Type-I interferons induce lung protease responses following respiratory syncytial virus infection via RIG-I-like receptors

Mucosal Immunology

Volumn 8, Issue 1, 2015, Pages 161-175

  Foronjy, R F ^a   Taggart, C C ^b   Dabo, A J ^a   Weldon, S ^b   Cummins, N ^a   Geraghty, P ^a  

^a ST LUKE S ROOSEVELT HOSPITAL CENTER   (United States)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BATIMASTAT; BETA INTERFERON; CATHEPSIN; CATHEPSIN B; CATHEPSIN E; CATHEPSIN G; CATHEPSIN H; COLLAGENASE 3; CYTOKINE; DIPEPTIDYL PEPTIDASE I; GELATINASE A; GELATINASE B; INTERFERON; INTERLEUKIN 4; MATRILYSIN; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 14; MELANOMA DIFFERENTIATION ASSOCIATED PROTEIN 5; MITOCHONDRIAL ANTIVIRAL SIGNALING PROTEIN; MITOCHONDRIAL PROTEIN; N [N (3 CARBOXYOXIRANE 2 CARBONYL)LEUCYL]AGMATINE; NEUTROPHIL COLLAGENASE; PATTERN RECOGNITION RECEPTOR; RETINOIC ACID INDUCIBLE PROTEIN I; RETINOIC ACID INDUCIBLE PROTEIN I LIKE RECEPTOR; RIBAVIRIN; STROMELYSIN; STROMELYSIN 2; TIR DOMAIN CONTAINING ADAPTER INDUCING INTERFERON BETA PROTEIN; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG; DDX58 PROTEIN, MOUSE; DEAD BOX PROTEIN; IPS-1 PROTEIN, MOUSE; LEUCINE; PHENYLALANINE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; THIOPHENE DERIVATIVE; TICAM-1 PROTEIN, MOUSE; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE RESPONSE; EPITHELIUM CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; LUNG LAVAGE; LUNG PARENCHYMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY SYNCYTIAL VIRUS INFECTION; RESPIRATORY TRACT ALLERGY; VIRAL CLEARANCE; ANALOGS AND DERIVATIVES; ANIMAL; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN RESPIRATORY SYNCYTIAL VIRUS; IMMUNOLOGY; INBRED MOUSE STRAIN; KNOCKOUT MOUSE; LUNG; METABOLISM; PHYSIOLOGY; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; VIROLOGY; VIRUS LOAD;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CATHEPSINS; DEAD-BOX RNA HELICASES; GENE EXPRESSION REGULATION, VIRAL; INTERFERON TYPE I; LEUCINE; LUNG; MATRIX METALLOPROTEINASES; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; PHENYLALANINE; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUSES; RIBAVIRIN; THIOPHENES; VIRAL LOAD;

EID: 84927654195     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2014.54     Document Type: Article

References (45)

1. Foronjy, R. F., Dabo, A. J., Taggart, C. C., Weldon, S. & Geraghty, P. Respiratory syncytial virus infections enhance cigarette smoke induced COPD in mice. PLoS One 9, e90567 (2014)
2. Foronjy, R. et al. Transgenic expression of matrix metalloproteinase-9 causes adult-onset emphysema inmice associated with the loss of alveolar elastin. Am. J. Physiol. Lung Cell. Mol. Physiol. 294, L1149-L1157 (2008)
3. Reeves, E. P. et al. Killing activity of neutrophils is mediated through activation of proteases by K flux. Nature 416, 291-297 (2002)
4. Kubo, Y., Hayashi, H.,Matsuyama, T., Sato, H. & Yamamoto, N. Retrovirus entry by endocytosis and cathepsin proteases. Adv. Virol. 2012, 640894 (2012)
5. Shiomi, T., Lemaitre, V., D'Armiento, J. & Okada, Y. Matrix metalloproteinases, a disintegrin and metalloproteinases, and a disintegrin and metalloproteinases with thrombospondin motifs in non-neoplastic diseases. Pathol. Int. 60, 477-496 (2010)
6. Zheng, T. et al. Inducible targeting of IL-13 to the adult lung causes matrix metalloproteinase-and cathepsin-dependent emphysema. J. Clin. Invest. 106, 1081-1093 (2000)
7. Falsey, A. R., Hennessey, P. A., Formica, M. A., Cox, C. & Walsh, E. E. Respiratory syncytial virus infection in elderly and high-risk adults. N. Engl. J. Med. 352, 1749-1759 (2005)
8. Hirakawa, S. et al. Marked induction of matrix metalloproteinase-10 by respiratory syncytial virus infection in human nasal epithelial cells. J. Med. Virol. 85, 2141-2150 (2013)
9. Schuurhof, A. et al. Proteins involved in extracellular matrix dynamics are associated with respiratory syncytial virus disease severity. Eur. Respir. J. 39, 1475-1481 (2012)
10. Yeo, S. J. et al. Respiratory syncytial virus infection induces matrix metalloproteinase-9 expression in epithelial cells. Arch. Virol. 147, 229-242 (2002)
11. Li, W. & Shen, H. H. Effect of respiratory syncytial virus on the activity of matrix metalloproteinase in mice. Chin. Med. J. (Engl.) 120, 5-11 (2007)
12. Agnes, J. T., Zekarias, B., Shao, M., Anderson, M. L., Gershwin, L. J. & Corbeil, L. B. Bovine respiratory syncytial virus and Histophilus somni interaction at the alveolar barrier. Infect. Immun. 81, 2592-2597 (2013)
13. Pierce, R. A., Sandefur, S., Doyle, G. A. & Welgus, H. G. Monocytic cell type-specific transcriptional induction of collagenase. J. Clin. Invest. 97, 1890-1899 (1996)
14. Geraghty,P.,Dabo,A. J. &D'Armiento, J. TLR4proteincontributestocigarette smoke-induced matrix metalloproteinase-1 (MMP-1) expression in chronic obstructive pulmonary disease. J. Biol. Chem. 286, 30211-30218 (2011)
15. Ritter,M., Mennerich, D.,Weith, A. & Seither, P. Characterization of Toll-like receptors in primary lung epithelial cells: strong impact of the TLR3 ligand poly(I:C) on the regulation of Toll-like receptors, adaptor proteins and inflammatory response. J. Inflamm. (Lond.) 2, 16 (2005)
16. Slater, L. et al. Co-ordinated role of TLR3, RIG-I and MDA5 in the innate response to rhinovirus in bronchial epithelium. PLoS Pathog. 6, e1001178 (2010)
17. Marr, N. et al. Attenuation of respiratory syncytial virus-induced and RIG-Idependent type I IFN responses in human neonates and very young children. J. Immunol. 192, 948-957 (2014)
18. Xie, X. H. et al. Resveratrol Inhibits respiratory syncytial virus-induced IL-6 production, decreases viral replication, and downregulates TRIF expression in airway epithelial cells. Inflammation 35, 1392-1401 (2012)
19. Scagnolari, C. et al. Gene expression of nucleic acid-sensing pattern recognition receptors in children hospitalized for respiratory syncytial virus-associated acute bronchiolitis. Clin. Vaccine Immunol. 16, 816-823 (2009)
20. Hou, F., Sun, L., Zheng, H., Skaug, B., Jiang, Q. X. & Chen, Z. J. MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell 146, 448-461 (2011)
21. Qu, L. et al. Disruption of TLR3 signaling due to cleavage of TRIF by the hepatitis A virus protease-polymerase processing intermediate, 3CD. PLoS Pathog. 7, e1002169 (2011)
22. D'Armiento, J. M. et al. Increased matrix metalloproteinase (MMPs) levels do not predict disease severity or progression in emphysema. PLoS One 8, e56352 (2013)
23. Zhang, L., Peeples, M. E., Boucher, R. C., Collins, P. L. & Pickles, R. J. Respiratory syncytial virus infection of human airway epithelial cells is polarized, specific to ciliated cells, and without obvious cytopathology. J. Virol. 76, 5654-5666 (2002)
24. Kennedy, A., Hennessy, M., Bergin, C., Mulcahy, F., Hopkins, S. & Spiers, J. P. Ribavirin and interferon alter MMP-9 abundance in vitro and in HIV-HCV-coinfected patients. Antivir. Ther. 16, 1237-1247 (2011)
25. Khaitov, M. R. et al. siRNAs targeted to IL-4 and RSV reduce airway inflammation in a mouse model of virus-induced asthma exacerbation. Hum. Gene Ther.; e-pub ahead of print (2014)
26. Abu-Harb, M. et al. IL-8 and neutrophil elastase levels in the respiratory tract of infants with RSV bronchiolitis. Eur. Respir. J. 14, 139-143 (1999)
27. Sun, Q. et al. The specific and essential role of MAVS in antiviral innate immune responses. Immunity 24, 633-642 (2006)
28. Martinez-Gil, L., Goff,P. H.,Hai, R.,Garcia-Sastre, A., Shaw, M. L. & Palese, P. A Sendai virus-derived RNA agonist of RIG-I as a virus vaccine adjuvant. J. Virol. 87, 1290-1300 (2013)
29. Rehwinkel, J. et al. RIG-I detects viral genomic RNAduring negative-strand RNA virus infection. Cell 140, 397-408 (2010)
30. Schlee, M. et al. Recognition of 5' triphosphate by RIG-I helicase requires short blunt double-stranded RNA as contained in panhandle of negativestrand virus. Immunity 31, 25-34 (2009)
31. Liu, P., Jamaluddin, M., Li, K., Garofalo, R. P., Casola, A. & Brasier, A. R. Retinoic acid-inducible gene I mediates early antiviral response and Tolllike receptor 3 expression in respiratory syncytial virus-infected airway epithelial cells. J. Virol. 81, 1401-1411 (2007)
32. Cataldo, D. D. et al. Matrix metalloproteinase-9 deficiency impairs cellular infiltration and bronchial hyperresponsiveness during allergen-induced airway inflammation. Am. J. Pathol. 161, 491-498 (2002)
33. Yamada, H., Le, Q. T., Kousaka, A., Higashi, Y., Tsukane, M. & Kido, H. Sendai virus infection up-regulates trypsin I and matrix metalloproteinase-9, triggering viralmultiplication and matrix degradation in rat lungs and lung L2 cells. Arch. Virol. 151, 2529-2537 (2006)
34. Lee, Y. H., Lai, C. L., Hsieh, S. H., Shieh, C. C., Huang, L. M. & Wu-Hsieh, B. A. Influenza A virus induction of oxidative stress and MMP-9 is associated with severe lung pathology in a mouse model. Virus Res. 178, 411-422 (2013)
35. Bradley, L. M., Douglass, M. F., Chatterjee, D., Akira, S. & Baaten, B. J. Matrix metalloprotease 9 mediates neutrophil migration into the airways in response to influenza virus-induced toll-like receptor signaling. PLoS Pathog. 8, e1002641 (2012)
36. Sulik, A., Wojtkowska, M. &Oldak, E. Elevated levels ofMMP-9and TIMP-1 in the cerebrospinal fluid of children with echovirus type 30 and mumps meningitis. Scand. J. Immunol. 68, 323-327 (2008)
37. Monick, M. M. et al. Activation of the epidermal growth factor receptor by respiratory syncytial virus results in increased inflammation and delayed apoptosis. J. Biol. Chem. 280, 2147-2158 (2005)
38. Jouneau, S. et al. EMMPRIN (CD147) regulation of MMP-9 in bronchial epithelial cells in COPD. Respirology 16, 705-712 (2011)
39. Guillot, S. et al. Increased extracellular matrix metalloproteinase inducer (EMMPRIN) expression in pulmonary fibrosis. Exp. Lung Res. 32, 81-97 (2006)
40. Matsumoto, F. et al. Cathepsins are required for Toll-like receptor 9 responses. Biochem. Biophys. Res. Commun. 367, 693-699 (2008)
41. Chockalingam, A., Cameron, J. L., Brooks, J. C. & Leifer, C. A. Negative regulation of signaling by a soluble form of toll-like receptor 9. Eur. J. Immunol. 41, 2176-2184 (2011)
42. Murray, M. Y. et al. Macrophage migration and invasion is regulated by MMP10 expression. PLoS One 8, e63555 (2013)
43. Beck, I. M. et al. MMP19 is essential for T cell development and T cellmediated cutaneous immune responses. PLoS One 3, e2343 (2008)
44. Gharib, S. A. et al. MMP28 promotes macrophage polarization toward M2 cells and augments pulmonary fibrosis. J. Leukoc. Biol. 95, 9-18 (2013)
45. Geraghty, P., Greene, C. M., O'Mahony, M., O'Neill, S. J., Taggart, C. C. & McElvaney, N. G. Secretory leucocyte protease inhibitor inhibits interferon-gamma-induced cathepsin S expression. J. Biol. Chem. 282, 33389-33395 (2007).