Stimulation of the RIG-I/MAVS pathway by polyinosinic: Polycytidylic acid upregulates IFN-β in airway epithelial cells with minimal costimulation of IL-8

Journal of Immunology

Volumn 195, Issue 6, 2015, Pages 2829-2841

  Dauletbaev, Nurlan ^a   Cammisano, Maria ^a   Herscovitch, Kassey ^a   Lands, Larry C ^b  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b MONTREAL CHILDREN S HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CARRIER PROTEINS AND BINDING PROTEINS; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 8; LIPOSOME; MITOCHONDRIAL ANTIVIRAL SIGNALING PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; POLYINOSINIC POLYCYTIDYLIC ACID; RETINOIC ACID INDUCIBLE PROTEIN I; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; UNCLASSIFIED DRUG; DDX58 PROTEIN, HUMAN; DEAD BOX PROTEIN; IL8 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; SIGNAL TRANSDUCING ADAPTOR PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TICAM1 PROTEIN, HUMAN; TLR3 PROTEIN, HUMAN; VESICULAR TRANSPORT ADAPTOR PROTEIN; VISA PROTEIN, HUMAN;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; ENCAPSULATION; EPITHELIUM CELL; HUMAN; HUMAN CELL; INFLAMMATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RESPIRATORY EPITHELIUM; SIGNAL TRANSDUCTION; UPREGULATION; BIOSYNTHESIS; CELL LINE; CYTOLOGY; GENETICS; IMMUNOLOGY; METABOLISM; RESPIRATORY TRACT MUCOSA; TRANSCRIPTION INITIATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADAPTOR PROTEINS, VESICULAR TRANSPORT; CELL LINE; DEAD-BOX RNA HELICASES; EPITHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; INFLAMMATION; INTERFERON-BETA; INTERLEUKIN-8; JNK MITOGEN-ACTIVATED PROTEIN KINASES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; POLY I-C; RESPIRATORY MUCOSA; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 84941751683     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400840     Document Type: Article

References (60)

1. Message, S. D., V. Laza-Stanca, P. Mallia, H. L. Parker, J. Zhu, T. Kebadze, M. Contoli, G. Sanderson, O. M. Kon, A. Papi, et al. 2008. 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 105: 13562-13567.
2. van Ewijk, B. E., M. M. van der Zalm, T. F. Wolfs, and C. K. van der Ent. 2005. Viral respiratory infections in cystic fibrosis. J. Cyst. Fibros. 4(Suppl. 2): 31-36.
3. Busse, W. W., R. F. Lemanske, Jr., and J. E. Gern. 2010. Role of viral respiratory infections in asthma and asthma exacerbations. Lancet 376: 826-834.
4. Sykes, A., M. R. Edwards, J. Macintyre, A. Del Rosario, V. Gielen, J. Haas, O. M. Kon, M. McHale, and S. L. Johnston. 2013. TLR3, TLR4 and TLRs7-9 induced interferons are not impaired in airway and blood cells in well controlled asthma. PLoS One 8: e65921.
5. Cakebread, J. A., Y. Xu, C. Grainge, V. Kehagia, P. H. Howarth, S. T. Holgate, and D. E. Davies. 2011. Exogenous IFN-b has antiviral and anti-inflammatory properties in primary bronchial epithelial cells from asthmatic subjects exposed to rhinovirus. J. Allergy Clin. Immunol. 127: 1148-1154.e9.
6. Sykes, A., J. Macintyre, M. R. Edwards, A. Del Rosario, J. Haas, V. Gielen, O. M. Kon, M. McHale, and S. L. Johnston. 2014. Rhinovirus-induced interferon production is not deficient in well controlled asthma. Thorax 69: 240-246.
7. Patel, D. A., Y. You, G. Huang, D. E. Byers, H. J. Kim, E. Agapov, M. L. Moore, R. S. Peebles, Jr., M. Castro, and K. Sumino, et al. 2014. Interferon response and respiratory virus control are preserved in bronchial epithelial cells in asthma. J. Allergy Clin. Immunol. 134: 1402-1412.e7.
8. Edwards, M. R., N. Regamey, M. Vareille, E. Kieninger, A. Gupta, A. Shoemark, S. Saglani, A. Sykes, J. Macintyre, J. Davies, et al. 2013. Impaired innate interferon induction in severe therapy resistant atopic asthmatic children. Mucosal Immunol. 6: 797-806.
9. Wark, P. A., S. L. Johnston, F. Bucchieri, R. Powell, S. Puddicombe, V. Laza-Stanca, S. T. Holgate, and D. E. Davies. 2005. Asthmatic bronchial epithelial cells have a deficient innate immune response to infection with rhinovirus. J. Exp. Med. 201: 937-947.
10. Gielen, V., A. Sykes, J. Zhu, B. Chan, J. Macintyre, N. Regamey, E. Kieninger, A. Gupta, A. Shoemark, and C. Bossley, et al. 2015. Increased nuclear suppressor of cytokine signaling 1 in asthmatic bronchial epithelium suppresses rhinovirus induction of innate interferons. J Allergy Clin. Immunol. 136: 177-188.e11.
11. Baraldo, S., M. Contoli, E. Bazzan, G. Turato, A. Padovani, B. Marku, F. Calabrese, G. Caramori, A. Ballarin, D. Snijders, et al. 2012. Deficient antiviral immune responses in childhood: distinct roles of atopy and asthma. J. Allergy Clin. Immunol. 130: 1307-1314.
12. Chattoraj, S. S., S. Ganesan, A. Faris, A. Comstock, W. M. Lee, and U. S. Sajjan. 2011. Pseudomonas aeruginosa suppresses interferon response to rhinovirus infection in cystic fibrosis but not in normal bronchial epithelial cells. Infect. Immun. 79: 4131-4145.
13. Contoli, M., K. Ito, A. Padovani, D. Poletti, B. Marku, M. R. Edwards, L. A. Stanciu, G. Gnesini, A. Pastore, A. Spanevello, et al. 2015. Th2 cytokines impair innate immune responses to rhinovirus in respiratory epithelial cells. Allergy 70: 910-920.
14. Logan, J., L. Chen, C. Gangell, P. D. Sly, E. Fantino, and K. Liu. 2014. Brief exposure to cigarette smoke impairs airway epithelial cell innate anti-viral defence. Toxicol. In Vitro 28: 1430-1435.
15. Wark, P. A., T. Grissell, B. Davies, H. See, and P. G. Gibson. 2009. Diversity in the bronchial epithelial cell response to infection with different rhinovirus strains. Respirology 14: 180-186.
16. Wu, W., K. B. Patel, J. L. Booth, W. Zhang, and J. P. Metcalf. 2011. Cigarette smoke extract suppresses the RIG-I-initiated innate immune response to influenza virus in the human lung. Am. J. Physiol. Lung Cell. Mol. Physiol. 300: L821-L830.
17. Becker, T. M., S. R. Durrani, Y. A. Bochkov, M. K. Devries, V. Rajamanickam, and D. J. Jackson. 2013. Effect of exogenous interferons on rhinovirus replication and airway inflammatory responses. Ann. Allergy Asthma Immunol. 111: 397-401.
18. Gaajetaan, G. R., T. H. Geelen, J. H. Vernooy, M. A. Dentener, N. L. Reynaert, G. G. Rohde, E. V. Beuken, G. E. Grauls, C. A. Bruggeman, and F. R. Stassen. 2013. Interferon-b induces a long-lasting antiviral state in human respiratory epithelial cells. J. Infect. 66: 163-169.
19. Raj, N. B., and P. M. Pitha. 1981. Analysis of interferon mRNA in human fibroblast cells induced to produce interferon. Proc. Natl. Acad. Sci. USA 78: 7426-7430.
20. Kumagai, Y., and S. Akira. 2010. Identification and functions of pattern-recognition receptors. J. Allergy Clin. Immunol. 125: 985-992.
21. Guillot, L., R. Le Goffic, S. Bloch, N. Escriou, S. Akira, M. Chignard, and M. Si-Tahar. 2005. Involvement of toll-like receptor 3 in the immune response of lung epithelial cells to double-stranded RNA and influenza A virus. J. Biol. Chem. 280: 5571-5580.
22. De Clercq, E. 2009. Antiviral drug discovery: ten more compounds, and ten more stories (part B). Med. Res. Rev. 29: 571-610.
23. Cohen-Cymberknoh, M., E. Kerem, T. Ferkol, and A. Elizur. 2013. Airway inflammation in cystic fibrosis: molecular mechanisms and clinical implications. Thorax 68: 1157-1162.
24. Jacquot, J., O. Tabary, and A. Clement. 2008. Hyperinflammation in airways of cystic fibrosis patients: what's new? Expert Rev. Mol. Diagn. 8: 359-363.
25. Rieber, N., A. Hector, M. Carevic, and D. Hartl. 2014. Current concepts of immune dysregulation in cystic fibrosis. Int. J. Biochem. Cell Biol. 52: 108-112.
26. Dauletbaev, N., D. Eklove, N. Mawji, M. Iskandar, S. Di Marco, I. E. Gallouzi, and L. C. Lands. 2011. 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. 286: 15998-16007.
27. Dauletbaev, N., J. Lam, D. Eklove, M. Iskandar, and L. C. Lands. 2010. Ibuprofen modulates NF-kB activity but not IL-8 production in cystic fibrosis respiratory epithelial cells. Respiration 79: 234-242.
28. Dauletbaev, N., K. Herscovitch, M. Das, H. Chen, J. Bernier, E. Matouk, J. Bérubé, S. Rousseau, and L. C. Lands. 2015. Down-regulation of IL-8 by highdose vitamin D is specific to hyperinflammatory macrophages and involves mechanisms beyond up-regulation of DUSP1. Br. J. Pharmacol. DOI: 10.1111/ bph.13249.
29. Hoffmann, E., O. Dittrich-Breiholz, H. Holtmann, and M. Kracht. 2002. Multiple control of interleukin-8 gene expression. J. Leukoc. Biol. 72: 847-855.
30. Oeckinghaus, A., M. S. Hayden, and S. Ghosh. 2011. Crosstalk in NF-kB signaling pathways. Nat. Immunol. 12: 695-708.
31. Shih, V. F., R. Tsui, A. Caldwell, and A. Hoffmann. 2011. A single NFkB system for both canonical and non-canonical signaling. Cell Res. 21: 86-102.
32. Sun, S. C. 2011. Non-canonical NF-kB signaling pathway. Cell Res. 21: 71-85.
33. Bérubé, J., C. Bourdon, Y. Yao, and S. Rousseau. 2009. Distinct intracellular signaling pathways control the synthesis of IL-8 and RANTES in TLR1/TLR2, TLR3 or NOD1 activated human airway epithelial cells. Cell. Signal. 21: 448-456.
34. Ohkuni, T., T. Kojima, N. Ogasawara, T. Masaki, J. Fuchimoto, R. Kamekura, J. Koizumi, S. Ichimiya, M. Murata, S. Tanaka, et al. 2011. Poly(I:C) reduces expression of JAM-A and induces secretion of IL-8 and TNF-a via distinct NFkB pathways in human nasal epithelial cells. Toxicol. Appl. Pharmacol. 250: 29-38.
35. Lukens, J. R., P. Vogel, G. R. Johnson, M. A. Kelliher, Y. Iwakura, M. Lamkanfi, and T. D. Kanneganti. 2013. RIP1-driven autoinflammation targets IL-1a independently of inflammasomes and RIP3. Nature 498: 224-227.
36. Rebeyrol, C., V. Saint-Criq, L. Guillot, L. Riffault, H. Corvol, K. Chadelat, D. W. Ray, A. Clement, O. Tabary, and P. Le Rouzic. 2012. Glucocorticoids reduce inflammation in cystic fibrosis bronchial epithelial cells. Cell. Signal. 24: 1093-1099.
37. Wilson, S. J., A.Wallin, G. Della-Cioppa, T. Sandström, and S. T. Holgate. 2001. Effects of budesonide and formoterol on NF-kappaB, adhesion molecules, and cytokines in asthma. Am. J. Respir. Crit. Care Med. 164: 1047-1052.
38. Kassel, O., A. Sancono, J. Krätzschmar, B. Kreft, M. Stassen, and A. C. Cato. 2001. Glucocorticoids inhibit MAP kinase via increased expression and decreased degradation of MKP-1. EMBO J. 20: 7108-7116.
39. Bladh, L. G., K. Johansson-Haque, I. Rafter, S. Nilsson, and S. Okret. 2009. Inhibition of extracellular signal-regulated kinase (ERK) signaling participates in repression of nuclear factor (NF)-kappaB activity by glucocorticoids. Biochim. Biophys. Acta 1793: 439-446.
40. Newcomb, D. C., U. Sajjan, S. Nanua, Y. Jia, A. M. Goldsmith, J. K. Bentley, and M. B. Hershenson. 2005. Phosphatidylinositol 3-kinase is required for rhinovirus-induced airway epithelial cell interleukin-8 expression. J. Biol. Chem. 280: 36952-36961.
41. Gitlin, L., W. Barchet, S. Gilfillan, M. Cella, B. Beutler, R. A. Flavell, M. S. Diamond, and M. Colonna. 2006. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. USA 103: 8459-8464.
42. Kato, H., O. Takeuchi, E. Mikamo-Satoh, R. Hirai, T. Kawai, K. Matsushita, A. Hiiragi, T. S. Dermody, T. Fujita, and S. Akira. 2008. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J. Exp. Med. 205: 1601-1610.
43. Wong, J. P., H. Yang, L. Nagata, M. Kende, H. Levy, G. Schnell, and K. Blasetti. 1999. Liposome-mediated immunotherapy against respiratory influenza virus infection using double-stranded RNA poly ICLC. Vaccine 17: 1788-1795.
44. Ichinohe, T., I. Watanabe, S. Ito, H. Fujii, M. Moriyama, S. Tamura, H. Takahashi, H. Sawa, J. Chiba, T. Kurata, et al. 2005. Synthetic doublestranded RNA poly(I:C) combined with mucosal vaccine protects against influenza virus infection. J. Virol. 79: 2910-2919.
45. Wong, J. P., M. E. Christopher, S. Viswanathan, N. Karpoff, X. Dai, D. Das, L. Q. Sun, M. Wang, and A. M. Salazar. 2009. Activation of toll-like receptor signaling pathway for protection against influenza virus infection. Vaccine 27: 3481-3483.
46. Boukhvalova, M. S., T. B. Sotomayor, R. C. Point, L. M. Pletneva, G. A. Prince, and J. C. Blanco. 2010. Activation of interferon response through toll-like receptor 3 impacts viral pathogenesis and pulmonary toll-like receptor expression during respiratory syncytial virus and influenza infections in the cotton rat Sigmodon hispidus model. J. Interferon Cytokine Res. 30: 229-242.
47. McNally, B., M. Willette, F. Ye, S. Partida-Sanchez, and E. Flano. 2012. Intranasal administration of dsRNA analog poly(I:C) induces interferon-a receptordependent accumulation of antigen experienced T cells in the airways. PLoS One 7: e51351.
48. Zhao, J., C. Wohlford-Lenane, J. Zhao, E. Fleming, T. E. Lane, P. B. McCray, Jr., and S. Perlman. 2012. Intranasal treatment with poly(IC) protects aged mice from lethal respiratory virus infections. J. Virol. 86: 11416-11424.
49. Meusel, T. R., K. E. Kehoe, and F. Imani. 2002. Protein kinase R regulates double-stranded RNA induction of TNF-alpha but not IL-1 beta mRNA in human epithelial cells. J. Immunol. 168: 6429-6435.
50. Rezaee, F., N. Meednu, J. A. Emo, B. Saatian, T. J. Chapman, N. G. Naydenov, A. De Benedetto, L. A. Beck, A. I. Ivanov, and S. N. Georas. 2011. Polyinosinic: polycytidylic acid induces protein kinase D-dependent disassembly of apical junctions and barrier dysfunction in airway epithelial cells. J. Allergy Clin. Immunol. 128: 1216-1224.e11.
51. Mitoma, H., S. Hanabuchi, T. Kim, M. Bao, Z. Zhang, N. Sugimoto, and Y. J. Liu. 2013. The DHX33 RNA helicase senses cytosolic RNA and activates the NLRP3 inflammasome. Immunity 39: 123-135.
52. De Miranda, J., K. Yaddanapudi, M. Hornig, and W. I. Lipkin. 2009. Astrocytes recognize intracellular polyinosinic-polycytidylic acid via MDA-5. FASEB J. 23: 1064-1071.
53. Lappalainen, J., J. Rintahaka, P. T. Kovanen, S. Matikainen, and K. K. Eklund. 2013. Intracellular RNA recognition pathway activates strong anti-viral response in human mast cells. Clin. Exp. Immunol. 172: 121-128.
54. Palchetti, S., D. Starace, P. De Cesaris, A. Filippini, E. Ziparo, and A. Riccioli. 2015. Transfected poly(I:C) activates different dsRNA receptors, leading to apoptosis or immunoadjuvant response in androgen-independent prostate cancer cells. J. Biol. Chem. 290: 5470-5483.
55. Reimer, T., M. Brcic, M. Schweizer, and T. W. Jungi. 2008. poly(I:C) and LPS induce distinct IRF3 and NF-kappaB signaling during type-I IFN and TNF responses in human macrophages. J. Leukoc. Biol. 83: 1249-1257.
56. Avril, T., M. de Tayrac, C. Leberre, and V. Quillien. 2009. Not all polyriboinosinic-polyribocytidylic acids (Poly I:C) are equivalent for inducing maturation of dendritic cells: implication for alpha-type-1 polarized DCs. J. Immunother. 32: 353-362.
57. Zhou, Y., M. Guo, X.Wang, J. Li, Y. Wang, L. Ye, M. Dai, L. Zhou, Y. Persidsky, andW. Ho. 2013. TLR3 activation efficiency by high or low molecular mass poly I:C. Innate Immun. 19: 184-192.
58. Krishnamurthy, S., M. A. Behlke, S. Ramachandran, A. K. Salem, P. B. McCray, Jr., and B. L. Davidson. 2012. Manipulation of cell physiology enables gene silencing in well-differentiated airway epithelia. Mol. Ther. Nucleic Acids 1: e41.
59. Arruda, E., T. R. Boyle, B. Winther, D. C. Pevear, J. M. Gwaltney, Jr., and F. G. Hayden. 1995. Localization of human rhinovirus replication in the upper respiratory tract by in situ hybridization. J. Infect. Dis. 171: 1329-1333.
60. Mallia, P., S. D. Message, V. Gielen, M. Contoli, K. Gray, T. Kebadze, J. Aniscenko, V. Laza-Stanca, M. R. Edwards, L. Slater, et al. 2011. Experimental rhinovirus infection as a human model of chronic obstructive pulmonary disease exacerbation. Am. J. Respir. Crit. Care Med. 183: 734-742.