Synthetic double-stranded RNA enhances airway inflammation and remodelling in a rat model of asthma

Immunology

Volumn 134, Issue 2, 2011, Pages 140-150

  Takayama, Satoshi ^a   Tamaoka, Meiyo ^a   Takayama, Koji ^a   Okayasu, Kaori ^a   Tsuchiya, Kimitake ^a   Miyazaki, Yasunari ^a   Sumi, Yuki ^a   Martin, James G ^b   Inase, Naohiko ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Airway remodelling; Asthma; Brown Norway rats; Double stranded RNA; Poly I:C

Indexed keywords

CHEMOKINE; CYTOKINE; DOUBLE STRANDED RNA; INTERLEUKIN 12; INTERLEUKIN 17; OVALBUMIN; POLYINOSINIC POLYCYTIDYLIC ACID; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; BROWN NORWAY RAT; CELL HYPERPLASIA; CELL PROLIFERATION; DISEASE EXACERBATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EOSINOPHIL; GENE EXPRESSION; GOBLET CELL; HISTOLOGY; LUNG LAVAGE; MALE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; RESPIRATORY EPITHELIUM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS INFECTION;

AIRWAY REMODELING; ANIMALS; ASTHMA; BRONCHOALVEOLAR LAVAGE FLUID; CELL PROLIFERATION; CYTOKINES; DISEASE MODELS, ANIMAL; GOBLET CELLS; LUNG; MALE; MUSCLE, SMOOTH; NEUTROPHILS; OVALBUMIN; POLY I-C; RATS; RNA, DOUBLE-STRANDED;

EID: 80052488055     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2011.03473.x     Document Type: Article

References (47)

1. Bousquet J, Jeffery PK, Busse WW, Johnson M, Vignola AM. Asthma. From bronchoconstriction to airways inflammation and remodeling. Am J Respir Crit Care Med 2000; 161:1720-45.
2. Nicholson KG, Kent J, Ireland DC. Respiratory viruses and exacerbations of asthma in adults. BMJ 1993; 307:982-6.
3. Atmar RL, Guy E, Guntupalli KK, Zimmerman JL, Bandi VD, Baxter BD, Greenberg SB. Respiratory tract viral infections in inner-city asthmatic adults. Arch Intern Med 1998; 158:2453-9.
4. Grissell TV, Powell H, Shafren DR, Boyle MJ, Hensley MJ, Jones PD, Whitehead BF, Gibson PG. Interleukin-10 gene expression in acute virus-induced asthma. Am J Respir Crit Care Med 2005; 172:433-9.
5. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001; 413:732-8.
6. Kato H, Takeuchi O, Sato S et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006; 441:101-5.
7. Kato H, Takeuchi O, Mikamo-Satoh E et al. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J Exp Med 2008; 205:1601-10.
8. Kulka M, Alexopoulou L, Flavell RA, Metcalfe DD. Activation of mast cells by double-stranded RNA: evidence for activation through Toll-like receptor 3. J Allergy Clin Immunol 2004; 114:174-82.
9. Matsukura S, Kokubu F, Kurokawa M et al. Synthetic double-stranded RNA induces multiple genes related to inflammation through Toll-like receptor 3 depending on NF-kappaB and/or IRF-3 in airway epithelial cells. Clin Exp Allergy 2006; 36:1049-62.
10. Gern JE, French DA, Grindle KA, Brockman-Schneider RA, Konno S, Busse WW. Double-stranded RNA induces the synthesis of specific chemokines by bronchial epithelial cells. Am J Respir Cell Mol Biol 2003; 28:731-7.
11. Zhu L, Lee PK, Lee WM, Zhao Y, Yu D, Chen Y. Rhinovirus-induced major airway mucin production involves a novel TLR3-EGFR-dependent pathway. Am J Respir Cell Mol Biol 2009; 40:610-9.
12. Sugiura H, Ichikawa T, Koarai A et al. Activation of Toll-like receptor 3 augments myofibroblast differentiation. Am J Respir Cell Mol Biol 2009; 40:654-62.
13. Shiraishi Y, Asano K, Niimi K et al. Cyclooxygenase-2/prostaglandin D2/CRTH2 pathway mediates double-stranded RNA-induced enhancement of allergic airway inflammation. J Immunol 2008; 180:541-9.
14. Jeon SG, Oh SY, Park HK et al. TH2 and TH1 lung inflammation induced by airway allergen sensitization with low and high doses of double-stranded RNA. J Allergy Clin Immunol 2007; 120:803-12.
15. Sapienza S, Du T, Eidelman DH, Wang NS, Martin JG. Structural changes in the airways of sensitized brown Norway rats after antigen challenge. Am Rev Respir Dis 1991; 144:423-7.
16. Pini L, Torregiani C, Martin JG, Hamid Q, Ludwig MS. Airway remodeling in allergen-challenged Brown Norway rats: distribution of proteoglycans. Am J Physiol Lung Cell Mol Physiol 2006; 290:L1052-8.
17. Hayashi A, Nakashima K, Yamagishi K, Hoshi T, Suzuki A, Baba H. Localization of annexin II in the paranodal regions and Schmidt-Lanterman incisures in the peripheral nervous system. Glia 2007; 55:1044-52.
18. Voisine C, Hubert FX, Trinité B, Heslan M, Josien R. Two phenotypically distinct subsets of spleen dendritic cells in rats exhibit different cytokine production and T cell stimulatory activity. J Immunol 2002; 169:2284-91.
19. Lin CC, Lin CY, Ma HY. Pulmonary function changes and increased Th-2 cytokine expression and nuclear factor kB activation in the lung after sensitization and allergen challenge in brown Norway rats. Immunol Lett 2000; 73:57-64.
20. Kruschinski C, Skripuletz T, Bedoui S et al. Postnatal life events affect the severity of asthmatic airway inflammation in the adult rat. J Immunol 2008; 180:3919-25.
21. Maghni K, Michoud MC, Alles M, Rubin A, Govindaraju V, Meloche C, Martin JG. Airway smooth muscle cells express functional neurokinin-1 receptors and the nerve-derived preprotachykinin-a gene: regulation by passive sensitization. Am J Respir Cell Mol Biol 2003; 28:103-10.
22. Muto S, Monnai M, Okuhara Y, Murakami M, Kuroda J, Ono T, Matsumoto K. Altered cytokine expression in mesenteric lymph nodes in a rat strain (Matsumoto Eosinophilic Shinshu) that spontaneously develops hypereosinophilia. Immunology 2005; 116:373-80.
23. Harty MW, Papa EF, Huddleston HM et al. Hepatic macrophages promote the neutrophil-dependent resolution of fibrosis in repairing cholestatic rat livers. Surgery 2008; 143:667-78.
24. Dai J, Gilks B, Price K, Churg A. Mineral dusts directly induce epithelial and interstitial fibrogenic mediators and matrix components in the airway wall. Am J Respir Crit Care Med 1998; 158:1907-13.
25. Woodruff PG, Dolganov GM, Ferrando RE et al. Hyperplasia of smooth muscle in mild to moderate asthma without changes in cell size or gene expression. Am J Respir Crit Care Med 2004; 169:1001-6.
26. Camateros P, Tamaoka M, Hassan M et al. Chronic asthma-induced airway remodeling is prevented by toll-like receptor-7/8 ligand S28463. Am J Respir Crit Care Med 2007; 175:1241-9.
27. Murakami D, Yamada H, Yajima T, Masuda A, Komune S, Yoshikai Y. Lipopolysaccharide inhalation exacerbates allergic airway inflammation by activating mast cells and promoting Th2 responses. Clin Exp Allergy 2007; 37:339-47.
28. Savov JD, Brass DM, Lawson BL, McElvania-Tekippe E, Walker JK, Schwartz DA. Toll-like receptor 4 antagonist (E5564) prevents the chronic airway response to inhaled lipopolysaccharide. Am J Physiol Lung Cell Mol Physiol 2005; 289:L329-37.
29. Lombardi V, Van Overtvelt L, Horiot S et al. Toll-like receptor 2 agonist Pam3CSK4 enhances the induction of antigen-specific tolerance via the sublingual route. Clin Exp Allergy 2008; 38:1819-29.
30. Kuo C, Lim S, King NJ et al. Rhinovirus infection induces expression of airway remodeling factors in vitro and in vivo. Respirology, Minneapolis, MN
31. Kuo C, Lim S, King NJ, Johnston SL, Burgess JK, Black JL, Oliver BG. Rhinovirus infection induces extracellular matrix protein deposition in asthmatic and non-asthmatic airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2011; 300:L951-7.
32. Vignola AM, Chanez P, Chiappara G et al. Transforming growth factor-beta expression in mucosal biopsies in asthma and chronic bronchitis. Am J Respir Crit Care Med 1997; 156:591-9.
33. McMillan SJ, Xanthou G, Lloyd CM. Manipulation of allergen-induced airway remodeling by treatment with anti-TGF-beta antibody: effect on the Smad signaling pathway. J Immunol 2005; 174:5774-80.
34. Larché M, Robinson DS, Kay AB. The role of T lymphocytes in the pathogenesis of asthma. J Allergy Clin Immunol 2003; 111:450-63.
35. + T cells in atopic asthma. Am J Respir Crit Care Med 2005; 171:224-30.
36. + T cells in asthma. Am J Respir Crit Care Med 2000; 161:1790-6.
37. Kim YK, Oh SY, Jeon SG et al. Airway exposure levels of lipopolysaccharide determine type 1 versus type 2 experimental asthma. J Immunol 2007; 178:5375-82.
38. Shannon J, Ernst P, Yamauchi Y et al. Differences in airway cytokine profile in severe asthma compared to moderate asthma. Chest 2008; 133:420-6.
39. Douwes J, Gibson P, Pekkanen J, Pearce N. Non-eosinophilic asthma: importance and possible mechanisms. Thorax 2002; 57:643-8.
40. Bullens DM, Truyen E, Coteur L, Dilissen E, Hellings PW, Dupont LJ, Ceuppens JL. IL-17 mRNA in sputum of asthmatic patients: linking T cell driven inflammation and granulocytic influx? Respir Res 2006; 7:135-43.
41. Molet S, Hamid Q, Davoine F et al. IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines. J Allergy Clin Immunol 2001; 108:430-8.
42. Chakir J, Shannon J, Molet S, Fukakusa M, Elias J, Laviolette M, Boulet LP, Hamid Q. Airway remodeling-associated mediators in moderate to severe asthma: effect of steroids on TGF-beta, IL-11, IL-17, and type I and type III collagen expression. J Allergy Clin Immunol 2003; 111:1293-8.
43. Agache I, Ciobanu C, Agache C, Anghel M. Increased serum IL-17 is an independent risk factor for severe asthma. Respir Med 2010; 104:1131-7.
44. Stowell NC, Seideman J, Raymond HA et al. Long-term activation of TLR3 by poly(I:C) induces inflammation and impairs lung function in mice. Respir Res 2009; 10:43-56.
45. Choi JP, Kim YS, Tae YM et al. A viral PAMP double-stranded RNA induces allergen-specific Th17 cell response in the airways which is dependent on VEGF and IL-6. Allergy 2010; 65:1322-30.
46. Shin TS, Lee BJ, Tae YM, Kim YS, Jeon SG, Gho YS, Choi DC, Kim YK. Role of inducible nitric oxide synthase on the development of virus-associated asthma exacerbation which is dependent on Th1 and Th17 cell responses. Exp Mol Med 2010; 42:721-30.
47. Torres D, Dieudonné A, Ryffel B et al. Double-stranded RNA exacerbates pulmonary allergic reaction through TLR3: implication of airway epithelium and dendritic cells. J Immunol 2010; 185:451-9.