Int J Sports Med 2012; 33(05): 402-409
DOI: 10.1055/s-0032-1301888
Immunology
© Georg Thieme Verlag KG Stuttgart · New York

Exercise Inhibits Allergic Lung Inflammation

A.C. D. Silva
1   Physical Therapy, University of São Paulo, Sao Paulo, Brazil
,
R. P. Vieira
2   Post Graduate Program in Biophotonics Applied to Health Sciences, Nove de Julho University, Säo Paulo, SP, Brazil
,
M. Nisiyama
1   Physical Therapy, University of São Paulo, Sao Paulo, Brazil
,
A.B. G. Santos
3   Pathology (LIM 05), University of Sao Paulo, Sao Paulo, Brazil
,
A. Perini
4   Clinical Medicine (LIM 20), University of Sao Paulo, Sao Paulo, Brazil
,
T. Mauad
3   Pathology (LIM 05), University of Sao Paulo, Sao Paulo, Brazil
,
M. Dolhnikoff
5   School of Medicine, Pathology, Sao Paulo University, Sao Paulo, Brazil
,
M. A. Martins
4   Clinical Medicine (LIM 20), University of Sao Paulo, Sao Paulo, Brazil
,
C. R. Carvalho
1   Physical Therapy, University of São Paulo, Sao Paulo, Brazil
› Author Affiliations
Further Information

Publication History



accepted after revision 28 December 2011

Publication Date:
17 April 2012 (online)

Abstract

Aerobic conditioning (AC) performed either during or after sensitization reduces allergic inflammation in mice; however, the effects of AC performed before and during allergic sensitization on airway inflammation are unknown. Mice were divided into Control, AC, OVA, and AC + OVA groups. Mice were trained in a treadmill followed by either ovalbumin (OVA) sensitization or saline administration. Peribronchial inflammation, OVA-specific IgE and IgG1 titers, the expression of Th1 and Th2 cytokines, and airway remodeling were evaluated, as well as the expression of Eotaxin, RANTES, ICAM-1, VCAM-1, TGF-β and VEGF. Aerobic conditioning performed before and during allergic sensitization displayed an inhibitory effect on the OVA-induced migration of eosinophils and lymphocytes to the airways, a reduction of IgE and IgG1 titers and an inhibition of the expression of Th2 cytokines. The AC + OVA group also demonstrated reduced expression of ICAM-1, VCAM-1, RANTES, TGF-β and VEGF, as well as decreased airway remodeling (p<0.05). The effects of AC before and during the sensitization process inhibit allergic airway inflammation and reduce the production of Th2 cytokines and allergen-specific IgE and IgG1.

 
  • References

  • 1 Araujo BB, Dolhnikoff M, Silva LFF, Elliot J, Lindeman JHN, Ferreira A, Ferreira DS, Mulder A, Gomes HA, Fernezlian SM, James A, Mauad T. Extracellular matrix components and regulators within the airway smooth muscle in asthma. Eur Respir J 2008; 32: 61-69
  • 2 Braun-Fahrländer CH, Gassner M, Grize L, Neu U, Sennhauser FH, Varonier HS, Vuille JC, Würthrich B. Prevalence of hay fever and allergic sensitization in farmer’s children and their peers living in the same rural community. Clin Exp Allergy 1999; 29: 28-34
  • 3 de Magalhaes Simoes S, dos Santos MA, da Silva Oliveira M, Fontes ES, Fernezlian S, Garippo AL, Castro I, Castro FF, de Arruda Martins M, Saldiva PH, Mauad T, Dolhnikoff M. Inflammatory cell mapping of the respiratory tract in fatal asthma. Clin Exp Allergy 2005; 35: 602-611
  • 4 Elovic AE, Ohyama H, Sauty A, McBride J, Tsuji T, Nagai M, Weller PF, Wong DT. IL-4-dependent regulation of TGF-alpha and TGF-beta 1 expression in human eosinophils. J Immunol 1998; 160: 6121-6127
  • 5 Fanelli A, Cabral AL, Neder JA, Martins MA, Carvalho CR. Exercise training on disease control and quality of life in asthmatic children. Med Sci Sports Exerc 2007; 39: 1474-1480
  • 6 Gleeson M. Immune function in sport and exercise. J Appl Physiol 2007; 103: 693-699
  • 7 Harriss DJ, Atkinson G. Update – Ethical Standards in Sport and Exercise Science Research. Int J Sports Med 2011; 32: 819-821
  • 8 Hewitt M, Creel A, Estell K, Davis IC, Schwiebert LM. Acute exercise decreases airway inflammation, but not responsiveness, in an allergic asthma model. Am J Resp Cell Mol Biol 2009; 40: 83-89
  • 9 Huber JP, Ramos HJ, Gill MA, Farrar JD. Cutting edge: Type I IFN reverses human Th2 commitment and stability by suppressing GATA3. J Immunol 2010; 185: 813-817
  • 10 James A. Airway remodeling in asthma. Curr Opin Pulm Med 2005; 11: 1-6
  • 11 Lancas T, Kasahara DI, Prado CM, Tiberio IF, Martins MA, Dolhnikoff M. Comparison of early and late responses to antigen of sensitized guinea pigs parenchymal lung strips. J Appl Physiol 2006; 100: 1610-1616
  • 12 Lee KS, Park SJ, Kim SR, Min KH, Lee KY, Choe YH, Hong SH, Lee YR, Kim JS, Hong SJ, Lee YC. Inhibition of VEGF blocks TGF-beta1 production through a PI3K/Akt signalling pathway. Eur Respir J 2008; 31: 523-531
  • 13 Luna LG. ed. Manual of Histopathologic Staining Method of the AFIP. New York: MCGraw Hill; 1968
  • 14 Marcus BH, Williams DM, Dubbert PM, Sallis JF, King AC, Yancey AK, Franklin BA, Buchner D, Daniels SR, Claytor RP. Physical Activity, and Metabolism. Circulation 2006; 114: 2739-2752
  • 15 Mauser PJ, Pitman AM, Fernandez X, Foran SK, Adams GR, Kreuter W, Egan RW, Chapman RW. Effects of an antibody to interleukin-5 in a monkey model of asthma. Am J Respir Crit Care Med 1995; 152: 467-472
  • 16 Mendes FA, Almeida FM, Cukier A, Stelmach R, Jacob-Filho W, Martins MA, Carvalho CR. Effects of aerobic training on airway inflammation in asthmatic patients. Med Sci Sports Exerc 2011; 43: 197-203
  • 17 Moldoveanu AI, Shepard RJ, Shek PN. The cytokine response to physical activity and training. Sports Med 2001; 31: 115-144
  • 18 Moreira A, Delgado L, Haahtela T, Fonseca J, Moreira P, Lopes C, Mota J, Santos P, Rytilä P, Castel-Branco MG. Physical training does not increase allergic inflammation in asthmatic children. Eur Respir J 2008; 32: 1570-1575
  • 19 Mota I, Perini A. A heat labile mercaptoethanol susceptible homocytotropic antibody in the guinea pig. Life Sci 1970; 9: 923-930
  • 20 Nieman DC. Exercise, upper respiratory tract infection, and the immune system. Med Sci Sports Exerc 1994; 26: 128-139
  • 21 Ngoc PL, Gold DR, Tzianabos AO, Weiss ST, Celedon JC. Cytokines, allergy, and asthma. Curr Opin Allergy Clin Immunol 2005; 5: 161-166
  • 22 Nieman DC. Exercise, infection and immunity. Int J Sport Med 1994; 15: S131-S141
  • 23 Ohkawara Y, Tamura G, Iwasaki T, Tanaka A, Kikuchi T, Shirato K. Activation and transforming growth factor beta production in eosinophils by hyaluronan. Am J Respir Cell Mol Biol 2000; 23: 444-451
  • 24 Ovary Z. ed. Passive Cutaneous Anaphylaxis. Oxford: Blackwell Scientific Publications; 1964
  • 25 Pastva A, Estell K, Schoeb TR, Atkinson TP, Schwiebert LM. Aerobic exercise attenuates airway inflammatory responses in a mouse model of atopic asthma. J Immunol 2004; 172: 4520-4526
  • 26 Pedersen BK, Hoffman-Goetz L. Exercise and the immune system: regulation, integration, and adaptation. Physiol Rev 2000; 80: 1055-1081
  • 27 Pedersen BK, Steensberg A, Fischer C, Keller C, Ostrowski K, Schjerling P. Exercise and cytokines with particular focus on muscle-derived IL-6. Exerc Immunol Rev 2001; 7: 18-31
  • 28 Petersen AMW, Pedersen BK. The antiinflammatory effect of exercise. J Appl Physiol 2005; 98: 1154-1162
  • 29 Racila DM, Kline JN. Perspectives in asthma: molecular use of microbial products in asthma prevention and treatment. J Allergy Clin Immunol 2005; 116: 1202-1205
  • 30 Renz H, Blumer N, Virna S, Sel S, Garn H. The immunological basis of the hygiene hypothesis. Chem Immunol Allergy 2006; 91: 30-48
  • 31 Robinson DS, Hamid Q, Ying S, Tsicopoulos A, Barkans J, Bentley AM, Corrigan C, Durham SR, Kay AB. Predominant TH2-like bronchoalveolar T lymphocyte population in atopic asthma. N Engl J Med 1992; 326: 298-304
  • 32 Sepp E, Julge K, Vasar M, Naaber P, Björksten B, Mikelsaar M. Intestinal microflora of Estonian and Swedish infants. Acta Paediatr 1997; 86: 956-961
  • 33 Shearer GM, Chougnet C, Shearer M. Atopic disease and immunologic response. Science 1997; 276: 17-18
  • 34 Silva RA, Vieira RP, Duarte AC, Lopes FD, Perini A, Mauad T, Martins MA, Carvalho CR. Aerobic training reverses airway inflammation and remodeling in asthma murine model. Eur Respir J 2010; 35: 994-1002
  • 35 Stam WB, Van Oosterhout AJ, Nijkamp FP. Pharmacologic modulation of Th1- and Th2-associated lymphokine production. Life Sci 1993; 53: 1921-1934
  • 36 Suzuki K, Nakaji S, Yamada M, Totsuka M, Sato K, Sugawara K. Systemic inflammatory response to exhaustive exercise. Exerc Immunol Rev 2002; 8: 6-48
  • 37 Vieira RP, Claudino RC, Duarte ACS, Santos ABG, Perini A, Faria Neto HCC, Mauad T, Martins MA, Dolhnikoff M, Carvalho CR. Aerobic exercise decreases chronic allergic lung inflammation and airway remodeling in mice. Am J Respir Crit Care Med 2007; 176: 871-887
  • 38 Vieira RP, de Andrade VF, Duarte AC, Dos Santos AB, Mauad T, Martins MA, Dolhnikoff M, Carvalho CR. Aerobic conditioning and allergic pulmonary inflammation in mice II: effects on lung vascular and parenchymal inflammation and remodeling. Am J Physiol 2008; 295: L670-L679
  • 39 Vieira RP, Duarte AC, Santos AB, Medeiros MC, Mauad T, Martins MA, Carvalho CR, Dolhnikoff M. Exercise reduces effects of creatine on lung. Int J Sports Med 2009; 30: 684-690
  • 40 Vieira RP, Toledo AC, Ferreira SC, Santos ABG, Medeiros MC, Hage M, Mauad T, Dolhnikoff M, Martins MA, Carvalho CRF. Airway epithelium mediates the anti-inflammatory effects of exercise on asthma. Respir Physiol Neurobiol 2011; 175: 383-389
  • 41 Vignola AM, Mirabella F, Costanzo G, Giorgi R, Gjomarkaj M, Bellia V, Bonsigniori G. Airway remodeling in asthma. Chest 2003; 123: 417-422
  • 42 Wang S, Fan Y, Han X, Yang J, Bilenki L, Yang Xi. IL-12-dependent vascular cell adhesion molecule-1 expression contributes to airway eosinophilic inflammation in a mouse model of asthma-like reaction. J Immunol 2001; 166: 2741-2749
  • 43 Wolyniec WW, Sanctis GT, Nabozny G, Torcellini C, Haynes N, Joetham A, Gelfand EW, Drazen JM, Noonan TC. Reduction of antigen-induced airway hyperreactivity and eosinophilia in ICAM-1-deficient mice. Am J Respir Cell Mol Biol 1998; 18: 777-785