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Int J Sports Med 2017; 38(06): 473-480
DOI: 10.1055/s-0042-121638
Immunology
© Georg Thieme Verlag KG Stuttgart · New York

Aerobic Exercise Decreases Lung Inflammation by IgE Decrement in an OVA Mice Model

Deborah Camargo Hizume-Kunzler
1   State University of Santa Catarina, Physical Therapy, Florianopolis, Brazil
,
Flavia R. Greiffo
2   Nove de Julho University – UNINOVE, Research, São Paulo, Brazil
,
Bárbara Fortkamp
1   State University of Santa Catarina, Physical Therapy, Florianopolis, Brazil
,
Gabriel Ribeiro Freitas
3   Universidade do Estado de Santa Catarina Centro de Ciencias da Departamento de Fisioterapia, Saude e do Esporte, Florianopolis, Brazil
,
Juliana Keller Nascimento
3   Universidade do Estado de Santa Catarina Centro de Ciencias da Departamento de Fisioterapia, Saude e do Esporte, Florianopolis, Brazil
,
Thayse Regina Bruggemann
4   School of Medicine of University of Sao Paulo, Internal Medicine, Sao Paulo, Brazil
,
Leonardo Melo Avila
1   State University of Santa Catarina, Physical Therapy, Florianopolis, Brazil
,
Adenir Perini
5   Faculdade de Medicina da Universidade de São Paulo, Departamento de Clínica Médica, São Paulo, Brazil
,
Franciane Bobinski
6   Department of Biological Science, Federal University of Santa Catarina, Florianopolis, Brazil
,
Morgana Duarte Silva
6   Department of Biological Science, Federal University of Santa Catarina, Florianopolis, Brazil
,
Fernanda Rocha Lapa
7   Universidade do Contestado Campus Concordia, Ciências Biológicas, Concordia, Brazil
,
Rodolfo Paula Vieira
8   Nove de Julho University (UNINOVE), Laboratory of Pulmonary and Exercise Immunology (LABPEI) and Brazilian Institute of Teaching and Research in Pulmonary and Exercise Immunology (IBEPIPE), Sao Paulo, Brazil
,
Verônica Vargas Horewicz
9   Universidade Federal de Santa Catarina, Departamento de Farmacologia, Florianopolis, Brazil
,
Adair Roberto Soares dos Santos
10   Universidade Federal de Santa Catarina, Departamento de Ciências Biológicas, Florianópolis, Brazil
,
Kelly Cattelan Bonorino
10   Universidade Federal de Santa Catarina, Departamento de Ciências Biológicas, Florianópolis, Brazil
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accepted after revision 25. Oktober 2016

Publikationsdatum:
07. April 2017 (online)

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Abstract

Aerobic exercise (AE) reduces lung function decline and risk of exacerbations in asthmatic patients. However, the inflammatory lung response involved in exercise during the sensitization remains unclear. Therefore, we evaluated the effects of exercise for 2 weeks in an experimental model of sensitization and single ovalbumin-challenge. Mice were divided into 4 groups: mice non-sensitized and not submitted to exercise (Sedentary, n=10); mice non-sensitized and submitted to exercise (Exercise, n=10); mice sensitized and exposed to ovalbumin (OVA, n=10); and mice sensitized, submitted to exercise and exposed to OVA (OVA+Exercise, n=10). 24 h after the OVA/saline exposure, we counted inflammatory cells from bronchoalveolar fluid (BALF), lung levels of total IgE, IL-4, IL-5, IL-10 and IL-1ra, measurements of OVA-specific IgG1 and IgE, and VEGF and NOS-2 expression via western blotting. AE reduced cell counts from BALF in the OVA group (p<0.05), total IgE, IL-4 and IL-5 lung levels and OVA-specific IgE and IgG1 titers (p<0.05). There was an increase of NOS-2 expression, IL-10 and IL-1ra lung levels in the OVA groups (p<0.05). Our results showed that AE attenuated the acute lung inflammation, suggesting immunomodulatory properties on the sensitization process in the early phases of antigen presentation in asthma.

Key words

asthma - inflammation - aerobic exercise - IgE
 

  • References

  • 1 Arantes-Costa FM, Lopes FD, Toledo AC, Magliarelli-Filho PA, Moriya HT, Carvalho-Oliveira R, Mauad T, Salvadiva PHN, Martins MA. Effect of residual oil fly ash (ROFA) in mice with chronic allergic pulmonary inflammation. Toxicol Pathol 2008; 36: 680-686
    CrossrefPubMedSuche in Google Scholar
  • 2 Arima M, Fuduka T. Prostaglandin D2 and TH2 inflammation in the pathogenesis of bronchial asthma. Korean J Intern Med 2011; 26: 8-18
    CrossrefPubMedSuche in Google Scholar
  • 3 Asai K, Kanazawa H, Kamoi H, Shiraishi S, Hirata K, Yoshikawa J. Increased levels of vascular endotelial growth fator in induced sputum in asthmatic patients. Clin Exp Allergy 2003; 33: 595-599
    CrossrefPubMedSuche in Google Scholar
  • 4 Ávila LC, Bruggemann TR, Bobinski F, da Silva MD, Oliveira RC, Martins DF, Mazzardo-Martins L, Duarte MM, de Souza LF, Dafre A, Vieira RP, Santos AR, Bonorino KC, Hizume Kunzler DC. Effects of high-intensity swimming on lung inflammation and oxidative stress in a murine model of DEP-induced injury. PLos One 2015; 10: e0137273
    CrossrefPubMedSuche in Google Scholar
  • 5 Barbato A, Turato G, Baraldo S, Bazzan E, Calabrese F, Panizzolo C. Epithelial damage and angiogenesis in the airways of children with asthma. Am J Respir Crit Care Med 2006; 174: 975-981
    CrossrefPubMedSuche in Google Scholar
  • 6 Bisset LR, Schmid-Grandelemeie P. Chemokines and their receptors in the pathogenesis of asthma: progress and perspective. Curr Opin Pulm Med 2005; 11: 35-42
    CrossrefPubMedSuche in Google Scholar
  • 7 Bonsignore MR, La Grutta S, Cibella F, Scichilone N, Cuttitta G, Interrante A, Marchese M, Veca M, Virzi’ M, Bonanno A, Profita M, Morici G. Effect of exercise training and montelukast in children with mild asthma. Med Sci Sports Exerc 2008; 40: 405-412
    CrossrefPubMedSuche in Google Scholar
  • 8 Broide DH, Finkelman F, Bochner BS, Rothenberg ME. Advances in mechanisms of asthma, allergy, and immunology in 2010. J Allergy Clin Immunol 2011; 127: 689-695
    CrossrefPubMedSuche in Google Scholar
  • 9 Brüggemann TR, Ávila LC, Fortkamp B, Greiffo FR, Bobinski F, Mazzardo-Martins L, Martins DF, Duarte MM, Dafre A, Santos AR, Silva MD, Souza LF, Vieira RP, Hizume-Kunzler DC. Effects of swimming on the inflammatory and redox response in a model of allergic asthma. Int J Sports Med 2015; 36: 579-584
    Thieme ConnectPubMedSuche in Google Scholar
  • 10 Dogra S, Kuk JL, Bajer J, Jamnik V. Exercise is associated with improved asthma control in adults. Eur Respir J 2010; 7: 318-323
    PubMedSuche in Google Scholar
  • 11 Fló C, Lopes FD, Kasahara DI, Silva AC, Jesus RC, Rivero DH, Saldiva PH, Martins MA, Jacob-Filho W. Effects of exercise training on papain-induced pulmonary emphysema in Wistar rats. J Appl Physiol 2006; 100: 281-285
    CrossrefPubMedSuche in Google Scholar
  • 12 Förstermann U, Sessa WC. Nitric oxide synthases: regulation and function. Eur Heart J 2012; 33: 829-837
    CrossrefPubMedSuche in Google Scholar
  • 13 Guidelines for the diagnosis and management of asthma. National Heart, Lung, and Blood Institute. National Asthma Education Program. Expert Panel Report. J Allergy Clin Imunol 1991; 88: 427-535
    CrossrefPubMedSuche in Google Scholar
  • 14 Hamid Q, Springall DR, Riveros-Moreno V, Chanez P, Howarth P, Redington A, Bousquet J, Godard P, Holgate S, Polak JM. Induction of nitric oxide synthase in asthma. Lancet 1993; 342: 1510-1513
    CrossrefPubMedSuche in Google Scholar
  • 15 Harriss DJ, Atkinson G. Ethical standards in sports and exercise science research: 2016 update. Int J Sports Med 2015; 36: 1121-1124
    Thieme ConnectPubMedSuche in Google Scholar
  • 16 Iijima H, Tulic MK, Duguet A, Shan J, Carbonara P, Hamid Q, Eidelman DH. NOS 1 is required for allergen-induced expression of NOS 2 in mice. Int Arch Allergy Immunol 2005; 138: 40-50
    CrossrefPubMedSuche in Google Scholar
  • 17 Kharitonov SA, Yates D, Robbins RA, Logan-Sinclair R, Shinebourne EA, Barnes PJ. Increased nitric oxide in exhaled air of asthmatic patients. Lancet 1994; 343: 133-135
    CrossrefPubMedSuche in Google Scholar
  • 18 Lee CG, Link H, Baluk P, Chapoval S, Bhandari V, Kang MJ, Cohn L, Kim YK, McDonald DM, Elias JA. Vascular endothelial growth factor (VEGF) induces remodeling and enhances TH2-mediated sensitization and inflammation in the lung. Nat Med 2004; 10: 1095-1103
    CrossrefPubMedSuche in Google Scholar
  • 19 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
    CrossrefPubMedSuche in Google Scholar
  • 20 Lukacs NW. Role of chemokines in the pathogenesis of asthma. Nat Rev Immunol 2001; 1: 108-116
    CrossrefPubMedSuche in Google Scholar
  • 21 Luks V, Burkett A, Turner L, Pakhale S. Effect of physical training on airway inflammation in animal models of asthma: a systematic review. BMC Pulm Med 2013; 24: 13-24
    PubMedSuche in Google Scholar
  • 22 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
    CrossrefPubMedSuche in Google Scholar
  • 23 Mendes FA, Gonçalves RC, Nunes MP. Effects of aerobic training on psychosocial morbidity and symptoms in patients with asthma: a randomized clinical trial. Chest 2010; 138: 331-337
    CrossrefPubMedSuche in Google Scholar
  • 24 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
    CrossrefPubMedSuche in Google Scholar
  • 25 Morton AR, Fitch KD. Australian association for exercise and sports Science position statement on exercise and asthma. J Sci Med Sport 2011; 14: 312-316
    CrossrefPubMedSuche in Google Scholar
  • 26 Mota I, Perini A. A heat labile mercaptoethanol susceptible homocytotropic antibody in the guinea pig. Life Sci 1970; 9: 923-930
    CrossrefPubMedSuche in Google Scholar
  • 27 Mura M, dos Santos CC, Stewart D, Liu M. Vascular endothelial growth fator and related molecules in acute lung injury. J Appl Physiol 2004; 97: 1605-1617
    CrossrefPubMedSuche in Google Scholar
  • 28 Official EU. Directive 2010/63/EU of the European Parliament and of the Council in: 20/10/2010 ed. 2010
    PubMed
  • 29 Olivo CR, Miyaji EN, Oliveira ML, Almeida FM, Lourenço JD, Abreu RM, Arantes PM, Lopes FD, Martins MA. Aerobic exercise attenuates pulmonary inflammation induced by Streptococcus pneumoniae. J Appl Physiol 2014; 117: 998-1007
    CrossrefPubMedSuche in Google Scholar
  • 30 Ovary Z. Passive cutaneous anaphylaxis. In: Ackroyd JF. editor. Immunological methods. Oxford, UK: Blackwell Scientific Publications; 1964
    Suche in Google Scholar
  • 31 Pastva A, Estell K, Schoeb TR, Atkinson TP, Schwiebert LM. Aerobic exercise attenuates airway inflammatory response in a mouse model of atopic asthma. J Immunol 2004; 172: 4520-4526
    CrossrefPubMedSuche in Google Scholar
  • 32 Prado CM, Leick-Maldonado EA, Kasahara DI, Capelozzi VL, Martins MA, Tibério IF. Effects of acute and chronic nitric oxide inhibition in an experimental model of chronic pulmonary allergic inflammation in guinea pigs. Am J Physiol 2005; 289: L677-683
    PubMedSuche in Google Scholar
  • 33 Prado CM, Leick-Maldonado EA, Yano L, Leme AS, Capelozzi VL, Martins MA, Tibério IF. Effects of nitric oxide synthases in chronic allergic airway inflammation and remodeling. Respir Cell Mol Biol 2006; 35: 457-465
    PubMedSuche in Google Scholar
  • 34 Prado CM, Martins MA, Tibério IF. Nitric oxide in asthma physiopathology. ISRN Allergy 2011 832560
    PubMed
  • 35 Ram FS, Robinson SM, Black PN. Effects of physical training in asthma: a systematic review. Br J Sports Med 2000; 34: 162-167
    CrossrefPubMedSuche in Google Scholar
  • 36 Rydell-Törmänen K, Johnson JR, Fattouh R, Jordana M, Erjefält JS. Induction of vascular remodeling in the lung by chronic house dust mite exposure. Am J Respir Cell Mol Biol 2008; 39: 61-67
    CrossrefPubMedSuche in Google Scholar
  • 37 Silva RA, Almeida FM, Olivo CR, Saraiva-Romanholo BM, Perini A, Martins MA, Carvalho CR. Comparison of the effects of aerobic conditioning before and after pulmonary allergic inflammation. Inflammation 2015; 38: 1229-1238
    CrossrefPubMedSuche in Google Scholar
  • 38 Silva RA, Vieira RP, Duarte AC, Lopes FD, Perini A, Mauad T, Martins MA, Carvalho CR. Aerobic training reverses airway inflammation and remodelling in asthma murine model. Eur Respir J 2010; 35: 994-1002
    CrossrefPubMedSuche in Google Scholar
  • 39 St-Laurent J, Boulet LP, Bissonnette E. Cigarette smoke differently alter normal and ovalbumin-sensitized bronchial epithelial cells frim rat. J Asthma 2009; 46: 577-581
    CrossrefPubMedSuche in Google Scholar
  • 40 Toledo AC, Magalhaes RM, Hizume DC, Vieira RP, Biselli PJ, Moriya HT, Mauad T, Lopes FD, Martins MA. Aerobic exercise attenuates pulmonary injury induced by exposure to cigarette smoke. Eur Respir J 2012; 39: 254-264
    CrossrefPubMedSuche in Google Scholar
  • 41 Törmänen KR, Uller L, Persson CG, Erjefält JS. Allergen exposure of mouse airway evokes remodeling of both bronchi and large pulmonary vessels. Am J Respir Crit Care Med 2005; 171: 19-25
    CrossrefPubMedSuche in Google Scholar
  • 42 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
    CrossrefPubMedSuche in Google Scholar
  • 43 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. Effect on lung vascular and parenchymal inflammation and remodeling. Am J Physiol 2008; 295: L670-L679
    PubMedSuche in Google Scholar
  • 44 Vieira RP, Silva RA, Oliveira-Juniro MC, Greiffo FR, Ligeiro-Oliveira AP, Martins MA, Carvalho CR. Exercises deactivates leucocytes in asthma. Int J Sports Med 2014; 35: 629-635
    Thieme ConnectPubMedSuche in Google Scholar
  • 45 Vieira RP, Toledo AC, Ferreira SC, Santos AB, Medeiros MC, Hage M, Mauad T, Martins Mde A, Dolhnikoff M, Carvalho CR. Airway epithelium mediates the anti-inflammatory effects of exercises on asthma. Respir Physiol Neurobiol 2011; 175: 383-389
    CrossrefPubMedSuche in Google Scholar
  • 46 Vrugt B, Wilson S, Bron A, Holgate ST, Djukanovic R, Aalbers R. Bronchial angiogenesis in severe glucocorticoid-dependent asthma. Eur Respir J 2000; 15: 1014-1021
    CrossrefPubMedSuche in Google Scholar
  • 47 Webb DC, McKenzie AN, Koskinen AM, Yang M, Mattes J, Foster PS. Integrated signals between IL-3, IL-4 and IL-5 regulate airways hyperreactivity. J Immunol 2000; 165: 108-113
    CrossrefPubMedSuche in Google Scholar
  • 48 Zebrowski BK, Yano S, Liu W, Hicklin DJ, Putnam Jr JB, Ellis LM. Vascular endothelial growth factor levels and induction of permeability in malignant pleural effusions. Clin Cancer Res 1999; 5: 3364-3368
    PubMedSuche in Google Scholar