Clinical and Experimental Pediatrics

The Korean Pediatric Society (대한소아청소년과학회)
권호 표지
DOI QR코드

DOI QR Code

The effect of rhinovirus on airway inflammation in a murine asthma model

  • Kim, Eugene (Department of Pediatrics, The Catholic University of Korea College of Medicine) ;
  • Lee, Huisu (Department of Pediatrics, The Catholic University of Korea College of Medicine) ;
  • Kim, Hyun Sook (Department of Pediatrics, The Catholic University of Korea College of Medicine) ;
  • Won, Sulmui (Department of Pediatrics, The Catholic University of Korea College of Medicine) ;
  • Lee, Eu Kyoung (Department of Pediatrics, The Catholic University of Korea College of Medicine) ;
  • Kim, Hwan Soo (Department of Pediatrics, The Catholic University of Korea College of Medicine) ;
  • Bang, Kyongwon (Department of Pediatrics, The Catholic University of Korea College of Medicine) ;
  • Chun, Yoon Hong (Department of Pediatrics, The Catholic University of Korea College of Medicine) ;
  • Yoon, Jong-Seo (Department of Pediatrics, The Catholic University of Korea College of Medicine) ;
  • Kim, Hyun Hee (Department of Pediatrics, The Catholic University of Korea College of Medicine) ;
  • Kim, Jin Tack (Department of Pediatrics, The Catholic University of Korea College of Medicine) ;
  • Lee, Joon Sung (Department of Pediatrics, The Catholic University of Korea College of Medicine)
  • Received : 2013.05.29
  • Accepted : 2013.08.21
  • Published : 2013.11.15
Download PDF
⟨ Previous Next ⟩

Abstract

Purpose: The aim of the present study was to investigate the differences in lower airway inflammatory immune responses, including cellular responses and responses in terms of inflammatory mediators in bronchoalveolar lavage fluid (BALF) and the airway, to rhinovirus (RV) infection on asthma exacerbation by comparing a control and a murine asthma model, with or without RV infection. Methods: BALB/c mice were intraperitoneally injected with a crude extract of Dermatophagoides farinae (Df ) or phosphate buffered saline (PBS) and were subsequently intranasally treated with a crude extract of Df or PBS. Airway responsiveness and cell infiltration, differential cell counts in BALF, and cytokine and chemokine concentrations in BALF were measured 24 hours after intranasal RV1B infection. Results: RV infection increased the enhanced pause (Penh) in both the Df sensitized and challenged mice (Df mice) and PBS-treated mice (PBS mice) (P<0.05). Airway eosinophil infiltration increased in Df mice after RV infection (P<0.05). The levels of interleukin (IL) 13, tumor necrosis factor alpha, and regulated on activation, normal T cells expressed and secreted (RANTES) increased in response to RV infection in Df mice, but not in PBS mice (P<0.05). The level of IL-10 significantly decreased following RV infection in Df mice (P<0.05). Conclusion: Our findings suggest that the augmented induction of proinflammatory cytokines, Th2 cytokines, and chemokines that mediate an eosinophil response and the decreased induction of regulatory cytokines after RV infection may be important manifestations leading to airway inflammation with eosinophil infiltration and changes in airway responsiveness in the asthma model.

Keywords

References

  1. Johnston SL, Pattemore PK, Sanderson G, Smith S, Lampe F, Josephs L, et al. Community study of role of viral infections in exacerbations of asthma in 9-11 year old children. BMJ 1995;310: 1225-9. https://doi.org/10.1136/bmj.310.6989.1225
  2. Kim WK. Human rhinoviruses and asthma in children. Korean J Pediatr 2010;53:129-35. https://doi.org/10.3345/kjp.2010.53.2.129
  3. Kelly JT, Busse WW. Host immune responses to rhinovirus: mechanisms in asthma. J Allergy Clin Immunol 2008;122:671-82. https://doi.org/10.1016/j.jaci.2008.08.013
  4. Spahn JD. Asthma biomarkers in sputum. Immunol Allergy Clin North Am 2012;32:387-99. https://doi.org/10.1016/j.iac.2012.06.004
  5. Silkoff PE, Trudeau JB, Gibbs R, Wenzel S. The relationship of induced-sputum inflammatory cells to BAL and biopsy. Chest 2003;123(3 Suppl):371S-372S.
  6. Message SD, Laza-Stanca V, Mallia P, Parker HL, Zhu J, Kebadze T, et al. Rhinovirus-induced lower respiratory illness is increased in asthma and related to virus load and Th1/2 cytokine and IL-10 production. Proc Natl Acad Sci U S A 2008;105:13562-7. https://doi.org/10.1073/pnas.0804181105
  7. Nagarkar DR, Bowman ER, Schneider D, Wang Q, Shim J, Zhao Y, et al. Rhinovirus infection of allergen-sensitized and -challenged mice induces eotaxin release from functionally polarized macrophages. J Immunol 2010;185:2525-35. https://doi.org/10.4049/jimmunol.1000286
  8. Bartlett NW, Walton RP, Edwards MR, Aniscenko J, Caramori G, Zhu J, et al. Mouse models of rhinovirus-induced disease and exacerbation of allergic airway inflammation. Nat Med 2008;14:199-204. https://doi.org/10.1038/nm1713
  9. Underwood S, Foster M, Raeburn D, Bottoms S, Karlsson JA. Timecourse of antigen-induced airway inflammation in the guinea-pig and its relationship to airway hyperresponsiveness. Eur Respir J 1995;8:2104-13. https://doi.org/10.1183/109031936.95.08122104
  10. Crapster-Pregont M, Yeo J, Sanchez RL, Kuperman DA. Dendritic cells and alveolar macrophages mediate IL-13-induced airway inflammation and chemokine production. J Allergy Clin Immunol 2012;129:1621-7.e3. https://doi.org/10.1016/j.jaci.2012.01.052
  11. Xatzipsalti M, Papadopoulos NG. Cellular and animals models for rhinovirus infection in asthma. Contrib Microbiol 2007;14:33-41.
  12. Grunberg K, Smits HH, Timmers MC, de Klerk EP, Dolhain RJ, Dick EC, et al. Experimental rhinovirus 16 infection. Effects on cell differentials and soluble markers in sputum in asthmatic subjects. Am J Respir Crit Care Med 1997;156(2 Pt 1):609-16. https://doi.org/10.1164/ajrccm.156.2.9610079
  13. Pacifico L, Iacobini M, Viola F, Werner B, Mancuso G, Chiesa C. Chemokine concentrations in nasal washings of infants with rhinovirus illnesses. Clin Infect Dis 2000;31:834-8. https://doi.org/10.1086/314049
  14. Newcomb DC, Sajjan US, Nagarkar DR, Goldsmith AM, Bentley JK, Hershenson MB. Cooperative effects of rhinovirus and TNF- {alpha} on airway epithelial cell chemokine expression. Am J Physiol Lung Cell Mol Physiol 2007;293:L1021-8. https://doi.org/10.1152/ajplung.00060.2007
  15. Hutchison S, Choo-Kang BS, Bundick RV, Leishman AJ, Brewer JM, McInnes IB, et al. Tumour necrosis factor-alpha blockade suppresses murine allergic airways inflammation. Clin Exp Immunol 2008;151:114-22.
  16. Berg K, Andersen H, Owen TC. The regulation of rhinovirus infection in vitro by IL-8, HuIFN-alpha, and TNF-alpha. APMIS 2004;112:172-82. https://doi.org/10.1111/j.1600-0463.2004.apm1120303.x
  17. Laza-Stanca V, Stanciu LA, Message SD, Edwards MR, Gern JE, Johnston SL. Rhinovirus replication in human macrophages induces NF-kappaB-dependent tumor necrosis factor alpha production. J Virol 2006;80:8248-58. https://doi.org/10.1128/JVI.00162-06
  18. Kim HK, Lee CH, Kim JM, Ayush O, Im SY, Lee HK. Biphasic late airway hyperresponsiveness in a murine model of asthma. Int Arch Allergy Immunol 2013;160:173-83. https://doi.org/10.1159/000341645
  19. Wilson EB, Brooks DG. The role of IL-10 in regulating immunity to persistent viral infections. Curr Top Microbiol Immunol 2011;350:39-65.
  20. McDougall CM, Helms PJ. Neutrophil airway inflammation in childhood asthma. Thorax 2006;61:739-41.

Cited by

  1. Rhinovirus infection in murine chronic allergic rhinosinusitis model vol.6, pp.11, 2013, https://doi.org/10.1002/alr.21805
  2. Therapeutic and prophylactic activity of itraconazole against human rhinovirus infection in a murine model vol.6, pp.None, 2013, https://doi.org/10.1038/srep23110
  3. Mouse models of acute exacerbations of allergic asthma vol.21, pp.5, 2016, https://doi.org/10.1111/resp.12760
  4. Neonatal Immunity, Respiratory Virus Infections, and the Development of Asthma vol.9, pp.None, 2013, https://doi.org/10.3389/fimmu.2018.01249
  5. Viruses and non-allergen environmental triggers in asthma vol.67, pp.7, 2013, https://doi.org/10.1136/jim-2019-001000