Impaired airway epithelial cell responses from children with asthma to rhinoviral infection

Clinical and Experimental Allergy

Volumn 46, Issue 11, 2016, Pages 1441-1455

  Kicic, A ^a,b,c,d   Stevens, P T ^b,c   Sutanto, E N ^a,c   Kicic Starcevich, E ^a,c   Ling, K M ^c   Looi, K ^c   Martinovich, K M ^c   Garratt, L W ^c   Iosifidis, T ^b,d   Shaw, N C ^c   Buckley, A G ^b   Rigby, P J ^b   Lannigan, F J ^e   Knight, D A ^f,g,h   Stick, S M ^a,b,c,d  

^a PRINCESS MARGARET HOSPITAL FOR CHILDREN   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^e UNIVERSITY OF NOTRE DAME   (Australia)

^f UNIVERSITY OF NEWCASTLE   (Australia)

^g HUNTER MEDICAL RESEARCH INSTITUTE   (Australia)

^h UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

airway epithelium; asthma; human rhinovirus; wound repair

Indexed keywords

BETA INTERFERON; CORTICOSTEROID; ALLERGEN; AUTACOID; CYTOKINE; IMMUNOGLOBULIN E; VIRUS RECEPTOR;

ADOLESCENT; AIRWAY EPITHELIAL CELL; APOPTOSIS; ARTICLE; ASTHMA; CELL PROLIFERATION; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ELECTIVE SURGERY; FEMALE; HUMAN; HUMAN RHINOVIRUS B14; INFLAMMATION; INNATE IMMUNITY; MALE; PRIMARY CULTURE; PRIORITY JOURNAL; PROGENY; RHINOVIRUS INFECTION; VIRUS REPLICATION; WOUND HEALING; CELL SURVIVAL; CLASSIFICATION; COMMON COLD; COMPLICATION; DISEASE EXACERBATION; GENETICS; IMMUNOLOGY; METABOLISM; PATHOLOGY; PICORNAVIRUS INFECTION; PRESCHOOL CHILD; RESPIRATORY MUCOSA; RHINOVIRUS; VIROLOGY; VIRUS LOAD;

ADOLESCENT; ALLERGENS; APOPTOSIS; ASTHMA; CELL PROLIFERATION; CELL SURVIVAL; CHILD; CHILD, PRESCHOOL; COMMON COLD; CYTOKINES; DISEASE PROGRESSION; FEMALE; HUMANS; IMMUNOGLOBULIN E; INFLAMMATION MEDIATORS; MALE; PICORNAVIRIDAE INFECTIONS; RECEPTORS, VIRUS; RESPIRATORY MUCOSA; RHINOVIRUS; VIRAL LOAD; VIRUS REPLICATION;

EID: 84978128762     PISSN: 09547894     EISSN: 13652222     Source Type: Journal    
DOI: 10.1111/cea.12767     Document Type: Article

References (59)

1. Jackson DJ, Gangnon RE, Evans MD et al. Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children. Am J Respir Crit Care Med 2008; 178:667–72.
2. Wark PA, Johnston SL, Bucchieri F et al. Asthmatic bronchial epithelial cells have a deficient innate immune response to infection with rhinovirus. J Exp Med 2005; 201:937–47.
3. 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; 14:180–6.
4. Contoli M, Message SD, Laza-Stanca V et al. Role of deficient type III interferon-lambda production in asthma exacerbations. Nat Med 2006; 12:1023–6.
5. Lopez-Sousa N, Favoreto S, Wong H et al. In vitro susceptibility to rhinovirus infection is greater for bronchial than for nasal airway epithelial cells in human subjects. J Allergy Clin Immunol 2009; 123:1384–90.
6. 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.
7. Edwards MR, Regamey N, Vareille M et al. Impaired innate interferon induction in severe therapy resistant atopic asthmatic children. Mucosal Immunol 2013; 4:797–806.
8. Baraldo S, Contoli M, Bazzan E et al. Deficient antiviral immune responses in childhood: distinct roles of atopy and asthma. J Allergy Clin Immunol 2012; 130:1307–14.
9. Spann KM, Baturcam E, Schagen J et al. Viral and host factors determine innate immune responses in airway epithelial cells from children with wheeze and atopy. Thorax 2013; 69:918–25.
10. Australian Centre for Asthma Monitoring. Asthma in Australia 2011. AIHW Asthma Series no.4. Cat. no. ACM 22. Canberra: AIHW, 2011.
11. Asher MI, Keil U, Anderson HR et al. International Study of Asthma and Allergies in Childhood (ISAAC): rationale and methods. Eur Respir J 1995; 8:483–91.
12. Ferris BG. Epidemiology Standardization Project (American Thoracic Society). Am Rev Respir Dis 1978; 118:1–120.
13. Kicic A, Sutanto EN, Stevens PT, Knight DA, Stick SM. Intrinsic biochemical and functional differences in bronchial epithelial cells of children with asthma. Am J Respir Crit Care Med 2006; 174:1110–8.
14. Lane C, Burgess S, Kicic A, Knight DA, Stick SM. The use of non-bronchoscopic brushings to study the paediatric airway. Respir Res 2005; 6:53–63.
15. Lane C, Knight DA, Burgess S et al. Epithelial inducible nitric oxide synthase activity is the major determinant of nitric oxide concentration in exhaled breath. Thorax 2004; 59:757–60.
16. McNamara PS, Kicic A, Sutanto EN, Stevens PT, Stick SM. Comparison of techniques for obtaining lower airway epithelial cells from children. Eur Respir J 2008; 32:763–8.
17. Jakiela B, Brockman-Schneider R, Amineva S, Lee WM, Gern JE. Basal cells of differentiated bronchial epithelium are more susceptible to rhinovirus infection. Am J Respir Cell Mol Biol 2008; 38:517–23.
18. Stevens PT, Kicic A, Sutanto EN, Knight DA, Stick SM. Dysregulated repair in asthmatic paediatric airway epithelial cells: the role of plasminogen activator inhibitor-1. Clin Exp Allergy 2008; 38:1901–10.
19. Kicic A, Hallstrand TS, Sutanto EN et al. Decreased fibronectin production significantly contributes to dysregulated repair of asthmatic epithelium. Am J Respir Crit Care Med 2010; 181:889–98.
20. Vermeer PD, Einwalter LA, Moninger TO et al. Segregation of receptor and ligand regulates activation of epithelial growth factor receptor. Nature 2003; 422:322–6.
21. Sutanto EN, Kicic A, Foo CJ et al. Innate inflammatory responses of pediatric cystic fibrosis airway epithelial cells: effect of nonviral and viral stimulation. Am J Respir Cell Mol Biol 2011; 44:761–7.
22. Cory AH, Owen TC, Barltrop JA, Cory JG. Use of an aqueous soluble tetrazolium/formazan assay for cell growth assays in culture. Cancer Commun 1991; 3:207–12.
23. Taylor AL, Hale J, Hales BJ, Dunstan JA, Thomas WR, Prescott SL. FOXP3 mRNA expression at 6 months of age is higher in infants who develop atopic dermatitis, but is not affected by giving probiotics from birth. Pediatr Allergy Immunol 2007; 18:10–9.
24. Wark PA, Bucchieri F, Johnston SL et al. IFN-gamma-induced protein 10 is a novel biomarker of rhinovirus-induced asthma exacerbations. J Allergy Clin Immunol 2007; 120:586–93.
25. Message SD, Laza-Stanca V, Mallia P et al. Rhinovirus-induced lower respiratory illness is increased in asthma and related to virus load and Th1/2 cytokine and IL-10 production. PNAS 2008; 105:13562–7.
26. Johnston SL. Innate immunity in the pathogenesis of virus-induced asthma exacerbations. Proc Am Thorac Soc 2007; 4:267–70.
27. Klein KA, Jackson WT. Human rhinovirus 2 induces the autophagic pathway and replicated more efficiently in autophagic cells. J Virol 2011; 85:9651–4.
28. Petrovski G, Ayna G, Majai G et al. Phagocytosis of cell dying through autophagy induces inflammasome activation and IL-1β release in human macrophages. Autophagy 2011; 7:321–30.
29. Fink SL, Cookson BT. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun 2005; 73:1907–16.
30. Takaoka A, Hayakawa S, Yanai H et al. Integration of Interferon α/β signalling to p53 responses in tumour suppression and antiviral defence. Nature 2003; 424:516–23.
31. Khaitov MR, Laza-Stanca V, Edwards MR et al. Respiratory virus induction of alpha-, beta- and lambda-interferons in bronchial epithelial cells and peripheral blood mononuclear cells. Allergy 2009; 64:375–86.
32. Cakebread JA, Xu Y, Grainge C et al. Exogenous IFN-β has antiviral and anti-inflammatory properties in primary bronchial epithelial cells from asthmatic subjects exposed to rhinovirus. J Allergy Clin Immunol 2011; 127:1148–54.
33. Sykes A, Edwards MR, Macintyre J et al. Rhinovirus 16-induced IFα and IFNβ are deficient in bronchoalveolar lavage cells in asthmatic children. J Allergy Clin Immunol 2012; 129:1506–14.
34. Schaper F, Kirchhoff S, Posern G et al. Functional domains of interferon regulatory factor I (IRF-1). Biochem J 1998; 335:147–57.
35. Sharf R, Azriel A, Lejbkowicz F, Winograd SS, Ehrlich R, Levi BZ. Functional domain analysis of interferon consensus sequence binding protein (ICSBP) and its association with interferon regulatory factors. J Biol Chem 1995; 270:13063-9.
36. Jayakumar A, Donovan MJ, Tripathi V, Ramalho-Ortigo M, McDowell MA. Leishmania major infection activates NF-kappaB and interferon regulatory factors 1 and 8 in human dendritic cells. Infect Immun 2008; 76:2138–48.
37. Reis LFL, Harada H, Wolchok JD, Taniguchi T, Vilcek J. Critical role of a common transcription factor, IRF-1, in the regulation of IFN-β and IFN-inducible genes. EMBO J 1992; 11:185–93.
38. Fujita T, Kimura Y, Miyamoto M, Barsoumian EL, Taniguchi T. Induction of endogenous IFN-alpha and IFN-beta genes by a regulatory transcription factor, IRF-1. Nature 1989; 337:270–2.
39. Odendall C, Dixit E, Stavru F et al. Diverse intracellular pathogens activate type III interferon expression from peroxisomes. Nature Immunol 2014; 15:717–26.
40. Li P, Wong J-Y, Sum C et al. IRF8 and IRF3 copoeratively regulate rapid interferon-β induction in human blood monocytes. Blood 2011; 117:2847–2854.
41. Honda K, Yanai H, Negishi H et al. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 2005; 434:772–7.
42. Bosco A, Ehteshami S, Panyala S, Martinez FD. IRF7 is a major hub connecting interferon-mediated responses in virus-induced asthma exacerbations in vivo. J Allergy Clin Immunol 2012; 239:88–94.
43. Bosco A, Wiehler S, Proud D. Interferon regulatory factor 7 regulates airway epithelial cell responses to human rhinovirus infection. BMC Genom 2016; 17:76 doi: 10.1186/s12864-016-2405-z.
44. Kaul P, Biagioli MC, Singh I, Turner RB. Rhinovirus-induced oxidative stress and interleukin-8 elaboration involves p47-phox but is independent of attachment to intercellular adhesion molecule-1 and viral replication. J Infect Dis 2000; 181:1885–90.
45. Johnston SL, Papi A, Bates PJ, Mastronarde JG, Monick MM, Hunninghake GW. Low grade rhinovirus infection induces a prolonged release of IL-8 in pulmonary epithelium. J Immunol 1998; 160:6172–81.
46. Nicholson KG, Kent J, Ireland DC. Respiratory viruses and exacerbations of asthma in adults. BMJ 1993; 307:982–6.
47. Nakajoh M, Fukushima T, Suzuki T et al. Retinoic acid inhibits elastase-induced injury in human lung epithelial cell lines. Am J Respir Cell Mol Biol 2003; 28:296–304.
48. Mattoli S, Marini M, Fasoli A. Expression of the potent inflammatory cytokines, GM-CSF, IL6, and IL8, in bronchial epithelial cells of asthmatic patients. Chest 1992; 101:27S–9S.
49. Barnes PJ. How Corticosteroids control inflammation: Quintiles Prize Lecture 2005. Brit J Pharmacol 2006; 148:245–54.
50. Bizzintino J, Lee W-M, Liang IA, et al. Association between human rhinovirus C and severity of acute asthma in children. Eur Respir J 2011; 37:1037–1042.
51. Teichtahl H, Buckmaster M, Pertnikovs E. The incidence of respiratory tract infection in adults requiring hospitalization for asthma. Chest 1997; 112:591–6.
52. Uematsu S, Akira S. Toll-like receptors and type 1 interferons. J Biol Chem 2007; 282:15319–23.
53. Liu J, Ma A. Interferon regulatory factor 8 regulates RANTES gene transcription in cooperation with interferon regulatory factor-1, NF-κB, and PU.1. J Biol Chem 2006; 281:19188–95.
54. Yang D, Thangaraju M, Greeneltch K et al. Repression of IFN regulatory factor 8 by DNA methylation is a molecular determinant of apoptotic resistance and metastatic phenotype in metastatic tumor cells. Cancer Res 2007; 67:3301–9.
55. Yang D, Thangaraju M, Browning DD et al. Interferon regulatory factor 8 mediates apoptosis in nonhemopoietic tumor cells via regulation of Fas expression. J Immunol 2007; 179:4775–82.
56. Sgarbanti M, Borsetti A, Moscufo N et al. Modulation of human immunodeficiency virus 1 replication by interferon regulatory factors. J Exp Med 2002; 195:1359–70.
57. Munier S, Delcroix-Genete D, Cathagena L, Gumez A, Hazan U. Characterization of two candidate genes, NCoA3, and IRF8, potentially involved in the control of HIV-1 latency. Retrovirology 2005; 2:73–86.
58. Minten C, Terry R, King N, Campbell I. Increased lethality but decreased encephalitis in IRF-8 deficient mice following West Nile Virus infection. J Immunol 2011; 186:154.1.
59. Tinton SA, Schepens B, Bruynooghe Y, Beyaert R, Cornelis S. Regulation and the cell-cycle -dependent internal ribosome entry site of the PITSLRE protein kinase: roles of Unr (upstream of N-ras) protein and phosphorylated translation initiation factor elF-2α. Biochem J 2005; 385:155–63.