Influenza A infection enhances antigen-induced airway inflammation and hyperresponsiveness in young but not aged mice

Clinical and Experimental Allergy

Volumn 44, Issue 9, 2014, Pages 1188-1199

  Birmingham, J M ^a   Gillespie, V L ^a   Srivastava, K ^a   Li, X M ^a   Busse, P J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Asthma; Influenza; Murine model

Indexed keywords

EOTAXIN; EOTAXIN 2; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; INTERLEUKIN 13; INTERLEUKIN 5; INTERLEUKIN 8; OVALBUMIN; RANTES; TUMOR NECROSIS FACTOR ALPHA; ANTIGEN; CYTOKINE;

AGE; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EOSINOPHIL; FEMALE; HISTOPATHOLOGY; INFLUENZA A; INFLUENZA VIRUS A; LEUKOCYTE; LUNG PARENCHYMA; MORBIDITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY TRACT ALLERGY; RESPIRATORY TRACT INFLAMMATION; VIRAL RESPIRATORY TRACT INFECTION; ANIMAL; ASTHMA; COMPLICATION; DISEASE MODEL; IMMUNOLOGY; LEUKOCYTE COUNT; LUNG; LUNG LAVAGE; METABOLISM; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; VIROLOGY;

AGE FACTORS; ANIMALS; ANTIGENS; ASTHMA; BRONCHOALVEOLAR LAVAGE FLUID; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; IMMUNOGLOBULIN E; INFLUENZA A VIRUS; LEUKOCYTE COUNT; LUNG; MICE; ORTHOMYXOVIRIDAE INFECTIONS; OVALBUMIN; RESPIRATORY HYPERSENSITIVITY;

EID: 84906222385     PISSN: 09547894     EISSN: 13652222     Source Type: Journal    
DOI: 10.1111/cea.12365     Document Type: Article

References (40)

1. Moorman JE, Rudd RA, Johnson CA et al. National surveillance for asthma-United States, 1980-2004. MMWR Surveill Summ 2007; 56:1-54.
2. Bauer BA, Reed CE, Yunginger JW, Wollan PC, Silverstein MD. Incidence and outcomes of asthma in the elderly. A population-based study in Rochester, Minnesota. Chest 1997; 111:303-10.
3. Nafstad P, Brunekreef B, Skrondal A, Nystad W. Early respiratory infections, asthma, and allergy: 10-year follow-up of the Oslo Birth Cohort. Pediatrics 2005; 116:e255-62.
4. Sigurs N, Gustafsson PM, Bjarnason R et al. Severe respiratory syncytial virus bronchiolitis in infancy and asthma and allergy at age 13. Am J Respir Crit Care Med 2005; 171:137-41.
5. Stein RT, Sherrill D, Morgan WJ et al. Respiratory syncytial virus in early life and risk of wheeze and allergy by age 13 years. Lancet 1999; 354:541-5.
6. Hollams EM, Deverell M, Serralha M et al. Elucidation of asthma phenotypes in atopic teenagers through parallel immunophenotypic and clinical profiling. J Allergy Clin Immunol 2009; 124:463-70, 70 e1-16.
7. Lemanske RF Jr, Jackson DJ, Gangnon RE et al. Rhinovirus illnesses during infancy predict subsequent childhood wheezing. J Allergy Clin Immunol 2005; 116:571-7.
8. Kusel MM, de Klerk NH, Holt PG, Kebadze T, Johnston SL, Sly PD. Role of respiratory viruses in acute upper and lower respiratory tract illness in the first year of life: a birth cohort study. Pediatr Infect Dis J 2006; 25:680-6.
9. Kusel MM, de Klerk NH, Kebadze T et al. Early-life respiratory viral infections, atopic sensitization, and risk of subsequent development of persistent asthma. J Allergy Clin Immunol 2007; 119:1105-10.
10. Holt PG, Strickland DH, Sly PD. Virus infection and allergy in the development of asthma: what is the connection? Curr Opin Allergy Clin Immunol 2012; 12:151-7.
11. Flurkey KCJ, Harrison DE. The mouse in aging research. In: Fox J, ed. The mouse in biomedical research: American college laboratory animal medicine (Elsevier). MA: Burlington, 2007:637-72.
12. Moltedo B, Lopez CB, Pazos M, Becker MI, Hermesh T, Moran TM. Cutting edge: stealth influenza virus replication precedes the initiation of adaptive immunity. J Immunol 2009; 183:3569-73.
13. GeurtsvanKessel CH, Willart MA, van Rijt LS et al. Clearance of influenza virus from the lung depends on migratory langerin+CD11b- but not plasmacytoid dendritic cells. J Exp Med 2008; 205:1621-34.
14. Toapanta FR, Ross TM. Impaired immune responses in the lungs of aged mice following influenza infection. Respir Res 2009; 10:112.
15. Bochner BS, Busse WW. Allergy and asthma. J Allergy Clin Immunol 2005; 115:953-9.
16. Gueders MM, Paulissen G, Crahay C et al. Mouse models of asthma: a comparison between C57BL/6 and BALB/c strains regarding bronchial responsiveness, inflammation, and cytokine production. Inflamm Res 2009; 58:845-54.
17. NAEPP Working Group Report: Considerations for Diagnosis and Managing Asthma in the Elderly. NIH, National Heart, Lung and Blood Institute, 1996.
18. Moran TM, Isobe H, Fernandez-Sesma A, Schulman JL. Interleukin-4 causes delayed virus clearance in influenza virus-infected mice. J Virol 1996; 70:5230-5.
19. Moran TM, Park H, Fernandez-Sesma A, Schulman JL. Th2 responses to inactivated influenza virus can be converted to Th1 responses and facilitate recovery from heterosubtypic virus infection. J Infect Dis 1999; 180:579-85.
20. Williams-Bey Y, Jiang J, Murasko DM. Expansion of regulatory T cells in aged mice following influenza infection. Mech Ageing Dev 2011; 132:163-70.
21. Murasko DM, Jiang J. Response of aged mice to primary virus infections. Immunol Rev 2005; 205:285-96.
22. Busse PJ, Zhang TF, Srivastava K, Schofield B, Li XM. Effect of ageing on pulmonary inflammation, airway hyperresponsiveness and T and B cell responses in antigen-sensitized and -challenged mice. Clin Exp Allergy 2007; 37:1392-403.
23. Birmingham JM, Patil S, Li XM, Busse PJ. The effect of oral tolerance on the allergic airway response in younger and aged mice. J Asthma 2013; 50:122-32.
24. Busse PJ, Lurslurchachai L, Sampson HA, Halm EA, Wisnivesky J. Perennial allergen-specific immunoglobulin E levels among inner-city elderly asthmatics. J Asthma 2010; 47(7):781-5.
25. Wohlleben G, Muller J, Tatsch U et al. Influenza A virus infection inhibits the efficient recruitment of Th2 cells into the airways and the development of airway eosinophilia. J Immunol 2003; 170:4601-11.
26. Al-Garawi AA, Fattouh R, Walker TD et al. Acute, but not resolved, influenza A infection enhances susceptibility to house dust mite-induced allergic disease. J Immunol 2009; 182:3095-104.
27. Hansen JS, Alberg T, Rasmussen H, Lovik M, Nygaard UC. Determinants of experimental allergic responses: interactions between allergen dose, sex and age. Scand J Immunol 2011; 73:554-67.
28. Zhang Y, Lamm WJ, Albert RK, Chi EY, Henderson WR Jr, Lewis DB. Influence of the route of allergen administration and genetic background on the murine allergic pulmonary response. Am J Respir Crit Care Med 1997; 155:661-9.
29. Garcia CC, Weston-Davies W, Russo RC et al. Complement C5 activation during influenza A infection in mice contributes to neutrophil recruitment and lung injury. PLoS ONE 2013; 8:e64443.
30. Chang YJ, Kim HY, Albacker LA et al. Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nat Immunol 2011; 12:631-8.
31. Mathur SK, Schwantes EA, Jarjour NN, Busse WW. Age-related changes in eosinophil function in human subjects. Chest 2008; 133:412-9.
32. Folkerts G, Busse WW, Nijkamp FP, Sorkness R, Gern JE. Virus-induced airway hyperresponsiveness and asthma. Am J Respir Crit Care Med 1998; 157:1708-20.
33. Matsumoto K, Aizawa H, Inoue H, Koto H, Nakano H, Hara N. Role of neutrophil elastase in ozone-induced airway responses in guinea-pigs. Eur Respir J 1999; 14:1088-94.
34. Busse WW, Vrtis RF, Steiner R, Dick EC. In vitro incubation with influenza virus primes human polymorphonuclear leukocyte generation of superoxide. Am J Respir Cell Mol Biol 1991; 4:347-54.
35. Aeffner F, Traylor ZP, Yu EN, Davis IC. Double-stranded RNA induces similar pulmonary dysfunction to respiratory syncytial virus in BALB/c mice. Am J Physiol Lung Cell Mol Physiol 2011; 301:L99-109.
36. Wolk KE, Lazarowski ER, Traylor ZP et al. Influenza A virus inhibits alveolar fluid clearance in BALB/c mice. Am J Respir Crit Care Med 2008; 178:969-76.
37. Bozanich EM, Gualano RC, Zosky GR et al. Acute Influenza A infection induces bronchial hyper-responsiveness in mice. Respir Physiol Neurobiol 2008; 162:190-6.
38. Nie Z, Scott GD, Weis PD, Itakura A, Fryer AD, Jacoby DB. Role of TNF-alpha in virus-induced airway hyperresponsiveness and neuronal M(2) muscarinic receptor dysfunction. Br J Pharmacol 2011; 164:444-52.
39. Solana R, Tarazona R, Gayoso I, Lesur O, Dupuis G, Fulop T. Innate immunosenescence: effect of aging on cells and receptors of the innate immune system in humans. Semin Immunol 2012; 24:331-41.
40. Lee HK, Lim MY, Bok SM et al. Age differences in cholinergic airway responsiveness in relation with muscarinic receptor subtypes. Life Sci 2007; 81:204-9.