Restraint-Induced Glucocorticoid Receptor Downregulation is Dysregulated in High Fat Diet-Fed Rats Likely from Impairment of miR-142-3p Expression in the Hypothalamus and Hippocampus
American Journal of Life Sciences
Volume 3, Issue 3-2, May 2015, Pages: 24-30
Received: Feb. 25, 2015; Accepted: Mar. 25, 2015; Published: May 6, 2015
Views 4036      Downloads 121
Takahiro Nemoto, Dept. Physiology, Nippon Medical School, Tokyo, Japan
Yoshihiko Kakinuma, Dept. Physiology, Nippon Medical School, Tokyo, Japan
Tamotsu Sibasaki, Dept. Physiology, Nippon Medical School, Tokyo, Japan
Article Tools
Follow on us
High fat diet (HFD) induces dysregulation of the hypothalamic-pituitary-adrenal (HPA) axis function. The HPA axis is controlled by the feedback of glucocortioids on the hypothalamus, hippocampus and pituitary. At least three miRNAs (miR-101a, miR-124, miR-142-3p) have been reported to suppress glucocorticoid receptor (GR) translation. Because their relation to stress-induced downregulation of GR expression and dysregulation of its expression in HFD feeding are unclear, we studied to identify which miRNAs are involved in restraint-induced downregulation of GR expression in the hypothalamus and hippocampus, and to compare the basal and restraint-modified miRNA expressions in these tissues in HFD-fed rats. Rats exposed to HFD were divided into two groups, HFD-induced obese (HFD-ob) and obesity resistant (HFD-obR) rats. Basal plasma corticosterone concentrations were higher in HFD-ob than in standard chow-fed (SC) rats and in HFD-obR. Restraint-induced elevation of plasma corticosterone was higher in HFD-obR than in the other groups. Restraint decreased GR expressions and increased miR-142-3p expression in the hypothalamus and hippocampus without affecting others expressions. miR-142-3p expressions in both areas were increased by dexamethasone and restraint-induced miR-142-3p expression was blocked in adrenalectomy. The basal expression of GR or miR-142-3p expression in both areas of HFD-fed rats did not differ from those of SC, and restraint induced no changes in GR or miR-142-3p expression in both areas in HFD-ob and HFD-obR. These results suggest that impairment of glucocorticoid-induced increase in miR-142-3p may be involved in dysregulation of stress-induced downregulation of GR expression in the hypothalamus and hippocampus of HFD-fed rats.
Stress, High Fat Diet, Hypothalamus, Hippocampus, microRNA
To cite this article
Takahiro Nemoto, Yoshihiko Kakinuma, Tamotsu Sibasaki, Restraint-Induced Glucocorticoid Receptor Downregulation is Dysregulated in High Fat Diet-Fed Rats Likely from Impairment of miR-142-3p Expression in the Hypothalamus and Hippocampus, American Journal of Life Sciences. Special Issue: Biology and Medicine of Peptide and Steroid Hormones. Vol. 3, No. 3-2, 2015, pp. 24-30. doi: 10.11648/j.ajls.s.2015030302.15
C. Dong, L. E. Sanchez, R. A. Price, "Relationship of obesity to depression: a family-based study," Int J Obesity Relat Metab Disorders, vol. 28, pp. 790-795, 2004.
R. G. Kathol, "Circannual rhythm and peak frequency of corticosteroid excretion: relationship to affective disorder," Psychiatric Med., vol. 3, pp. 53-63, 1985.
B. J. Carroll, A. Iranmanesh, D. M. Keenan, F. Cassidy, W. H. Wilson, J. D. Veldhuis, "Pathophysiology of hypercortisolism in depression: pituitary and adrenal responses to low glucocorticoid feedback," Acta Psychiatr Scand., vol. 125, pp. 478-491, 2012.
B. Claustrat, G. Chazot, J. Brun, D. Jordan, G. Sassolas, "A chronobiological study of melatonin and cortisol secretion in depressed subjects: plasma melatonin, a biochemical marker in major depression," Biol Psychiatry., vol. 19, pp. 1215-1228, 1984.
C. Anacker, P. A. Zunszain, L. A. Carvalho, C. M. Pariante, "The glucocorticoid receptor: pivot of depression and of antidepressant treatment?," Psychoneuroendocrinol., vol. 36, pp. 415-425, 2011.
P. Cano, V. Jimenez-Ortega, A. Larrad, C. F. Reyes Toso, D. P. Cardinali, A. I. Esquifino, "Effect of a high-fat diet on 24-h pattern of circulating levels of prolactin, luteinizing hormone, testosterone, corticosterone, thyroid-stimulating hormone and glucose, and pineal melatonin content, in rats," Endocrine, vol. 33, pp. 118-125, 2008.
B. M. Tannenbaum, D. N. Brindley, G. S. Tannenbaum, M. F. Dallman, M. D. McArthur, M. J. Meaney, "High-fat feeding alters both basal and stress-induced hypothalamic-pituitary-adrenal activity in the rat," Am J Physiol., vol. 273, pp. E1168-1177, 1997.
B. L. Roland, Z. S. Krozowski, J. W. Funder, "Glucocorticoid receptor, mineralocorticoid receptors, 11 beta-hydroxysteroid dehydrogenase-1 and -2 expression in rat brain and kidney: in situ studies," Mol Cell Endocrinol., vol. 111, pp. R1-7, 1995.
M. Morimoto, N. Morita, H. Ozawa, K. Yokoyama, M. Kawata, "Distribution of glucocorticoid receptor immunoreactivity and mRNA in the rat brain: an immunohistochemical and in situ hybridization study," Neurosci Res., vol. 26, pp. 235-269, 1996.
F. Han, H. Ozawa, K. Matsuda, M. Nishi, M. Kawata, "Colocalization of mineralocorticoid receptor and glucocorticoid receptor in the hippocampus and hypothalamus," Neurosci Res., vol. 51, pp. 371-381, 2005.
S. Makino, T. Kaneda, M. Nishiyama, K. Asaba, K. Hashimoto, "Lack of decrease in hypothalamic and hippocampal glucocorticoid receptor mRNA during starvation," Neuroendocrinol., vol. 74, pp. 120-128, 2001.
R. W. Carthew, E. J. Sontheimer, "Origins and Mechanisms of miRNAs and siRNAs," Cell, vol. 136, pp. 642-655, 2009.
A. Riester, O, Issler, A. Spyroglou, S. H. Rodrig, A. Chen, F. Beuschlein, "ACTH-dependent regulation of microRNA as endogenous modulators of glucocorticoid receptor expression in the adrenal gland," Endocrinol., vol. 153, pp. 212-222, 2012.
C. Ledderose, P. Mohnle, E. Limbeck, S. Schutz, F. Weis, J. Rink, J. Briegel, S. Kreth, "Corticosteroid resistance in sepsis is influenced by microRNA-124--induced downregulation of glucocorticoid receptor-alpha," Critical Care Med., vol. 40, pp. 2745-2753, 2012.
B. E. Levin, A. C. Sullivan, "Glucose-induced sympathetic activation in obesity-prone and resistant rats," Int J Obesity, vol. 13, pp. 235-246, 1989.
T. Nemoto, A. Iwasaki-Sekino, N. Yamauchi, T. Shibasaki, "Role of urocortin 2 secreted by the pituitary in the stress-induced suppression of luteinizing hormone secretion in rats," Am J Physiol Endocrinol Metab., vol. 299, pp. E567-575, 2010.
S. Makino, K. Hashimoto, P. W. Gold, PW "Multiple feedback mechanisms activating corticotropin-releasing hormone system in the brain during stress," Pharmacol Biochem Behav., vol. 73, pp. 147-158, 2002.
R. M. Sapolsky, S. Zola-Morgan, L. R. Squire, "Inhibition of glucocorticoid secretion by the hippocampal formation in the primate," J. Neurosci., vol. 11, pp. 3695-3704, 1991.
L. Jacobson, R. Sapolsky, "The role of the hippocampus in feedback regulation of the hypothalamic-pituitary- adrenocortical axis," Endocrine Reviews, vol. 12, pp. 118-134, 1991.
E. Kitraki, D. Karandrea, C. Kittas, "Long-lasting effects of stress on glucocorticoid receptor gene expression in the rat brain," Neuroendocrinol., vol. 69, pp. 331-338, 1999.
J. P. Herman, M. M. Ostrander, N. K. Mueller, H. Figueiredo, Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis," Prog Neuropsychopharmacol Biol Psychiatry, vol. 29, pp. 1201-1213, 2005.
M. W. Schwartz, D. G. Baskin, T. R. Bukowski, J. L. Kuijper, D. Foster, G. Lasser, D. E. Prunkard, D. Jr., Porte, S. C. Woods, R. J. Seeley, D. S. Weigle, "Specificity of leptin action on elevated blood glucose levels and hypothalamic neuropeptide Y gene expression in ob/ob mice," Diabetes, vol. 45, pp. 531-535, 1996.
B. Beck, R. Kozak, A. Stricker-Krongrad, C. Burlet, "Neuropeptide Y release in the paraventricular nucleus of Long-Evans rats treated with leptin," Biochem Biophys Res Commun, vol. 242, pp. 636-639, 1998.
M. Jang, A. Mistry, A. G. Swick, D. R. Romsos, "Leptin rapidly inhibits hypothalamic neuropeptide Y secretion and stimulates corticotropin-releasing hormone secretion in adrenalectomized mice," J. Nutrition, vol. 130, pp. 2813-2820, 2000.
A. Stricker-Krongrad, F. Cumin, C. Burlet, B. Beck, "Hypothalamic neuropeptide Y and plasma leptin after long-term high-fat feeding in the rat," Neurosci Lett . vol. 254, pp. 157-160, 1998.
A. Stofkova, M. Skurlova, A. Kiss, B. Zelezna, S. Zorad, J. Jurcovicova, "Activation of hypothalamic NPY, AgRP, MC4R, AND IL-6 mRNA levels in young Lewis rats with early-life diet-induced obesity," Endocrine Regulations, vol. 43, pp. 99-106, 2009.
J. P. Herman JP, "Regulation of adrenocorticosteroid receptor mRNA expression in the central nervous system," Cell. Mol. Neurobiol., vol. 13, pp. 349-372, 1993.
N. Tritos, E. Kitraki, H. Philippidis, F. Stylianopoulou, "Neurotransmitter modulation of glucocorticoid receptor mRNA levels in the rat hippocampus," Neuroendocrinol., vol. 69, pp. 324-330, 1999.
S. Okret, L. Poellinger, Y. Dong, J. A. Gustafsson, "Down-regulation of glucocorticoid receptor mRNA by glucocorticoid hormones and recognition by the receptor of a specific binding sequence within a receptor cDNA clone," Proc Natl Acad Sci U S A, vol. 83, pp. 5899-5903, 1986.
Y. Dong, L. Poellinger, J. A. Gustafsson, S. Okret S, "Regulation of glucocorticoid receptor expression: evidence for transcriptional and posttranslational mechanisms," Mol. Endocrinol., vol. 2, pp. 1256-1264, 1988.
W. V. Vedeckis, M. Ali, H. R. Allen, "Regulation of glucocorticoid receptor protein and mRNA levels," Cancer Res, vol. 49, pp. 2295s-2302s, 1989.
J. Li, Y. Tang, D. Cai, "IKKbeta/NF-kappaB disrupts adult hypothalamic neural stem cells to mediate a neurodegenerative mechanism of dietary obesity and pre-diabetes," Nature cell biology, vol. 14, pp. 999-1012, 2012.
Y. Shpilberg, J. L. Beaudry, A. D'Souza, J. E. Campbell, A. Peckett, M. C. Riddell, "A rodent model of rapid-onset diabetes induced by glucocorticoids and high-fat feeding," Disease models & mechanisms, vol. 5, pp. 671-680, 2012.
Science Publishing Group
1 Rockefeller Plaza,
10th and 11th Floors,
New York, NY 10020
Tel: (001)347-983-5186