Differential Involvement of the Suprachiasmatic Nucleus in Lipopolysaccharide-Induced Plasma Glucose and Corticosterone Responses

REFERENCES

• Beynon AL, Coogan AN. (2010). Diurnal, age, and immune regulation of interleukin-1β and interleukin-1 type 1 receptor in the mouse suprachiasmatic nucleus. Chronobiol. Int. 27:1546–1563.
   PubMed Web of Science ®Google Scholar
• Bloesch D, Keller U, Spinas GA, Kury D, Girard J, Stauffacher W. (1993). Effects of endotoxin on leucine and glucose kinetics in man: contribution of prostaglandin E2 assessed by a cyclooxygenase inhibitor. J. Clin. Endocrinol.Metab. 77:1156–1163.
   PubMedGoogle Scholar
• Boggio VI, Castrillon PO, Perez Lloret S, Riccio P, Esquifino AI, Cardinali DP, Cutrera RA. (2003). Cerebroventricular administration of interferon-gamma modifies locomotor activity in the golden hamster. Neurosignals 12:89–94.
   PubMedGoogle Scholar
• Born J, Lange T, Hansen K, Molle M, Fehm HL. (1997). Effects of sleep and circadian rhythm on human circulating immune cells. J. Immunology 158:4454–4464.
   PubMed Web of Science ®Google Scholar
• Buijs RM, Wortel J, Van Heerikhuize JJ, Kalsbeek A. (1997). Novel environment induced inhibition of corticosterone secretion: physiological evidence for a suprachiasmatic nucleus mediated neuronal hypothalamo-adrenal cortex pathway. Brain Res. 758:229–236.
   PubMed Web of Science ®Google Scholar
• Buijs RM, van der Vliet J, Garidou ML, Huitinga I, Escobar C. (2008). Spleen vagal denervation inhibits the production of antibodies to circulating antigens. PLoS ONE 3:e3152.
   PubMed Web of Science ®Google Scholar
• Cailotto C, La Fleur SE, Van Heijningen C, Wortel J, Kalsbeek A, Feenstra M, Pévet P, Buijs RM. (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. 22:2531–2540.
   PubMed Web of Science ®Google Scholar
• Cavadini G, Petrzilka S, Kohler P, Jud C, Tobler I, Birchler T, Fontana A. (2007). TNF-a suppresses the expression of clock genes by interfering with E-box-mediated transcription. Proc. Natl. Acad. Sci. U. S. A. 104:12843–12848.
   PubMed Web of Science ®Google Scholar
• Cearley C, Churchill L, Krueger JM. (2003). Time of day differences in IL1b and TNFa mRNA levels in specific regions of the rat brain. Neurosci. Lett. 352:61–63.
   PubMedGoogle Scholar
• Coogan AN, Wyse CA. (2008). Neuroimmunology of the circadian clock. Brain Res. 1232:104–112.
   PubMed Web of Science ®Google Scholar
• Cornell RP, Schwartz DB. (1989). Central administration of interleukin 1 elicits hyperinsulinemia in rats. Am. J. Physiol. 256:R772–R777.
   Google Scholar
• Del Rey A, Roggero E, Randolf A, Mahuad C, McCann S, Rettori V, Besedovsky HO. (2006). IL-1 resets glucose homeostasis at central levels. Proc. Natl. Acad. Sci. U. S. A. 103:16039–16044.
   PubMed Web of Science ®Google Scholar
• Dickmeis T. (2009). Glucocorticoids and the circadian clock. J. Endocrinol. 200:3–22.
   PubMed Web of Science ®Google Scholar
• Drijfhout WJ, Kemper RHA, Meerlo P, Koolhaas JM, Grol CJ, Westerink BHC. (1995). A telemetry study on the chronic effects of microdialysis probe implantation on the activity pattern and temperature rhythm of the rat. J. Neurosci. Methods 61:191–196.
   PubMed Web of Science ®Google Scholar
• Du YZ, Fan SJ, Meng QH, Wang GQ, Tong J. (2005). Circadian expression of clock and screening of clock-controlled genes in peripheral lymphocytes of rat. Biochem. Biophys. Res. Commun. 336:1069–1073.
   PubMedGoogle Scholar
• Fu L, Lee CC. (2003). The circadian clock: pacemaker and tumour suppressor. Nat. Rev. Cancer 3:350–361.
   PubMed Web of Science ®Google Scholar
• Gautron L, Mingam R, Moranis A, Combe C, Laye S. (2005). Influence of feeding status on neuronal activity in the hypothalamus during lipopolysaccharide-induced anorexia in rats. Neuroscience 134:933–946.
   PubMed Web of Science ®Google Scholar
• Gaykema RP, Chen CC, Goehler LE. (2007). Organization of immune-responsive medullary projections to the bed nucleus of the stria terminalis, central amygdala, and paraventricular nucleus of the hypothalamus: evidence for parallel viscerosensory pathways in the rat brain. Brain Res. 1130:130–145.
   PubMed Web of Science ®Google Scholar
• Giovambattista A, Chisari AN, Corro L, Gaillard RC, Spinedi E. (2000). Metabolic, neuroendocrine and immune functions in basal conditions and during the acute-phase response to endotoxic shock in undernourished rats. Neuroimmunomodulation 7:92–98.
   PubMedGoogle Scholar
• Givalois L, Becq H, Siaud P, Ixart G, Assenmacher I, Barbanel G. (1999). Serotonergic and suprachiasmatic nucleus involvement in the corticotropic response to systemic endotoxin challenge in rats. J. Neuroendocrinol. 11:629–636.
   PubMedGoogle Scholar
• Guo AL, Petraglia F, Criscuolo M, Ficarra G, Nappi RE, Palumbo M, Valentini A, Genazzani AR. (1994). Acute stress- or lipopolysaccharide-induced corticosterone secretion in female rats is independent of the oestrous cycle. Eur. J. Endocrinol. 131:535–539.
   PubMedGoogle Scholar
• Guo AL, Petraglia F, Nappi RE, Criscuolo M, Ficarra G, Salvestroni C, Genazzani AD, Trentini GP, Genazzani AR. (1996). Bicuculline enhances the corticosterone secretion induced by lipopolysaccharide and interleukin-1a in male rats. J. Endocrinol. Invest. 19:83–87.
   PubMedGoogle Scholar
• Habbal OA, Al-Jabri AA. (2009). Circadian rhythm and the immune response: a review. Int. Rev. Immunol. 28:93–108.
   PubMed Web of Science ®Google Scholar
• Halberg F, Johnson EA, Brown BW, Bittner JJ. (1960). Susceptibility rhythm to E. coli endotoxin and bioassay. Proc. Soc. Exp. Biol. Med. 103:142–144.
   PubMed Web of Science ®Google Scholar
• Hermann C, von Aulock S, Dehus O, Keller M, Okigami H, Gantner F, Wendel A, Hartung T. (2006). Endogenous cortisol determines the circadian rhythm of lipopolysaccharide- but not lipoteichoic acid–inducible cytokine release. Eur. J. Immunol. 36:371–379.
   PubMedGoogle Scholar
• Jortay J, Senou M, Delaigle A, Noel L, Funahashi T, Maeda N, Many MC, Brichard SM. (2010). Local induction of adiponectin reduces lipopolysaccharide-triggered skeletal muscle damage. Endocrinology 151:4840–4851.
   PubMedGoogle Scholar
• Kalsbeek A, Buijs RM. (1996). Rhythms of inhibitory and excitatory output from the circadian timing system as revealed by in vivo microdialysis. In Buijs RM, Kalsbeek A, Romijn HJ, Pennartz CMA, Mirmiran M(eds.). Progress in brain research, Vol. 111, Hypothalamic integration of circadian rhythms, Amsterdam: Elsevier Science, 271–291.
   Google Scholar
• Kalsbeek A, Fliers E, Romijn JA, La Fleur SE, Wortel J, Bakker O, Endert E, Buijs RM. (2001). The suprachiasmatic nucleus generates the diurnal changes in plasma leptin levels. Endocrinology 142:2677–2685.
   PubMed Web of Science ®Google Scholar
• Kalsbeek A, Ruiter M, La Fleur SE, Van Heijningen C, Buijs RM. (2003). The diurnal modulation of hormonal responses in the rat varies with different stimuli. J. Neuroendocrinol. 15:1144–1155.
   PubMed Web of Science ®Google Scholar
• Kalsbeek A, La Fleur SE, Van Heijningen C, Buijs RM. (2004). Suprachiasmatic GABAergic inputs to the paraventricular nucleus control plasma glucose concentrations in the rat via sympathetic innervation of the liver. J. Neurosci. 24:7604–7613.
   PubMed Web of Science ®Google Scholar
• Kalsbeek A, Yi CX, La Fleur SE, Fliers E. (2010). The hypothalamic clock and its control of glucose homeostasis. Trends Endocrinol. Metab. 21:402–410.
   PubMed Web of Science ®Google Scholar
• Kant GJ, Mougey EH, Meyerhoff JL. (1986). Diurnal variation in neuroendocrine response to stress in rats: plasma ACTH, β-endorphin, β-LPH, corticosterone, prolactin and pituitary cyclic AMP responses. Neuroendocrinology 43:383–390.
   PubMed Web of Science ®Google Scholar
• Kelleher DL, Fong BC, Bagby GJ, Spitzer JJ. (1982). Metabolic and hormonal changes following endotoxin administration to diabetic rats. Am. J. Physiol. 243:R77–R81.
   Google Scholar
• Koyanagi S, Ohdo S. (2002). Alteration of intrinsic biological rhythms during interferon treatment and its possible mechanism. Mol. Pharmacol. 62:1393–1399.
   PubMed Web of Science ®Google Scholar
• La Fleur SE, Kalsbeek A, Wortel J, Fekkes ML, Buijs RM. (2001). A daily rhythm in glucose tolerance. A role for the suprachiasmatic nucleus. Diabetes 50:1237–1243.
   PubMed Web of Science ®Google Scholar
• Lang CH. (1995). Neural regulation of the enhanced uptake of glucose in skeletal muscle after endotoxin. Am. J. Physiol. 269:R437–R444.
   Google Scholar
• Lang CH, Molina PE, Yousef KA, Tepper PG, Abumrad NN. (1993). Role of IL-1α in central nervous system immunomodulation of glucoregulation. Brain Res. 624:53–60.
   PubMedGoogle Scholar
• Lang CH, Cooney R, Vary TC. (1996). Central interleukin-1 partially mediates endotoxin-induced changes in glucose metabolism. Am. J. Physiol. 271:E309–E316.
   Google Scholar
• Lange T, Dimitrov S, Born J. (2010). Effects of sleep and circadian rhythm on the human immune system. Ann. N. Y. Acad. Sci. 1193:48–59.
   PubMed Web of Science ®Google Scholar
• Leone MJ, Marpegan L, Bekinschtein TA, Costas MA, Golombek DA. (2006). Suprachiasmatic astrocytes as an interface for immune-circadian signalling. J. Neurosci. Res. 84:1521–1527.
   PubMed Web of Science ®Google Scholar
• Lundkvist GB, Robertson B, Mhlanga JDM, Rottenberg ME, Kristensson K. (1998). Expression of an oscillating interferon-t receptor in the suprachiasmatic nuclei. Neuroreport 9:1059–1063.
   PubMed Web of Science ®Google Scholar
• Lundkvist GB, Hill RH, Kristensson K. (2002). Disruption of circadian rhythms in synaptic activity of the suprachiasmatic nuclei by African trypanosomes and cytokines. Neurobiol. Dis. 11:20–27.
   PubMedGoogle Scholar
• Maitra SR, Gestring ML, El-Maghrabi MR, Lang CH, Henry MC. (1999). Endotoxin-induced alterations in hepatic glucose-6-phosphatase activity and gene expression. Mol. Cell. Biochem. 196:79–83.
   PubMedGoogle Scholar
• Marpegan L, Bekinschtein TA, Costas MA, Golombek DA. (2005). Circadian responses to endotoxin treatment in mice. J. Neuroimmunol. 160:102–109.
   PubMed Web of Science ®Google Scholar
• Marpegan L, Leone MJ, Katz ME, Sobrero PM, Bekinstein TA, Golombek DA. (2009). Diurnal variation in endotoxin-induced mortality in mice: correlation with proinflammatory factors. Chronobiol. Int. 26:1430–1442.
   PubMed Web of Science ®Google Scholar
• Mathias S, Schiffelholz T, Linthorst ACE, Pollmacher T, Lancel M. (2000). Diurnal variations in lipopolysaccharide-induced sleep, sickness behavior and changes in corticosterone levels in the rat. Neuroendocrinology 71:375–385.
   PubMed Web of Science ®Google Scholar
• Mazzoccoli G, Sothern RB, Greco A, Pazienza V, Vinciguerra M, Liu S, Cai Y. (2011). Time-related dynamics of variation in core clock gene expression levels in tissues relevant to the immune system. Int. J. Immunopathol. Pharmacol. 24:869–879.
   PubMed Web of Science ®Google Scholar
• Morrow JD, Opp MR. (2005). Diurnal variation of lipopolysaccharide-induced alterations in sleep and body temperature of interleukin-6-deficient mice. Brain Behav. Immun. 19:40–51.
   PubMed Web of Science ®Google Scholar
• Nava F, Carta G, Haynes LW. (2000). Lipopolysaccharide increases arginine-vasopressin release from rat suprachiasmatic nucleus slice cultures. Neurosci. Lett. 288:228–230.
   PubMedGoogle Scholar
• Oguri S, Motegi K, Iwakura Y, Endo Y. (2002). Primary role of interleukin-1 alpha and interleukin-1 beta in lipopolysaccharide-induced hypoglycemia in mice. Clin. Diagn. Lab. Immunol. 9:1307–1312.
   PubMedGoogle Scholar
• Ohdo S, Koyanagi S, Suyama H, Higuchi S, Aramaki H. (2001). Changing the dosing schedule minimizes the disruptive effects of interferon on clock function. Nat. Med. 7:356–360.
   PubMed Web of Science ®Google Scholar
• Okada K, Yano M, Doki Y, Azama T, Iwanaga H, Miki H, Nakayama M, Miyata H, Takiguchi S, Fujiwara Y, Yasuda T, Ishida N, Monden M. (2008). Injection of LPS causes transient suppression of biological clock genes in rats. J. Surg. Res. 145:5–12.
   PubMed Web of Science ®Google Scholar
• Ota K, Wildmann J, Ota T, Besedovsky HO, Del Rey A. (2009). Interleukin-1beta and insulin elicit different neuroendocrine responses to hypoglycemia. Ann. N. Y. Acad. Sci. 1153:82–88.
   PubMedGoogle Scholar
• Ottlakan A, Spolarics Z, Lang CH, Spitzer JJ. (1993). Adrenergic blockade attenuates endotoxin-induced hepatic glucose uptake. Circ. Shock 39:74–79.
   PubMedGoogle Scholar
• Pacak K, Palkovits M, Yadid G, Kvetnansky R, Kopin IJ, Goldstein DS. (1998). Heterogeneous neurochemical responses to different stressors: a test of Selye's doctrine of nonspecificity. Am. J. Physiol. 275:R1247–R1255.
   PubMed Web of Science ®Google Scholar
• Paladino N, Leone MJ, Plano SA, Golombek DA. (2010). Paying the circadian toll: the circadian response to LPS injection is dependent on the Toll-like receptor 4. J. Neuroimmunol. 225:62–67.
   PubMedGoogle Scholar
• Palomba M, Bentivoglio M. (2008). Chronic inflammation affects the photic response of the suprachiasmatic nucleus. J. Neuroimmunol. 193:24–27.
   PubMed Web of Science ®Google Scholar
• Penicaud L, Le Magnen J. (1980). Aspects of the neuroendocrine bases of the diurnal metabolic cycle in rats. Neurosci. Biobehav. Rev. 4:S39–S42.
   PubMed Web of Science ®Google Scholar
• Perreau-Lenz S, Kalsbeek A, Garidou ML, Wortel J, Van Der Vliet J, Van Heijningen C, Simonneaux V, Pévet P, Buijs RM. (2003). Suprachiasmatic control of melatonin synthesis in rats: inhibitory and stimulatory mechanisms. Eur. J. Neurosci. 17:221–228.
   PubMed Web of Science ®Google Scholar
• Portaluppi F, Smolensky MH, Touitou Y. (2010). Ethics and methods for biological rhythm research on animals and human beings. Chronobiol. Int. 27:1911–1929.
   PubMed Web of Science ®Google Scholar
• Raetzsch CF, Brooks NL, Alderman JM, Moore KS, Hosick PA, Klebanov S, Akira S, Bear JE, Baldwin AS, Mackman N, Combs TP. (2009). Lipopolysaccharide inhibition of glucose production through the Toll-like receptor-4, myeloid differentiation factor 88, and nuclear factor kappa B pathway. Hepatology 50:592–600.
   PubMedGoogle Scholar
• Sadki A, Bentivoglio M, Kristensson K, Nygard M. (2007). Suppressors, receptors and effects of cytokines on the aging mouse biological clock. Neurobiol. Aging 28:296–305.
   PubMedGoogle Scholar
• Seggie JA, Brown GM. (1975). Stress response patterns of plasma corticosterone, prolactin, and growth hormone in the rat, following handling or exposure to novel environment. Can. J. Physiol. Pharmacol. 53:629–637.
   PubMed Web of Science ®Google Scholar
• Singh AK, Jiang Y. (2004). How does peripheral lipopolysaccharide induce gene expression in the brain of rats? Toxicology 201:197–207.
   PubMed Web of Science ®Google Scholar
• Steffens AB. (1969). A method for frequent sampling blood and continuous infusion of fluids in the rat without disturbing the animal. Physiol. Behav. 4:833–836.
   Web of Science ®Google Scholar
• Sugimoto N, Shido O, Sakurada S, Nagasaka T. (1996). Day-night variations of behavioral and autonomic thermoregulatory responses to lipopolysaccharide in rats. Japn. J. Physiol. 46:451–456.
   PubMedGoogle Scholar
• Suzuki S, Toyabe S, Moroda T, Tada T, Tsukahara A, Iiai T, Minagawa M, Maruyama S, Hatakeyama K, Endoh K, Abo T. (1997). Circadian rhythm of leucocytes and lymphocyte subsets and its possible correlation with the function of the autonomic nervous system. Clin. Exp. Immunol. 110:500–508.
   PubMed Web of Science ®Google Scholar
• Takahashi S, Yokota S, Hara R, Kobayashi T, Akiyama M, Moriya T, Shibata S. (2001). Physical and inflammatory stressors elevate circadian clock gene mPer1 mRNA levels in the paraventricular nucleus of the mouse. Endocrinology 142:4910–4917.
   PubMed Web of Science ®Google Scholar
• Takebe K, Setaishi C, Hirama M, Yamamoto M, Horiuchi Y. (1966). Effects of a bacterial pyrogen on the pituitary-adrenal axis at various times in the 24 hours. J. Clin. Endocrinol. Metab. 26:437–442.
   PubMedGoogle Scholar
• Tsuchiya Y, Minami I, Kadotani H, Nishida E. (2005). Resetting of peripheral circadian clock by prostaglandin E2. EMBO Rep. 6:256–261.
   PubMed Web of Science ®Google Scholar
• Tweedell A, Mulligan KX, Martel JE, Chueh FY, Santomango T, McGuinness OP. (2011). Metabolic response to endotoxin in vivo in the conscious mouse: role of interleukin-6. Metabolism 60:92–98.
   PubMedGoogle Scholar
• Van der Crabben SN, Blumer RM, Stegenga ME, Ackermans MT, Endert E, Tanck MW, Serlie MJ, van der Poll T, Sauerwein HP. (2009). Early endotoxemia increases peripheral and hepatic insulin sensitivity in healthy humans. J. Clin. Endocrinol. Metab. 94:463–468.
   PubMed Web of Science ®Google Scholar
• Vives-Pi M, Somoza N, Fernandez-Alvarez J, Vargas F, Caro P, Alba A, Gomis R, Labeta MO, Pujol-Borrell R. (2003). Evidence of expression of endotoxin receptors CD14, toll-like receptors TLR4 and TLR2 and associated molecule MD-2 and of sensitivity to endotoxin (LPS) in islet beta cells. Clin. Exp. Immunol. 133:208–218.
   PubMed Web of Science ®Google Scholar
• Wachulec M, Li H, Tanaka H, Peloso E, Satinoff E. (1997). Suprachiasmatic nuclei lesions do not eliminate homeostatic thermoregulatory responses in rats. J. Biol. Rhythms 12:226–234.
   PubMed Web of Science ®Google Scholar
• Wallington J, Ning J, Titheradge MA. (2008). The control of hepatic glycogen metabolism in an in vitro model of sepsis. Mol. Cell. Biochem. 308:183–192.
   PubMedGoogle Scholar
• Yamamoto H, Nagai K, Nakagawa H. (1984). Bilateral lesions of the suprachiasmatic nucleus enhance glucose tolerance in rats. Biomed. Res. 5:47–54.
   Google Scholar
• Yamamura Y, Yano I, Kudo T, Shibata S. (2010). Time-dependent inhibitory effect of liposaccharide injection on PER1 and PER2 gene expression in the mouse heart and liver. Chronobiol. Int. 27:213–232.
   PubMed Web of Science ®Google Scholar
• Yi CX, Serlie MJ, Ackermans MT, Foppen E, Buijs RM, Sauerwein HP, Fliers E, Kalsbeek A. (2009). A major role for perifornical orexin neurons in the control of glucose metabolism in rats. Diabetes 58:1998–2005.
   PubMedGoogle Scholar
• Yousef KA, Lang CH. (1994). Modulation of endotoxin-induced changes in hemodynamics and glucose metabolism by an N-methyl-d-aspartate receptor antagonist. Shock 1:335–342.
   PubMedGoogle Scholar
• Zhang YH, Lu J, Elmquist JK, Saper CB. (2000). Lipopolysaccharide activates specific populations of hypothalamic and brainstem neurons that project to the spinal cord. J. Neurosci. 20:6578–6586.
   PubMedGoogle Scholar