Rhinovirus load is high despite preserved interferon-β response in cystic fibrosis bronchial epithelial cells

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Dauletbaev, Nurlan ^a   Das, Mithun ^a   Cammisano, Maria ^a   Chen, He ^a   Singh, Sareen ^a   Kooi, Cora ^b   Leigh, Richard ^b   Beaudoin, Trevor ^c   Rousseau, Simon ^c   Lands, Larry C ^a,d  

^a MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d MONTREAL CHILDREN S HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2',5' OLIGOADENYLATE SYNTHETASE; BETA INTERFERON; IL8 PROTEIN, HUMAN; INTERLEUKIN 8; OAS1 PROTEIN, HUMAN; RECOMBINANT PROTEIN; VIRUS RNA;

ADULT; BRONCHUS; CELL LINE; CYSTIC FIBROSIS; CYTOLOGY; EPITHELIUM CELL; FEMALE; GENETICS; GENOTYPE; HUMAN; LUNG DISEASE; MALE; METABOLISM; PATHOGENICITY; PRIMARY CELL CULTURE; PSEUDOMONAS AERUGINOSA; RHINOVIRUS; VIROLOGY; VIRULENCE; VIRUS LOAD; YOUNG ADULT;

2',5'-OLIGOADENYLATE SYNTHETASE; ADULT; BRONCHI; CELL LINE; CYSTIC FIBROSIS; EPITHELIAL CELLS; FEMALE; GENOTYPE; HUMANS; INTERFERON-BETA; INTERLEUKIN-8; LUNG DISEASES; MALE; PRIMARY CELL CULTURE; PSEUDOMONAS AERUGINOSA; RECOMBINANT PROTEINS; RHINOVIRUS; RNA, VIRAL; VIRAL LOAD; VIRULENCE; YOUNG ADULT;

EID: 84957937742     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0143129     Document Type: Article

References (44)

1. Goffard A, Lambert V, Salleron J, Herwegh S, Engelmann I, Pinel C, et al. Virus and cystic fibrosis: rhinoviruses are associated with exacerbations in adult patients. J Clin Virol. 2014; 60(2):147-53. Epub 2014/03/19. doi: 10.1016/j.jcv.2014.02.005 PMID: 24637203.
2. Flight WG, Bright-Thomas RJ, Tilston P, Mutton KJ, Guiver M, Morris J, et al. Incidence and clinical impact of respiratory viruses in adults with cystic fibrosis. Thorax. 2014; 69(3):247-53. Epub 2013/10/16. doi: 10.1136/thoraxjnl-2013-204000 PMID: 24127019.
3. Burns JL, Emerson J, Kuypers J, Campbell AP, Gibson RL, McNamara S, et al. Respiratory viruses in children with cystic fibrosis: viral detection and clinical findings. Influenza Other Respir Viruses. 2012; 6 (3):218-23. Epub 2011/10/01. doi: 10.1111/j.1750-2659.2011.00292.x PMID: 21955319.
4. Esposito S, Dacco V, Daleno C, Gambazza S, Montinaro V, Bisogno A, et al. Human rhinovirus infection in children with cystic fibrosis. Jpn J Infect Dis. 2014; 67(5):399-401. Epub 2014/09/23. PMID: 25241695.
5. Kieninger E, Singer F, Tapparel C, Alves MP, Latzin P, Tan HL, et al. High rhinovirus burden in lower airways of children with cystic fibrosis. Chest. 2013; 143(3):782-90. Epub 2012/11/29. doi: 10.1378/chest.12-0954 PMID: 23188200.
6. Worlitzsch D, Tarran R, Ulrich M, Schwab U, Cekici A, Meyer KC, et al. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest. 2002; 109 (3):317-25. Epub 2002/02/06. doi: 10.1172/jci13870 PMID: 11827991; PubMed Central PMCID: PMCPmc150856.
7. Wu Q, Lu Z, Verghese MW, Randell SH. Airway epithelial cell tolerance to Pseudomonas aeruginosa. Respir Res. 2005; 6:26. Epub 2005/04/05. doi: 10.1186/1465-9921-6-26 PMID: 15804356; PubMed Central PMCID: PMCPmc1087506.
8. Dauletbaev N, Eklove D, Mawji N, Iskandar M, Di Marco S, Gallouzi IE, et al. Down-regulation of cytokine-induced interleukin-8 requires inhibition of p38 mitogen-activated protein kinase (MAPK) via MAPK phosphatase 1-dependent and -independent mechanisms. J Biol Chem. 2011; 286(18):15998-6007. Epub 2011/04/02. doi: 10.1074/jbc.M110.205724 PMID: 21454676; PubMed Central PMCID: PMCPmc3091209.
9. Dauletbaev N, Lam J, Eklove D, Iskandar M, Lands LC. Ibuprofen modulates NF-kB activity but not IL-8 production in cystic fibrosis respiratory epithelial cells. Respiration. 2010; 79(3):234-42. Epub 2009/11/06. doi: 10.1159/000255342 PMID: 19887769.
10. Gruenert DC, Willems M, Cassiman JJ, Frizzell RA. Established cell lines used in cystic fibrosis research. J Cyst Fibros. 2004; 3 Suppl 2:191-6. Epub 2004/10/07. doi: 10.1016/j.jcf.2004.05.040 PMID: 15463957.
11. Bruscia E, Sangiuolo F, Sinibaldi P, Goncz KK, Novelli G, Gruenert DC. Isolation of CF cell lines corrected at DeltaF508-CFTR locus by SFHR-mediated targeting. Gene Ther. 2002; 9(11):683-5. Epub 2002/05/29. doi: 10.1038/sj.gt.3301741 PMID: 12032687.
12. Sanders SP, Siekierski ES, Porter JD, Richards SM, Proud D. Nitric oxide inhibits rhinovirus-induced cytokine production and viral replication in a human respiratory epithelial cell line. J Virol. 1998; 72 (2):934-42. Epub 1998/01/28. PMID: 9444985; PubMed Central PMCID: PMCPmc124563.
13. Winther B, Gwaltney JM Jr., Mygind N, Turner RB, Hendley JO. Sites of rhinovirus recovery after point inoculation of the upper airway. Jama. 1986; 256(13):1763-7. Epub 1986/10/03. PMID: 3018306.
14. Bardin PG, Johnston SL, Sanderson G, Robinson BS, Pickett MA, Fraenkel DJ, et al. Detection of rhinovirus infection of the nasal mucosa by oligonucleotide in situ hybridization. Am J Respir Cell Mol Biol. 1994; 10(2):207-13. Epub 1994/02/01. doi: 10.1165/ajrcmb.10.2.8110476 PMID: 8110476.
15. Arruda E, Boyle TR, Winther B, Pevear DC, Gwaltney JM Jr., Hayden FG. Localization of human rhinovirus replication in the upper respiratory tract by in situ hybridization. J Infect Dis. 1995; 171(5):1329-33. Epub 1995/05/01. PMID: 7751712.
16. Mosser AG, Brockman-Schneider R, Amineva S, Burchell L, Sedgwick JB, Busse WW, et al. Similar frequency of rhinovirus-infectible cells in upper and lower airway epithelium. J Infect Dis. 2002; 185 (6):734-43. Epub 2002/03/29. doi: 10.1086/339339 PMID: 11920291.
17. Shabram P, Aguilar-Cordova E. Multiplicity of infection/multiplicity of confusion. Mol Ther. 2000; 2 (5):420-1. Epub 2000/11/18. doi: 10.1006/mthe.2000.0212 PMID: 11082315.
18. Stott EJ, Heath GF. Factors affecting the growth of Rhinovirus 2 in suspension cultures of L132 cells. J Gen Virol. 1970; 6(1):15-24. Epub 1970/01/01. PMID: 4313398.
19. Haff RF, Wohlsen B, Force EE, Stewart RC. Growth characteristics of two rhinovirus strains in WI-26 and monkey kidney cells. J Bacteriol. 1966; 91(6):2339-42. Epub 1966/06/01. PMID: 4287588; PubMed Central PMCID: PMCPmc316216.
20. Lonberg-Holm K, Korant BD. Early interaction of rhinoviruses with host cells. J Virol. 1972; 9(1):29-40. Epub 1972/01/01. PMID: 4333543; PubMed Central PMCID: PMCPmc356259.
21. Ponomarieva TI, Dreisin RS, Vikhnovich EM, Borovkova NM. Study of rhinoviral infection by fluorescent staining in human embryo fibroblast cells. Arch Gesamte Virusforsch. 1972; 39(1):92-7. Epub 1972/01/01. PMID: 4344150.
22. Berube J, Roussel L, Nattagh L, Rousseau S. Loss of cystic fibrosis transmembrane conductance regulator function enhances activation of p38 and ERK MAPKs, increasing interleukin-6 synthesis in airway epithelial cells exposed to Pseudomonas aeruginosa. J Biol Chem. 2010; 285(29):22299-307. Epub 2010/05/13. doi: 10.1074/jbc.M109.098566 PMID: 20460375; PubMed Central PMCID: PMCPmc2903409.
23. Schogler A, Kopf BS, Edwards MR, Johnston SL, Casaulta C, Kieninger E, et al. Novel antiviral properties of azithromycin in cystic fibrosis airway epithelial cells. Eur Respir J. 2014. Epub 2014/11/02. doi: 10.1183/09031936.00102014 PMID: 25359346.
24. 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(10):4131-45. Epub 2011/08/10. doi: 10.1128/iai.05120-11 PMID: 21825067; PubMed Central PMCID: PMCPmc3187241.
25. Roussel L, Martel G, Berube J, Rousseau S. P. aeruginosa drives CXCL8 synthesis via redundant tolllike receptors and NADPH oxidase in CFTRF508 airway epithelial cells. J Cyst Fibros. 2011; 10 (2):107-13. Epub 2010/12/24. doi: 10.1016/j.jcf.2010.11.005 PMID: 21176887.
26. DiMango E, Zar HJ, Bryan R, Prince A. Diverse Pseudomonas aeruginosa gene products stimulate respiratory epithelial cells to produce interleukin-8. J Clin Invest. 1995; 96(5):2204-10. Epub 1995/11/01. doi: 10.1172/jci118275 PMID: 7593606; PubMed Central PMCID: PMCPMC185870.
27. Dauletbaev N, Herscovitch K, Das M, Chen H, Bernier J, Matouk E, et al. Down-regulation of IL-8 by high-dose vitamin D is specific to hyperinflammatory macrophages and involves mechanisms beyond up-regulation of DUSP1. British journal of pharmacology. 2015; 172(19):4757-71. Epub 2015/07/17. doi: 10.1111/bph.13249 PMID: 26178144; PubMed Central PMCID: PMCPmc4594277.
28. Zhang SY, Jouanguy E, Sancho-Shimizu V, von Bernuth H, Yang K, Abel L, et al. Human Toll-like receptor-dependent induction of interferons in protective immunity to viruses. Immunol Rev. 2007; 220:225-36. Epub 2007/11/06. doi: 10.1111/j.1600-065X.2007.00564.x PMID: 17979850.
29. Amineva SP, Aminev AG, Gern JE, Palmenberg AC. Comparison of rhinovirus A infection in human primary epithelial and HeLa cells. J Gen Virol. 2011; 92(Pt 11):2549-57. Epub 2011/07/15. doi: 10.1099/vir.0.031302-0 PMID: 21752966; PubMed Central PMCID: PMCPmc3352362.
30. Nakagome K, Bochkov YA, Ashraf S, Brockman-Schneider RA, Evans MD, Pasic TR, et al. Effects of rhinovirus species on viral replication and cytokine production. J Allergy Clin Immunol. 2014; 134 (2):332-41. Epub 2014/03/19. doi: 10.1016/j.jaci.2014.01.029 PMID: 24636084; PubMed Central PMCID: PMCPmc4119842.
31. Newcomb DC, Sajjan US, Nagarkar DR, Wang Q, Nanua S, Zhou Y, et al. Human rhinovirus 1B exposure induces phosphatidylinositol 3-kinase-dependent airway inflammation in mice. Am J Respir Crit Care Med. 2008; 177(10):1111-21. Epub 2008/02/16. doi: 10.1164/rccm.200708-1243OC PMID: 18276942; PubMed Central PMCID: PMCPmc2383993.
32. Sutanto EN, Kicic A, Foo CJ, Stevens PT, Mullane D, Knight DA, et al. Innate inflammatory responses of pediatric cystic fibrosis airway epithelial cells: effects of nonviral and viral stimulation. Am J Respir Cell Mol Biol. 2011; 44(6):761-7. Epub 2011/02/15. doi: 10.1165/rcmb.2010-0368OC PMID: 21317379.
33. Khaitov MR, Laza-Stanca V, Edwards MR, Walton RP, Rohde G, Contoli M, et al. Respiratory virus induction of alpha-, beta- and lambda-interferons in bronchial epithelial cells and peripheral blood mononuclear cells. Allergy. 2009; 64(3):375-86. Epub 2009/01/30. doi: 10.1111/j.1398-9995.2008. 01826.x PMID: 19175599.
34. Tomassini JE, Graham D, DeWitt CM, Lineberger DW, Rodkey JA, Colonno RJ. cDNA cloning reveals that the major group rhinovirus receptor on HeLa cells is intercellular adhesion molecule 1. Proc Natl Acad Sci U S A. 1989; 86(13):4907-11. Epub 1989/07/01. PMID: 2544880; PubMed Central PMCID: PMCPmc297524.
35. Staunton DE, Merluzzi VJ, Rothlein R, Barton R, Marlin SD, Springer TA. A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell. 1989; 56(5):849-53. Epub 1989/03/10. PMID: 2538244.
36. Hofer F, Gruenberger M, Kowalski H, Machat H, Huettinger M, Kuechler E, et al. Members of the low density lipoprotein receptor family mediate cell entry of a minor-group common cold virus. Proc Natl Acad Sci U S A. 1994; 91(5):1839-42. Epub 1994/03/01. PMID: 8127891; PubMed Central PMCID: PMCPmc43259.
37. Kelly C, Canning P, Buchanan PJ, Williams MT, Brown V, Gruenert DC, et al. Toll-like receptor 4 is not targeted to the lysosome in cystic fibrosis airway epithelial cells. Am J Physiol Lung Cell Mol Physiol. 2013; 304(5):L371-82. Epub 2013/01/15. doi: 10.1152/ajplung.00372.2011 PMID: 23316065; PubMed Central PMCID: PMCPmc4073939.
38. Bruscia EM, Zhang PX, Satoh A, Caputo C, Medzhitov R, Shenoy A, et al. Abnormal trafficking and degradation of TLR4 underlie the elevated inflammatory response in cystic fibrosis. J Immunol. 2011; 186(12):6990-8. Epub 2011/05/20. doi: 10.4049/jimmunol.1100396 PMID: 21593379; PubMed Central PMCID: PMCPmc3111054.
39. Boyle MP, Bell SC, Konstan MW, McColley SA, Rowe SM, Rietschel E, et al. A CFTR corrector (lumacaftor) and a CFTR potentiator (ivacaftor) for treatment of patients with cystic fibrosis who have a phe508del CFTR mutation: a phase 2 randomised controlled trial. Lancet Respir Med. 2014; 2(7):527-38. Epub 2014/06/29. doi: 10.1016/s2213-2600(14)70132-8 PMID: 24973281.
40. Djukanovic R, Harrison T, Johnston SL, Gabbay F, Wark P, Thomson NC, et al. The effect of inhaled IFN-beta on worsening of asthma symptoms caused by viral infections. A randomized trial. Am J Respir Crit Care Med. 2014; 190(2):145-54. Epub 2014/06/18. doi: 10.1164/rccm.201312-2235OC PMID: 24937476.
41. Dauletbaev N, Cammisano M, Herscovitch K, Lands LC. Stimulation of the RIG-I/MAVS Pathway by Polyinosinic:Polycytidylic Acid Upregulates IFN-beta in Airway Epithelial Cells with Minimal Costimulation of IL-8. J Immunol. 2015; 195(6):2829-41. Epub 2015/08/19. doi: 10.4049/jimmunol.1400840 PMID: 26283481.
42. Becker TM, Durrani SR, Bochkov YA, Devries MK, Rajamanickam V, Jackson DJ. Effect of exogenous interferons on rhinovirus replication and airway inflammatory responses. Ann Allergy Asthma Immunol. 2013; 111(5):397-401. Epub 2013/10/16. doi: 10.1016/j.anai.2013.07.029 PMID: 24125148; PubMed Central PMCID: PMCPmc3845219.
43. Lopez-Souza N, Dolganov G, Dubin R, Sachs LA, Sassina L, Sporer H, et al. Resistance of differentiated human airway epithelium to infection by rhinovirus. Am J Physiol Lung Cell Mol Physiol. 2004; 286 (2):L373-81. Epub 2004/01/09. doi: 10.1152/ajplung.00300.2003 PMID: 14711802.
44. Bai J, Smock SL, Jackson GR Jr., MacIsaac KD, Huang Y, Mankus C, et al. Phenotypic responses of differentiated asthmatic human airway epithelial cultures to rhinovirus. PLoS One. 2015; 10(2): e0118286. Epub 2015/02/24. doi: 10.1371/journal.pone.0118286 PMID: 25706956; PubMed Central PMCID: PMCPMC4338293.