Calorie restriction dose-dependently abates lipopolysaccharide-induced fever, sickness behavior, and circulating interleukin-6 while increasing corticosterone

Brain, Behavior, and Immunity

Volumn 40, Issue , 2014, Pages 18-26

  MacDonald, Leah ^a   Hazi, Agnes ^a   Paolini, Antonio G ^a   Kent, Stephen ^a  

^a LA TROBE UNIVERSITY   (Australia)

Author keywords

Corticosterone; Cytokines; Dietary restriction; Fever; Food restriction; Interleukin 10; Interleukin 6; Lipopolysaccharide; Sickness behavior

Indexed keywords

CORTICOSTERONE; INTERLEUKIN 10; INTERLEUKIN 6; LIPOPOLYSACCHARIDE;

ANIMAL EXPERIMENT; ANOREXIA; ARTICLE; BODY WEIGHT; CACHEXIA; CALORIC RESTRICTION; COHORT ANALYSIS; CONTROLLED STUDY; CORE TEMPERATURE; FEVER; FOOD INTAKE; ILLNESS BEHAVIOR; LIPOPOLYSACCHARIDE INDUCED FEVER; LOCOMOTION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RAT; TELEMETRY; WEIGHT REDUCTION; ANIMAL; BLOOD; DIET THERAPY; EATING; INFLAMMATION; MOTOR ACTIVITY; SPRAGUE DAWLEY RAT;

ANIMALS; BODY WEIGHT; CALORIC RESTRICTION; CORTICOSTERONE; EATING; FEVER; ILLNESS BEHAVIOR; INFLAMMATION; INTERLEUKIN-10; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MALE; MOTOR ACTIVITY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84904111233     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2014.01.005     Document Type: Article

References (51)

1. Asarian L., Langhans W. A new look on brain mechanisms of acute illness anorexia. Physiol. Behav. 2010, 100:464-471.
2. Barnes P.J. Anti-inflammatory actions of glucocorticoids: molecular mechanisms. Clin. Sci. 1998, 94:557-572.
3. Begg D.P., Kent S., McKinley M.J., Mathai M.L. Suppression of endotoxin-induced fever in near-term pregnant rats is mediated by brain nitric oxide. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292:R2174-R2178.
4. Besedovsky H., Sorkin E., Keller M., Muller J. Changes in blood hormone levels during the immune response. Proc. Soc. Exp. Biol. Med. 1975, 150:466-470.
5. Bevilacqua L., Ramsey J.J., Hagopian K., Weindruch R., Harper M. Effects of short- and medium-term calorie restriction on muscle mitochondrial proton leak and reactive oxygen species production. Am. J. Physiol. Endocrinol. Metab. 2004, 286:E852-E861.
6. Bogdan C., Vodovotz Y., Nathan C. Macrophage deactivation by interleukin 10. J. Exp. Med. 1991, 174:1549-1555.
7. Brady L.S., Smith M.A., Gold P.W., Herkenham M. Altered expression of hypothalamic neuropeptide mRNAs in food-restricted and food-deprived rats. Neuroendocrinology 1990, 52:441-447.
8. Campfield L., Smith F., Guisez Y., Devos R., Burn P. Recombinant mouse OB protein: evidence for a peripheral signal linking adiposity and central neural networks. Science 1995, 269:546-549.
9. Campisi J., Hansen M.K., O'Connor K.A., Biedenkapp J.C., Watkins L.R., Maier S.F., Fleshner M. Circulating cytokines and endotoxin are not necessary for the activation of the sickness or corticosterone response produced by peripheral E. coli challenge. J. Appl. Physiol. 2003, 95:1873-1882.
10. Cao S.X., Dhahbi J.M., Mote P.L., Spindler S.R. Genomic profiling of short- and long-term caloric restriction effects in the liver of aging mice. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:10630-10635.
11. Capel F., Klimčáková E., Viguerie N., Roussel B., Vítková M., Kováčiková M., Polák J., Kováčová Z., Galitzky J., Maoret J.-J., Hanáček J., Pers T.H., Bouloumié A., Štich V., Langin D. Macrophages and adipocytes in human obesity: adipose tissue gene expression and insulin sensitivity during calorie restriction and weight stabilization. Diabetes 2009, 58:1558-1567.
12. Cartmell T., Poole S., Turnbull A.V., Rothwell N.J., Luheshi G.N. Circulating interleukin-6 mediates the febrile response to localised inflammation in rats. J. Physiol. (Lond.) 2000, 526:653-661.
13. Cassatella M.A., Gasperini S., Bovolenta C., Calzetti F., Vollebregt M., Scapini P., Marchi M., Suzuki R., Suzuki A., Yoshimura A. Interleukin-10 (IL-10) selectively enhances CIS3/SOCS3 mRNA expression in human neutrophils: evidence for an IL-10-induced pathway that is independent of STAT protein activation. Blood 1999, 94:2880-2889.
14. Chai Z., Gatti S., Toniatti C., Poli V., Bartfai T. Interleukin (IL)-6 gene expression in the central nervous system is necessary for fever response to lipopolysaccharide or IL-1 beta: a study on IL-6-deficient mice. J. Exp. Med. 1996, 183:311-316.
15. Conn C.A., Kozak W.E., Tooten P.C.J., Gruys E., Borer K.T., Kluger M.J. Effect of voluntary exercise and food restriction in response to lipopolysaccharide in hamsters. J. Appl. Physiol. 1995, 78:466-477.
16. Felies M., von Horsten S., Pabst R., Nave H. Neuropeptide Y stabilizes body temperature and prevents hypotension in endotoxaemic rats. J. Physiol. (Lond.) 2004, 561:245-252.
17. Gutman R., Hacmon-Keren R., Choshniak I., Kronfeld-Schor N. Effect of food availability and leptin on the physiology and hypothalamic gene expression of the golden spiny mouse: a desert rodent that does not hoard food. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 295:R2015-R2023.
18. Han E.N.L., Bengani N., Roberts J.L., Suh Y., Karelus K., Nelson J.F. Hyperadrenocorticism and food restriction-induced life extension in the rat: evidence for divergent regulation of pituitary proopiomelanocortin RNA and adrenocorticotropic hormone biosynthesis. J. Gerontol. A Biol. Sci. Med. Sci. 1995, 50:B288-B294.
19. Hart B.L. Biological basis of the behavior of sick animals. Neurosci. Biobehav. Rev. 1988, 21:123-137.
20. Heiderstadt K.M., McLaughlin R.M., Wright D.C., Walker S.E., Gomez-Sanchez C.E. The effect of chronic food and water restriction on open-field behaviour and serum corticosterone levels in rats. Lab. Anim. 2000, 34:20-28.
21. 2C and corticosteroid receptor gene expression in the hippocampus with food restriction and glucocorticoids. J. Neurosci. 1997, 17:4056-4065.
22. Institute for Laboratory Animal Research Nutrient Requirements of Laboratory Animals 1995, The National Academy of Sciences, Washington, DC.
23. Kumar S.P., Roy S.J., Tokumo K., Reddy B.S. Effect of different levels of calorie restriction on azoxymethane-induced colon carciogenesis in male F344 rats. Cancer Res. 1990, 50:5761-5766.
24. Lang R., Pauleau A., Parganas E., Takahashi Y., Mages J., Ihle J., Rutschman R., Murray P.J. SOCS3 regulates the plasticity of gp130 signaling. Nat. Immunol. 2003, 4:546-550.
25. Layé S., Gheusi G., Cremona S., Combe C., Kelley K., Dantzer R., Parnet P. Endogenous brain IL-1 mediates LPS-induced anorexia and hypothalamic cytokine expression. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2000, 279:R93-R98.
26. Ledeboar A., Binnekade R., Brevé J.J.P., Bol J.G.J.M., Tilders F.J.H., Van Dam A.-M. Site-specific modulation of LPS-induced fever and interleukin-1 beta expression in rats byinterleukin-10. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2002, 282:R1762-R1772.
27. LeMay L.G., Vander A.J., Kluger M.J. Role of interleukin 6 in fever in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1990, 258:R798-R803.
28. Leon L.R., Kozak W.E., Rudolph K., Kluger M.J. An antipyretic role for interleukin-10 in LPS fever in mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1999, 45:R81-R89.
29. Levay E.A., Govic A., Penman J., Paolini A.G., Kent S. Effects of adult-onset calorie restriction on anxiety-like behavior in rats. Physiol. Behav. 2007, 92:889-896.
30. Levay E.A., Tammer A.H., Penman J., Paolini A.G., Kent S. Calorie restriction at increasing levels leads to augmented concentrations of corticosterone and decreasing concentrations of testosterone in rats. Nutr. Res. 2010, 30:366-373.
31. Levin B.E., Dunn-Meynell A.A. Dysregulation of arcuate nucleus preproneuropeptide Y mRNA in diet-induced obese rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1997, 272:R1365-R1370.
32. Linthorst A., Flachskamm C., Muller-Preuss P., Holsboer F., Reul J. Effect of bacterial endotoxin and interleukin-1 beta on hippocampal serotonergic neurotransmission, behavioral activity, and free corticosterone levels: an in vivo microdialysis study. J. Neurosci. 1995, 15:2920-2934.
33. Luheshi G.N., Gardner J.D., Rushforth D.A., Loudon A.S., Rothwell N.J. Leptin actions on food intake and body temperature are mediated by IL-1. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:7047-7052.
34. Lynn S.E., Breuner C.W., Wingfield J.C. Short-term fasting affects locomotor activity, corticosterone, and corticoterone binding globulin in a migratory songbird. Horm. Behav. 2003, 43:150-157.
35. MacDonald L., Radler M., Paolini A.G., Kent S. Calorie restriction attenuates LPS-induced sickness behavior and shifts hypothalamic signaling pathways to an anti-inflammatory bias. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 301:R172-R184.
36. MacDonald L., Begg D., Weisinger R., Kent S. Calorie restricted rats do not increase metabolic rate post-LPS, but do seek out warmer ambient temperatures to behaviourally induce a fever. Physiol. Behav. 2012, 107:762-772.
37. Mascarucci P., Taub D., Saccani S., Paloma M.A., Dawson H., Roth G.S., Lane M.A., Ingram D.K. Cytokine responses in young and old rhesus monkeys: effect of calorie restriction. J. Interferon Cytokine Res. 2002, 22:565-571.
38. Maswood N., Young J., Tilmont E., Zhang Z., Gash D.M., Gerhardt G.A., Grondin R., Roth G.S., Mattison J., Lane M.A., Carson R.E., Cohen R.M., Mouton P.R., Quigley C., Mattson M.P., Ingram D.K. Caloric restriction increases neurotrophic factor level and attenuates neurochemical and behavioral deficits in a primate model of Parkinson's disease. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:18171-18176.
39. Matsuzaki J., Yamaji R., Kiyomiya K., Kurebe M., Inui H., Nakano Y. Implanted tumor growth is suppressed and survival is prolonged in sixty percent of food-restricted mice. J. Nutr. 2000, 130:111-115.
40. Mrosovsky N., Molony L.A., Conn C.A., Kluger M.J. Anorexic effects of interleukin 1 in the rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1989, 257:R1315-R1321.
41. Ogimoto K., Harris M.K., Wisse B.E. MyD88 is a key mediator of anorexia, but not weight loss, induced by lipopolysaccharide and interleukin-1β. Endocrinology 2006, 147:4445-4453.
42. Patel N.V., Finch C.E. The glucocorticoid paradox of caloric restriction in slowing brain aging. Neurobiol. Aging 2002, 23:707-717.
43. Poole S., Stephenson J.D. Body temperature regulation and thermoneutrality in rats. Exp. Physiol. 1977, 62:143-149.
44. Rummel C., Matsumura K., Luheshi G.N. Circulating IL-6 contributes to peripheral LPS-induced mPGES-1 expression in the rat brain. Brain Res. Bull. 2011, 86:319-325.
45. Skinner G.W., Mitchell D., Harden L.M. Avoidance of physical activity is a sensitive indicator of illness. Physiol. Behav. 2009, 96:421-427.
46. Smoak K.A., Cidlowski J.A. Mechanism of glucocorticoid receptor signaling during inflammation. Mech. Ageing Dev. 2004, 125:697-706.
47. Sonti G., Ilyin S.E., Plata-Salamán C.R. Neuropeptide Y blocks and reverses interleukin-1 beta-induced anorexia in rats. Peptides 1996, 17:517-520.
48. Soos S., Balasko M., Jech-Mihalffy A., Szekely M., Petervari E. Anorexic Vs. metabolic effects of central leptin infusion in rats of various ages and nutritional states. J. Mol. Neurosci. 2010, 41:97-104.
49. Tabachnick B.G., Fidell L.S. Using Multivariate Statistics 1996, Harper Collins College Publishers, New York.
50. Weindruch R., Walford R.L., Fligiel S., Guthrie D. The retardation of aging in mice by dietary restriction: longevity, cancer, immunity and lifetime energy intake. J. Nutr. 1986, 116:641-654.
51. Wisse B.E., Ogimoto K., Tang J., Harris J.M.K., Raines E.W., Schwartz M.W. Evidence that lipopolysaccharide-induced anorexia depends upon central, rather than peripheral, inflammatory signals. Endocrinology 2007, 148:5230-5237.