Freewheel training decreases pro- and increases anti-inflammatory cytokine expression in mouse intestinal lymphocytes

Brain, Behavior, and Immunity

Volumn 24, Issue 7, 2010, Pages 1105-1115

  Hoffman Goetz, L ^a   Pervaiz, N ^a   Packer, N ^a   Guan, J ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Apoptosis; Caspase 7; IL 10; IL 6; Intestinal lymphocytes; Mice; TNF ; Voluntary exercise

Indexed keywords

CASPASE 3; CASPASE 7; CYTOKINE; INTERLEUKIN 10; INTERLEUKIN 10 ANTIBODY; INTERLEUKIN 17; INTERLEUKIN 6; PROTEIN BCL 2; TRANSFORMING GROWTH FACTOR ALPHA;

AEROBIC EXERCISE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; FEMALE; INTESTINE CELL; LYMPHOCYTE COUNT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RUNNING; TRAINING; TREADMILL EXERCISE;

ANIMALS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; BLOTTING, WESTERN; CASPASE 3; CASPASE 7; CYTOKINES; DOWN-REGULATION; FEMALE; INTERLEUKIN-10; INTERLEUKIN-17; INTERLEUKIN-6; INTESTINES; LYMPHOCYTES; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; PHYSICAL CONDITIONING, ANIMAL; PROTO-ONCOGENE PROTEINS C-BCL-2; RUNNING; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84755161372     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2010.05.001     Document Type: Article

References (74)

1. Ashe P.C., Berry M.D. Apoptotic signaling cascades. Prog. Neuro-Psychopha. 2003, 27:199-214.
2. Avula C.P., Muthukumar A.R., Zaman K., McCarter R., Fernandes G. Inhibitory effects of voluntary wheel exercise on apoptosis in splenic lymphocyte subsets of C57BL/6 mice. J. Appl. Physiol. 2001, 91:2546-2552.
3. Beagley K.W., Husband A.J. Intraepithelial lymphocytes: origins, distribution, and function. Crit. Rev. Immunol. 1998, 18:237-254.
4. Bi L., Triadafilopoulos G. Exercise and gastrointestinal function and disease: an evidence-based review of risks and benefits. Clin. Gastroenterol. Hepatol. 2003, 1:345-355.
5. Boudreau J., Hoffman-Goetz L. Long-duration freewheel running and submandibular lymphocyte response to forced exercise in older mice. Can. J. Physiol. Pharmacol. 2006, 84:565-572.
6. Bredesen D.E. Key note lecture: toward a mechanistic taxonomy for cell death programs. Stroke 2007, 38:652-660.
7. Brown D.A., Johnson M.S., Armstrong C.J., Lynch J.M., Caruso N.M., Ehlers L.B., Fleshner M., Spencer R.L., Moore R.L. Short-term treadmill running in the rat: what kind of stressor is it?. J. Appl. Physiol. 2007, 103:1979-1985.
8. Campisi J., Leem T.H., Fleshner M. Acute stress decreases inflammation at the site of infection. A role for nitric oxide. Physiol. Behav. 2002, 77:291-299.
9. Carter S.L., Rennie C.D., Hamilton S.J., Tarnopolsky M.A. Changes in skeletal muscle in males and females following endurance training. Can. J. Physiol. Pharmacol. 2001, 79:386-392.
10. Chi M.M., Hintz C.S., Coyle E.F., Martin W.H.3., Ivy J.L., Nemeth P.M., Holloszy J.O., Lowry O.H. Effects of detraining on enzymes of energy metabolism in individual human muscle fibers. Am. J. Physiol. 1983, 244:C276-C287.
11. Clement L.T. Isoforms of the CD45 common leukocyte antigen family: markers for human T-cell differentiation. J. Clin. Immunol. 1992, 12:1-10.
12. Corwin E.J. Understanding cytokines part I: physiology and mechanism of action. Biol. Res. Nurs. 2000, 2:30-40.
13. Davidson S.R., Burnett M., Hoffman-Goetz L. Training effects in mice after long-term voluntary exercise. Med. Sci. Sports Exerc. 2006, 38:250-255.
14. Del Puerto H.L., Martins A.S., Moro L., Milsted A., Alves F., Braz G.F., Vasconcelos A.C. Caspase-3/-8/-9, Bax and Bcl-2 expression in the cerebellum, lymph nodes and leukocytes of dogs naturally infected with canine distemper virus. Genet. Mol. Res. 2010, 9:151-161.
15. Duzova H., Karakoc Y., Hanifi Emre M., Yilmaz Dogan Z., Kilinc E. Effects of acute moderate and strenuous exercise bouts on IL-17 production and inflammatory response in trained rats. J. Sports Sci. Med. 2009, 8:219-224.
16. Eikelboom R. Human parallel to voluntary wheel running: exercise. Anim. Behav. 1999, 57:F11-F12.
17. Fujino S., Andoh A., Bamba S., Ogawa A., Hata K., Araki Y., Bamba T., Fujiyama Y. Increased expression of interleukin 17 in inflammatory bowel disease. Gut 2003, 52:65-70.
18. Goldhammer E., Tanchilevitch A., Maor I., Beniamini Y., Rosenschein U., Sagiv M. Exercise training modulates cytokines activity in coronary heart disease patients. Int. J. Cardiol. 2005, 100:93-99.
19. Gomez-Merino D., Drogou C., Guezennec C.Y., Chennaoui M. Effects of chronic exercise on cytokine production in white adipose tissue and skeletal muscle of rats. Cytokine 2007, 40:23-29.
20. Haaland D.A., Sabljic T.F., Baribeau D.A., Muhovozow I.M., Hart L.E. Is regular exercise a friend or foe of the aging immune system? A systematic review. Clin. J. Sport Med. 2008, 18:539-548.
21. Haddad J.J., Fahlman C.S. Nuclear factor-kappa B-independent regulation of lipopolysaccharide-mediated interleukin-6 biosynthesis. Biochem. Biophys. Res. Commun. 2002, 291:1045-1051.
22. Hirose L., Nosaka K., Newton M., Laveder A., Kano M., Peake J. Changes in inflammatory mediators following eccentric exercise of the elbow flexors. Exerc. Immunol. Rev. 2004, 10:75-90.
23. Hoffman-Goetz L., Pervaiz N., Guan J. Voluntary exercise training in mice increases the expression of antioxidant enzymes and decreases the expression of TNF-alpha in intestinal lymphocytes. Brain Behav. Immun. 2009, 23:498-506.
24. Hoffman-Goetz L., Quadrilatero J. Treadmill exercise in mice increases intestinal lymphocyte loss via apoptosis. Acta Physiol. Scand. 2003, 179:289-297.
25. Hoffman-Goetz L., Spagnuolo P.A. Effect of repeated exercise stress on caspase 3, Bcl-2, HSP 70 and CuZn-SOD protein expression in mouse intestinal lymphocytes. J. Neuroimmunol. 2007, 187:94-101.
26. Hoffman-Goetz L., Spagnuolo P.A. Freewheel exercise training modifies pro- and anti-apoptotic protein expression in mouse splenic lymphocytes. Int. J. Sports Med. 2007, 28:787-791.
27. Hoffman-Goetz L., Spagnuolo P.A., Guan J. Repeated exercise in mice alters expression of IL-10 and TNF-alpha in intestinal lymphocytes. Brain Behav. Immun. 2008, 22:195-199.
28. Houle-Leroy P., Garland T., Swallow J.G., Guderley H. Effects of voluntary activity and genetic selection on muscle metabolic capacities in house mice Mus domesticus. J. Appl. Physiol. 2000, 89:1608-1616.
29. Hyun J.G., Mayer M. Mechanisms underlying inflammatory bowel disease. Drug Discov. Today 2006, 3:457-462.
30. Gibala M.J., Little J.P., van Essen M., Wilkin G.P., Burgomaster K.A., Safdar A., Raha S., Tarnopolsky M.A. Short-term sprint interval training versus traditional endurance training: similar initial adaptations in human skeletal muscle and exercise performance. J. Physiol. 2006, 575:901-911.
31. Kasimay O., Güzel E., Gemici A., Abdyli A., Sulovari A., Ercan F., Yeĝen B.C. Colitis-induced oxidative damage of the colon and skeletal muscle is ameliorated by regular exercise in rats: the anxiolytic role of exercise. Exp. Physiol. 2006, 91:897-906.
32. Keller C., Steensberg A., Pilegaard H., Osada T., Saltin B., Pedersen B.K., Neufer P.D. Transcriptional activation of the IL-6 gene in human contracting skeletal muscle: influence of muscle glycogen content. FASEB J. 2001, 15:2748-2750.
33. Kohut M.L., McCann D.A., Russell D.W., Konopka D.N., Cunnick J.E., Franke W.D., Castillo M.C., Reighard A.E., Vanderah E. Aerobic exercise, but not flexibility/resistance exercise, reduces serum IL-18, CRP, and IL-6 independent of beta-blockers, BMI, and psychosocial factors in older adults. Brain Behav. Immun. 2006, 20:201-209.
34. Koteja P., Garland T., Sax J.K., Swallow J.G., Carter P.A. Behavior of house mice artificially selected for high levels of voluntary wheel running. Anim. Behav. 1999, 58:1307-1318.
35. Lakhani S.A., Masud A., Kuida K., Porter G.A.J., Booth C.J., Mehal W.Z., Inayat I., Flavell R.A. Caspases 3 and 7: key mediators of mitochondrial events of apoptosis. Science 2006, 311:847-851.
36. Lamkanfi M., Kanneganti T.D. Caspase-7: a protease involved in apoptosis and inflammation. Int. J. Biochem. Cell Biol. 2010, 42:21-24.
37. Lira F.S., Koyama C.H., Yamashita A.S., Rosa Neto J.C., Zanchi N.E., Batista M.L.J., Seelaender M.C. Chronic exercise decreases cytokine production in healthy rat skeletal muscle. Cell Biochem. Funct. 2009, 27:458-461.
38. Lira F.S., Rosa Neto J.C., Yamashita A.S., Koyama C.H., Batista M.L.J., Seelaender M. Endurance training induces depot-specific changes in IL-10/TNF-alpha ratio in rat adipose tissue. Cytokine 2009, 45:80-85.
39. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
40. Mahoney D.J., Parise G., Melov S., Safdar A., Tarnopolsky M.A. Analysis of global mRNA expression in human skeletal muscle during recovery from endurance exercise. FASEB J. 2005, 19:1498-1500.
41. Malisch J.L., Saltzman W., Gomes F.R., Rezende E.L., Jeske D.R., Garland T.J. Baseline and stress-induced plasma corticosterone concentrations of mice selectively bred for high voluntary wheel running. Physiol. Biochem. Zool. 2007, 80:146-156.
42. Marra S., Burnett M., Hoffman-Goetz L. Intravenous catecholamine administration affects mouse intestinal lymphocyte number and apoptosis. J. Neuroimmunol. 2005, 158:76-85.
43. Marra S., Hoffman-Goetz L. Beta-adrenergic receptor blockade during exercise decreases intestinal lymphocyte apoptosis but not cell loss in mice. Can. J. Physiol. Pharm. 2004, 82:465-473.
44. Moore K.W., de Waal Malefyt R., Coffman R.L., O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 2001, 19:683-765.
45. Mooren F.C., Blöming D., Lechtermann A., Lerch M.M., Völker K. Lymphocyte apoptosis after exhaustive and moderate exercise. J. Appl. Physiol. 2002, 93:147-153.
46. Murch S.H., Braegger C.P., Walker-Smith J.A., MacDonald T.T. Location of tumour necrosis factor alpha by immunohistochemistry in chronic inflammatory bowel disease. Gut 1993, 34:1705-1709.
47. Narula N., Fedorak R.N. Exercise and inflammatory bowel disease. Can. J. Gasteroenterol. 2008, 22:497-504.
48. Ng V., Millard W., Lebrun C., Howard J. Low-intensity exercise improves quality of life in patients with Crohn's disease. Clin. J. Sport Med. 2007, 17:384-388.
49. Packer N., Hoffman-Goetz L., Ward G. Does physical activity affect quality of life, disease symptoms and immune measures in patients with inflammatory bowel disease? A systematic review. J. Sport. Med. Phys. Fit. 2010, 50:1-18.
50. Patrono C., FitzGerald G.A. Isoprostanes: potential markers of oxidant stress in atherothrombotic disease. Arterioscler. Thromb. Vasc. Biol. 1997, 17:2309-2315.
51. Pedersen M., Steensberg A., Keller C., Osada T., Zacho M., Saltin B., Febbraio M.A., Pederson B.K. Does the aging skeletal muscle maintain its endocrine function?. Exerc. Immunol. Rev. 2004, 10:42-55.
52. Pérez C.A. Prescription of physical exercise in Crohn's disease. J. Crohn's Colitis. 2009, 3:225-231.
53. Perrson P., Leijonmarck C., Bernell O., Hellers G., Ahlbom A. Risk indicators of inflammatory bowel disease. Int. J. Epidemiol. 1993, 22:268-272.
54. Petersen A.M., Pedersen B.K. The role of IL-6 in mediating the anti-inflammatory effects of exercise. J. Physiol. Pharmacol. 2006, 57:43-51.
55. Poldolsky D.K. The current future understanding of inflammatory bowel disease. Best Pract. Res. Clin. Gastroenterol. 2002, 16:933-943.
56. Porter A.G., Janicke R.U. Emerging roles of caspase-3 in apoptosis. Cell Death Differ. 1999, 6:99-104.
57. Quadrilatero J., Bombardier E., Norris S.M., Talanian J.L., Palmer M.S., Logan H.M., Tupling A.R., Heigenhauser G.J., Spriet L.L. Prolonged moderate-intensity aerobic exercise does not alter apoptotic signaling and DNA fragmentation in human skeletal muscle. Am. J. Physiol. 2010, 298:E534-E547.
58. Quadrilatero J., Hoffman-Goetz L. N-Acetyl-L-cysteine prevents exercise-induced intestinal lymphocyte apoptosis by maintaining intracellular glutathione levels and reducing mitochondrial membrane depolarization. Biochem. Biophys. Res. Commun. 2004, 319:894-901.
59. Quadrilatero J., Hoffman-Goetz L. Mouse thymocyte apoptosis and cell loss in response to exercise and antioxidant administration. Brain Behav. Immun. 2005, 19:436-444.
60. Quadrilatero J., Hoffman-Goetz L. In vivo corticosterone administration at levels occurring with intense exercise does not induce intestinal lymphocyte apoptosis in mice. J. Neuroimmunol. 2005, 162:137-148.
61. Rosa Neto J.C., Lira F.S., Oyama L.M., Zanchi N.E., Yamashita A.S., Batista M.L.J., Oller do Nascimento C.M., Seelaender M. Exhaustive exercise causes an anti-inflammatory effect in skeletal muscle and a pro-inflammatory effect in adipose tissue in rats. Eur. J. Appl. Physiol. 2009, 106:697-704.
62. Schaller K., Mechau D., Scharmann H.G., Weiss M., Baum M., Liesen H. Increased training load and the β-adrenergic-receptor system on human lymphocytes. J. Appl. Physiol. 1999, 87:317-324.
63. Shih D.Q., Targan S.R. Immunopathogenesis of inflammatory bowel disease. World J. Gastroenterol. 2008, 14:390-400.
64. Sonnenberg A. Occupational distribution of inflammatory bowel disease among German employees. Gut 1990, 31:1037-1040.
65. Spagnuolo P.A., Hoffman-Goetz L. Effect of dextran sulfate sodium and acute exercise on mouse intestinal inflammation and lymphocyte cytochrome c levels. J. Sport. Med. Phys. Fit. 2009, 49:112-121.
66. Steensberg A., Morrow J., Toft A.D., Bruunsgaard H., Pedersen B.K. Prolonged exercise, lymphocyte apoptosis and F2-isoprostanes. Eur. J. Appl. Physiol. 2002, 87:38-42.
67. Stennicke H.R., Jürgensmeier J.M., Shin H., Deveraux Q., Wolf B.B., Yang X., Zhou Q., Ellerby H.M., Ellerby L.M., Bredesen D., Green D.R., Reed J.C., Froelich C.J., Salvesen G.S. Pro-caspase-3 is a major physiologic target of caspase-8. J. Biol. Chem. 1998, 273:27084-27090.
68. Strober W., Fuss I.J., Blumberg R.S. The immunology of mucosal models of inflammation. Annu. Rev. Immunol. 2002, 20:495-549.
69. Targan S.R. Biology of inflammation in Crohn's disease: mechanisms of action of anti-TNF-a therapy. Can. J. Gasteroenterol. 2000, 14:13C-16C.
70. Trowbridge I.S., Thomas M.L. CD45: an emerging role as a protein tyrosine phosphatase required for lymphocyte activation and development. Annu. Rev. Immunol. 1994, 12:85-116.
71. Vahsen N., Candé C., Brière J.J., Bénit P., Joza N., Larochette N., Mastroberardino P.G., Pequignot M.O., Casares N., Lazar V., Feraud O., Debili N., Wissing S., Engelhardt S., Madeo F., Piacentini M., Penninger J.M., Schägger H., Rustin P., Kroemer G. AIF deficiency compromises oxidative phosphorylation. EMBO J. 2004, 23:4679-4689.
72. Walsh J.G., Cullen S.P., Sheridan C., Lüthi A.U., Gener C., Martin S.J. Executioner caspase-3 and caspase-7 are functionally distinct proteases. Proc. Natl. Acad. Sci. USA 2008, 105:12815-12819.
73. Xie Y., Frede S., Harnish M.J., Exton M.S., Schedlowski M. Β-adrenoreceptor-induced inhibition of rat splenocyte proliferation: cytokine gene transcription as the target of action. Immunobiol. 2002, 206:345-353.
74. Zaldivar F., Wang-Rodriguez J., Nemet D., Schwindt C., Galassetti P., Mills P.J., Wilson L.D., Cooper D.M. Constitutive pro- and anti-inflammatory cytokine and growth factor response to exercise in leukocytes. J. Appl. Physiol. 2006, 100:1124-1133.