Cigarette smoke attenuates the RIG-I-initiated innate antiviral response to influenza infection in two murine models

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 307, Issue 11, 2014, Pages L848-L858

  Wu, Wenxin ^a   Zhang, Wei ^a   More, Sunil ^b   Booth, J Leland ^a   Duggan, Elizabeth S ^a   Liu, Lin ^b   Zhao, Yan D ^c   Metcalf, Jordan P ^a,d  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b OKLAHOMA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Cytokine; Lung; Mouse; Retinoic acid inducible gene I; Toll like receptor 3

Indexed keywords

BETA INTERFERON; CIGARETTE SMOKE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 6; RETINOIC ACID INDUCIBLE PROTEIN I; TOLL LIKE RECEPTOR 3; TUMOR NECROSIS FACTOR ALPHA; CXCL10 PROTEIN, MOUSE; DDX58 PROTEIN, MOUSE; DEAD BOX PROTEIN; SMOKE; TLR3 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE RESPONSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HOST RESISTANCE; IMMUNOSUPPRESSIVE TREATMENT; IN VIVO STUDY; INFECTION SENSITIVITY; INFLUENZA A; INFLUENZA VIRUS A; INNATE IMMUNITY; LUNG; LUNG INJURY; LUNG LAVAGE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; VIRUS IMMUNITY; VIRUS PNEUMONIA; VIRUS REPLICATION; ADVERSE EFFECTS; ANIMAL; BIOSYNTHESIS; BRONCHOALVEOLAR LAVAGE FLUID; C57BL MOUSE; DRUG EFFECTS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; INFLUENZA A VIRUS (H1N1); ORTHOMYXOVIRIDAE INFECTIONS; SMOKE; SMOKING; TOBACCO;

ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CHEMOKINE CXCL10; DEAD-BOX RNA HELICASES; FEMALE; IMMUNE TOLERANCE; IMMUNITY, INNATE; INFLUENZA A VIRUS, H1N1 SUBTYPE; INTERFERON-BETA; INTERLEUKIN-6; LUNG; MICE; MICE, INBRED C57BL; ORTHOMYXOVIRIDAE INFECTIONS; SMOKE; SMOKING; TOBACCO; TOLL-LIKE RECEPTOR 3; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84913592369     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00158.2014     Document Type: Article

References (36)

1. Arcavi L, Benowitz NL. Cigarette smoking and infection. Arch Intern Med 164: 2206-2216, 2004.
2. Bagaitkar J, Demuth DR, Scott DA. Tobacco use increases susceptibility to bacterial infection (Abstract). Tob Induc Dis 4: 12, 2008.
3. Carp H, Janoff A. Possible mechanisms of emphysema in smokers. In vitro suppression of serum elastase-inhibitory capacity by fresh cigarette smoke and its prevention by antioxidants. Am Rev Respir Dis 118: 617-621, 1978.
4. Churg A, Cosio M, Wright JL. Mechanisms of cigarette smoke-induced COPD: insights from animal models. Am J Physiol Lung Cell Mol Physiol 294: L612-L631, 2008.
5. Eddleston J, Lee RU, Doerner AM, Herschbach J, Zuraw BL. Cigarette smoke decreases innate responses of epithelial cells to rhinovirus infection. Am J Respir Cell Mol Biol 44: 118-126, 2011.
6. Elliott MK, Sisson JH, West WW, Wyatt TA. Differential in vivo effects of whole cigarette smoke exposure versus cigarette smoke extract on mouse ciliated tracheal epithelium. Exp Lung Res 32: 99-118, 2006.
7. Feng Y, Kong Y, Barnes PF, Huang FF, Klucar P, Wang X, Samten B, Sengupta M, Machona B, Donis R, Tvinnereim AR, Shams H. Exposure to cigarette smoke inhibits the pulmonary T-cell response to influenza virus and Mycobacterium tuberculosis. Infect Immun 79: 229-237, 2011.
8. Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, Golen-bock DT, Coyle AJ, Liao SM, Maniatis T. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 4: 491–496, 2003.
9. Gualano RC, Hansen MJ, Vlahos R, Jones JE, Park-Jones RA, Deliyannis G, Turner SJ, Duca KA, Anderson GP. Cigarette smoke worsens lung inflammation and impairs resolution of influenza infection in mice (Abstract). Respir Res 9: 53, 2008.
10. Guillot L, Le Goffic R, Bloch S, Escriou N, Akira S, Chignard M, Si-Tahar M. 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, 2005.
11. Hanshaoworakul W, Simmerman JM, Narueponjirakul U, Sanasut-tipun W, Shinde V, Kaewchana S, Areechokechai D, Levy J, Ungchu-sak K. Severe human influenza infections in Thailand: oseltamivir treatment and risk factors for fatal outcome. PLoS One 4: e6051, 2009.
12. Heinz S, Haehnel V, Karaghiosoff M, Schwarzfischer L, Muller M, Krause SW, Rehli M. Species-specific regulation of Toll-like receptor 3 genes in men and mice. J Biol Chem 278: 21502-21509, 2003.
13. Horvath KM, Brighton LE, Zhang W, Carson JL, Jaspers I. Epithelial cells from smokers modify dendritic cell responses in the context of influenza infection. Am J Respir Cell Mol Biol 45: 237-245, 2011.
14. Huang J, Okuka M, McLean M, Keefe DL, Liu L. Effects of cigarette smoke on fertilization and embryo development in vivo. Fertil Steril 92: 1456-1465, 2009.
15. Imaizumi T, Kumagai M, Taima K, Fujita T, Yoshida H, Satoh K. Involvement of retinoic acid-inducible gene-I in the IFN--//STAT1 signalling pathway in BEAS-2B cells. Eur Respir J 25: 1077-1083, 2005.
16. Jaspers I, Horvath KM, Zhang W, Brighton LE, Carson JL, Noah TL. Reduced expression of IRF7 in nasal epithelial cells from smokers after infection with influenza. Am J Respir Cell Mol Biol 43: 368-375, 2010.
17. Kark JD, Lebiush M. Smoking and epidemic influenza-like illness in female military recruits: a brief survey. Am J Public Health 71: 530-532, 1981.
18. Koarai A, Yanagisawa S, Sugiura H, Ichikawa T, Akamatsu K, Hirano T, Nakanishi M, Matsunaga K, Minakata Y, Ichinose M. Cigarette smoke augments the expression and responses of toll-like receptor 3 in human macrophages. Respirology 17: 1018-1025, 2012.
19. Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK, Langer JA, Sheikh F, Dickensheets H, Donnelly RP. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol 4: 69–77, 2003.
20. Le Goffic R, Balloy V, Lagranderie M, Alexopoulou L, Escriou N, Flavell R, Chignard M, Si-Tahar M. Detrimental contribution of the Toll-like receptor (TLR)3 to influenza A virus-induced acute pneumonia. PLoS Pathog 2: e53, 2006.
21. Liu S, Sun J, Cai J, Miao Z, Lu M, Qin S, Wang X, Lv H, Yu Z, Amer S, Chai C. Epidemiological, clinical and viral characteristics of fatal cases of human avian influenza A (H7N9) virus in Zhejiang Province, China. J Infect 16: 00239–00239, 2013.
22. Mancini DA, Mendonca RM, Mendonca RZ, do Prado JA, Andrade Cde M. Immune response to vaccine against influenza in smokers, non-smokers and, in individuals holding respiratory complications. Boll Chim Farm 137: 21–25, 1998.
23. Peat JK, Keena V, Harakeh Z, Marks G. Parental smoking and respiratory tract infections in children. Paediatr Respir Rev 2: 207–213, 2001.
24. Pichlmair A, Schulz O, Tan CP, Naslund TI, Liljestrom P, Weber F, Reis e Sousa C. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5=-phosphates. Science 314: 997–1001, 2006.
25. Pyhala R, Takala J, Turunen A, Aho K. Smoking and influenza in the elderly: a sero-epidemiological study. Eur J Respir Dis 64: 212–216, 1983.
26. Robbins CS, Bauer CM, Vujicic N, Gaschler GJ, Lichty BD, Brown EG, Stampfli MR. Cigarette smoke impacts immune inflammatory responses to influenza in mice. Am J Respir Crit Care Med 174: 1342–1351, 2006.
27. Sayers NM, Drucker DB. Animal models used to test the interactions between infectious agents and products of cigarette smoked implicated in sudden infant death syndrome. FEMS Immunol Med Microbiol 25: 115–123, 1999.
28. Sherman CB. The health consequences of cigarette smoking. Pulmonary diseases. Med Clin North Am 76: 355–375, 1992.
29. Simet SM, Sisson JH, Pavlik JA, Devasure JM, Boyer C, Liu X, Kawasaki S, Sharp JG, Rennard SI, Wyatt TA. Long-term cigarette smoke exposure in a mouse model of ciliated epithelial cell function. Am J Respir Cell Mol Biol 43: 635–640, 2010.
30. Singanayagam A, Joshi PV, Mallia P, Johnston SL. Viruses exacerbating chronic pulmonary disease: the role of immune modulation (Abstract). BMC Med 10: 27, 2012.
31. Slotkin TA. Nicotine and the adolescent brain: insights from an animal model. Neurotoxicol Teratol 24: 369–384, 2002.
32. Taima K, Imaizumi T, Yamashita K, Ishikawa A, Fujita T, Yoshida H, Takanashi S, Okumura K, Satoh K. Expression of IP-10/CXCL10 is upregulated by double-stranded RNA in BEAS-2B bronchial epithelial cells. Respiration 73: 360–364, 2006.
33. Todt JC, Freeman CM, Brown JP, Sonstein J, Ames TM, McCubbrey AL, Martinez FJ, Chensue SW, Beck JM, Curtis JL. Smoking decreases the response of human lung macrophages to double-stranded RNA by reducing TLR3 expression (Astract). Respir Res 14: 33, 2013.
34. Wang JH, Kim H, Jang YJ. Cigarette smoke extract enhances rhinovi-rus-induced toll-like receptor 3 expression and interleukin-8 secretion in A549 cells. Am J Rhinol Allergy 23: e5–e9, 2009.
35. Wu W, Patel KB, Booth JL, Zhang W, Metcalf JP. 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, 2011.
36. Zhang H, Air GM. Expression of functional influenza virus A polymerase proteins and template from cloned cDNAS in recombinant vaccinia virus infected cells. Biochem Biophys Res Commun 200: 95–101, 1994.