Rhinovirus-induced MMP-9 expression is dependent on Fra-1, which is modulated by formoterol and dexamethasone

Journal of Immunology

Volumn 188, Issue 9, 2012, Pages 4621-4630

  Tacon, Claire E ^a   Newton, Robert ^a   Proud, David ^a   Leigh, Richard ^a  

^a University of Calgary and Alberta Health Services   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DEXAMETHASONE; FORMOTEROL; GELATINASE B; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; PROTEIN FOS; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR FRA 1;

ARTICLE; BRONCHUS MUCOSA; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; EPITHELIUM CELL; HUMAN; HUMAN CELL; HUMAN RHINOVIRUS; HUMAN RHINOVIRUS 16; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RHINOVIRUS INFECTION; VIRUS CELL INTERACTION;

ANTI-INFLAMMATORY AGENTS; BRONCHODILATOR AGENTS; BUTADIENES; CELL LINE; DEXAMETHASONE; ENZYME INHIBITORS; ETHANOLAMINES; FLAVONOIDS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MAP KINASE KINASE 1; MAP KINASE KINASE 2; MAP KINASE SIGNALING SYSTEM; MATRIX METALLOPROTEINASE 9; NITRILES; PHOSPHORYLATION; PICORNAVIRIDAE INFECTIONS; PROTO-ONCOGENE PROTEINS C-FOS; RESPONSE ELEMENTS; RHINOVIRUS; TRANSCRIPTION FACTOR AP-1;

EID: 84860320293     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101666     Document Type: Article

References (57)

1. Broide, D. 2008. New perspectives on mechanisms underlying chronic allergic inflammation and asthma in 2007. J. Allergy Clin. Immunol. 122: 475-480.
2. Cockcroft, D. W., and B. E. Davis. 2006. Mechanisms of airway hyperresponsiveness. J. Allergy Clin. Immunol. 118: 551-559; quiz 560-551. (Pubitemid 44301418)
3. O'Byrne, P. M., G. M. Gauvreau, and J. D. Brannan. 2009. Provoked models of asthma: what have we learnt? Clin. Exp. Allergy 39: 181-192.
4. Nicholson, K. G., J. Kent, and D. C. Ireland. 1993. Respiratory viruses and exacerbations of asthma in adults. BMJ 307: 982-986. (Pubitemid 23306765)
5. Johnston, S. L., P. K. Pattemore, G. Sanderson, S. Smith, F. Lampe, L. Josephs, P. Symington, S. O'Toole, S. H. Myint, D. A. Tyrrell, et al. 1995. Community study of role of viral infections in exacerbations of asthma in 9-11 year old children. BMJ 310: 1225-1229.
6. Kotaniemi-Syrjänen, A., R. Vainionpää, T. M. Reijonen, M. Waris, K. Korhonen, and M. Korppi. 2003. Rhinovirus-induced wheezing in infancy - the first sign of childhood asthma? J. Allergy Clin. Immunol. 111: 66-71. (Pubitemid 36143293)
7. Kusel, M. M., N. H. de Klerk, T. Kebadze, V. Vohma, P. G. Holt, S. L. Johnston, and P. D. Sly. 2007. Early-life respiratory viral infections, atopic sensitization, and risk of subsequent development of persistent asthma. J. Allergy Clin. Immunol. 119: 1105-1110. (Pubitemid 46654175)
8. Jackson, D. J., R. E. Gangnon, M. D. Evans, K. A. Roberg, E. L. Anderson, T. E. Pappas, M. C. Printz, W. M. Lee, P. A. Shult, E. Reisdorf, et al. 2008. Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children. Am. J. Respir. Crit. Care Med. 178: 667-672.
9. Jackson, D. J., and S. L. Johnston. 2010. The role of viruses in acute exacerbations of asthma. J. Allergy Clin. Immunol. 125: 1178-1187; quiz 1188-1179.
10. Spurrell, J. C., S. Wiehler, R. S. Zaheer, S. P. Sanders, and D. Proud. 2005. Human airway epithelial cells produce IP-10 (CXCL10) in vitro and in vivo upon rhinovirus infection. Am. J. Physiol. Lung Cell. Mol. Physiol. 289: L85-L95. (Pubitemid 40863558)
11. Proud, D., J. M. Gwaltney, Jr., J. O. Hendley, C. A. Dinarello, S. Gillis, and R. P. Schleimer. 1994. Increased levels of interleukin-1 are detected in nasal secretions of volunteers during experimental rhinovirus colds. J. Infect. Dis. 169: 1007-1013. (Pubitemid 24303219)
12. Leigh, R., W. Oyelusi, S. Wiehler, R. Koetzler, R. S. Zaheer, R. Newton, and D. Proud. 2008. Human rhinovirus infection enhances airway epithelial cell production of growth factors involved in airway remodeling. J. Allergy Clin. Immunol. 121: 1238-1245.
13. Tacon, C. E., S. Wiehler, N. S. Holden, R. Newton, D. Proud, and R. Leigh. 2010. Human rhinovirus infection up-regulates MMP-9 production in airway epithelial cells via NF-κB. Am. J. Respir. Cell Mol. Biol. 43: 201-209.
14. Hoshino, M., Y. Nakamura, J. Sim, J. Shimojo, and S. Isogai. 1998. Bronchial subepithelial fibrosis and expression of matrix metalloproteinase-9 in asthmatic airway inflammation. J. Allergy Clin. Immunol. 102: 783-788. (Pubitemid 28543528)
15. Vignola, A. M., L. Riccobono, A. Mirabella, M. Profita, P. Chanez, V. Bellia, G. Mautino, P. D'accardi, J. Bousquet, and G. Bonsignore. 1998. Sputum metalloproteinase-9/tissue inhibitor of metalloproteinase-1 ratio correlates with airflow obstruction in asthma and chronic bronchitis. Am. J. Respir. Crit. Care Med. 158: 1945-1950. (Pubitemid 29008837)
16. Mattos, W., S. Lim, R. Russell, A. Jatakanon, K. F. Chung, and P. J. Barnes. 2002. Matrix metalloproteinase-9 expression in asthma: effect of asthma severity, allergen challenge, and inhaled corticosteroids. Chest 122: 1543-1552. (Pubitemid 35366062)
17. Tanaka, H., N. Miyazaki, K. Oashi, S. Tanaka, M. Ohmichi, and S. Abe. 2000. Sputum matrix metalloproteinase-9: tissue inhibitor of metalloproteinase-1 ratio in acute asthma. J. Allergy Clin. Immunol. 105: 900-905. (Pubitemid 30324397)
18. Wenzel, S. E., S. Balzar, M. Cundall, and H. W. Chu. 2003. Subepithelial basement membrane immunoreactivity for matrix metalloproteinase 9: association with asthma severity, neutrophilic inflammation, and wound repair. J. Allergy Clin. Immunol. 111: 1345-1352. (Pubitemid 36683691)
19. Lagente, V., and E. Boichot. 2010. Role of matrix metalloproteinases in the inflammatory process of respiratory diseases. J. Mol. Cell. Cardiol. 48: 440-444.
20. Atkinson, J. J., and R. M. Senior. 2003. Matrix metalloproteinase-9 in lung remodeling. Am. J. Respir. Cell Mol. Biol. 28: 12-24. (Pubitemid 36017046)
21. Broide, D. H. 2008. Immunologic and inflammatory mechanisms that drive asthma progression to remodeling. J. Allergy Clin. Immunol. 121: 560-570; quiz 571-562. (Pubitemid 351323873)
22. Gum, R., H. Wang, E. Lengyel, J. Juarez, and D. Boyd. 1997. Regulation of 92 kDa type IV collagenase expression by the jun aminoterminal kinase- and the extracellular signal-regulated kinase-dependent signaling cascades. Oncogene 14: 1481-1493. (Pubitemid 27182438)
23. Hong, S., K. K. Park, J. Magae, K. Ando, T. S. Lee, T. K. Kwon, J. Y. Kwak, C. H. Kim, and Y. C. Chang. 2005. Ascochlorin inhibits matrix metalloproteinase-9 expression by suppressing activator protein-1-mediated gene expression through the ERK1/2 signaling pathway: inhibitory effects of ascochlorin on the invasion of renal carcinoma cells. J. Biol. Chem. 280: 25202-25209. (Pubitemid 40934613)
24. Churchill, L., F. H. Chilton, J. H. Resau, R. Bascom, W. C. Hubbard, and D. Proud. 1989. Cyclooxygenase metabolism of endogenous arachidonic acid by cultured human tracheal epithelial cells. Am. Rev. Respir. Dis. 140: 449-459. (Pubitemid 19218364)
25. Gern, J. E., R. Vrtis, E. A. Kelly, E. C. Dick, and W. W. Busse. 1996. Rhinovirus produces nonspecific activation of lymphocytes through a monocyte-dependent mechanism. J. Immunol. 157: 1605-1612. (Pubitemid 126449100)
26. Sanders, S. P., E. S. Siekierski, J. D. Porter, S. M. Richards, and D. Proud. 1998. Nitric oxide inhibits rhinovirus-induced cytokine production and viral replication in a human respiratory epithelial cell line. J. Virol. 72: 934-942. (Pubitemid 28116870)
27. Mosser, A. G., R. Brockman-Schneider, S. Amineva, L. Burchell, J. B. Sedgwick, W. W. Busse, and J. E. Gern. 2002. Similar frequency of rhinovirus-infectible cells in upper and lower airway epithelium. J. Infect. Dis. 185: 734-743. (Pubitemid 34226201)
28. Song, Y., L. Qian, S. Song, L. Chen, Y. Zhang, G. Yuan, H. Zhang, Q. Xia, M. Hu, M. Yu, et al. 2008. Fra-1 and Stat3 synergistically regulate activation of human MMP-9 gene. Mol. Immunol. 45: 137-143. (Pubitemid 47331648)
29. Westermarck, J., and V. M. Kähäri. 1999. Regulation of matrix metalloproteinase expression in tumor invasion. FASEB J. 13: 781-792. (Pubitemid 29220691)
30. Chandrasekar, B., S. Mummidi, L. Mahimainathan, D. N. Patel, S. R. Bailey, S. Z. Imam, W. C. Greene, and A. J. Valente. 2006. Interleukin-18- induced human coronary artery smooth muscle cell migration is dependent on NF-kappaB-and AP-1-mediated matrix metalloproteinase-9 expression and is inhibited by atorvastatin. J. Biol. Chem. 281: 15099-15109. (Pubitemid 43855099)
31. Holden, N. S., and C. E. Tacon. 2011. Principles and problems of the electrophoretic mobility shift assay. J. Pharmacol. Toxicol. Methods 63: 7-14.
32. Basbous, J., D. Chalbos, R. Hipskind, I. Jariel-Encontre, and M. Piechaczyk. 2007. Ubiquitin-independent proteasomal degradation of Fra-1 is antagonized by Erk1/2 pathway-mediated phosphorylation of a unique C-terminal destabilizer. Mol. Cell. Biol. 27: 3936-3950. (Pubitemid 47010992)
33. Zaheer, R. S., R. Koetzler, N. S. Holden, S. Wiehler, and D. Proud. 2009. Selective transcriptional down-regulation of human rhinovirus-induced production of CXCL10 from airway epithelial cells via the MEK1 pathway. J. Immunol. 182: 4854-4864.
34. National Asthma Education and Prevention Program. 2007. Expert Panel Report 3 (EPR-3): Guidelines for the Diagnosis and Management of Asthma-Summary Report 2007. J. Allergy Clin. Immunol. 120(5, Suppl): S94-S138.
35. Bateman, E. D., S. S. Hurd, P. J. Barnes, J. Bousquet, J. M. Drazen, M. FitzGerald, P. Gibson, K. Ohta, P. O'Byrne, S. E. Pedersen, et al. 2008. Global strategy for asthma management and prevention: GINA executive summary. Eur. Respir. J. 31: 143-178.
36. Erlewyn-Lajeunesse, M. D., L. P. Hunt, P. Pohunek, S. J. Dobson, P. Kochhar, J. A. Warner, and J. O. Warner. 2008. Bronchoalveolar lavage MMP-9 and TIMP-1 in preschool wheezers and their relationship to persistent wheeze. Pediatr. Res. 64: 194-199.
37. Glasheen, B. M., R. M. Robbins, C. Piette, G. J. Beitel, and A. Page-McCaw. 2010. A matrix metalloproteinase mediates airway remodeling in Drosophila. Dev. Biol. 344: 772-783.
38. Funkhouser, A. W., J. A. Kang, A. Tan, J. Li, L. Zhou, M. K. Abe, J. Solway, and M. B. Hershenson. 2004. Rhinovirus 16 3C protease induces interleukin-8 and granulocyte-macrophage colony-stimulating factor expression in human bronchial epithelial cells. Pediatr. Res. 55: 13-18. (Pubitemid 38018686)
39. Takagi, S., S. Simizu, and H. Osada. 2009. RECK negatively regulates matrix metalloproteinase-9 transcription. Cancer Res. 69: 1502-1508.
40. Zhang, Q., S. R. Kleeberger, and S. P. Reddy. 2004. DEP-induced fra-1 expression correlates with a distinct activation of AP-1-dependent gene transcription in the lung. Am. J. Physiol. Lung Cell. Mol. Physiol. 286: L427-L436. (Pubitemid 38129525)
41. Young, M. R., and N. H. Colburn. 2006. Fra-1 a target for cancer prevention or intervention. Gene 379: 1-11. (Pubitemid 44247331)
42. Young, M. R., R. Nair, N. Bucheimer, P. Tulsian, N. Brown, C. Chapp, T. C. Hsu, and N. H. Colburn. 2002. Transactivation of Fra-1 and consequent activation of AP-1 occur extracellular signal-regulated kinase dependently. Mol. Cell. Biol. 22: 587-598. (Pubitemid 34027503)
43. Global Initiative for Asthma. 2009. Available at: http://www.ginasthma. org/guidelines-gina-report-global-strategy-for-asthma.html. Accessed: February 26, 2012.
44. Farr, B. M., J. M. Gwaltney, Jr., J. O. Hendley, F. G. Hayden, R. M. Naclerio, T. McBride, W. J. Doyle, J. V. Sorrentino, D. K. Riker, and D. Proud. 1990. A randomized controlled trial of glucocorticoid prophylaxis against experimental rhinovirus infection. J. Infect. Dis. 162: 1173-1177. (Pubitemid 20353601)
45. Gustafson, L. M., D. Proud, J. O. Hendley, F. G. Hayden, and J. M. Gwaltney, Jr. 1996. Oral prednisone therapy in experimental rhinovirus infections. J. Allergy Clin. Immunol. 97: 1009-1014. (Pubitemid 26116996)
46. Stellato, C. 2007. Glucocorticoid actions on airway epithelial responses in immunity: functional outcomes and molecular targets. J. Allergy Clin. Immunol. 120: 1247-1263; quiz 1264-1245. (Pubitemid 350216618)
47. Kim, J., S. P. Sanders, E. S. Siekierski, V. Casolaro, and D. Proud. 2000. Role of NF-kappa B in cytokine production induced from human airway epithelial cells by rhinovirus infection. J. Immunol. 165: 3384-3392.
48. Matsukura, S., F. Kokubu, M. Kurokawa, M. Kawaguchi, H. Kuga, K. Ieki, M. Odaka, S. Suzuki, S. Watanabe, H. Takeuchi, et al. 2004. Molecular mechanisms of repression of eotaxin expression with fluticasone propionate in airway epithelial cells. Int. Arch. Allergy Immunol. 134(Suppl 1): 12-20. (Pubitemid 38721121)
49. Newton, R., L. A. Hart, D. A. Stevens, M. Bergmann, L. E. Donnelly, I. M. Adcock, and P. J. Barnes. 1998. Effect of dexamethasone on interleukin-1beta- (IL-1beta)-induced nuclear factor-kappaB (NF-kappaB) and kappaB-dependent transcription in epithelial cells. Eur. J. Biochem. 254: 81-89. (Pubitemid 28255072)
50. Holden, N. S., C. F. Rider, M. J. Bell, J. Velayudhan, E. M. King, M. Kaur, M. Salmon, M. A. Giembycz, and R. Newton. 2010. Enhancement of inflammatory mediator release by beta(2)-adrenoceptor agonists in airway epithelial cells is reversed by glucocorticoid action. Br. J. Pharmacol. 160: 410-420.
51. LeVan, T. D., F. D. Behr, K. K. Adkins, R. L. Miesfeld, and J. W. Bloom. 1997. Glucocorticoid receptor signaling in a bronchial epithelial cell line. Am. J. Physiol. 272: L838-L843.
52. Newton, R., R. Leigh, and M. A. Giembycz. 2010. Pharmacological strategies for improving the efficacy and therapeutic ratio of glucocorticoids in inflammatory lung diseases. Pharmacol. Ther. 125: 286-327.
53. Chivers, J. E., W. Gong, E. M. King, J. Seybold, J. C. Mak, L. E. Donnelly, N. S. Holden, and R. Newton. 2006. Analysis of the dissociated steroid RU24858 does not exclude a role for inducible genes in the anti-inflammatory actions of glucocorticoids. Mol. Pharmacol. 70: 2084-2095. (Pubitemid 44771924)
54. Kaur, M., J. E. Chivers, M. A. Giembycz, and R. Newton. 2008. Long-acting beta2-adrenoceptor agonists synergistically enhance glucocorticoid-dependent transcription in human airway epithelial and smooth muscle cells. Mol. Pharmacol. 73: 203-214. (Pubitemid 350294211)
55. King, E. M., N. S. Holden, W. Gong, C. F. Rider, and R. Newton. 2009. Inhibition of NF-kappaB-dependent transcription by MKP-1: transcriptional repression by glucocorticoids occurring via p38 MAPK. J. Biol. Chem. 284: 26803-26815.
56. Prazma, C. M., K. M. Kral, N. Gul, S. W. Yancey, and D. A. Stempel. 2010. Controller medications and their effects on asthma exacerbations temporally associated with upper respiratory infections. Respir. Med. 104: 780-787.
57. Reddel, H. K., C. Jenkins, S. Quirce, M. R. Sears, E. D. Bateman, P. M. O'Byrne, M. Humbert, R. Buhl, T. Harrison, G. G. Brusselle, et al. 2011. Effect of different asthma treatments on risk of cold-related exacerbations. Eur. Respir. J. 38: 584-593.