TGF-β-induced IL-6 prevents development of acute lung injury in influenza A virus-infected F508del CFTR-heterozygous mice

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 308, Issue 11, 2015, Pages L1136-L1144

  Woods, Parker S ^a   Tazi, Mia F ^a   Chesarino, Nicholas M ^a   Amer, Amal O ^a   Davis, Ian C ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Acute lung injury; Cystic fibrosis transmembrane conductance regulator; Influenza; Interleukin 6; Transforming growth factor

Indexed keywords

CXCL1 CHEMOKINE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; ENROFLOXACIN; GAMMA INTERFERON; INTERLEUKIN 6; TRANSFORMING GROWTH FACTOR BETA;

ACUTE LUNG INJURY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR MOUSE; GENOTYPE; HYPOXEMIA; IMMUNOHISTOCHEMISTRY; INFLUENZA A; LIQUID; LUNG ALVEOLUS MACROPHAGE; LUNG DISEASE; LUNG EDEMA; LUNG LAVAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; VIRUS INFECTION; VIRUS NEUTRALIZATION; VIRUS REPLICATION; WEIGHT REDUCTION; WILD TYPE; 129 MOUSE; ANIMAL; BRONCHOALVEOLAR LAVAGE FLUID; C57BL MOUSE; GENE DELETION; GENETICS; IMMUNOLOGY; INFLUENZA A VIRUS; INNATE IMMUNITY; ORTHOMYXOVIRUS INFECTION; PHYSIOLOGY; SECRETION (PROCESS); VIROLOGY;

ACUTE LUNG INJURY; ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; IMMUNITY, INNATE; INFLUENZA A VIRUS; INTERLEUKIN-6; MACROPHAGES, ALVEOLAR; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, INBRED CFTR; ORTHOMYXOVIRIDAE INFECTIONS; SEQUENCE DELETION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84930853629     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00078.2015     Document Type: Article

References (70)

1. Aeffner F, Abdulrahman B, Hickman-Davis JM, Janssen PM, Amer A, Bedwell DM, Sorscher EJ, Davis IC. Heterozygosity for the F508del mutation in the cystic fibrosis transmembrane conductance regulator anion channel attenuates influenza severity. J Infect Dis 208: 780-789, 2013.
2. Aeffner F, Bratasz A, Flaño E, Powell KA, Davis IC. Post-infection A77-1726 treatment improves cardiopulmonary function in H1N1 influenza-infected mice. Am J Respir Cell Mol Biol 47: 543-551, 2012.
3. Aeffner F, Woods PS, Davis IC. Activation of A1-adenosine receptors promotes leukocyte recruitment to the lung and attenuates acute lung injury in mice infected with influenza A/WSN/33 (H1N1) virus. J Virol 88: 10214-10227, 2014.
4. Aoki H, Ohnishi H, Hama K, Shinozaki S, Kita H, Yamamoto H, Osawa H, Sato K, Tamada K, Sugano K. Existence of autocrine loop between interleukin-6 and transforming growth factor-p1 in activated rat pancreatic stellate cells. J Cell Biochem 99: 221-228, 2006.
5. Boucher RC, Chinet T, Willumsen N, Knowles MR, Stutts MJ. Ion transport in normal and CF airway epithelia. Adv Exp Med Biol 290: 105-115, 1991.
6. Carey MA, Bradbury JA, Rebolloso YD, Graves JP, Zeldin DC, Germolec DR. Pharmacologic inhibition of COX-1 and COX-2 in influenza A viral infection in mice. PLoS One 5: e11610, 2010.
7. Carlson CM, Turpin EA, Moser LA, O’Brien KB, Cline TD, Jones JC, Tumpey TM, Katz JM, Kelley LA, Gauldie J, Schultz-Cherry S. Transforming growth factor- fj activation by neuraminidase and role in highly pathogenic H5N1 influenza pathogenesis. PLoS Pathog 6: e1001136, 2010.
8. Cauthen AN, Swayne DE, Schultz-Cherry S, Perdue ML, Suarez DL. Continued circulation in China of highly pathogenic avian influenza viruses encoding the hemagglutinin gene associated with the 1997 H5N1 outbreak in poultry and humans. J Virol 74: 6592-6599, 2000.
9. Charu V, Simonsen L, Lustig R, Steiner C, Viboud C. Mortality burden of the 2009-10 influenza pandemic in the United States: improving the timeliness of influenza severity estimates using inpatient mortality records. Influenza Other Respir Viruses 7: 863-871, 2013.
10. Cheung CY, Poon LLM, Lau AS, Luk W, Lau YL, Shortridge KF, Gordon S, Guan Y, Peiris JSM. Induction of proinflammatory cytokines in human macrophages by influenza A (H5N1) viruses: a mechanism for the unusual severity of human disease? Lancet 360: 1831-1837, 2002.
11. Clark N, Lynch J. Influenza: epidemiology, clinical features, therapy, prevention. Semin Respir Crit Care Med 32: 373-392, 2011.
12. Cochrane Neuraminidase Inhibitors Review Team. Does oseltamivir really reduce complications of influenza? Clin Infect Dis 53: 1302-1303, 2011.
13. Cohen JC, Lundblad LK, Bates JH, Levitzky M, Larson JE. The “Goldilocks effect” in cystic fibrosis: identification of a lung phenotype in the cftr knockout and heterozygous mouse. BMC Genet 5: 21, 2004.
14. Davis IC, Lazarowski ER, Chen FP, Hickman-Davis JM, Sullender WM, Matalon S. Post-infection A77-1726 blocks pathophysiologic sequelae of respiratory syncytial virus infection. Am J Respir Cell Mol Biol 37: 379-386, 2007.
15. Davis IC, Matalon S. Epithelial sodium channels in the adult lung-important modulators of pulmonary health and disease. Adv Exp Med Biol 618: 127-140, 2007.
16. de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, Chau TN, Hoang DM, Chau NV, Khanh TH, Dong VC. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytoki-nemia. Nat Med 12: 1203-1207, 2006.
17. Dienz O, Rud JG, Eaton SM, Lanthier PA, Burg E, Drew A, Bunn J, Suratt BT, Haynes L, Rincon M. Essential role of IL-6 in protection against H1N1 influenza virus by promoting neutrophil survival in the lung. Mucosal Immunol 5: 258-266, 2012.
18. 18. Dunn AG, Arachi D, Hudgins J, Tsafnat G, Coiera E, Bourgeois FT. Financial conflicts of interest and conclusions about neuraminidase inhibitors for influenza: An analysis of systematic reviews. Ann Intern Med 161: 513-518, 2014.
19. Dybing JK, Schultz-Cherry S, Swayne DE, Suarez DL, Perdue ML. Distinct pathogenesis of Hong Kong-origin H5N1 viruses in mice compared with that of other highly pathogenic H5 avian influenza viruses. J Virol 74: 1443-1450, 2000.
20. Gabriel SE, Brigman KN, Koller BH, Boucher RC, Stutts MJ. Cystic fibrosis heterozygote resistance to cholera toxin in the cystic fibrosis mouse model. Science 266: 107-109, 1994.
21. Ge Q, Moir LM, Black JL, Oliver BG, Burgess JK. TGFfj1 induces IL-6 and inhibits IL-8 release in human bronchial epithelial cells: The role of Smad2/3. J Cell Physiol 225: 846-854, 2010.
22. Goldstein E, Viboud C, Charu V, Lipsitch M. Improving the estimation of influenza-related mortality over a seasonal baseline. Epidemiology 23: 829-838, 2012.
23. Grohskopf LA, Olsen SJ, Sokolow LZ, Bresee JS, Cox NJ, Broder KR, Karron RA, Walter EB. Prevention and control of seasonal influenza with vaccines: Recommendations of the Advisory Committee on Immunization Practices (ACIP) - United States, 2014-2015 influenza season. MMWR Morb Mortal Wkly Rep 63: 691-697, 2014.
24. Harris WT, Muhlebach MS, Oster RA, Knowles MR, Noah TL. Transforming growth factor-p1 in bronchoalveolar lavage fluid from children with cystic fibrosis. Pediatr Pulmonol 44: 1057-1064, 2009.
25. Hickman-Davis J, Gibbs-Erwin J, Lindsey JR, Matalon S. Surfactant protein A mediates mycoplasmacidal activity of alveolar macrophages by production of peroxynitrite. Proc Natl Acad Sci USA 96: 4953–4958, 1999.
26. Hofer CC, Woods PS, Davis IC. Infection of mice with influenza A/WSN/33 (H1N1) virus alters alveolar type II cell phenotype. Am J Physiol Lung Cell Mol Physiol 308: L628-L638, 2015.
27. Howe K, Gauldie J, McKay DM. TGF-p effects on epithelial ion transport and barrier: reduced Cl~ secretion blocked by a p38 MAPK inhibitor. Am J Physiol Cell Physiol 283: C1667-C1674, 2002.
28. Howe KL, Wang A, Hunter MM, Stanton BA, McKay DM. TGFp down-regulation of the CFTR: a means to limit epithelial chloride secretion. Exp Cell Res 298: 473-484, 2004.
29. Huang FF, Barnes PF, Feng Y, Donis R, Chroneos ZC, Idell S, Allen T, Perez DR, Whitsett JA, Dunussi-Joannopoulos K, Shams H. GM-CSF in the lung protects against lethal influenza infection. Am J Respir Crit Care Med 184: 259-268, 2011.
30. Ibricevic A, Pekosz A, Walter MJ, Newby C, Battaile JT, Brown EG, Holtzman MJ, Brody SL. Influenza virus receptor specificity and cell tropism in mouse and human airway epithelial cells. J Virol 80: 7469-7480, 2006.
31. Jewell NA, Vaghefi N, Mertz SE, Akter P, Peebles RS Jr, Bakaletz LO, Durbin RK, Flaño E, Durbin JE. Differential type I interferon induction by respiratory syncytial virus and influenza A virus in vivo. J Virol 81: 9790-9800, 2007.
32. Kaiser L, Wat C, Mills T, Mahoney P, Ward P, Hayden F. Impact of oseltamivir treatment on influenza-related lower respiratory tract complications and hospitalizations. Arch Intern Med 163: 1667-1672, 2003.
33. Kash JC, Tumpey TM, Proll SC, Carter V, Perwitasari O, Thomas MJ, Basler CF, Palese P, Taubenberger JK, García-Sastre A, Swayne DE, Katze MG. Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus. Nature 443: 578-581, 2006.
34. Kolliputi N, Waxman AB. IL-6 cytoprotection in hyperoxic acute lung injury occurs via PI3K/Akt-mediated Bax phosphorylation. Am J Physiol Lung Cell Mol Physiol 297: L6-L16, 2009.
35. Li G, Yilmaz M, Kojicic M, Fernández-Pérez E, Wahab R, Huskins WC, Afessa B, Truwit JD, Gajic O. Outcome of critically ill patients with influenza virus infection. J Clin Virol 46: 275-278, 2009.
36. Li K, Guo D, Zhu H, Hering-Smith KS, Hamm LL, Ouyang J, Dong Y. Interleukin-6 stimulates epithelial sodium channels in mouse cortical collecting duct cells. Am J Physiol Regul Integr Comp Physiol 299: R590-R595, 2010.
37. Marois I, Cloutier A, Garneau Ë, Richter MV. Initial infectious dose dictates the innate, adaptive, and memory responses to influenza in the respiratory tract. J Leukoc Biol 92: 107-121, 2012.
38. Matthay MA, Folkesson HG, Clerici C. Lung epithelial fluid transport and the resolution of pulmonary edema. Physiol Rev 82: 569-600, 2002.
39. Murphy EA, Davis JM, McClellan JL, Carmichael MD, Rooijen NV, Gangemi JD. Susceptibility to infection and inflammatory response following influenza virus (H1N1, A/PR/8/34) challenge: role of macrophages. J Interferon Cytokine Res 31: 501-508, 2011.
40. O’Brien KB, Vogel P, Duan S, Govorkova EA, Webby RJ, McCullers JA, Schultz-Cherry S. Impaired wound healing predisposes obese mice to severe influenza virus infection. J Infect Dis 205: 252-261, 2012.
41. Osterholm MT, Ballering KS, Kelley NS. Major challenges in providing an effective and timely pandemic vaccine for influenza A(H7N9). JAMA 309: 2557-2558, 2013.
42. Osterholm MT, Kelley NS, Sommer A, Belongia EA. Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect Dis 12: 36-44, 2012.
43. Paquette SG, Banner D, Zhao Z, Fang Y, Huang SSH, León AJ, Ng DCK, Almansa R, Martin-Loeches I, Ramirez P, Socias L, Loza A, Blanco J, Sansonetti P, Rello J, Andaluz D, Shum B, Rubino S, de Lejarazu RO, Tran D, Delogu G, Fadda G, Krajden S, Rubin BB, Bermejo-Martin JF, Kelvin AA, Kelvin DJ. Interleukin-6 is a potential biomarker for severe pandemic H1N1 influenza A infection. PLoS One 7: e38214, 2012.
44. Parsons PE, Eisner MD, Thompson BT, Matthay MA, Ancukiewicz M, Bernard GR, Wheeler AP. Lower tidal volume ventilation and plasma cytokine markers of inflammation in patients with acute lung injury. Crit Care Med 33: 1-6, 2005.
45. Peiris JS, de Jong MD, Guan Y. Avian influenza virus (H5N1): a threat to human health. Clin Microbiol Rev 20: 243-267, 2007.
46. Perrone LA, Plowden JK, García-Sastre A, Katz JM, Tumpey TM. H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog 4: e1000115, 2008.
47. Prulière-Escabasse V, Fanen P, Dazy AC, Lechapt-Zalcman E, Rideau D, Edelman A, Escudier E, Coste A. TGF-fj1 downregulates CFTR expression and function in nasal polyps of non-CF patients. Am J Physiol Lung Cell Mol Physiol 288: L77-L83, 2005.
48. Quandelacy TM, Viboud C, Charu V, Lipsitch M, Goldstein E. Age-and sex-related risk factors for influenza-associated mortality in the United States between 1997-2007. Am J Epidemiol 179: 156-167, 2014.
49. Rello J, Pop-Vicas A. Clinical review: Primary influenza viral pneumonia. Crit Care 13: 235, 2009.
50. Robertson JS, Inglis SC. Prospects for controlling future pandemics of influenza. Virus Res 162: 39-46, 2011.
51. Rolfes M, Blanton L, Brammer L, Smith S, Mustaquim D, Steffens C, Cohen J, Leon M, Chaves SS, Abd Elal AI, Gubareva L, Hall H, Wallis T, Villanueva J, Bresee J, Cox N, Finelli L; Centers for Disease Control and Prevention (CDC). Update: Influenza activity - United States, September 28-December 6, 2014. MMWR Morb Mortal Wkly Rep 63: 1189-1194, 2014.
52. Roux J, Carles M, Koh H, Goolaerts A, Ganter MT, Chesebro BB, Howard M, Houseman BT, Finkbeiner W, Shokat KM, Paquet AC, Matthay MA, Pittet JF. Transforming growth factor p1 inhibits cystic fibrosis transmembrane conductance regulator-dependent cAMP-stimu-lated alveolar epithelial fluid transport via a phosphatidylinositol 3-kinase-dependent mechanism. J Biol Chem 285: 4278-4290, 2010.
53. Salomon R, Webster RG. The influenza virus enigma. Cell 136: 402-410, 2009.
54. Salomon R, Hoffmann E, Webster RG. Inhibition of the cytokine response does not protect against lethal H5N1 influenza infection. Proc Natl Acad Sci USA 104: 12479-12481, 2007.
55. Santibañez JF, Quintanilla M, Bernabeu C. TGF-fj/TGF-fj receptor system and its role in physiological and pathological conditions. Clin Sci (Lond) 121: 233-251, 2011.
56. Smith JH, Nagy T, Barber J, Brooks P, Tompkins SM, Tripp RA. Aerosol inoculation with a sub-lethal influenza virus leads to exacerbated morbidity and pulmonary disease pathogenesis. Viral Immunol 24: 131-142, 2011.
57. Snodgrass SM, Cihil KM, Cornuet PK, Myerburg MM, Swiatecka-Urban A. TGF-fj1 inhibits Cftr biogenesis and prevents functional rescue of DF508-Cftr in primary differentiated human bronchial epithelial cells. PLoS One 8: e63167, 2013.
58. Szretter KJ, Gangappa S, Lu X, Smith C, Shieh WJ, Zaki SR, Sambhara S, Tumpey TM, Katz JM. Role of host cytokine responses in the pathogenesis of avian H5N1 influenza viruses in mice. J Virol 81: 2736-2744, 2007.
59. Tate MD, Pickett DL, Van Rooijen N, Brooks AG, Reading PC. Critical role of airway macrophages in modulating disease severity during influenza virus infection of mice. J Virol 84: 7569-7580, 2010.
60. Taubenberger JK, Morens DM. Influenza: the once and future pandemic. Public Health Rep 125, Suppl 3: 16-26, 2010.
61. Thompson CI, Barclay WS, Zambon MC, Pickles RJ. Infection of human airway epithelium by human and avian strains of influenza A virus. J Virol 80: 8060-8068, 2006.
62. Tisoncik JR, Korth MJ, Simmons CP, Farrar J, Martin TR, Katze MG. Into the eye of the cytokine storm. Microbiol Mol Biol Rev 76: 16-32, 2012.
63. Traylor ZP, Aeffner F, Davis IC. Influenza A H1N1 induces declines in alveolar gas exchange in mice consistent with rapid post-infection progression from acute lung injury to ARDS. Influenza Other Respir Viruses 7: 472–479, 2013.
64. Tumpey TM, García-Sastre A, Taubenberger JK, Palese P, Swayne DE, Pantin-Jackwood MJ, Schultz-Cherry S, Solorzano A, van Rooijen N, Katz JM, Basler CF. Pathogenicity of influenza viruses with genes from the 1918 pandemic virus: functional roles of alveolar macrophages and neutrophils in limiting virus replication and mortality in mice. J Virol 79: 14933-14944, 2005.
65. Tuvim MJ, Evans SE, Clement CG, Dickey BF, Gilbert BE. Augmented lung inflammation protects against influenza A pneumonia. PLoS One 4: e4176, 2009.
66. Ware LB, Matthay MA. Alveolar fluid clearance is impaired in the majority of patients with acute lung injury and the acute respiratory distress syndrome. Am J Respir Crit Care Med 163: 1376-1383, 2001.
67. Westall G, Paraskeva M. H1N1 influenza: Critical care aspects. Semin Respir Crit Care Med 32: 400-408, 2011.
68. Wolk KE, Lazarowski ER, Traylor ZP, Yu EN, Jewell NA, Durbin RK, Durbin JE, Davis IC. Influenza A virus inhibits alveolar fluid clearance in BALB/c mice. Am J Respir Crit Care Med 178: 969-976, 2008.
69. Wolters PJ, Wray C, Sutherland RE, Kim SS, Koff J, Mao Y, Frank JA. Neutrophil-derived IL-6 limits alveolar barrier disruption in experimental ventilator-induced lung injury. J Immunol 182: 8056-8062, 2009.
70. Zeiher BG, Eichwald E, Zabner J, Smith JJ, Puga AP, McCray PB, Capecchi MR, Welsh MJ, Thomas KR. A mouse model for the delta F508 allele of cystic fibrosis. J Clin Invest 96: 2051-2064, 1995.