Effects of voluntary wheel running on LPS-induced sickness behavior in aged mice

Brain, Behavior, and Immunity

Volumn 29, Issue , 2013, Pages 113-123

  Martin, Stephen A ^a   Pence, Brandt D ^a   Greene, Ryan M ^a   Johnson, Stephanie J ^a   Dantzer, Robert ^b   Kelley, Keith W ^a   Woods, Jeffrey A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Aging; Exercise; Inflammation; Sickness behavior

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA;

ADIPSIA; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOREXIA; ARTICLE; BODY COMPOSITION; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOKINE RESPONSE; EXERCISE TOLERANCE; FAT BODY; FATIGUE; FLUID INTAKE; FOOD INTAKE; GENE EXPRESSION; ILLNESS BEHAVIOR; LOCOMOTION; MALE; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RUNNING; WEIGHT REDUCTION;

AGING; ANIMALS; BODY WEIGHT; CYTOKINES; DRINKING; EATING; FATIGUE; GENE EXPRESSION; ILLNESS BEHAVIOR; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; REAL-TIME POLYMERASE CHAIN REACTION; RNA; RUNNING;

EID: 84873448590     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2012.12.014     Document Type: Article

References (42)

1. Abraham J., Johnson R.W. Central inhibition of interleukin-1beta ameliorates sickness behavior in aged mice. Brain Behav. Immun. 2009, 23:396-401.
2. Barrientos R.M., Frank M.G., Crysdale N.Y., Chapman T.R., Ahrendsen J.T., Day H.E., Campeau S., Watkins L.R., Patterson S.L., Maier S.F. Little exercise, big effects: reversing aging and infection-induced memory deficits, and underlying processes. J. Neurosci. 2011, 31:11578-11586.
3. Besedovsky H., del Rey A., Sorkin E., Dinarello C.A. Immunoregulatory feedback between interleukin-1 and glucocorticoid hormones. Science 1986, 233:652-654.
4. Chen H.I., Hsieh S.Y., Yang F.L., Hsu Y.H., Lin C.C. Exercise training attenuates septic responses in conscious rats. Med. Sci. Sports Exerc. 2007, 39:435-442.
5. Chen J., Buchanan J.B., Sparkman N.L., Godbout J.P., Freund G.G., Johnson R.W. Neuroinflammation and disruption in working memory in aged mice after acute stimulation of the peripheral innate immune system. Brain Behav. Immun. 2008, 22:301-311.
6. Conn C.A., Kozak W.E., Tooten P.C., 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.
7. Cortese G.P., Barrientos R.M., Maier S.F., Patterson S.L. Aging and a peripheral immune challenge interact to reduce mature brain-derived neurotrophic factor and activation of TrkB, PLCgamma1, and ERK in hippocampal synaptoneurosomes. J. neurosci. off. J. Soc. Neurosci. 2011, 31:4274-4279.
8. Criswell D.S., Henry K.M., DiMarco N.M., Grossie V.B. Chronic exercise and the pro-inflammatory response to endotoxin in the serum and heart. Immunol. Lett. 2004, 95:213-220.
9. Dantzer R. Cytokine-induced sickness behavior: mechanisms and implications. Ann. N. Y. Acad. Sci. 2001, 933:222-234.
10. Dantzer R., Kelley K.W. Twenty years of research on cytokine-induced sickness behavior. Brain Behav. Immun. 2007, 21:153-160.
11. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 2008, 9:46-56.
12. Dilger R.N., Johnson R.W. Aging, microglial cell priming, and the discordant central inflammatory response to signals from the peripheral immune system. J. Leukoc. Biol. 2008, 84:932-939.
13. Funk J.A., Gohlke J., Kraft A.D., McPherson C.A., Collins J.B., Jean Harry G. Voluntary exercise protects hippocampal neurons from trimethyltin injury: possible role of interleukin-6 to modulate tumor necrosis factor receptor-mediated neurotoxicity. Brain Behav. Immun. 2011, 25:1063-1077.
14. Gavazzi G., Krause K.H. Ageing and infection. Lancet Infect. Dis. 2002, 2:659-666.
15. Godbout J.P., Chen J., Abraham J., Richwine A.F., Berg B.M., Kelley K.W., Johnson R.W. Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system. FASEB J. 2005, 19:1329-1331.
16. Goldmann O., Lehne S., Medina E. Age-related susceptibility to streptococcus pyogenes infection in mice. underlying immune dysfunction and strategy to enhance immunity. J. Pathol. 2010, 220:521-529.
17. Hung C.H., Chen Y.W., Shao D.Z., Chang C.N., Tsai Y.Y., Cheng J.T. Exercise pretraining attenuates endotoxin-induced hemodynamic alteration in type I diabetic rats. Appl. Physiol. Nutr. Metab. 2008, 33:976-983.
18. Jeneson J.A., de Snoo M.W., Verlinden N.A., Joosten B.J., Doornenbal A., Schot A., Everts M.E. Treadmill but not wheel running improves fatigue resistance of isolated extensor digitorum longus muscle in mice. Acta Physiologica 2007, 190:151-161.
19. Keylock K.T., Vieira V.J., Wallig M.A., DiPietro L.A., Schrementi M., Woods J.A. Exercise accelerates cutaneous wound healing and decreases wound inflammation in aged mice. Am. J. Physiol. Regul. Integr. Compar. Physiol. 2008, 294:R179-R184.
20. Kluger M.J. Fever: Its Biology, Evolution, and Function 1979, Princeton University Press, Princeton, NJ.
21. Kohman R.A., Tarr A.J., Byler S.L., Boehm G.W. Age increases vulnerability to bacterial endotoxin-induced behavioral decrements. Physiol. Behav. 2007, 91:561-565.
22. Leasure J.L., Jones M. Forced and voluntary exercise differentially affect brain and behavior. Neuroscience 2008, 156:456-465.
23. Lenczowski M.J., Bluthe R.M., Roth J., Rees G.S., Rushforth D.A., van Dam A.M., Tilders F.J., Dantzer R., Rothwell N.J., Luheshi G.N. Central administration of rat IL-6 induces HPA activation and fever but not sickness behavior in rats. Am. J. Physiol. 1999, 276:R652-R658.
24. Lowder T., Padgett D.A., Woods J.A. Moderate exercise early after influenza virus infection reduces the Th1 inflammatory response in lungs of mice. Exerc. Immunol. Rev. 2006, 12:97-111.
25. Murray M.J., Murray A.B. Anorexia of infection as a mechanism of host defense. Am. J. Clin. Nutr. 1979, 32:593-596.
26. Nickerson M., Elphick G.F., Campisi J., Greenwood B.N., Fleshner M. Physical activity alters the brain Hsp72 and IL-1beta responses to peripheral E. coli challenge. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 289:R1665-R1674.
27. Oliveira A.G., Carvalho B.M., Tobar N., Ropelle E.R., Pauli J.R., Bagarolli R.A., Guadagnini D., Carvalheira J.B., Saad M.J. Physical exercise reduces circulating lipopolysaccharide and TLR4 activation and improves insulin signaling in tissues of DIO rats. Diabetes 2011, 60:784-796.
28. Park S.E., Dantzer R., Kelley K.W., McCusker R.H. Central administration of insulin-like growth factor-I decreases depressive-like behavior and brain cytokine expression in mice. J. Neuroinflam. 2011, 8:12.
29. Pawelec G., Larbi A., Derhovanessian E. Senescence of the human immune system. J. Comp. Pathol. 2010, 142(Suppl 1):S39-S44.
30. Rowsey P.J., Metzger B.L., Carlson J., Gordon C.J. Effects of chronic exercise conditioning on thermal responses to lipopolysaccharide and turpentine abscess in female rats. Arch. Toxicol. 2006, 80:81-87.
31. Shanley D.P., Aw D., Manley N.R., Palmer D.B. An evolutionary perspective on the mechanisms of immunosenescence. Trends Immunol. 2009, 30:374-381.
32. Silvia O.J., Urosevic N. Variations in LPS responsiveness among different mouse substrains of C3H lineage and their congenic derivative sublines. Immunogenetics 1990, 50:354-357.
33. Starkie R., Ostrowski S.R., Jauffred S., Febbraio M., Pedersen B.K. Exercise and IL-6 infusion inhibit endotoxin-induced TNF-alpha production in humans. FASEB J. 2003, 17:884-886.
34. Starr M.E., Evers B.M., Saito H. Age-associated increase in cytokine production during systemic inflammation: adipose tissue as a major source of IL-6. J. Gerontol. A Biol. Sci. Med. Sci. 2009, 64:723-730.
35. Tanaka Y., Kawanishi N., Shiva D., Tsutsumi N., Uchida M., Kitamura H., Kato Y., Yano H. Exhaustive exercise reduces tumor necrosis factor-alpha production in response to lipopolysaccharide in mice. Neuroimmunomodulation 2010, 17:279-286.
36. Vieira V.J., Valentine R.J., Wilund K.R., Antao N., Baynard T., Woods J.A. Effects of exercise and low-fat diet on adipose tissue inflammation and metabolic complications in obese mice. Am. J. Physiol. Endocrinol. Metab. 2009, 296:E1164-E1171.
37. Vieira V.J., Valentine R.J., Wilund K.R., Woods J.A. Effects of diet and exercise on metabolic disturbances in high-fat diet-fed mice. Cytokine 2009, 46:339-345.
38. Wu C.W., Chen Y.C., Yu L., Chen H.I., Jen C.J., Huang A.M., Tsai H.J., Chang Y.T., Kuo Y.M. Treadmill exercise counteracts the suppressive effects of peripheral lipopolysaccharide on hippocampal neurogenesis and learning and memory. J. Neurochem. 2007, 103:2471-2481.
39. Wu R., Zhou M., Dong W., Ji Y., Miksa M., Marini C.P., Ravikumar T.S., Wang P. Ghrelin hyporesponsiveness contributes to age-related hyperinflammation in septic shock. Ann. Surg. 2009, 250:126-133.
40. Wu S.Y., Wang T.F., Yu L., Jen C.J., Chuang J.I., Wu F.S., Wu C.W., Kuo Y.M. Running exercise protects the substantia nigra dopaminergic neurons against inflammation-induced degeneration via the activation of BDNF signaling pathway. Brain Behav. Immun. 2011, 25:135-146.
41. Wynne A.M., Henry C.J., Huang Y., Cleland A., Godbout J.P. Protracted downregulation of CX3CR1 on microglia of aged mice after lipopolysaccharide challenge. Brain Behav. Immun. 2010, 24:1190-1201.
42. Zoladz J.A., Pilc A. The effect of physical activity on the brain derived neurotrophic factor: from animal to human studies. J. Physiol. Pharmacol. 2010, 61:533-541.