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Chronobiology International
The Journal of Biological and Medical Rhythm Research
Volume 32, 2015 - Issue 2
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Original Article

Effects of adrenalectomy on daily gene expression rhythms in the rat suprachiasmatic and paraventricular hypothalamic nuclei and in white adipose tissue

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Pages 211-224 | Received 25 Apr 2014, Accepted 04 Sep 2014, Published online: 30 Sep 2014

References

  • Ando H, Yanagihara H, Hayashi Y, et al. (2005). Rhythmic messenger ribonucleic acid expression of clock genes and adipocytokines in mouse isceral adipose tissue. Endocrinology. 146:5631–6
  • Arletti R, Benelli A, Bertolini A. (1990). Oxytocin inhibits food and fluid intake in rats. Physiol Behav. 48:825–30
  • Aronsson M, Fuxe K, Dong Y, et al. (1988). Localization of glucocorticoid receptor mRNA in the male rat brain by in situ hybridization. Proc Natl Acad Sci USA. 85:9331–5
  • Asai M, Yoshinobu Y, Kaneko S, et al. (2001). Circadian profile of Per gene mRNA expression in the suprachiasmatic nucleus, paraventricular nucleus, and pineal body of aged rats. J Neurosci Res. 66:1133–9
  • Balakrishnan A, Stearns AT, Ashley SW, et al. (2010). Restricted feeding phase shifts clock gene and sodium glucose cotransporter 1 (SGLT1) expression in rats. J Nutr. 140:908–14
  • Balsalobre A, Brown SA, Marcacci L, et al. (2000). Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science. 289:2344–7
  • Bates PJ, Sanderson G, Holgate ST, Johnston SL. (1997). A comparison of RT-PCR, in-situ hybridisation and in-situ RT-PCR for the detection of rhinovirus infection in paraffin sections. J Virol Methods. 67:153–60
  • Brun RP, Kim JB, Hu E, Spiegelman BM. (1997). Peroxisome proliferator-activated receptor gamma and the control of adipogenesis. Curr Opin Lipidol. 8:212–18
  • Burbach JP, Liu B, Voorhuis TA, Van Tol HH. (1988). Diurnal variation in vasopressin and oxytocin messenger RNAs in hypothalamic nuclei of the rat. Brain Res. 464:157–60
  • Cai A, Wise PM. (1996). Age-related changes in the diurnal rhythm of CRH gene expression in the paraventricular nuclei. Am J Physiol. 270:E238–43
  • Cailotto C, La Fleur SE, Van Heijningen C, et al. (2005). The suprachiasmatic nucleus controls the daily variation of plasma glucose via the autonomic output to the liver: Are the clock genes involved? Eur J Neurosci. 22:2531–40
  • Cailotto C, van Heijningen C, van der Vliet J, et al. (2008). Daily rhythms in metabolic liver enzymes and plasma glucose require a balance in the autonomic output to the liver. Endocrinology. 149:1914–25
  • Calvani M, Scarfone A, Granato L, et al. (2004). Restoration of adiponectin pulsatility in severely obese subjects after weight loss. Diabetes. 53:939–47
  • Campbell JE, Peckett AJ, D'souza AM, et al. (2011). Adipogenic and lipolytic effects of chronic glucocorticoid exposure. Am J Physiol Cell Physiol. 300:C198–209
  • Caprio M, Fève B, Claës A, et al. (2007). Pivotal role of the mineralocorticoid receptor in corticosteroid-induced adipogenesis. FASEB J. 21:2185–94
  • Chen SF, Zhu XT, Shu G, et al. (2007). PPARgamma and C/EBPalpha mRNA expression in the primary culture of rat preadipocytes during differentiation. Fen Zi Xi Bao Sheng Wu Xue Bao. 40:272–5
  • Christ-Crain M, Kola B, Lolli F, et al. (2008). AMP-activated protein kinase mediates glucocorticoid-induced metabolic changes: A novel mechanism in Cushing's syndrome. FASEB J. 22:1672–83
  • Cintra A, Bhatnagar M, Chadi G, et al. (1994a). Glial and neuronal glucocorticoid receptor immunoreactive cell populations in developing, adult, and aging brain. Ann NY Acad Sci. 746:42–61
  • Cintra A, Zoli M, Rosen L, et al. (1994b). Mapping and computer assisted morphometry and microdensitometry of glucocorticoid receptor immunoreactive neurons and glial cells in the rat central nervous system. Neuroscience. 62:843–97
  • De Vos P, Lefebvre AM, Shrivo I, et al. (1998). Glucocorticoids induce the expression of the leptin gene through a non-classical mechanism of transcriptional activation. Eur J Biochem. 253:619–26
  • Dzirbíková Z, Kiss A, Okuliarová M, et al. (2011). Expressions of per1 clock gene and genes of signaling peptides vasopressin, vasoactive intestinal peptide, and oxytocin in the suprachiasmatic and paraventricular nuclei of hypertensive TGR[mREN2]27 rats. Cell Mol Neurobiol. 31:225–32
  • Ferrini MG, Grillo CA, Piroli G, et al. (1997). Sex difference in glucocorticoid regulation of vasopressin mRNA in the paraventricular hypothalamic nucleus. Cell Mol Neurobiol. 17:671–86
  • Fujihara Y, Kondo H, Noguchi T, Togari A. (2014). Glucocorticoids mediate circadian timing in peripheral osteoclasts resulting in the circadian expression rhythm of osteoclast-related genes. Bone. 61:1–9
  • García-Bueno B, Madrigal JL, Pérez-Nievas BG, Leza JC. (2008). Stress mediators regulate brain prostaglandin synthesis and peroxisome proliferator-activated receptor-gamma activation after stress in rats. Endocrinology. 149:1969–78
  • Gilhooley MJ, Pinnock SB, Herbert J. (2011). Rhythmic expression of per1 in the dentate gyrus is suppressed by corticosterone: Implications for neurogenesis. Neurosci Lett. 489:177–81
  • Girotti M, Weinberg MS, Spencer RL. (2009). Diurnal expression of functional and clock-related genes throughout the rat HPA axis: System-wide shifts in response to a restricted feeding schedule. Am J Physiol Endocrinol Metab. 296:E888–97
  • Goto T, Lee JY, Teraminami A, et al. (2011). Activation of peroxisome proliferator-activated receptor-alpha stimulates both differentiation and fatty acid oxidation in adipocytes. J Lipid Res. 52:873–84
  • Gozes I, Avidor R, Giladi E, et al. (1994). Adrenalectomy decreases vasoactive intestinal peptide mRNA levels in the rat suprachiasmatic nucleus. Neurosci Lett. 167:24–8
  • Guillaumond F, Dardente H, Giguère V, Cermakian N. (2005). Differential control of Bmal1 circadian transcription by REV-ERB and ROR nuclear receptors. J Biol Rhythms. 20:391–403
  • Han F, Ozawa H, Matsuda KI, et al. (2007). Changes in the expression of corticotrophin-releasing hormone, mineralocorticoid receptor and glucocorticoid receptor mRNAs in the hypothalamic paraventricular nucleus induced by fornix transection and adrenalectomy. J Neuroendocrinol. 19:229–38
  • Härfstrand A, Fuxe K, Cintra A, et al. (1986). Glucocorticoid receptor immunoreactivity in monoaminergic neurons of rat brain. Proc Natl Acad Sci USA. 83:9779–83
  • Herman JP, Watson SJ, Chao HM, et al. (1987). Diurnal regulation of glucocorticoid receptor and mineralocorticoid receptor mRNAs in rat hippocampus. Neuroendocrinology. 45:407–12
  • Hermes ML, Ruijter JM, Klop A, et al. (2000). Vasopressin increases GABAergic inhibition of rat hypothalamic paraventricular nucleus neurons in vitro. J Neurophy. 83:705–11
  • Holmes MC, Yau JL, French KL, Seckl JR. (1995). The effect of adrenalectomy on 5-hydroxytryptamine and corticosteroid receptor subtype messenger RNA expression in rat hippocampus. Neuroscience. 64:327–37
  • Isobe Y, Isobe M. (1998). Circadian rhythm of Arg-vasopressin contents in the suprachiasmatic nucleus in relation to corticosterone. Brain Res. 800:78–85
  • Isobe Y, Torii T, Kawaguchi T, Nishino H. (2004). Dexamethasone induces different wheel running activity than corticosterone through vasopressin release from the suprachiasmatic nucleus. Brain Res. 1028:219–24
  • Itoi K, Mouri T, Takahashi K, et al. (1987). Suppression by glucocorticoid of the immunoreactivity of corticotropin-releasing factor and vasopressin in the paraventricular nucleus of rat hypothalamus. Neurosci Lett. 73:231–6
  • Kalsbeek A, Buijs RM, Engelmann M, et al. (1995). In vivo measurement of a diurnal variation in vasopressin release in the rat suprachiasmatic nucleus. Brain Res. 682:75–82
  • Kalsbeek A, Palm IF, La Fleur SE, et al. (2006). SCN outputs and the hypothalamic balance of life. J Biol Rhythms. 21:458–69
  • Kalsbeek A, Verhagen LA, Schalij I, et al. (2008). Opposite actions of hypothalamic vasopressin on circadian corticosterone rhythm in nocturnal versus diurnal species. Eur J Neurosci. 27:818–27
  • Kasting NW. (1988). Simultaneous and independent release of vasopressin and oxytocin in the rat. Can J Physiol Pharmacol. 66:22–6
  • Kim HE, Bae E, Jeong DY, et al. (2013). Lipin1 regulates PPARγ transcriptional activity. Biochem J. 453:49–60
  • Kiss JZ, Mezey E, Skirboll L. (1984). Corticotropin-releasing factor-immunoreactive neurons of the paraventricular nucleus become vasopressin positive after adrenalectomy. Proc Natl Acad Sci USA. 81:1854–8
  • Kobayashi H, Oishi K, Hanai S, Ishida N. (2004). Effect of feeding on peripheral circadian rhythms and behaviour in mammals. Genes Cells. 9:857–64
  • Koh YK, Lee MY, Kim JW, et al. (2008). Lipin1 is a key factor for the maturation and maintenance of adipocytes in the regulatory network with CCAAT/enhancer-binding protein alpha and peroxisome proliferator-activated receptor gamma 2. J Biol Chem. 283:34896–906
  • Lamia KA, Sachdeva UM, DiTacchio L, et al. (2009). AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation. Science. 326:437–40
  • Larsen PJ, Vrang N, Møller M, et al. (1994). The diurnal expression of genes encoding vasopressin and vasoactive intestinal peptide within the rat suprachiasmatic nucleus is influenced by circulating glucocorticoids. Brain Res Mol Brain Res. 27:342–6
  • Lemberger T, Staels B, Saladin R, et al. (1994). Regulation of the peroxisome proliferator-activated receptor alpha gene by glucocorticoids. J Biol Chem. 269:24527–30
  • Ma XM, Camacho C, Aguilera G. (2001). Regulation of corticotropin-releasing hormone (CRH) transcription and CRH mRNA stability by glucocorticoids. Cell Mol Neurobiol. 21:465–75
  • Meyer J. (1985). Biochemical effects of corticosteroids on neural tissues. Physiol Rev. 65:946–1020
  • Minokoshi Y, Kim YB, Peroni OD, et al. (2002). Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature. 415:339–43
  • Mohr E, Schmitz E. (1991). Functional characterization of estrogen and glucocorticoid responsive elements in the rat oxytocin gene. Brain Res Mol Brain Res. 9:293–8
  • Morimoto M, Morita N, Ozawa H, et al. (1996). Distribution of glucocorticoid receptor immunoreactivity and mRNA in the rat brain: An immunohistochemical and in situ hybridization study. Neurosci Res. 26:235–69
  • Nishioka T, Anselmo-Franci JA, Li P, et al. (1998). Stress increases oxytocin release within the hypothalamic paraventricular nucleus. Brain Res. 781:56–60
  • Noguchi T, Makino S, Matsumoto R, et al. (2010). Regulation of glucocorticoid receptor transcription and nuclear translocation during single and repeated immobilization stress. Endocrinology. 151:4344–55
  • Oishi K, Amagai N, Shirai H, et al. (2005). Genome-wide expression analysis reveals 100 adrenal gland-dependent circadian genes in the mouse liver. DNA Res. 12:191–202
  • Oishi K, Sakamoto K, Okada T, et al. (1998a). Humoral signals mediate the circadian expression of rat period homologue (rPer2) mRNA in peripheral tissues. Neurosci Lett. 256:117–119
  • Oishi K, Sakamoto K, Okada T, et al. (1998b). Antiphase circadian expression between BMAL1 and period homologue mRNA in the suprachiasmatic nucleus and peripheral tissues of rats. Biochem Biophys Res Commun. 1998;253:199–203
  • Okamura H, Yamaguchi S, Yagita K. (2002). Molecular machinery of the circadian clock in mammals. Cell Tissue Res. 309:47–56
  • Oster H, Damerow S, Hut RA, Eichele G. (2006). Transcriptional profiling in the adrenal gland reveals circadian regulation of hormone biosynthesis genes and nucleosome assembly genes. J Biol Rhythms. 21:350–61
  • Piroli GG, Grillo CA, Reznikov LR, et al. (2007). Corticosterone impairs insulin-stimulated translocation of GLUT4 in the rat hippocampus. Neuroendocrinology. 85:71–80
  • Portaluppi F, Smolensky MH, Touitou Y. (2010). Ethics and methods for biological rhythm research on animals and human beings. Chronobiol Int. 27:1911–29
  • Ralph MR, Foster RG, Davis FC, Menaker M. (1990). Transplanted suprachiasmatic nucleus determines circadian period. Science. 247:975–8
  • Rosenfeld P, Van Eekelen JA, Levine S, De Kloet ER. (1988). Ontogeny of the type 2 glucocorticoid receptor in discrete rat brain regions: An immunocytochemical study. Brain Res. 470:119–27
  • Saad MF, Riad-Gabriel MG, Khan A, et al. (1998). Diurnal and ultradian rhythmicity of plasma leptin: Effects of gender and adiposity. J Clin Endocrinol Metab. 83:453–9
  • Sage D, Ganem J, Guillaumond F, et al. (2004). Influence of the corticosterone rhythm on photic entrainment of locomotor activity in rats. J Biol Rhythms. 19:144–56
  • Sakoda H, Ogihara T, Anai M, et al. (2000). Dexamethasone-induced insulin resistance in 3T3-L1 adipocytes is due to inhibition of glucose transport rather than insulin signal transduction. Diabetes. 49:1700–8
  • Salgado-Delgado RC, Saderi N, Mdel BC, et al. (2013). Shift work or food intake during the rest phase promotes metabolic disruption and desynchrony of liver genes in male rats. PLoS One. 8:e60052
  • Segall LA, Perrin JS, Walker CD, et al. (2006). Glucocorticoid rhythms control the rhythm of expression of the clock protein, Period2, in oval nucleus of the bed nucleus of the stria terminalis and central nucleus of the amygdala in rats. Neuroscience. 140:753–7
  • Slavin BG, Ong JM, Kern PA. (1994). Hormonal regulation of hormone-sensitive lipase activity and mRNA levels in isolated rat adipocytes. J Lipid Res. 35:1535–41
  • Sousa RJ, Tannery NH, Lafer EM. (1989). In situ hybridization mapping of glucocorticoid receptor messenger ribonucleic acid in rat brain. Mol Endocrinol. 3:481–94
  • Stokkan KA, Yamazaki S, Tei H, et al. (2001). Entrainment of the circadian clock in the liver by feeding. Science. 291:490–3
  • Sujino M, Furukawa K, Koinuma S, et al. (2012). Differential entrainment of peripheral clocks in the rat by glucocorticoid and feeding. Endocrinology. 153:2277–6
  • Surjit M, Ganti KP, Mukherji A, et al. (2011). Widespread negative response elements mediate direct repression by agonist-liganded glucocorticoid receptor. Cell. 145:224–41
  • Sutanto W, van Eekelen JA, Reul JM, de Kloet ER. (1988). Species-specific topography of corticosteroid receptor types in rat and hamster brain. Neuroendocrinology. 47:398–404
  • Svec F, Gordon S, Tate D. (1989). Glucocorticoid receptor regulation: The effects of adrenalectomy, exogenous glucocorticoid, and stress on hepatic receptor number in male and female mice. Biochem Med Metab Biol. 41:224–33
  • Swanson LW, Kuypers HG. (1980). The paraventricular nucleus of the hypothalamus: Cytoarchitectonic subdivisions and organization of projections to the pituitary, dorsal vagal complex, and spinal cord as demonstrated by retrograde fluorescence double-labeling methods. J Comp Neurol. 194:555–70
  • Swanson LW, Simmons DM. (1989). Differential steroid hormone and neural influences on peptide mRNA levels in CRH cells of the paraventricular nucleus: A hybridization histochemical study in the rat. J Comp Neurol. 285:413–35
  • Torra IP, Tsibulsky V, Delaunay F, et al. (2000). Circadian and glucocorticoid regulation of Rev-erbalpha expression in liver. Endocrinology. 141:3799–806
  • Wakil SJ, Abu-Elheiga LA. (2009). Fatty acid metabolism: Target for metabolic syndrome. J Lipid Res. 50:S138–43
  • Womac AD, Burkeen JF, Neuendorff N, et al. (2009). Circadian rhythms of extracellular ATP accumulation in suprachiasmatic nucleus cells and cultured astrocytes. Eur J Neurosci. 30:869–76
  • Wotjak CT, Naruo T, Muraoka S, et al. (2001). Forced swimming stimulates the expression of vasopressin and oxytocin in magnocellular neurons of the rat hypothalamic paraventricular nucleus. Eur J Neurosci. 13:2273–81
  • Wuarin J, Schibler U. (1990). Expression of the liver-enriched transcriptional activator protein DBP follows a stringent circadian rhythm. Cell. 63:1257–66
  • Xu C, He J, Jiang H, et al. (2009). Direct effect of glucocorticoids on lipolysis in adipocytes. Mol Endocrinol. 23:1161–70
  • Yamamoto T, Nakahata Y, Tanaka M, et al. (2005). Acute physical stress elevates mouse period1 mRNA expression in mouse peripheral tissues via a glucocorticoid-responsive element. J Biol Chem. 280:42036–43
  • Yamauchi T, Kamon J, Minokoshi Y, et al. (2002). Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med. 8:1288–95
  • Yamazaki S, Numano R, Abe M, et al. (2000). Resetting central and peripheral circadian oscillators in transgenic rats. Science. 288:682–5
  • Yambe Y, Arima H, Kakiya S, et al. (2002). Diurnal changes in arginine vasopressin gene transcription in the rat suprachiasmatic nucleus. Brain Res Mol Brain Res. 104:132–6
  • Yi SJ, Masters JN, Baram TZ. (1994). Glucocorticoid receptor mRNA ontogeny in the fetal and postnatal rat forebrain. Mol Cell Neurosci. 5:385–93
  • Yoo SH, Yamazaki S, Lowrey PL, et al. (2004). PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci USA. 101:5339–46
  • Young WS 3rd, Mezey E, Siegel RE. (1986). Quantitative in situ hybridization histochemistry reveals increased levels of corticotropin-releasing factor mRNA after adrenalectomy in rats. Neurosci Lett. 70:198–203
  • Zhang P, O'Loughlin L, Brindley DN, Reue K. (2008). Regulation of lipin-1 gene expression by glucocorticoids during adipogenesis. J Lipid Res. 49:1519–28
  • Zhou YT, Wang ZW, Higa M, et al. (1999). Reversing adipocyte differentiation: Implications for treatment of obesity. Proc Natl Acad Sci USA. 96:2391–5

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