Download PDF
Int J Sports Med 2014; 35(07): 629-635
DOI: 10.1055/s-0033-1358477
Immunology
© Georg Thieme Verlag KG Stuttgart · New York

Exercise Deactivates Leukocytes in Asthma

R. P. Vieira
1   Nove de Julho University, São Paulo, Brazil
,
R. A. Silva
3   Physical Therapy (LIM 34), University of São Paulo, Brazil
,
M. C. Oliveira-Junior
1   Nove de Julho University, São Paulo, Brazil
,
F. R. Greiffo
1   Nove de Julho University, São Paulo, Brazil
,
A. P. Ligeiro-Oliveira
1   Nove de Julho University, São Paulo, Brazil
,
M. A. Martins
2   Clinical Medicine (LIM 20), University of São Paulo, Brazil
,
C. R. F. Carvalho
3   Physical Therapy (LIM 34), University of São Paulo, Brazil
› Author Affiliations
Further Information

Publication History



accepted after revision 23 September 2013

Publication Date:
20 November 2013 (online)

Also available at
    Permissions and Reprints

Abstract

Leukocytes play a central role in asthma physiopathology. Aerobic training (AT) reduces leukocytes recruitment to the airways, but the effects of AT on some aspects of leukocytes activation in asthma are unknown. Therefore, the effects of 4 weeks of AT on airway inflammation, pulmonary and systemic Th2 cytokines levels, leukocytes expression of pro and anti-inflammatory, pro-fibrotic, oxidants and anti-oxidants mediators in an experimental model of asthma was investigated. AT reduced the levels of IL-4, IL-5, IL-13 in bronchoalveolar lavage fluid (BALF) (p<0.001), serum levels of IL-5, while increased BALF and serum levels of IL-10 (p<0.001). In addition, AT reduced leukocytes activation, showed through decreased expression of Th2 cytokines (IL-4, IL-5, IL-13; p<0.001), chemokines (CCL5, CCL10; p<0.001), adhesion molecules (VCAM-1, ICAM-1; p<0.05), reactive oxygen and nitrogen species (GP91phox and 3-nitrotyrosine; p<0.001), inducible nitric oxide synthase (iNOS; p<0.001), nuclear factor kB (NF-kB; p<0.001) while increased the expression of anti-inflammatory cytokine (IL-10; p<0.001). AT also decreased the expression of growth factors (TGF-beta, IGF-1, VEGF and EGFr; p<0.001). We conclude that AT reduces the activation of peribronchial leukocytes in a mouse model of allergic asthma, resulting in decreased airway inflammation and Th2 response.

Key words

asthma - exercise - immunology - allergy - cytokines
 

  • References

  • 1 Al-Muhsen S, Johnson JR, Hamid Q. Remodeling in asthma. J Allergy Clin Immunol 2011; 128: 451-462
    CrossrefPubMedGoogle Scholar
  • 2 American Association of Cardiovascular & Pulmonary Rehabilitation . Guidelines of Pulmonary Rehabilitation Programmes. 2nd ed Human Kinetics Publishers; Champaign, Illinois, USA: 1998
    Google Scholar
  • 3 Brooks AM, Bates ME, Vrtis RF, Jarjour NN, Bertics PJ, Sedgwick JB. Urokinase-type plasminogen activator modulates airway eosinophil adhesion in asthma. Am J Respir Cell Mol Biol 2006; 35: 503-511
    CrossrefPubMedGoogle Scholar
  • 4 Coleman JM, Naik C, Holguin F, Ray A, Ray P, Trudeau JB, Wenzel SE. Epithelial eotaxin-2 and eotaxin-3 expression: relation to asthma severity, luminal eosinophilia and age at onset. Thorax 2012; 67: 1061-1066
    CrossrefPubMedGoogle Scholar
  • 5 Disabella V, Sherman C. Exercise for asthma patients: little risk, big rewards. Phys Sportsmed 1998; 26: 75-84
    PubMedGoogle Scholar
  • 6 Engström I, Fällström K, Karlberg E, Sten G, Bjure J. Psychological and respiratory physiological effects of a physical exercise programme on boys with severe asthma. Acta Paediatr Scand 1991; 80: 1058-1065
    PubMedGoogle Scholar
  • 7 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
    PubMedGoogle Scholar
  • 8 Ferreira SC, Toledo AC, Hage M, Santos AB, Medeiros MC, Martins MA, Carvalho CR, Dolhnikoff M, Vieira RP. Creatine activates airway epithelium in asthma. Int J Sports Med 2010; 31: 906-912
    Article in Thieme ConnectPubMedGoogle Scholar
  • 9 Gonçalves RC, Nunes MPT, Cukier A, Stelmach R, Martins MA, Carvalho CRF. Effects of an aerobic physical training program on psychosocial characteristics quality-of-life, symptoms and exhaled nitric oxide in individuals with moderate or severe persistent asthma. Rev Bras Fisioter 2008; 12: 127-135
    CrossrefPubMedGoogle Scholar
  • 10 Harriss DJ, Atkinson G. Update – ethical standards in sport and exercise science research. Int J Sports Med 2011; 32: 819-821
    Article in Thieme ConnectPubMedGoogle Scholar
  • 11 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 Respir Cell Mol Biol 2009; 40: 83-89
    CrossrefPubMedGoogle Scholar
  • 12 Hewitt M, Estell K, Davis IC, Schwiebert LM. Repeated bouts of moderate-intensity aerobic exercise reduce airway reactivity in a murine asthma model. Am J Respir Cell Mol Biol 2010; 42: 243-249
    CrossrefPubMedGoogle Scholar
  • 13 Huang SW, Veiga R, Sila U, Reed E, Hines S. The effect of swimming in asthmatic children-participants in a swimming program in the city of Baltimore. J Asthma 1989; 26: 117-121
    CrossrefPubMedGoogle Scholar
  • 14 Imanifooladi AA, Yazdani S, Nourani MR. The role of nuclear factor-kappaB in inflammatory lung disease. Inflamm Allergy Drug Targets 2010; 9: 197-205
    CrossrefPubMedGoogle Scholar
  • 15 Janssen-Heininger YM, Poynter ME, Aesif SW, Pantano C, Ather JL, Reynaert NL, Ckless K, Anathy V, van der Velden J, Irvin CG, van der Vliet A. Nuclear factor kappaB, airway epithelium, and asthma: avenues for redox control. Proc Am Thorac Soc 2009; 6: 249-255
    CrossrefPubMedGoogle Scholar
  • 16 Kelly EA, Jarjour NN. Role of matrix metalloproteinases in asthma. Curr Opin Pulm Med 2003; 9: 28-33
    CrossrefPubMedGoogle Scholar
  • 17 Ligeiro de Oliveira AP, Peron JPS, Lino-dos-Santos-Franco A, Acceturi BG, Vieira RP, Ibanez OM, Cabrera WHK, Franco M, Rizzo LV, Vargafitg BB, Tavares-de-Lima W. Ovariectomized OVA-sensitized mice display increased frequency of CD4+Foxp3+ T regulatory cells in the periphery. Plos One 2013; 8: e65674
    CrossrefPubMedGoogle Scholar
  • 18 Ligeiro de Oliveira AP, Lino-dos-Santos-Franco A, Acceturi BG, Hamasato EK, Machado ID, Gimenes Júnior JA, Vieira RP, Damazo AS, Farsky SH, Tavares-de-Lima W, Palermo-Neto J. Long-term amphetamine treatment exacerbates inflammatory lung reaction while decreases airway hyper-responsiveness after allergic stimulus in rats. Int Immunopharmacol 2012; 14: 523-529
    CrossrefPubMedGoogle Scholar
  • 19 Livingstone JL, Gillespie M. Value of breathing exercises in asthma. Lancet 1935; 2: 705
    PubMedGoogle Scholar
  • 20 Lowder T, Dugger K, Deshane J, Estell K, Schwiebert LM. Repeated bouts of aerobic exercise enhance regulatory T cell responses in a murine asthma model. Brain Behav Immun 2010; 24: 153-159
    CrossrefPubMedGoogle Scholar
  • 21 Mauad T, Bel EH, Sterk PJ. Asthma therapy and airway remodeling. J Allergy Clin Immunol 2007; 120: 997-1009 quiz 1010–1011
    CrossrefPubMedGoogle Scholar
  • 22 Mays LE, Ammon-Treiber S, Mothes B, Alkhaled M, Rottenberger J, Müller-Hermelink ES, Grimm M, Mezger M, Beer-Hammer S, Von Stebut E, Rieber N, Nürnberg B, Schwab M, Handgretinger R, Idzko M, Hartl D, Kormann MS. Modified Foxp3 mRNA protects against asthma through an IL-10-dependent mechanism. J Clin Invest 2013; 123: 1216-1228
    CrossrefPubMedGoogle Scholar
  • 23 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
    PubMedGoogle Scholar
  • 24 Mendes FA, Gonçalves RC, Nunes MP, Saraiva-Romanholo BM, Cukier A, Stelmach R, Jacob-Filho W, Martins MA, Carvalho CR. Effects of aerobic training on psychosocial morbidity and symptoms in patients with asthma: a randomized clinical trial. Chest 2010; 138: 331-337
    CrossrefPubMedGoogle Scholar
  • 25 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
    CrossrefPubMedGoogle Scholar
  • 26 Neder JA, Nery LE, Silva AC, Cabral AL, Fernandes AL. Short-term effects of aerobic training in the clinical management of moderate to severe asthma in children. Thorax 1999; 54: 202-206
    CrossrefPubMedGoogle Scholar
  • 27 Olivo CR, Vieira RP, Arantes-Costa FM, Perini A, Martins MA, Carvalho CRF. Effects of aerobic exercise on chronic allergic airway inflammation and remodeling in guinea pigs. Resp Physiol Neurobiol 2012; 182: 81-87
    CrossrefPubMedGoogle Scholar
  • 28 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
    CrossrefPubMedGoogle Scholar
  • 29 Pastva A, Estell K, Schoeb TR, Schwiebert LM. RU486 blocks the anti-inflammatory effects of exercise in a murine model of allergen-induced pulmonary inflammation. Brain Behav Immun 2005; 19: 413-422
    CrossrefPubMedGoogle Scholar
  • 30 Pearson RS. The management of asthma. Br Med J 1950; 1: 1311-1314
    CrossrefPubMedGoogle Scholar
  • 31 Ram FS, Robinson SM, Black PN, Picot J. Physical training for asthma. Cochrane Database Syst Rev 2005; CD001116
    PubMedGoogle Scholar
  • 32 Ramazanoglu YM, Kraemer R. Cardiorespiratory response to physical conditioning in children with bronchial asthma. Pediatr Pulmonol 1985; 1: 272-277
    CrossrefPubMedGoogle Scholar
  • 33 Sevin CM, Newcomb DC, Toki S, Han W, Sherrill TP, Boswell MG, Zhu Z, Collins RD, Boyd KL, Goleniewska K, Huckabee MM, Blackwell TS, Peebles Jr RS. Deficiency of gp91phox inhibits allergic airway inflammation. Am J Respir Cell Mol Biol 2013; [Epub ahead of print]
    PubMedGoogle Scholar
  • 34 Silva ACD, Vieira RP, Nisiyama M, Santos ABG, Perini A, Mauad T, Dolhnikoff M, Martins MA, Carvalho CRF. Exercise inhibits allergic lung inflammation. Int J Sports Med 2012; 33: 402-409
    Article in Thieme ConnectPubMedGoogle Scholar
  • 35 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
    CrossrefPubMedGoogle Scholar
  • 36 Szentágothai K, Gyene I, Szócska M, Osváth P. Physical exercise program for children with bronchial asthma. Pediatr Pulmonol 1987; 3: 166-172
    CrossrefPubMedGoogle Scholar
  • 37 Vieira RP, Claudino RC, Duarte AC, Santos AB, Perini A, Faria Neto HC, 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: 871-877
    CrossrefPubMedGoogle Scholar
  • 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; 29: L670-L679
    PubMedGoogle Scholar
  • 39 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
    CrossrefPubMedGoogle Scholar
  • 40 Walsh GM. Antagonism of eosinophil accumulation in asthma. Recent Pat Inflamm Allergy Drug Discov 2010; 4: 210-213
    CrossrefPubMedGoogle Scholar
  • 41 Yamamoto M, Tochino Y, Chibana K, Trudeau JB, Holguin F, Wenzel SE. Nitric oxide and related enzymes in asthma: relation to severity, enzyme function and inflammation. Clin Exp Allergy 2012; 42: 760-768
    CrossrefPubMedGoogle Scholar