Differential susceptibilities of human lung primary cells to H1N1 influenza viruses

Journal of Virology

Volumn 89, Issue 23, 2015, Pages 11935-11944

  Travanty, Emily ^a,e   Zhou, Bin ^b,f   Zhang, Hongbo ^c   Peter Di, Y ^c   Alcorn, John F ^d   Wentworth, David E ^b,g   Mason, Robert ^a   Wang, Jieru ^d  

^a DEPARTMENT OF MEDICINE   (United States)

^b J CRAIG VENTER INSTITUTE   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^e State of Colorado   (United States)

^f NEW YORK UNIVERSITY   (United States)

^g NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE; HEMAGGLUTININ;

AGE; AMINO ACID SUBSTITUTION; ARTICLE; CELL DAMAGE; CONTROLLED STUDY; EPITHELIUM; GENDER; HUMAN; HUMAN CELL; INFECTION SENSITIVITY; INFLUENZA A (H1N1); LUNG ALVEOLUS CELL; OBESITY; PRIORITY JOURNAL; SMOKING; VIRUS STRAIN; BIOSYNTHESIS; COMPARATIVE STUDY; COMPLICATION; CYTOLOGY; DISEASE PREDISPOSITION; EPITHELIUM CELL; FLOW CYTOMETRY; GENETICS; HOST PATHOGEN INTERACTION; INFLUENZA; INFLUENZA A VIRUS (H1N1); LUNG; LUNG ALVEOLUS; MACROPHAGE; METABOLISM; NONPARAMETRIC TEST; PATHOGENICITY; PATHOPHYSIOLOGY; SPECIES DIFFERENCE; VIROLOGY;

ADIPOSITY; CYTOKINES; DISEASE SUSCEPTIBILITY; EPITHELIAL CELLS; FLOW CYTOMETRY; HEMAGGLUTININS; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA, HUMAN; LUNG; MACROPHAGES; OBESITY; PULMONARY ALVEOLI; SPECIES SPECIFICITY; STATISTICS, NONPARAMETRIC;

EID: 84942847887     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01792-15     Document Type: Article

References (49)

1. Smith GJ, Vijaykrishna D, Bahl J, Lycett SJ, Worobey M, Pybus OG, Ma SK, Cheung CL, Raghwani J, Bhatt S, Peiris JS, Guan Y, Rambaut A. 2009. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459:1122-1125. http://dx.doi.org/10.1038/nature08182.
2. Basu A, Shelke V, Chadha M, Kadam D, Sangle S, Gangodkar S, Mishra A. 2011. Direct imaging of pH1N1 2009 influenza virus replication in alveolar pneumocytes in fatal cases by transmission electron microscopy. J Electron Microsc 60:89-93. http://dx.doi.org/10.1093/jmicro/dfq081.
3. Shieh WJ, Blau DM, Denison AM, Deleon-Carnes M, Adem P, Bhatnagar J, Sumner J, Liu L, Patel M, Batten B, Greer P, Jones T, Smith C, Bartlett J, Montague J, White E, Rollin D, Gao R, Seales C, Jost H, Metcalfe M, Goldsmith CS, Humphrey C, Schmitz A, Drew C, Paddock C, Uyeki TM, Zaki SR. 2010. 2009 pandemic influenza A (H1N1): pathology and pathogenesis of 100 fatal cases in the United States. Am J Pathol 177:166-175. http://dx.doi.org/10.2353/ajpath.2010.100115.
4. Mauad T, Hajjar LA, Callegari GD, da Silva LF, Schout D, Galas FR, Alves VA, Malheiros DM, Auler JO, Jr, Ferreira AF, Borsato MR, Bezerra SM, Gutierrez PS, Caldini ET, Pasqualucci CA, DolhnikoffM, Saldiva PH. 2010. Lung pathology in fatal novel human influenza A (H1N1) infection. Am J Respir Crit Care Med 181:72-79. http://dx.doi.org/10.1164/rccm.200909-1420OC.
5. Wu W, Munday DC, Howell G, Platt G, Barr JN, Hiscox JA. 2011. Characterization of the interaction between human respiratory syncytial virus and the cell cycle in continuous cell culture and primary human airway epithelial cells. J Virol 85:10300-10309. http://dx.doi.org/10.1128/JVI.05164-11.
6. Wang J, Oberley-Deegan R, Wang S, Nikrad M, Funk CJ, Hartshorn KL, Mason RJ. 2009. Differentiated human alveolar type II cells secrete antiviral IL-29 (IFN-lambda 1) in response to influenza A infection. J Immunol 182: 1296-1304. http://dx.doi.org/10.4049/jimmunol.182.3.1296.
7. Nicholls JM, Chan MC, Chan WY, Wong HK, Cheung CY, Kwong DL, Wong MP, Chui WH, Poon LL, Tsao SW, Guan Y, Peiris JS. 2007. Tropism of avian influenza A (H5N1) in the upper and lower respiratory tract. Nat Med 13:147-149. http://dx.doi.org/10.1038/nm1529.
8. Tumpey TM, Garcia-Sastre A, Taubenberger JK, Palese P, Swayne DE, Pantin-Jackwood MJ, Schultz-Cherry S, Solorzano A, Van Rooijen N, Katz JM, Basler CF. 2005. 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. http://dx.doi.org/10.1128/JVI.79.23.14933-14944.2005.
9. Kim HM, Kang YM, Ku KB, Park EH, Yum J, Kim JC, Jin SY, Lee JS, Kim HS, Seo SH. 2013. The severe pathogenicity of alveolar macrophagedepleted ferrets infected with 2009 pandemic H1N1 influenza virus. Virology 444:394-403. http://dx.doi.org/10.1016/j.virol.2013.07.006.
10. Zhou B, Wentworth DE. 2012. Influenza A virus molecular virology techniques. Methods Mol Biol 865:175-192. http://dx.doi.org/10.1007/978-1-61779-621-0_11.
11. Zhou B, Jerzak G, Scholes DT, Donnelly ME, Li Y, Wentworth DE. 2011. Reverse genetics plasmid for cloning unstable influenza A virus gene segments. J Virol Methods 173:378-383. http://dx.doi.org/10.1016/j.jviromet.2011.01.021.
12. Wang J, Nikrad MP, Phang T, Gao B, Alford T, Ito Y, Edeen K, Travanty EA, Kosmider B, Hartshorn K, Mason RJ. 2011. Innate immune response to influenza A virus in differentiated human alveolar type II cells. Am J Respir Cell Mol Biol 45:582-591. http://dx.doi.org/10.1165/rcmb.2010-0108OC.
13. Wang J, Edeen K, Manzer R, Chang Y, Wang S, Chen X, Funk CJ, Cosgrove GP, Fang X, Mason RJ. 2007. Differentiated human alveolar epithelial cells and reversibility of their phenotype in vitro. Am J Respir Cell Mol Biol 36:661-668. http://dx.doi.org/10.1165/rcmb.2006-0410OC.
14. Gonzalez RF, Allen L, Gonzales L, Ballard PL, Dobbs LG. 2010. HTII-280, a biomarker specific to the apical plasma membrane of human lung alveolar type II cells. J Histochem Cytochem 58:891-901. http://dx.doi.org/10.1369/jhc.2010.956433.
15. Yu WC, Chan RW, Wang J, Travanty EA, Nicholls JM, Peiris JS, Mason RJ, Chan MC. 2011. Viral replication and innate host responses in pri-mary human alveolar epithelial cells and alveolar macrophages infected with influenza H5N1 and H1N1 viruses. J Virol 85:6844-6855. http://dx.doi.org/10.1128/JVI.02200-10.
16. Kosmider B, Messier EM, Janssen WJ, Nahreini P, Wang J, Hartshorn KL, Mason RJ. 2012. Nrf2 protects human alveolar epithelial cells against injury induced by influenza A virus. Respir Res 13:43. http://dx.doi.org/10.1186/1465-9921-13-43.
17. Wang J, Nikrad MP, Travanty EA, Zhou B, Phang T, Gao B, Alford T, Ito Y, Nahreini P, Hartshorn K, Wentworth D, Dinarello CA, Mason RJ. 2012. Innate immune response of human alveolar macrophages during influenza A infection. PLoS One 7:e29879. http://dx.doi.org/10.1371/journal.pone.0029879.
18. van den Brand JM, Stittelaar KJ, van Amerongen G, van de Bildt MW, Leijten LM, Kuiken T, Osterhaus AD. 2010. Experimental pandemic (H1N1) 2009 virus infection of cats. Emerg Infect Dis 16:1745-1747. http://dx.doi.org/10.3201/eid1611.100845.
19. Guarner J, Falcon-Escobedo R. 2009. Comparison of the pathology caused by H1N1, H5N1, and H3N2 influenza viruses. Arch Med Res 40: 655-661. http://dx.doi.org/10.1016/j.arcmed.2009.10.001.
20. Löndt BZ, Brookes SM, Nash BJ, Nunez A, Stagg DA, Brown IH. 2013. The infectivity of pandemic 2009 H1N1 and avian influenza viruses for pigs: an assessment by ex vivo respiratory tract organ culture. Influenza Other Respir Viruses 7:393-402. http://dx.doi.org/10.1111/j.1750-2659.2012.00397.x.
21. Weinheimer VK, Becher A, Tonnies M, Holland G, Knepper J, Bauer TT, Schneider P, Neudecker J, Ruckert JC, Szymanski K, Temmesfeld-Wollbrueck B, Gruber AD, Bannert N, Suttorp N, Hippenstiel S, WolffT, Hocke AC. 2012. Influenza A viruses target type II pneumocytes in the human lung. J Infect Dis 206:1685-1694. http://dx.doi.org/10.1093/infdis/jis455.
22. Gill JR, Sheng ZM, Ely SF, Guinee DG, Beasley MB, Suh J, Deshpande C, Mollura DJ, Morens DM, Bray M, Travis WD, Taubenberger JK. 2010. Pulmonary pathologic findings of fatal 2009 pandemic influenza A/H1N1 viral infections. Arch Pathol Lab Med 134:235-243.
23. Ye J, Sorrell EM, Cai Y, Shao H, Xu K, Pena L, Hickman D, Song H, Angel M, Medina RA, Manicassamy B, Garcia-Sastre A, Perez DR. 2010. Variations in the hemagglutinin of the 2009 H1N1 pandemic virus: potential for strains with altered virulence phenotype? PLoS Pathog 6:e1001145. http://dx.doi.org/10.1371/journal.ppat.1001145.
24. Safronetz D, Rockx B, Feldmann F, Belisle SE, Palermo RE, Brining D, Gardner D, Proll SC, Marzi A, Tsuda Y, Lacasse RA, Kercher L, York A, Korth MJ, Long D, Rosenke R, Shupert WL, Aranda CA, Mattoon JS, Kobasa D, Kobinger G, Li Y, Taubenberger JK, Richt JA, Parnell M, Ebihara H, Kawaoka Y, Katze MG, Feldmann H. 2011. Pandemic swine-origin H1N1 influenza A virus isolates show heterogeneous virulence in macaques. J Virol 85:1214-1223. http://dx.doi.org/10.1128/JVI.01848-10.
25. Belser JA, Wadford DA, Pappas C, Gustin KM, Maines TR, Pearce MB, Zeng H, Swayne DE, Pantin-Jackwood M, Katz JM, Tumpey TM. 2010. Pathogenesis of pandemic influenza A (H1N1) and triple-reassortant swine influenza A (H1) viruses in mice. J Virol 84:4194-4203. http://dx.doi.org/10.1128/JVI.02742-09.
26. Tscherne DM, Garcia-Sastre A. 2011. Virulence determinants of pandemic influenza viruses. J Clin Invest 121:6-13. http://dx.doi.org/10.1172/JCI44947.
27. Watanabe T, Shinya K, Watanabe S, Imai M, Hatta M, Li C, Wolter BF, Neumann G, Hanson A, Ozawa M, Yamada S, Imai H, Sakabe S, Takano R, Iwatsuki-Horimoto K, Kiso M, Ito M, Fukuyama S, Kawakami E, Gorai T, Simmons HA, Schenkman D, Brunner K, Capuano SV, III, Weinfurter JT, Nishio W, Maniwa Y, Igarashi T, Makino A, Travanty EA, Wang J, Kilander A, Dudman SG, Suresh M, Mason RJ, Hungnes O, Friedrich TC, Kawaoka Y. 2011. Avian-type receptor-binding ability can increase influenza virus pathogenicity in macaques. J Virol 85:13195-13203. http://dx.doi.org/10.1128/JVI.00859-11.
28. Chutinimitkul S, Herfst S, Steel J, Lowen AC, Ye J, van Riel D, Schrauwen EJ, Bestebroer TM, Koel B, Burke DF, Sutherland-Cash KH, Whittleston CS, Russell CA, Wales DJ, Smith DJ, Jonges M, Meijer A, Koopmans M, Rimmelzwaan GF, Kuiken T, Osterhaus AD, Garcia-Sastre A, Perez DR, Fouchier RA. 2010. Virulence-associated substitution D222G in the hemagglutinin of 2009 pandemic influenza A(H1N1) virus affects receptor binding. J Virol 84:11802-11813. http://dx.doi.org/10.1128/JVI.01136-10.
29. Camp JV, Chu YK, Chung DH, McAllister RC, Adcock RS, Gerlach RL, Wiemken TL, Peyrani P, Ramirez JA, Summersgill JT, Jonsson CB. 2013. Phenotypic differences in virulence and immune response in closely related clinical isolates of influenza A 2009 H1N1 pandemic viruses in mice. PLoS One 8:e56602. http://dx.doi.org/10.1371/journal.pone.0056602.
30. van Riel D, Leijten LM, van der Eerden M, Hoogsteden HC, Boven LA, Lambrecht BN, Osterhaus AD, Kuiken T. 2011. Highly pathogenic avian influenza virus H5N1 infects alveolar macrophages without virus production or excessive TNF-alpha induction. PLoS Pathog 7:e1002099. http://dx.doi.org/10.1371/journal.ppat.1002099.
31. Kobasa D, Jones SM, Shinya K, Kash JC, Copps J, Ebihara H, Hatta Y, Kim JH, Halfmann P, Hatta M, Feldmann F, Alimonti JB, Fernando L, Li Y, Katze MG, Feldmann H, Kawaoka Y. 2007. Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 445:319-323. http://dx.doi.org/10.1038/nature05495.
32. de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, Chau TN, Hoang DM, Chau NV, Khanh TH, Dong VC, Qui PT, Cam BV, Ha do Q, Guan Y, Peiris JS, Chinh NT, Hien TT, Farrar J. 2006. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 12:1203-1207. http://dx.doi.org/10.1038/nm1477.
33. Cheng XW, Lu J, Wu CL, Yi LN, Xie X, Shi XD, Fang SS, Zan H, Kung HF, He ML. 2011. Three fatal cases of pandemic 2009 influenza A virus infection in Shenzhen are associated with cytokine storm. Respir Physiol Neurobiol 175:185-187. http://dx.doi.org/10.1016/j.resp.2010.11.004.
34. Louie JK, Acosta M, Samuel MC, Schechter R, Vugia DJ, Harriman K, Matyas BT, California Pandemic (H1N1) Working Group. 2011. A novel risk factor for a novel virus: obesity and 2009 pandemic influenza A (H1N1). Clin Infect Dis 52:301-312. http://dx.doi.org/10.1093/cid/ciq152.
35. Morgan OW, Bramley A, Fowlkes A, Freedman DS, Taylor TH, Gargiullo P, Belay B, Jain S, Cox C, Kamimoto L, Fiore A, Finelli L, Olsen SJ, Fry AM. 2010. Morbid obesity as a risk factor for hospitalization and death due to 2009 pandemic influenza A (H1N1) disease. PLoS One 5:e9694. http://dx.doi.org/10.1371/journal.pone.0009694.
36. Jain S, Kamimoto L, Bramley AM, Schmitz AM, Benoit SR, Louie J, Sugerman DE, Druckenmiller JK, Ritger KA, Chugh R, Jasuja S, Deutscher M, Chen S, Walker JD, Duchin JS, Lett S, Soliva S, Wells EV, Swerdlow D, Uyeki TM, Fiore AE, Olsen SJ, Fry AM, Bridges CB, Finelli L, 2009 Pandemic Influenza A (H1N1) Virus Hospitalizations Investigation Team. 2009. Hospitalized patients with 2009 H1N1 influenza in the United States, April-June 2009. N Engl J Med 361:1935-1944. http://dx.doi.org/10.1056/NEJMoa0906695.
37. Van Kerkhove MD, Vandemaele KA, Shinde V, Jaramillo-Gutierrez G, Koukounari A, Donnelly CA, Carlino LO, Owen R, Paterson B, Pelletier L, Vachon J, Gonzalez C, Hongjie Y, Zijian F, Chuang SK, Au A, Buda S, Krause G, Haas W, Bonmarin I, Taniguichi K, Nakajima K, Shobayashi T, Takayama Y, Sunagawa T, Heraud JM, Orelle A, Palacios E, van der Sande MA, Wielders CC, Hunt D, Cutter J, Lee VJ, Thomas J, Santa-Olalla P, Sierra-Moros MJ, Hanshaoworakul W, Ungchusak K, Pebody R, Jain S, Mounts AW, WHO Working Group for Risk Factors for Severe H1N1pdm Infection. 2011. Risk factors for severe outcomes following 2009 influenza A (H1N1) infection: a global pooled analysis. PLoS Med 8:e1001053. http://dx.doi.org/10.1371/journal.pmed.1001053.
38. Radigan KA, Morales-Nebreda L, Soberanes S, Nicholson T, Nigdelioglu R, Cho T, Chi M, Hamanaka RB, Misharin AV, Perlman H, Budinger GR, Mutlu GM. 2014. Impaired clearance of influenza A virus in obese, leptin receptor deficient mice is independent of leptin signaling in the lung epithelium and macrophages. PLoS One 9:e108138. http://dx.doi.org/10.1371/journal.pone.0108138.
39. Srivastava B, Blazejewska P, Hessmann M, Bruder D, Geffers R, Mauel S, Gruber AD, Schughart K. 2009. Host genetic background strongly influences the response to influenza a virus infections. PLoS One 4:e4857. http://dx.doi.org/10.1371/journal.pone.0004857.
40. Hermann G, Tovar CA, Beck FM, Allen C, Sheridan JF. 1993. Restraint stress differentially affects the pathogenesis of an experimental influenza viral infection in three inbred strains of mice. J Neuroimmunol 47:83-94. http://dx.doi.org/10.1016/0165-5728(93)90287-9.
41. Horby P, Nguyen NY, Dunstan SJ, Baillie JK. 2012. The role of host genetics in susceptibility to influenza: a systematic review. PLoS One 7:e33180. http://dx.doi.org/10.1371/journal.pone.0033180.
42. Everitt AR, Clare S, Pertel T, John SP, Wash RS, Smith SE, Chin CR, Feeley EM, Sims JS, Adams DJ, Wise HM, Kane L, Goulding D, Digard P, Anttila V, Baillie JK, Walsh TS, Hume DA, Palotie A, Xue Y, Colonna V, Tyler-Smith C, Dunning J, Gordon SB, Gen II, Investigators M, Smyth RL, Openshaw PJ, Dougan G, Brass AL, Kellam P. 2012. IFITM3 restricts the morbidity and mortality associated with influenza. Nature 484:519-523. http://dx.doi.org/10.1038/nature10921.
43. Zúñiga J, Buendia-Roldan I, Zhao Y, Jimenez L, Torres D, Romo J, Ramirez G, Cruz A, Vargas-Alarcon G, Sheu CC, Chen F, Su L, Tager AM, Pardo A, Selman M, Christiani DC. 2012. Genetic variants associated with severe pneumonia in A/H1N1 influenza infection. Eur Respir J 39:604-610. http://dx.doi.org/10.1183/09031936.00020611.
44. Calafell i Majó F, Gonzalez Candelas F. 2011. Genetic factors in severe cases of (H1N1) 2009 influenza. Rev Esp Salud Publica 85:33-36. (In Spanish.)
45. Horby P, Sudoyo H, Viprakasit V, Fox A, Thai PQ, Yu H, Davila S, Hibberd M, Dunstan SJ, Monteerarat Y, Farrar JJ, Marzuki S, Hien NT. 2010. What is the evidence of a role for host genetics in susceptibility to influenza A/H5N1? Epidemiol Infect 138:1550-1558. http://dx.doi.org/10.1017/S0950268810000518.
46. Zhou B, Pearce MB, Li Y, Wang J, Mason RJ, Tumpey TM, Wentworth DE. 2013. Asparagine substitution at PB2 residue 701 enhances the replication, pathogenicity, and transmission of the 2009 pandemic H1N1 influenza A virus. PLoS One 8:e67616. http://dx.doi.org/10.1371/journal.pone.0067616.
47. Puzelli S, Facchini M, Spagnolo D, De Marco MA, Calzoletti L, Zanetti A, Fumagalli R, Tanzi ML, Cassone A, Rezza G, Donatelli I, Surveillance Group for Pandemic A (H1N1) 2009 Influenza Virus in Italy. 2010. Transmission of hemagglutinin D222G mutant strain of pandemic (H1N1) 2009 virus. Emerg Infect Dis 16:863-865. http://dx.doi.org/10.3201/eid1605.091858.
48. Zheng B, Chan KH, Zhang AJ, Zhou J, Chan CC, Poon VK, Zhang K, Leung VH, Jin DY, Woo PC, Chan JF, To KK, Chen H, Yuen KY. 2010. D225G mutation in hemagglutinin of pandemic influenza H1N1 (2009) virus enhances virulence in mice. Exp Biol Med 235:981-988. http://dx.doi.org/10.1258/ebm.2010.010071.
49. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Res 14:1188-1190. http://dx.doi.org/10.1101/gr.849004.