Immune cell inflammatory cytokine responses differ between central and systemic compartments in response to acute exercise in mice

Exercise Immunology Review

Volumn 18, Issue , 2012, Pages 141-156

  Pervaiz, Nabeel ^a   Hoffman Goetz, Laurie ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Acute exercise; Apoptosis; Cytokines; Hippocampus; Intestinal lymphocytes; Oxidative stress

Indexed keywords

CORTICOSTERONE; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; EXERCISE; FEMALE; FLOW CYTOMETRY; HIPPOCAMPUS; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; MOUSE; NECROSIS; NONHUMAN; SEDENTARY LIFESTYLE; TREADMILL EXERCISE; WESTERN BLOTTING;

EID: 84862081874     PISSN: 10775552     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (57)

1. Ackigoz O, Aksu I, Topcu A, and Kayatekin BM. Acute exhaustive exercise does not alter lipid peroxidation levels and antioxidant enzyme activities in rat hippocampus, prefrontal cortex and striatum. Neurosci Lett 406: 148-151, 2006. (Pubitemid 44278387)
2. Adrain C, Murphy BM, and Martin SJ. Molecular ordering of the caspase activation cascade initiated by the cytotoxic T lymphocyte/natural killer (CTL/NK) protease Granzyme B. J Biol Chem 280: 4663-4673, 2005. (Pubitemid 40288636)
3. Audet M, Mangano EN, and Anisman H. Behavior and pro-inflammatory cytokine variations among submissive and dominant mice engaged in aggressive encounters: moderation by corticosterone activity. Front Behav Neurosci 4: 1-12, 2010.
4. Barber AE, Coyle SM, Marano MA, Fischer E, Calvano SE, Fong Y, Moldawer LL, and Lowry SF. Glucocorticoid therapy alters hormonal and cytokine response to endotoxin in man. J Immunol 150: 1999-2006, 1993. (Pubitemid 23129678)
5. Barella LA, Etnier JL, and Chang YK. The immediate and delayed effects of an acute bout of exercise on cognitive performance of healthy older adults. J Aging Phys Act 18: 87-98, 2010.
6. Beishuizen A and Thijs LG. Endotoxin and the hypothalamo-pituitary- adrenal (HPA) axis. J Endotoxin Res 9: 3-24, 2003. (Pubitemid 36322480)
7. Brown DA, Johnson MS, Armstrong CJ, Lynch JM, Caruso NM, Ehlers LB, Fleshner M, Spencer RL, and Moore RL. Short-term treadmill running in the rat: what kind of stressor is it? J Appl Physiol 103: 1979-1985, 2007. (Pubitemid 350232380)
8. Carmichael MD, Davis JM, Murphy EA, Brown AS, Carson JA, Mayer EP, and Ghaffar A. Recovery of running performance following muscle-damaging exercise: relationship to brain IL-1 beta. Brain Behav Immun 19: 445-452, 2005. (Pubitemid 41074783)
9. Carmichael MD, Davis JM, Murphy EA, Brown AS, Carson JA, Mayer EP, and Ghaffar A. Role of brain IL-1 beta on fatigue after exercise-induced muscle damage. Am J Physiol Regul Integr Comp Physiol 291: R1344-R1348, 2006.
10. Carmichael MD, Davis, JM, Murphy EA, Carson J, Van Rooijen N, Mayer E, and Ghaffar A. Role of brain macrophages on IL-1 beta and fatigue following eccentric exercise-induced muscle damage. Brain Behav Immun 24: 564-568, 2010.
11. Chen R, Zhou H, Beltran J, Malellari L, and Chang SL. Differential expression of cytokines in the brain and serum during endotoxin tolerance. J Neuroimmunol 163: 53-72, 2005. (Pubitemid 40692949)
12. Cotman CW, Berchtold NC, and Christie LA. Exercise builds brain health: key roles of growth factor cascades and inflammation. Trends Neurosci 30: 464-472, 2007. (Pubitemid 47374831)
13. De Bono JP, Adlam D, Paterson DJ, and Channon KM. Novel quantitative phenotypes of exercise training in mouse models. Am J Physiol Reg I 290: R296-R934, 2006.
14. De Kloet ER. Hormones and the stressed brain. Ann NY Acad Sci 1018: 1-15, 2004. (Pubitemid 38951385)
15. Degterev A, Boyce M, and Yuan J. A decade of caspases. Oncogene 22: 8543-8567, 2003. (Pubitemid 38028527)
16. Hassan NF, Rifat S, Campbell DE, McCawley LJ, and Douglas SD. Isolation and flow cytometric characterization of newborn mouse brain-derived microglia maintained in vitro. J Leukocyte Biol 50: 86-92, 1991.
17. Hoffman-Goetz L and Quadrilatero J. Treadmill exercise in mice increases intestinal lymphocyte loss via apoptosis. Acta Physiol Scand 179: 289-297, 2003. (Pubitemid 37464114)
18. Hoffman-Goetz L and Spagnuolo PA. Effects of repeated exercise stress on caspase 3, Bcl-2, HSP 70 and CuZn-SOD protein expression in mouse intestinal lymphocytes. J Neuroimmunol 187: 94-101, 2007. (Pubitemid 47001545)
19. Hoffman-Goetz L, Pervaiz N, and Guan J. Voluntary exercise training in mice increases the expression of antioxidant enzymes and decreases the expression of TNF-a in intestinal lymphocytes. Brain Behav Immun 23: 498-506, 2009.
20. Hoffman-Goetz L, Pervaiz N, Packer N, and Guan J. Freewheel training decreases pro- and increases anti-inflammatory cytokine expression in mouse intestinal lymphocytes. Brain Behav Immun 24: 1105-1115, 2010.
21. Huang CJ, Webb HE, Evans RK, McCleod KA, Tangsilsat SE, Kamimori GH, and Acevedo EO. Psychological stress during exercise: immunoendocrine and oxidative responses. Exp Biol Med 235: 1498-1504, 2010.
22. Kakanis MW, Peake J, Brenu EW, Simmonds M, Gray B, Hooper SL, and Marshall- Gradisnik SM. The open window of susceptibility to infection after acute exercise in healthy young male elite athletes. Exerc Immunol Rev 119: 119-137, 2010.
23. Kim D, Ko I, Kim B, Kim T, Kim S, Shin M, Kim C, Kim H, Kim K, and Baek S. Treadmill exercise inhibits traumatic brain injury-induced hippocampal apoptosis. Physiol Behav 101: 660-665, 2010.
24. Lambourne K and Tomporowski P. The effect of exercise-induced arousal on cognitive task performance: a meta-regression analysis. Brain Res 1341: 12-24, 2010.
25. Liburt NR, Adams AA, Betancourt A, Horohov DW, and McKeever KH. Exerciseinduced increases in inflammatory cytokines in muscle and blood of horses. Equine Vet J 42: 280-288, 2010.
26. Lin Y, Kuo H, Kuo C, Wang S, Yang B, and Chen H. Antioxidant administration inhibits exercise-induced thymocyte apoptosis in rats. Med Sci Sports Exer 31: 1598-1598, 1999.
27. Mars M, Govender S, Weston A, Naicker V, and Chuturgoon A. High intensity exercise: a cause of lymphocyte apoptosis? Biochem Bioph Res Co 249: 366-370, 1998. (Pubitemid 28431759)
28. McEwen BS, Weiss JM, and Schwarz LS. Uptake of corticosterone by rat brain and its concentration by certain limbic structures. Brain Res 16: 227-241, 1969.
29. Mooren FC, Blöming D, Lechtermann A, Lerch MM, and Völker K. Lymphocyte apoptosis after exhaustive and moderate exercise. J Appl Physiol 93: 147-153, 2002. (Pubitemid 34686205)
30. Mormède C, Castanon N, Médina C, Moze E, Lestage J, Neveu PJ, and Dantzer R. Chronic mild stress in mice decreases peripheral cytokine and increases central cytokine expression independently of IL-10 regulation of the cytokine network. Ann NY Acad Sci 10: 359-366, 2002. (Pubitemid 36980746)
31. Navalta JW, McFarlin, BK, and Lyons TS. Does exercise really induce lymphocyte apoptosis? Front Biosci 2: 478-488, 2010.
32. Nemet D, Oh Y, Kim H, Hill MA, and Cooper DM. Effect of intense exercise on inflammatory cytokines and growth mediators in adolescent boys. Pediatrics 110: 681-689, 2002.
33. Neves G, Cooke SF, and Bliss TVP. Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nat Rev Neurosci 9: 65-75, 2008. (Pubitemid 350295694)
34. Nieman D. Current perspective on exercise immunology. Cur Sports Med Rep 2: 239-242, 2003
35. Nybo L, Nielsen B, Pedersen BK, Møller K, and Secher NH. Interleukin-6 release from the human brain during prolonged exercise. J Physiol 542: 991-995, 2002. (Pubitemid 34947290)
36. Ostrowski K, Rohde T, Asp S, Schjerling P, and Pedersen BK. Pro- and anti-inflammatory cytokine balance in strenuous exercise in humans. J Physiol 515.1: 287-291, 1999. (Pubitemid 29092641)
37. Pace TWW and Miller AH. Cytokines and glucocorticoid receptor signalling - relevance to major depression. Ann NY Acad Sci 1179: 86-105, 2009.
38. Packer N, Pervaiz N, and Hoffman-Goetz L. Does exercise protect from cognitive decline by altering brain cytokine and apoptotic protein levels? A systematic review of the literature. Exerc Immunol Rev 16: 138-162, 2010.
39. Pedersen BK and Febbraio M. Muscle-derived interleukin-6 - a possible link between skeletal muscle, adipose tissue, liver, and brain. Brain Behav Immun 19: 371-376, 2005. (Pubitemid 41074774)
40. Pedersen BK and Hoffman-Goetz L. Exercise and the immune system: regulation, integration, and adaptation. Physiol Rev 80: 1055-1081, 2000. (Pubitemid 30452011)
41. Pedersen BK. Edward F. Adolph distinguished lecture: Muscle as an endocrine organ: IL-6 and other myokines. J Appl Physiol 107: 1006-1014, 2009.
42. Phaneuf S and Leeuwenburgh C. Apoptosis and exercise. Med Sci Sport Exer 33: 393-396, 2001. (Pubitemid 32209658)
43. Quadrilatero J and Hoffman-Goetz L. In vivo corticosterone administration at levels occurring with intense exercise does not reduce intestinal lymphocyte apoptosis in mice. J Neuroimmunol 162: 137-148, 2005.
44. Quadrilatero J and Hoffman-Goetz L. N-acetyl-L-cysteine prevents exercise-induced intestinal lymphocyte apoptosis by maintaining intracellular glutathione levels and reducing mitochondrial membrane depolarization. Biochem Bioph Res Co 319: 894-901, 2004. (Pubitemid 38739405)
45. Radák Z, Katsumi, A, Kizaki T, Shuji O, Masaya I, and Hideki O. Acute bout of exercise does not alter the antioxidant enzyme status and lipid peroxidation of rat hippocampus and cerebellum. Pathophysiol 2: 243-245, 1995.
46. Radák Z, Sasvari M, Nyakas C, Kaneko T, Tahara S, Ohno H, and Goto S. Single bout of exercise eliminates the immobilization-induced oxidative stress in rat brain. Neurochem Int 39: 33-38, 2001. (Pubitemid 32304453)
47. Scopel D, Fochessato C, Cimarosti H, Rabbo M, Belló-Klein A, Salbego C, Netto CA, and Siqueira IR. Exercise intensity influences cell injury in rat hippocampal slices exposed to oxygen and glucose deprivation. Brain Res Bull 71: 155-159, 2006. (Pubitemid 44750432)
48. Sies H. Oxidative stress: oxidants and antioxidants. Exp Physiol 82: 291-295, 1997. (Pubitemid 27182306)
49. Somani SM, Husain K, Diaz-Phillips L, Lanzotti, DK, Kareti KR, and Trammell GL. Interaction of exercise and ethanol on antioxidant enzymes in brain regions of the rat. Alcohol 13: 603-610, 1996. (Pubitemid 26404181)
50. Starkie R, Ostrowski SR, Jauffred S, Febbraio M, and Pedersen BK. Exercise and IL-6 infusion inhibit endotoxin-induced TNF-α production in humans. FASEB J 17: 884-886, 2003.
51. Starkie RL, Angus DJ, Rolland J, Hargreaves M, and Febbraio MA. Effect of prolonged submaximal exercise and carbohydrate ingestion on monocyte intracellular cytokine production in humans. J Physiol 528.3: 647-655, 2000.
52. Steensberg A, Dalsgaard MK, Secher NH, and Pedersen BK. Cerebrospinal fluid IL- 6, HSP72, and TNF-alpha in exercising humans. Brain Behav Immun 20: 585-589, 2006. (Pubitemid 44550169)
53. Steinacker JM, Lormes W, Reissnecker S, and Liu Y. New aspects of the hormone cytokine response to training. Eur J Appl Physiol 87: 38-42, 2004.
54. Um HS, Kang EB, Leem YH, Cho IH, Yang CH, Chae KR, Hwang DY, and Cho JY. Exercise training acts as therapeutic strategy for reduction of the pathogenic phenotypes for Alzheimer's disease in an NSE/APPsw-transgenic model. Int J Mol Med 22: 529-539, 2008.
55. Vedder H, Schreiber W, Schuld A, Kainz M, Lauer CJ, Krieg J, Holsboer F, and Pollmächer T. Immune-endocrine host response to endotoxin in major depression. J Psychiat Res 41: 280-289, 2007. (Pubitemid 44854998)
56. Wilson CJ, Finch CE, and Cohen HJ. Cytokines and cognition - the case for a headto- tose inflammatory paradigm. J Am Geriatr Soc 50: 2041-2056, 2002. (Pubitemid 35462453)
57. Zaldivar F, Wang-Rodriguez J, Nemet D, Schwindt C, Galassetti P, Mills PJ, Wilson, LD, and Cooper DM. Constitutive pro- and anti-inflammatory cytokine and growth factor response to exercise in leukocytes. J Appl Physiol 100: 1123-1133, 2006.