kama, T, Vickers, MH. Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J Physiol. 2009; 587, 905–915.CrossRefGoogle ScholarPubMed
11.Bjorntorp, P. Do stress reactions cause abdominal obesity and comorbidities? Obes Rev. 2001; 2, 73–86.CrossRefGoogle ScholarPubMed
12.Marin, P, Darin, N, Amemiva, T, et al. Cortisol secretion in relation to body fat distribution in obese premenopausal women. Metabolism. 1992; 41, 882–886.CrossRefGoogle ScholarPubMed
13.Rosmond, R, Bjorntorp, P. The interactions between hypothalamic-pituitary-adrenal axis activity, testosterone, insulin-like growth factor I and abdominal obesity with metabolism and blood pressure in men. Int J Obes Relat Metab Disord. 1998; 22, 1184–1196.CrossRefGoogle ScholarPubMed
14.Rosmond, R, Dallman, MF, Bjorntorp, P. Stress-related cortisol secretion in men: relationships with abdominal obesity and endocrine, metabolic and hemodynamic abnormalities. J Clin Endocrinol Metab. 1998; 83, 61853–61859.Google ScholarPubMed
15.Rutters, F, Nieuwenhuizen, AG, Lemmens, SG, Born, JM, Westerterp-Plantenga, MS. Hypothalamus-Pituitary-Adrenal (HPA) axis functioning in relation to body fat distribution. Clin Endocrinol. 2010; 72, 738–743.CrossRefGoogle Scholar
16.Lesage, J, Blondeau, B, Grino, M, Breant, B, Dupouy, JP. Maternal undernutrition during late gestation induces fetal overexposure to glucocorticoids and intrauterine growth retardation, and disturbs the hypothalamo-pituitary adrenal axis in the newborn rat. Endocrinology. 2001; 142, 1692–1702.CrossRefGoogle ScholarPubMed
17.Bloomfield, FH, Oliver, MH, Giannoulias, CD, et al. Brief undernutrition in late-gestation sheep programs the hypothalamic-pituitary-adrenal axis in adult offspring. Endocrinology. 2003; 144, 2933–2940.CrossRefGoogle ScholarPubMed
18.Entringer, S, Kumsta, R, Hellhammer, DH, Wadhwa, PD, Wust, S. Prenatal exposure to maternal psychosocial stress and HPA axis regulation in young adults. Horm Behav. 2009; 55, 292–298.CrossRefGoogle ScholarPubMed
19.King, BM, Smith, RL. Hypothalamic obesity after hypophysectomy or adrenalectomy: dependence on corticosterone. Am J Physiol. 1985; 249, R522–R526.Google ScholarPubMed
20.Freedman, MR, Horwitz, BA, Stern, JS. Effect of adrenalectomy and glucocorticoid replacement on the development of obesity. Am J Physiol. 1986; 250, R595–R607.Google ScholarPubMed
21.Cherradi, N, Capponi, AM, Gaillard, RC, Pralong, FP. Decreased expression of steroidogenic acute regulatory protein: a novel mechanism participating in the leptin-induced inhibition of glucocorticoid biosynthesis. Endocrinology. 2001; 142, 3302–3308.CrossRefGoogle ScholarPubMed
22.Hsu, HT, Chang, YC, Chiu, YN, et al. Leptin interferes with adrenocorticotropin/3′,5′-cyclic adenosine monophosphate (cAMP) signaling, possibly through a Janus kinase 2-phosphatidylinositol 3-kinase/Akt-phosphodiesterase 3-cAMP pathway, to down-regulate cholesterol side-chain cleavage cytochrome P450 enzyme in human adrenocortical NCI-H295 cell line. J Clin Endocrinol Metab. 2006; 91, 2761–2769.CrossRefGoogle Scholar
23.Shibuya, I, Utsunomiya, K, Toyohira, Y, et al. Regulation of catecholamine synthesis by leptin. Ann N Y Acad Sci. 2002; 971, 522–527.CrossRefGoogle ScholarPubMed
24.Trevenzoli, IH, Valle, MM, Machado, FB, et al. Neonatal hyperleptinaemia programmes adrenal medullary function in adult rats: effects on cardiovascular parameters. J Physiol. 2007; 580, 629–637.CrossRefGoogle ScholarPubMed
25.Glasgow, A, Haidan, A, Hilbers, U, et al. Expression of Ob receptor in normal human adrenals: differential regulation of adrenocortical and adrenomedullary function by leptin. J Clin Endocrinol Metab. 1998; 83, 4459–4466.Google Scholar
26.Pralong, FP, Roduit, R, Waeber, G, et al. Leptin inhibits directly glucocorticoid secretion by normal human and rat adrenal gland. Endocrinology. 1998; 139, 4264–4268.CrossRefGoogle ScholarPubMed
27.Chelikani, PK, Glimm, DR, Kennelly, JJ. Tissue distribution of leptin and leptin receptor mRNA in the bovine. J Dairy Sci. 2003; 86, 2369–2372.CrossRefGoogle ScholarPubMed
28.Cao, GY, Considine, RV, Lynn, RB. Leptin receptors in the adrenal medulla of the rat. Am J Physiol. 1997; 273, E448–E452.Google ScholarPubMed
29.Takekoshi, K, Motooka, M, Isobe, K, et al. Leptin directly stimulates catecholamine secretion and synthesis in cultured porcine adrenal medullary cells. Biochem Biophys Res Commun. 1999; 261, 426–431.CrossRefGoogle Scholar
30.Malendowicz, LK, Rucinski, M, Belloni, AS, Ziolkowska, A, Nussdorfer, GG. Leptin and the regulation of the hypothalamic-pituitary-adrenal axis. Int Rev Cytol. 2007; 263, 63–102.CrossRefGoogle ScholarPubMed
31.Kelner, KL, Pollard, HB. Glucocorticoid receptors and regulation of phenylethanolamine-N-methyltransferase activity in cultured chromaffin cells. J Neurosci. 1985; 5, 2161–2168.CrossRefGoogle ScholarPubMed
32.Vander Tuig, JG, Kerner, J, Romsos, DR. Hypothalamic obesity, brown adipose tissue, and sympathoadrenal activity in rats. Am J Physiol Endocrinol Metab. 1985; 248, E607–E617.CrossRefGoogle ScholarPubMed
33.Wurtman, RJ, Axelrod, J. Control of enzymatic synthesis of adrenaline in the adrenal medulla by adrenal cortical steroids. J Biol Chem. 1966; 241, 2301–2305.CrossRefGoogle ScholarPubMed
34.Thoenen, H, Mueller, RA, Axelrod, J. Neuronally dependent induction of phenylethanolamlne-N-methyl transferase by 6-hydroxydopamine. Biochem Pharmacol. 1970; 19, 669–673.CrossRefGoogle ScholarPubMed
35.Zhu, W, Huang, X, Li, M, Neubauer, H. Elevated plasma homocysteine in obese schoolchildren with early atherosclerosis. Eur J Pediatr. 2005; 165, 326–331.CrossRefGoogle ScholarPubMed
36.Karatela, RA, Sainani, GS. Plasma homocysteine in obese, overweight and normal weight hypertensives and normotensives. Indian Heart J. 2009; 61, 156–159.Google ScholarPubMed
37.Austin, RC, Lentz, SR, Werstuck, GH. Role of hyperhomocysteinemia in endothelial dysfunction and atherothrombotic disease. Cell Death Differ. 2004; 11, S56–S64.CrossRefGoogle ScholarPubMed
38.Franken, DG, Boers, GHJ, Blom, HJ, Trijibels, FJM, Kloppenborg, PW. Treatment of mild hyperhomocysteinemia in vascular disease patients. Arterioscler Thromb. 1994; 14, 465–470.CrossRefGoogle ScholarPubMed
39.Selhub, J, Jacques, PF, Wilson, PWF, Rush, D, Rosenberg, IH. Vitamin status and intake as primary determinants of homocysteinemia in an elderly population. JAMA. 1993; 270, 2693–2698.CrossRefGoogle Scholar
40.Mudd, SH, Havlik, R, Levy, HL, McKusick, VA, Feinleib, M. Cardiovascular risk in heterozygotes for homocystinuria. Am J Hum Gen. 1982; 34, 1018–1021.Google ScholarPubMed
41.Frosst, P, Blom, HJ, Milos, R, et al. A candidate genetic risk factor for vascular disease: a common mutation in methylenetetrahydrofolate reductase. Nat Genet. 1995; 10, 111–113.CrossRefGoogle ScholarPubMed
42.Austin, RC, Lentz, SR, Werstuck, GH. Role of hyperhomocysteinemia in endothelial dysfunction and atherothrombotic disease. Cell Death Differ. 2004; 11, S56–S64.CrossRefGoogle ScholarPubMed
43.Martin, JL, Begun, J, McLeish, MJ, Caine, JM, Grunewald, GL. Getting the adrenaline going: crystal structure of the adrenaline-synthesizing enzyme PNMT. Structure. 2001; 9, 977–985.CrossRefGoogle ScholarPubMed
44.Rozen, S, Skaletsky, HJ. Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics Methods and Protocols: Methods in Molecular Biology, 1st edn (eds. Krawetz S, Misener S), 2000; pp. 365–386. Humana Press, Totowa, New Jersey.Google Scholar
45.Viegas, MS, Martins, TC, Seco, F, do Carmo, A. An improved and cost-effective methodology for the reduction of autofluorescence in direct immunofluorescence studies on formalin-fixed paraffin-embedded tissues. Euro J Histochem. 2007; 51, 59–66.Google ScholarPubMed
46.Gardner, DS, Van Bon, BW, Dandrea, J, et al. Effect of periconceptional undernutrition and gender on hypothalamic-pituitary-adrenal axis function in young adult sheep. J Endocrinol. 2006; 190, 203–212.CrossRefGoogle ScholarPubMed
47.Connor, KL, Bloomfield, FH, Oliver, MH, Harding, JE, Challis, JRG. Effect of periconceptional undernutrition in sheep on late gestation expression of mRNA and protein from genes involved in fetal adrenal steroidogenesis and placental prostaglandin production. Reprod Sci. 2009; 16, 573–583.CrossRefGoogle ScholarPubMed
48.Salzmann, C, Otis, M, Long, H, et al. Inhibition of steroidogenic response to adrenocrticotropin by leptin: implications for the adrenal response to maternal separation in neonatal rats. Endocrinology. 2004; 145, 1810–1822.CrossRefGoogle ScholarPubMed
49.Utsunomiya, K, Yanagihara, N, Tachikawa, E, et al. Stimulation of catecholamine synthesis in cultured bovine adrenal medullary cells by leptin. J Neurochem. 2001; 76, 926–934.CrossRefGoogle ScholarPubMed
50.Haycock, JW, Ahn, NG, Cobb, MH, Krebs, EG. ERK1 and ERK2, two microtubule-associated protein 2 kinases, mediate the phosphorylation of tyrosine hydroxylase at serine-31 in situ. Proc Natl Acad Sci USA. 1992; 89, 2365–2369.CrossRefGoogle ScholarPubMed
51.Shibuya, I, Utsunomiya, K, Toyohira, Y, et al. Regulation of catecholamine synthesis by leptin. Ann N Y Acad Sci. 2002; 971, 522–527.CrossRefGoogle ScholarPubMed
52.Boushey, CJ, Beresford, SA, Omenn, GS, Motulsky, AG. A quantitative assessment of plasma homocysteine as a risk factor for vascular disease. Probable benefits of increasing folic acid intakes. JAMA. 1995; 274, 1049–1057.CrossRefGoogle ScholarPubMed
53.Siow, YL, Dakshinamurti, K. Effect of pyridoxine deficiency on aromatic L-amino acid decarboxylase in adult rat brain. Exp Brain Res. 1984; 59, 575–581.Google Scholar
54.Rees, WD. Manipulating the sulfur amino acid content of the early diet and its implications for long-term health. Proc Nutr Soc. 2002; 61, 71–77.CrossRefGoogle ScholarPubMed
55.Langley-Evans, SC, Lilley, C, McMullen, S. Maternal protein restriction and fetal growth: lack of evidence of a role for homocysteine in fetal programming. Br J Nutr. 2006; 96, 578–586.CrossRefGoogle ScholarPubMed
56.Engeham, SF, Haase, A, Langley-Evans, SC. Supplementation of a maternal low-protein diet in rat pregnancy with folic acid ameliorates programming effects upon feeding behaviour in the absence of disturbances to the methionine-homocysteine cycle. Br J Nutr. 2009; 27, 1–12.Google Scholar
57.Malendowicz, LK, Neri, G, Markowska, A, et al. Effects of leptin and leptin fragments on steroid secretion of freshly dispersed rat adrenocortical cells. J Steroid Biochem Mol Bio. 2003; 87, 265–268.CrossRefGoogle ScholarPubMed
58.Rucinski, M, Tortorella, C, Ziolkowska, A, Nowak, M, Nussdorfer, GG, Malendowicz, LK. Steroidogenic acute regulatory protein gene expression, steroid-hormone secretion and proliferative activity of adrenocortical cells in the presence of proteasome inhibitors: In vivo studies on the regenerating rat adrenal cortex. Int J Mol Med. 2008; 21, 593–597.Google ScholarPubMed