Viruses exacerbating chronic pulmonary disease: The role of immune modulation

BMC Medicine

Volumn 10, Issue , 2012, Pages

  Singanayagam, Aran ^a,b   Joshi, Priya V ^b   Mallia, Patrick ^a,b   Johnston, Sebastian L ^a,b  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^b IMPERIAL COLLEGE HEALTHCARE NHS TRUST   (United Kingdom)

Author keywords

Asthma; Chronic obstructive pulmonary disease; Cystic fibrosis; Interferon; Respiratory viruses; Rhinovirus

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; LEUKOTRIENE B4; NITRIC OXIDE; RETINOIC ACID INDUCIBLE PROTEIN I; SECRETORY LEUKOCYTE PROTEINASE INHIBITOR; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TRANSMEMBRANE CONDUCTANCE REGULATOR;

ASTHMA; BACTERIAL VIRULENCE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CYTOKINE PRODUCTION; DISEASE EXACERBATION; HAEMOPHILUS INFLUENZAE; HUMAN; IMMUNOFLUORESCENCE TEST; IMMUNOMODULATION; INNATE IMMUNITY; LUNG FIBROSIS; NONHUMAN; PARAINFLUENZA VIRUS; PEAK EXPIRATORY FLOW; PSEUDOMONAS AERUGINOSA; REVIEW; RHINOVIRUS INFECTION; VIRAL CLEARANCE; VIRAL RESPIRATORY TRACT INFECTION; VIRUS ENTRY; VIRUS LOAD; VIRUS REPLICATION; CHRONIC DISEASE; CYSTIC FIBROSIS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; LUNG DISEASE; PATHOGENICITY; PATHOLOGY; VIROLOGY; VIRUS; VIRUS INFECTION;

ASTHMA; CHRONIC DISEASE; CYSTIC FIBROSIS; HOST-PATHOGEN INTERACTIONS; HUMANS; LUNG DISEASES; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; VIRUS DISEASES; VIRUSES;

EID: 84858114622     PISSN: None     EISSN: 17417015     Source Type: Journal    
DOI: 10.1186/1741-7015-10-27     Document Type: Review

References (118)

1. Yach D, Hawkes C, Gould CL, Hofman KJ. The global burden of chronic diseases: overcoming impediments to prevention and control. JAMA 2004, 291:2616-2622. 10.1001/jama.291.21.2616, 15173153.
2. Mathers CD, Loncar D. Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med 2006, 3:e442. 10.1371/journal.pmed.0030442, 1664601, 17132052.
3. Sigurs N, Bjarnason R, Sigurbergsson F, Kjellman B. Respiratory syncytial virus bronchiolitis in infancy is an important risk factor for asthma and allergy at age 7. Am J Respir Crit Care Med 2000, 161:1501-1507.
4. Jackson DJ, Gangnon RE, Evans MD, Roberg KA, Anderson EL, Pappas TE, Printz MC, Lee WM, Shult PA, Reisdorf E, Carlson-Dakes KT, Salazar LP, DaSilva DF, Tisler CJ, Gern JE, Lemanske RF. Wheezing rhinovirus illnesses in early life predict asthma development in high- risk children. Am J Respir Crit Care Med 2008, 178:667-672. 10.1164/rccm.200802-309OC, 2556448, 18565953.
5. Thomsen SF, van der Sluis S, Stensballe LG, Posthuma D, Skytthe A, Kyvik KO, Duffy DL, Backer V, Bisgaard H. Exploring the association between severe respiratory syncytial virus infection and asthma: a registry- based twin study. Am J Respir Crit Care Med 2009, 179:1091-1097. 10.1164/rccm.200809-1471OC, 19286626.
6. Jackson DJ, Evans MD, Gangnon RE, Tisler CJ, Pappas TE, Lee WM, Gern JE, Lemanske RF. Evidence for a causal relationship between allergic sensitization and rhinovirus wheezing in early life. Am J Respir Crit Care Med 2012, 185:281-285. 10.1164/rccm.201104-0660OC, 21960534.
7. Stein RT, Martinez FD. Respiratory syncytial virus and asthma: still no final answer. Thorax 2010, 65:1033-1034. 10.1136/thx.2009.133967, 20978023.
8. Masoli M, Fabian D, Holt S, Beasley R. The global burden of asthma: executive summary of the GINA Dissemination Committee report. Allergy 2004, 59:469-478. 10.1111/j.1398-9995.2004.00526.x, 15080825.
9. Pauwels RA, Lofdahl CG, Postma DS, Tattersfield AE, O'Byrne P, Barnes PJ, Ullman A. Effect of inhaled formoterol and budesonide on exacerbations of asthma. Formoterol and Corticosteroids Establishing Therapy (FACET) International Study Group. N Engl J Med 1997, 337:1405-1411. 10.1056/NEJM199711133372001, 9358137.
10. Moore WC, Bleecker ER, Curran-Everett D, Erzurum SC, Ameredes BT, Bacharier L, Calhoun WJ, Castro M, Chung KF, Clark MP, Dweik RA, Fitzpatrick AM, Gaston B, Hew M, Hussain I, Jarjour NN, Israel E, Levy BD, Murphy JR, Peters SP, Teague WG, Meyers DA, Busse WW, Wenzel SE. Characterization of the severe asthma phenotype by the National Heart, Lung, and Blood Institute's Severe Asthma Research Program. J Allergy Clin Immunol 2007, 119:405-413. 10.1016/j.jaci.2006.11.639, 2837934, 17291857.
11. Peters SP, Jones CA, Haselkorn T, Mink DR, Valacer DJ, Weiss ST. Real- world Evaluation of Asthma Control and Treatment (REACT): findings from a national web- based survey. J Allergy Clin Immunol 2007, 119:1454-1461. 10.1016/j.jaci.2007.03.022, 17481716.
12. Rabe KF, Vermeire PA, Soriano JB, Maier WC. Clinical management of asthma in 1999: the Asthma Insights and Reality in Europe (AIRE) study. Eur Respir J 2000, 16:802-807. 10.1183/09031936.00.16580200, 11153575.
13. Johnston SL, Sanderson G, Pattemore PK, Smith S, Bardin PG, Bruce CB, Lambden PR, Tyrrell DA, Holgate ST. Use of polymerase chain reaction for diagnosis of picornavirus infection in subjects with and without respiratory symptoms. J Clin Microbiol 1993, 31:111-117. 262631, 8380179.
14. Leung TF, To MY, Yeung AC, Wong YS, Wong GW, Chan PK. Multiplex molecular detection of respiratory pathogens in children with asthma exacerbation. Chest 2010, 137:348-354. 10.1378/chest.09-1250, 19749009.
15. Lee WM, Kiesner C, Pappas T, Lee I, Grindle K, Jartti T, Jakiela B, Lemanske RF, Shult PA, Gern JE. A diverse group of previously unrecognized human rhinoviruses are common causes of respiratory illnesses in infants. PLoS ONE 2007, 2:e966. 10.1371/journal.pone.0000966, 1989136, 17912345.
16. Khetsuriani N, Kazerouni NN, Erdman DD, Lu X, Redd SC, Anderson LJ, Teague WG. Prevalence of viral respiratory tract infections in children with asthma. J Allergy Clin Immunol 2007, 119:314-321. 10.1016/j.jaci.2006.08.041, 17140648.
17. Green RM, Custovic A, Sanderson G, Hunter J, Johnston SL, Woodcock AA. Synergism between allergens and viruses and risk of hospital admission with asthma: case- control study. BMJ 2002, 324:763. 100316, 11923159.
18. Murray CS, Poletti G, Kebadze T, Morris J, Woodcock A, Johnston SL, Custovic A. Study of modifiable risk factors for asthma exacerbations: virus infection and allergen exposure increase the risk of asthma hospital admissions in children. Thorax 2006, 61:376-382. 10.1136/thx.2005.042523, 2111190, 16384881.
19. Chauhan AJ, Inskip HM, Linaker CH, Smith S, Schreiber J, Johnston SL, Holgate ST. Personal exposure to nitrogen dioxide (NO2) and the severity of virus- induced asthma in children. Lancet 2003, 361:1939-1944. 10.1016/S0140-6736(03)13582-9, 12801737.
20. Corne JM, Marshall C, Smith S, Schreiber J, Sanderson G, Holgate ST, Johnston SL. Frequency, severity, and duration of rhinovirus infections in asthmatic and non-asthmatic individuals: a longitudinal cohort study. Lancet 2002, 359:831-834. 10.1016/S0140-6736(02)07953-9, 11897281.
21. Message SD, Laza-Stanca V, Mallia P, Parker HL, Zhu J, Kebadze T, Contoli M, Sanderson G, Kon OM, Papi A, Jeffery PK, Stanciu LA, Johnston SL. 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 USA 2008, 105:13562-13567. 10.1073/pnas.0804181105, 2528869, 18768794.
22. Slater L, Bartlett NW, Haas JJ, Zhu J, Message SD, Walton RP, Sykes A, Dahdaleh S, Clarke DL, Belvisi MG, Kon OM, Fujita T, Jeffery PK, Johnston SL, Edwards MR. Co- ordinated role of TLR3, RIG- I and MDA5 in the innate response to rhinovirus in bronchial epithelium. PLoS Pathog 2010, 6:e1001178. 10.1371/journal.ppat.1001178, 2973831, 21079690.
23. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, Taira K, Akira S, Fujita T. The RNA helicase RIG- I has an essential function in double- stranded RNA-induced innate antiviral responses. Nat Immunol 2004, 5:730-737. 10.1038/ni1087, 15208624.
24. Zhu Z, Tang W, Gwaltney JM, Wu Y, Elias JA. Rhinovirus stimulation of interleukin- 8 in vivo and in vitro: role of NF- kappaB. Am J Physiol 1997, 273:L814-L824.
25. Edwards MR, Haas J, Panettieri RA, Johnson M, Johnston SL. Corticosteroids and beta2 agonists differentially regulate rhinovirus- induced interleukin- 6 via distinct Cis- acting elements. J Biol Chem 2007, 282:15366-15375. 10.1074/jbc.M701325200, 17395587.
26. Spurrell JC, Wiehler S, Zaheer RS, Sanders SP, Proud D. Human airway epithelial cells produce IP- 10 (CXCL10) in vitro and in vivo upon rhinovirus infection. Am J Physiol Lung Cell Mol Physiol 2005, 289:L85-L95. 10.1152/ajplung.00397.2004, 15764644.
27. Zhu Z, Tang W, Ray A, Wu Y, Einarsson O, Landry ML, Gwaltney J, Elias JA. Rhinovirus stimulation of interleukin- 6 in vivo and in vitro. Evidence for nuclear factor kappa B-dependent transcriptional activation. J Clin Invest 1996, 97:421-430. 10.1172/JCI118431, 507033, 8567963.
28. Ieki K, Matsukura S, Kokubu F, Kimura T, Kuga H, Kawaguchi M, Odaka M, Suzuki S, Watanabe S, Takeuchi H, Schleimer RP, Adachi M. Double- stranded RNA activates RANTES gene transcription through co- operation of nuclear factor- kappaB and interferon regulatory factors in human airway epithelial cells. Clin Exp Allergy 2004, 34:745-752. 10.1111/j.1365-2222.2004.1941.x, 15144466.
29. Biron CA, Nguyen KB, Pien GC, Cousens LP, Salazar-Mather TP. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu Rev Immunol 1999, 17:189-220. 10.1146/annurev.immunol.17.1.189, 10358757.
30. Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK, Langer JA, Sheikh F, Dickensheets H, Donnelly RP. IFN- lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol 2003, 4:69-77.
31. Wark PA, Johnston SL, Bucchieri F, Powell R, Puddicombe S, Laza-Stanca V, Holgate ST, Davies DE. Asthmatic bronchial epithelial cells have a deficient innate immune response to infection with rhinovirus. J Exp Med 2005, 201:937-947. 10.1084/jem.20041901, 2213100, 15781584.
32. Cakebread JA, Xu Y, Grainge C, Kehagia V, Howarth PH, Holgate ST, Davies DE. Exogenous IFN- beta has antiviral and anti- inflammatory properties in primary bronchial epithelial cells from asthmatic subjects exposed to rhinovirus. J Allergy Clin Immunol 2011, 127:1148-1154. 10.1016/j.jaci.2011.01.023, 21329968.
33. Wark PA, Grissell T, Davies B, See H, Gibson PG. Diversity in the bronchial epithelial cell response to infection with different rhinovirus strains. Respirology 2009, 14:180-186. 10.1111/j.1440-1843.2009.01480.x, 19207121.
34. Gehlhar K, Bilitewski C, Reinitz-Rademacher K, Rohde G, Bufe A. Impaired virus- induced interferon- alpha2 release in adult asthmatic patients. Clin Exp Allergy 2006, 36:331-337. 10.1111/j.1365-2222.2006.02450.x, 16499644.
35. Bufe A, Gehlhar K, Grage-Griebenow E, Ernst M. Atopic phenotype in children is associated with decreased virus- induced interferon- alpha release. Int Arch Allergy Immunol 2002, 127:82-88. 10.1159/000048173, 11893858.
36. Roponen M, Yerkovich ST, Hollams E, Sly PD, Holt PG, Upham JW. Toll- like receptor 7 function is reduced in adolescents with asthma. Eur Respir J 2010, 35:64-71. 10.1183/09031936.00172008, 19643938.
37. Gill MA, Bajwa G, George TA, Dong CC, Dougherty II, Jiang N, Gan VN, Gruchalla RS. Counterregulation between the FcepsilonRI pathway and antiviral responses in human plasmacytoid dendritic cells. J Immunol 2010, 184:5999-6006. 10.4049/jimmunol.0901194, 20410486.
38. Contoli M, Message SD, Laza-Stanca V, Edwards MR, Wark PA, Bartlett NW, Kebadze T, Mallia P, Stanciu LA, Parker HL, Slater L, Lewis-Antes A, Kon OM, Holgate ST, Davies DE, Kotenko SV, Papi A, Johnston SL. Role of deficient type III interferon- lambda production in asthma exacerbations. Nat Med 2006, 12:1023-1026. 10.1038/nm1462, 16906156.
39. Bochkov YA, Hanson KM, Keles S, Brockman-Schneider RA, Jarjour NN, Gern JE. Rhinovirus- induced modulation of gene expression in bronchial epithelial cells from subjects with asthma. Mucosal Immunol 2010, 3:69-80. 10.1038/mi.2009.109, 2884103, 19710636.
40. Lopez-Souza N, Favoreto S, Wong H, Ward T, Yagi S, Schnurr D, Finkbeiner WE, Dolganov GM, Widdicombe JH, Boushey HA, Avila PC. In vitro susceptibility to rhinovirus infection is greater for bronchial than for nasal airway epithelial cells in human subjects. J Allergy Clin Immunol 2009, 123:1384-1390. 10.1016/j.jaci.2009.03.010, 2744461, 19428098.
41. DeMore JP, Weisshaar EH, Vrtis RF, Swenson CA, Evans MD, Morin A, Hazel E, Bork JA, Kakumanu S, Sorkness R, Busse WW, Gern JE. Similar colds in subjects with allergic asthma and nonatopic subjects after inoculation with rhinovirus- 16. J Allergy Clin Immunol 2009, 124:245-252. 10.1016/j.jaci.2009.05.030, 2737589, 19596142.
42. Piganis RA, De Weerd NA, Gould JA, Schindler CW, Mansell A, Nicholson SE, Hertzog PJ. Suppressor of cytokine signaling (SOCS) 1 inhibits type I interferon (IFN) signaling via the interferon alpha receptor (IFNAR1)- associated tyrosine kinase Tyk2. J Biol Chem 2011, 286:33811-33818. 10.1074/jbc.M111.270207, 21757742.
43. Lee C, Kolesnik TB, Caminschi I, Chakravorty A, Carter W, Alexander WS, Jones J, Anderson GP, Nicholson SE. Suppressor of cytokine signalling 1 (SOCS1) is a physiological regulator of the asthma response. Clin Exp Allergy 2009, 39:897-907. 10.1111/j.1365-2222.2009.03217.x, 19309352.
44. Fukuyama S, Nakano T, Matsumoto T, Oliver BG, Burgess JK, Moriwaki A, Tanaka K, Kubo M, Hoshino T, Tanaka H, McKenzie AN, Matsumoto K, Aizawa H, Nakanishi Y, Yoshimura A, Black JL, Inoue H. Pulmonary suppressor of cytokine signaling- 1 induced by IL- 13 regulates allergic asthma phenotype. Am J Respir Crit Care Med 2009, 179:992-998. 10.1164/rccm.200806-992OC, 19299500.
45. Fleming HE, Little FF, Schnurr D, Avila PC, Wong H, Liu J, Yagi S, Boushey HA. Rhinovirus-16 colds in healthy and in asthmatic subjects: similar changes in upper and lower airways. Am J Respir Crit Care Med 1999, 160:100-108.
46. de Kluijver J, Grunberg K, Pons D, de Klerk EP, Dick CR, Sterk PJ, Hiemstra PS. Interleukin-1beta and interleukin- 1ra levels in nasal lavages during experimental rhinovirus infection in asthmatic and non- asthmatic subjects. Clin Exp Allergy 2003, 33:1415-1418. 10.1046/j.1365-2222.2003.01770.x, 14519149.
47. Grunberg K, Smits HH, Timmers MC, de Klerk EP, Dolhain RJ, Dick EC, Hiemstra PS, Sterk PJ. Experimental rhinovirus 16 infection. Effects on cell differentials and soluble markers in sputum in asthmatic subjects. Am J Respir Crit Care Med 1997, 156:609-616.
48. Grissell TV, Powell H, Shafren DR, Boyle MJ, Hensley MJ, Jones PD, Whitehead BF, Gibson PG. Interleukin- 10 gene expression in acute virus- induced asthma. Am J Respir Crit Care Med 2005, 172:433-439. 10.1164/rccm.200412-1621OC, 15894599.
49. Norzila MZ, Fakes K, Henry RL, Simpson J, Gibson PG. Interleukin- 8 secretion and neutrophil recruitment accompanies induced sputum eosinophil activation in children with acute asthma. Am J Respir Crit Care Med 2000, 161:769-774.
50. Wark PA, Johnston SL, Moric I, Simpson JL, Hensley MJ, Gibson PG. Neutrophil degranulation and cell lysis is associated with clinical severity in virus- induced asthma. Eur Respir J 2002, 19:68-75. 10.1183/09031936.02.00226302, 11852895.
51. Denlinger LC, Sorkness RL, Lee WM, Evans M, Wolff M, Mathur SK, Crisafi GM, Gaworski KL, Pappas TE, Vrtis RF, Kelly EA, Gern JE, Jarjour NN. Lower airway rhinovirus burden and the seasonal risk of asthma exacerbation. Am J Respir Crit Care Med 2011,
52. Ordonez CL, Shaughnessy TE, Matthay MA, Fahy JV. Increased neutrophil numbers and IL- 8 levels in airway secretions in acute severe asthma: Clinical and biologic significance. Am J Respir Crit Care Med 2000, 161:1185-1190.
53. 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, 80:8248-8258. 10.1128/JVI.00162-06, 1563804, 16873280.
54. Fraenkel DJ, Bardin PG, Sanderson G, Lampe F, Johnston SL, Holgate ST. Lower airways inflammation during rhinovirus colds in normal and in asthmatic subjects. Am J Respir Crit Care Med 1995, 151:879-886.
55. Laza-Stanca V, Message SD, Edwards MR, Parker HL, Zdrenghea MT, Kebadze T, Kon OM, Mallia P, Stanciu LA, Johnston SL. The role of IL- 15 deficiency in the pathogenesis of virus- induced asthma exacerbations. PLoS Pathog 2011, 7:e1002114. 10.1371/journal.ppat.1002114, 3136447, 21779162.
56. Plummeridge MJ, Armstrong L, Birchall MA, Millar AB. Reduced production of interleukin 12 by interferon gamma primed alveolar macrophages from atopic asthmatic subjects. Thorax 2000, 55:842-847. 10.1136/thorax.55.10.842, 1745617, 10992536.
57. Ho LP, Davis M, Denison A, Wood FT, Greening AP. Reduced interleukin- 18 levels in BAL specimens from patients with asthma compared to patients with sarcoidosis and healthy control subjects. Chest 2002, 121:1421-1426. 10.1378/chest.121.5.1421, 12006423.
58. Gern JE, Vrtis R, Grindle KA, Swenson C, Busse WW. Relationship of upper and lower airway cytokines to outcome of experimental rhinovirus infection. Am J Respir Crit Care Med 2000, 162:2226-2231.
59. Guerra S, Lohman IC, Halonen M, Martinez FD, Wright AL. Reduced interferon gamma production and soluble CD14 levels in early life predict recurrent wheezing by 1 year of age. Am J Respir Crit Care Med 2004, 169:70-76.
60. Stern DA, Guerra S, Halonen M, Wright AL, Martinez FD. Low IFN- gamma production in the first year of life as a predictor of wheeze during childhood. J Allergy Clin Immunol 2007, 120:835-841. 10.1016/j.jaci.2007.05.050, 17689598.
61. Gern JE, Brooks GD, Meyer P, Chang A, Shen K, Evans MD, Tisler C, Dasilva D, Roberg KA, Mikus LD, Rosenthal LA, Kirk CJ, Shult PA, Bhattacharya A, Li Z, Gangnon R, Lemanske RF. Bidirectional interactions between viral respiratory illnesses and cytokine responses in the first year of life. J Allergy Clin Immunol 2006, 117:72-78. 10.1016/j.jaci.2005.10.002, 16387587.
62. Pauwels RA, Buist AS, Calverley PM, Jenkins CR, Hurd SS, . The GOLD Scientific Committee Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease. NHLBI/WHO Global Initiative for Chronic Obstructive Lung Disease (GOLD) Workshop summary. Am J Respir Crit Care Med 2001, 163:1256-1276. The GOLD Scientific Committee.
63. Hurst JR, Vestbo J, Anzueto A, Locantore N, Mullerova H, Tal-Singer R, Miller B, Lomas DA, Agusti A, Macnee W, Calverley P, Rennard S, Wouters EF, Wedzicha JA, . Evaluation of COPD Longitudinally to Identify Predictive Surrogate Endpoints (ECLIPSE) Investigators Susceptibility to exacerbation in chronic obstructive pulmonary disease. N Engl J Med 2010, 363:1128-1138. 10.1056/NEJMoa0909883, 20843247, Evaluation of COPD Longitudinally to Identify Predictive Surrogate Endpoints (ECLIPSE) Investigators.
64. Kanner RE, Anthonisen NR, Connett JE, . The Lung Health Study Research Group Lower respiratory illnesses promote FEV(1) decline in current smokers but not ex- smokers with mild chronic obstructive pulmonary disease: results from the lung health study. Am J Respir Crit Care Med 2001, 164:358-364. The Lung Health Study Research Group.
65. Seemungal TA, Donaldson GC, Paul EA, Bestall JC, Jeffries DJ, Wedzicha JA. Effect of exacerbation on quality of life in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1998, 157:1418-1422.
66. Jenkins CR, Celli B, Anderson JA, Ferguson GT, Jones PW, Vestbo J, Yates JC, Calverley PM. Seasonality and determinants of moderate and severe COPD exacerbations in the TORCH study. Eur Respir J 2012, 39:38-45. 10.1183/09031936.00194610, 21737561.
67. Seemungal T, Harper-Owen R, Bhowmik A, Moric I, Sanderson G, Message S, Maccallum P, Meade TW, Jeffries DJ, Johnston SL, Wedzicha JA. Respiratory viruses, symptoms, and inflammatory markers in acute exacerbations and stable chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2001, 164:1618-1623.
68. Smith CB, Golden CA, Kanner RE, Renzetti AD. Association of viral and Mycoplasma pneumoniae infections with acute respiratory illness in patients with chronic obstructive pulmonary diseases. Am Rev Respir Dis 1980, 121:225-232.
69. Buscho RO, Saxtan D, Shultz PS, Finch E, Mufson MA. Infections with viruses and Mycoplasma pneumoniae during exacerbations of chronic bronchitis. J Infect Dis 1978, 137:377-383. 10.1093/infdis/137.4.377, 206630.
70. Papi A, Bellettato CM, Braccioni F, Romagnoli M, Casolari P, Caramori G, Fabbri LM, Johnston SL. Infections and airway inflammation in chronic obstructive pulmonary disease severe exacerbations. Am J Respir Crit Care Med 2006, 173:1114-1121. 10.1164/rccm.200506-859OC, 16484677.
71. Rohde G, Wiethege A, Borg I, Kauth M, Bauer TT, Gillissen A, Bufe A, Schultze-Werninghaus G. Respiratory viruses in exacerbations of chronic obstructive pulmonary disease requiring hospitalisation: a case- control study. Thorax 2003, 58:37-42. 10.1136/thorax.58.1.37, 1746460, 12511718.
72. Qiu Y, Zhu J, Bandi V, Atmar RL, Hattotuwa K, Guntupalli KK, Jeffery PK. Biopsy neutrophilia, neutrophil chemokine and receptor gene expression in severe exacerbations of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2003, 168:968-975. 10.1164/rccm.200208-794OC, 12857718.
73. Tan WC, Xiang X, Qiu D, Ng TP, Lam SF, Hegele RG. Epidemiology of respiratory viruses in patients hospitalized with near- fatal asthma, acute exacerbations of asthma, or chronic obstructive pulmonary disease. Am J Med 2003, 115:272-277. 10.1016/S0002-9343(03)00353-X, 12967691.
74. Mohan A, Chandra S, Agarwal D, Guleria R, Broor S, Gaur B, Pandey RM. Prevalence of viral infection detected by PCR and RT- PCR in patients with acute exacerbation of COPD: a systematic review. Respirology 2010, 15:536-542. 10.1111/j.1440-1843.2010.01722.x, 20415983.
75. Mallia P, Message SD, Gielen V, Contoli M, Gray K, Kebadze T, Aniscenko J, Laza-Stanca V, Edwards MR, Slater L, Papi A, Stanciu LA, Kon OM, Johnson M, Johnston SL. Experimental rhinovirus infection as a human model of chronic obstructive pulmonary disease exacerbation. Am J Respir Crit Care Med 2011, 183:734-742. 10.1164/rccm.201006-0833OC, 3081284, 20889904.
76. Aaron SD, Angel JB, Lunau M, Wright K, Fex C, Le Saux N, Dales RE. Granulocyte inflammatory markers and airway infection during acute exacerbation of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2001, 163:349-355.
77. Fujimoto K, Yasuo M, Urushibata K, Hanaoka M, Koizumi T, Kubo K. Airway inflammation during stable and acutely exacerbated chronic obstructive pulmonary disease. Eur Respir J 2005, 25:640-646. 10.1183/09031936.05.00047504, 15802337.
78. Perera WR, Hurst JR, Wilkinson TM, Sapsford RJ, Mullerova H, Donaldson GC, Wedzicha JA. Inflammatory changes, recovery and recurrence at COPD exacerbation. Eur Respir J 2007, 29:527-534. 10.1183/09031936.00092506, 17107990.
79. Gompertz S, O'Brien C, Bayley DL, Hill SL, Stockley RA. Changes in bronchial inflammation during acute exacerbations of chronic bronchitis. Eur Respir J 2001, 17:1112-1119. 10.1183/09031936.01.99114901, 11491152.
80. Rohde G, Borg I, Wiethege A, Kauth M, Jerzinowski S, An Duong DT, Bauer TT, Bufe A, Schultz-Werninghaus G. Inflammatory response in acute viral exacerbations of COPD. Infection 2008, 36:427-433. 10.1007/s15010-008-7327-5, 18795228.
81. Seemungal TA, Harper-Owen R, Bhowmik A, Jeffries DJ, Wedzicha JA. Detection of rhinovirus in induced sputum at exacerbation of chronic obstructive pulmonary disease. Eur Respir J 2000, 16:677-683. 10.1034/j.1399-3003.2000.16d19.x, 11106212.
82. Quint JK, Donaldson GC, Goldring JJ, Baghai-Ravary R, Hurst JR, Wedzicha JA. Serum IP- 10 as a biomarker of human rhinovirus infection at exacerbation of COPD. Chest 2009, 137:812-822. 2851557, 19837822.
83. Bafadhel M, McKenna S, Terry S, Mistry V, Reid C, Haldar P, McCormick M, Haldar K, Kebadze T, Duvoix A, Lindblad K, Patel H, Rugman P, Dodson P, Jenkins M, Saunders M, Newbold P, Green RH, Venge P, Lomas DA, Barer MR, Johnston SL, Pavord ID, Brightling CE. Acute exacerbations of COPD: identification of biological clusters and their biomarkers. Am J Respir Crit Care Med 2011, 184:662-671. 10.1164/rccm.201104-0597OC, 21680942.
84. Hurst JR, Wilkinson TM, Perera WR, Donaldson GC, Wedzicha JA. Relationships among bacteria, upper airway, lower airway, and systemic inflammation in COPD. Chest 2005, 127:1219-1226. 10.1378/chest.127.4.1219, 15821198.
85. S Sajjan U, Ganesan S, Comstock AT, Shim J, Wang Q, Nagarkar DR, Zhao Y, Goldsmith AM, Sonstein J, Linn MJ, Curtis JL, Hershenson MB. Elastase-and LPS- exposed mice display altered responses to rhinovirus infection. Am J Physiol Lung Cell Mol Physiol 2009, 297:L931-L944. 10.1152/ajplung.00150.2009, 2777490, 19748999.
86. Sonnenfeld G, Hudgens RW. Effect of sidestream and mainstream smoke exposure on in vitro interferon- alpha/beta production by L- 929 cells. Cancer Res 1986, 46:2779-2783.
87. Schneider D, Ganesan S, Comstock AT, Meldrum CA, Mahidhara R, Goldsmith AM, Curtis JL, Martinez F, Hershenson MB, Sajjan U. Increased cytokine response of rhinovirus-infected airway epithelial cells in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2010, 182:332-340. 10.1164/rccm.200911-1673OC, 2921598, 20395558.
88. Di Stefano A, Maestrelli P, Roggeri A, Turato G, Calabro S, Potena A, Mapp CE, Ciaccia A, Convacev L, Fabbri LM, Saetta M. Upregulation of adhesion molecules in the bronchial mucosa of subjects with chronic obstructive bronchitis. Am J Respir Crit Care Med 1994, 149:803-810.
89. Wilkinson TM, Donaldson GC, Johnston SL, Openshaw PJ, Wedzicha JA. Respiratory syncytial virus, airway inflammation, and FEV1 decline in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2006, 173:871-876. 10.1164/rccm.200509-1489OC, 16456141.
90. Borg I, Rohde G, Loseke S, Bittscheidt J, Schultze-Werninghaus G, Stephan V, Bufe A. Evaluation of a quantitative real- time PCR for the detection of respiratory syncytial virus in pulmonary diseases. Eur Respir J 2003, 21:944-951. 10.1183/09031936.03.00088102, 12797486.
91. Sikkel MB, Quint JK, Mallia P, Wedzicha JA, Johnston SL. Respiratory syncytial virus persistence in chronic obstructive pulmonary disease. Pediatr Infect Dis J 2008, 27:S63-S70. 10.1097/INF.0b013e3181684d67, 18820581.
92. Matsuse T, Hayashi S, Kuwano K, Keunecke H, Jefferies WA, Hogg JC. Latent adenoviral infection in the pathogenesis of chronic airways obstruction. Am Rev Respir Dis 1992, 146:177-184.
93. Meshi B, Vitalis TZ, Ionescu D, Elliott WM, Liu C, Wang XD, Hayashi S, Hogg JC. Emphysematous lung destruction by cigarette smoke. The effects of latent adenoviral infection on the lung inflammatory response. Am J Respir Cell Mol Biol 2002, 26:52-57.
94. McManus TE, Marley AM, Baxter N, Christie SN, Elborn JS, Heaney LG, Coyle PV, Kidney JC. Acute and latent adenovirus in COPD. Respir Med 2007, 101:2084-2090. 10.1016/j.rmed.2007.05.015, 17631991.
95. Wang EE, Prober CG, Manson B, Corey M, Levison H. Association of respiratory viral infections with pulmonary deterioration in patients with cystic fibrosis. N Engl J Med 1984, 311:1653-1658. 10.1056/NEJM198412273112602, 6504106.
96. Ong EL, Ellis ME, Webb AK, Neal KR, Dodd M, Caul EO, Burgess S. Infective respiratory exacerbations in young adults with cystic fibrosis: role of viruses and atypical microorganisms. Thorax 1989, 44:739-742. 10.1136/thx.44.9.739, 462055, 2588211.
97. Smyth AR, Smyth RL, Tong CY, Hart CA, Heaf DP. Effect of respiratory virus infections including rhinovirus on clinical status in cystic fibrosis. Arch Dis Child 1995, 73:117-120. 10.1136/adc.73.2.117, 1511210, 7574853.
98. Ramsey BW, Gore EJ, Smith AL, Cooney MK, Redding GJ, Foy H. The effect of respiratory viral infections on patients with cystic fibrosis. Am J Dis Child 1989, 143:662-668.
99. Armstrong D, Grimwood K, Carlin JB, Carzino R, Hull J, Olinsky A, Phelan PD. Severe viral respiratory infections in infants with cystic fibrosis. Pediatr Pulmonol 1998, 26:371-379. 10.1002/(SICI)1099-0496(199812)26:6<371::AID-PPUL1>3.0.CO;2-N, 9888211.
100. Wat D, Gelder C, Hibbitts S, Cafferty F, Bowler I, Pierrepoint M, Evans R, Doull I. The role of respiratory viruses in cystic fibrosis. J Cyst Fibros 2008, 7:320-328. 10.1016/j.jcf.2007.12.002, 18255355.
101. de Almeida MB, Zerbinati RM, Tateno AF, Oliveira CM, Romao RM, Rodrigues JC, Pannuti CS, da Silva Filho LV. Rhinovirus C and respiratory exacerbations in children with cystic fibrosis. Emerg Infect Dis 2010, 16:996-999. 3086221, 20507756.
102. Zheng S, De BP, Choudhary S, Comhair SA, Goggans T, Slee R, Williams BR, Pilewski J, Haque SJ, Erzurum SC. Impaired innate host defense causes susceptibility to respiratory virus infections in cystic fibrosis. Immunity 2003, 18:619-630. 10.1016/S1074-7613(03)00114-6, 12753739.
103. van Ewijk BE, van der Zalm MM, Wolfs TF, Fleer A, Kimpen JL, Wilbrink B, van der Ent CK. Prevalence and impact of respiratory viral infections in young children with cystic fibrosis: prospective cohort study. Pediatrics 2008, 122:1171-1176. 10.1542/peds.2007-3139, 19047230.
104. Sutanto EN, Kicic A, Foo CJ, Stevens PT, Mullane D, Knight DA, Stick SM, . Australian Respiratory Early Surveillance Team for Cystic Fibrosis Innate inflammatory responses of pediatric cystic fibrosis airway epithelial cells: effects of nonviral and viral stimulation. Am J Respir Cell Mol Biol 2011, 44:761-767. 10.1165/rcmb.2010-0368OC, 21317379, Australian Respiratory Early Surveillance Team for Cystic Fibrosis.
105. Black HR, Yankaskas JR, Johnson LG, Noah TL. Interleukin- 8 production by cystic fibrosis nasal epithelial cells after tumor necrosis factor- alpha and respiratory syncytial virus stimulation. Am J Respir Cell Mol Biol 1998, 19:210-215.
106. Kieninger E, Vareille M, Kopf BS, Blank F, Alves MP, Gisler FM, Latzin P, Casaulta C, Geiser T, Johnston SL, Edwards MR, Regamey N. Lack of an exaggerated inflammatory response upon virus infection in cystic fibrosis. Eur Respir J 2012, 39:297-304. 10.1183/09031936.00054511, 21719483.
107. Vareille M, Kieninger E, Alves MP, Kopf BS, Moller A, Geiser T, Johnston SL, Edwards MR, Regamey N. Impaired type I and type III interferon induction and rhinovirus control in human cystic fibrosis airway epithelial cells. Thorax
108. Holtzman M, Patel D, Kim H, You Y, Zhang Y. Hypersusceptibility to respiratory viruses as a shared mechanism for asthma, chronic obstructive pulmonary disease, and cystic fibrosis. Am J Respir Cell Mol Biol 2011, 44:739-742. 10.1165/rcmb.2011-0120ED, 21653905.
109. McCullers JA. Insights into the interaction between influenza virus and pneumococcus. Clin Microbiol Rev 2006, 19:571-582. 10.1128/CMR.00058-05, 1539103, 16847087.
110. Hussell T, Cavanagh MM. The innate immune rheostat: influence on lung inflammatory disease and secondary bacterial pneumonia. Biochem Soc Trans 2009, 37:811-813. 10.1042/BST0370811, 19614599.
111. Wang JH, Kwon HJ, Jang YJ. Rhinovirus enhances various bacterial adhesions to nasal epithelial cells simultaneously. Laryngoscope 2009, 119:1406-1411. 10.1002/lary.20498, 19434681.
112. Ishizuka S, Yamaya M, Suzuki T, Takahashi H, Ida S, Sasaki T, Inoue D, Sekizawa K, Nishimura H, Sasaki H. Effects of rhinovirus infection on the adherence of Streptococcus pneumoniae to cultured human airway epithelial cells. J Infect Dis 2003, 188:1928-1939. 10.1086/379833, 14673774.
113. Sajjan U, Wang Q, Zhao Y, Gruenert DC, Hershenson MB. Rhinovirus disrupts the barrier function of polarized airway epithelial cells. Am J Respir Crit Care Med 2008, 178:1271-1281. 10.1164/rccm.200801-136OC, 2599868, 18787220.
114. Oliver BG, Lim S, Wark P, Laza-Stanca V, King N, Black JL, Burgess JK, Roth M, Johnston SL. Rhinovirus exposure impairs immune responses to bacterial products in human alveolar macrophages. Thorax 2008, 63:519-525. 10.1136/thx.2007.081752, 18245149.
115. Chattoraj SS, Ganesan S, Jones AM, Helm JM, Comstock AT, Bright-Thomas R, LiPuma JJ, l Hershenson MB, Sajjan U. Rhinovirus infection liberates planktonic bacteria from biofilm and increases chemokine responses in cystic fibrosis airway epithelial cells. Thorax 2011, 66:333-339. 10.1136/thx.2010.151431, 3208236, 21289024.
116. Sajjan US, Jia Y, Newcomb DC, Bentley JK, Lukacs NW, LiPuma JJ, Hershenson MB. H. influenzae potentiates airway epithelial cell responses to rhinovirus by increasing ICAM- 1 and TLR3 expression. FASEB J 2006, 20:2121-2123. 10.1096/fj.06-5806fje, 16914605.
117. Chattoraj SS, Ganesan S, Faris A, Comstock A, Lee WM, Sajjan US. Pseudomonas aeruginosa suppresses interferon response to rhinovirus infection in cystic fibrosis but not in normal bronchial epithelial cells. Infect Immun 2011, 79:4131-4145. 10.1128/IAI.05120-11, 21825067.
118. Hilty M, Burke C, Pedro H, Cardenas P, Bush A, Bossley C, Davies J, Ervine A, Poulter L, Pachter L, Moffatt MF, Cookson WO. Disordered microbial communities in asthmatic airways. PLoS ONE 2010, 5:e8578. 10.1371/journal.pone.0008578, 2798952, 20052417.