Autophagy mediates avian influenza H5N1 pseudotyped particle-induced lung inflammation through NF-κB and p38 MAPK signaling pathways

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 306, Issue 2, 2014, Pages

  Pan, Hong ^a   Zhang, Yijuan ^a   Luo, Zichao ^a   Li, Ping ^a   Liu, Lanlan ^a   Wang, Ce ^a   Wang, Hanzhong ^b   Li, Hongchang ^a   Ma, Yifan ^a  

^a SHENZHEN INSTITUTES OF ADVANCED TECHNOLOGY   (China)

^b WUHAN INSTITUTE OF VIROLOGY   (China)

Author keywords

Autophagy; Avian influenza h5n1 virus; Lung inflammation; NF B; P38 MAPK

Indexed keywords

3 METHYLADENINE; AUTOPHAGY PROTEIN 5; BECLIN 1; BETA ACTIN; CXCL2 CHEMOKINE; HEMAGGLUTININ; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; AVIAN INFLUENZA; CELL STRAIN HEK293; CONTROLLED STUDY; EPITHELIUM CELL; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; INFLUENZA VIRUS A H5N1; LUNG ALVEOLUS CELL; LUNG ALVEOLUS EPITHELIUM; LUNG PARENCHYMA; LYSOSOME; MURINE LEUKEMIA VIRUS; PNEUMONIA; POSITIVE FEEDBACK; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REPORTER GENE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; UPREGULATION; VIRUS PARTICLE; WESTERN BLOTTING;

AUTOPHAGY; AVIAN INFLUENZA H5N1 VIRUS; LUNG INFLAMMATION; NF-ΚB; P38 MAPK;

ADENOCARCINOMA; ANIMALS; AUTOPHAGY; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; FEMALE; HEK293 CELLS; HUMANS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA, HUMAN; LUNG NEOPLASMS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; NF-KAPPA B; ORTHOMYXOVIRIDAE INFECTIONS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PNEUMONIA; RESPIRATORY MUCOSA;

EID: 84892604558     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00147.2013     Document Type: Article

References (57)

1. Boon AC, Finkelstein D, Zheng M, Liao G, Allard J, Klumpp K, Webster R, Peltz G, Webby RJ. H5N1 influenza virus pathogenesis in genetically diverse mice is mediated at the level of viral load. MBio 2: e00171-11, 2011.
2. Braber S, Verheijden KA, Henricks PA, Kraneveld AD, Folkerts G. A comparison of fixation methods on lung morphology in a murine model of emphysema. Am J Physiol Lung Cell Mol Physiol 299: L843-L851, 2010.
3. Buchweitz JP, Karmaus PW, Harkema JR, Williams KJ, Kaminski NE. Modulation of airway responses to influenza A/PR/8/34 by Delta9-tetrahydrocannabinol in C57BL/6 mice. J Pharmacol Exp Ther 323: 675-683, 2007.
4. Cheng X, Xu Q, Song E, Yang CF, Kemble G, Jin H. The hemagglu-tinin protein of influenza A/Vietnam/1203/2004 (H5N1) contributes to hyperinduction of proinflammatory cytokines in human epithelial cells. Virology 406: 28-36, 2010.
5. Cheung CY, Poon LL, Lau AS, Luk W, Lau YL, Shortridge KF, Gordon S, Guan Y, Peiris JS. 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.
6. Choi AM, Ryter SW, Levine B. Autophagy in human health and disease. N Engl J Med 368: 651-662, 2013.
7. Copetti T, Bertoli C, Dalla E, Demarchi F, Schneider C. p65/RelA modulates BECN1 transcription and autophagy. Mol Cell Biol 29: 2594-2608, 2009.
8. Criollo A, Senovilla L, Authier H, Maiuri MC, Morselli E, Vitale I, Kepp O, Tasdemir E, Galluzzi L, Shen S, Tailler M, Delahaye N, Tesniere A, De Stefano D, Younes AB, Harper F, Pierron G, Lavan-dero S, Zitvogel L, Israel A, Baud V, Kroemer G. The IKK complex contributes to the induction of autophagy. EMBO J 29: 619-631, 2010.
9. Dai JP, Li WZ, Zhao XF, Wang GF, Yang JC, Zhang L, Chen XX, Xu YX, Li KS. A drug screening method based on the autophagy pathway and studies of the mechanism of evodiamine against influenza A virus. PLoS One 7: e42706, 2012.
10. 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 DQ, Guan Y, Peiris JS, Chinh NT, Hien TT, Farrar J. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 12: 1203-1207, 2006.
11. Droebner K, Reiling SJ, Planz O. Role of hypercytokinemia in NF-kappaB p50-deficient mice after H5N1 influenza A virus infection. J Virol 82: 11461-11466, 2008.
12. Fader CM, Colombo MI. Autophagy and multivesicular bodies: two closely related partners. Cell Death Differ 16: 70-78, 2009.
13. Flory E, Kunz M, Scheller C, Jassoy C, Stauber R, Rapp UR, Ludwig S. Influenza virus-induced NF-kappaB-dependent gene expression is mediated by overexpression of viral proteins and involves oxidative radicals and activation of IkappaB kinase. J Biol Chem 275: 8307-8314, 2000.
14. Gambotto A, Barratt-Boyes SM, de Jong MD, Neumann G, Kawaoka Y. Human infection with highly pathogenic H5N1 influenza virus. Lancet 371: 1464-1475, 2008.
15. Gannage M, Dormann D, Albrecht R, Dengjel J, Torossi T, Ramer PC, Lee M, Strowig T, Arrey F, Conenello G, Pypaert M, Andersen J, Garcia-Sastre A, Munz C. Matrix protein 2 of influenza A virus blocks autophagosome fusion with lysosomes. Cell Host Microbe 6: 367-380, 2009.
16. Garcia JM, Lai JC. Production of influenza pseudotyped lentiviral particles and their use in influenza research and diagnosis: an update. Expert Rev Anti Infect Ther 9: 443-455, 2011.
17. Guan Y, Poon LL, Cheung CY, Ellis TM, Lim W, Lipatov AS, Chan KH, Sturm-Ramirez KM, Cheung CL, Leung YH, Yuen KY, Webster RG, Peiris JS. H5N1 influenza: a protean pandemic threat. Proc Natl Acad Sci USA 101: 8156-8161, 2004.
18. Heymann D. Autophagy: a protective mechanism in response to stress and inflammation. Curr Opin Investig Drugs 7: 443-450, 2006.
19. Hui KP, Lee SM, Cheung CY, Ng IH, Poon LL, Guan Y, Ip NY, Lau AS, Peiris JS. Induction of proinflammatory cytokines in primary human macrophages by influenza A virus (H5N1) is selectively regulated by IFN regulatory factor 3 and p38 MAPK. J Immunol 182: 1088-1098, 2009.
20. Ichimura Y, Komatsu M. Selective degradation of p62 by autophagy. Semin Immunopathol 32: 431-436, 2010.
21. Ilyushina NA, Hay A, Yilmaz N, Boon AC, Webster RG, Govorkova EA. Oseltamivir-ribavirin combination therapy for highly pathogenic H5N1 influenza virus infection in mice. Antimicrob Agents Chemother 52: 3889-3897, 2008.
22. Johansen T, Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy 7: 279-296, 2011.
23. Julkunen I, Sareneva T, Pirhonen J, Ronni T, Melen K, Matikainen S. Molecular pathogenesis of influenza A virus infection and virus-induced regulation of cytokine gene expression. Cytokine Growth Factor Rev 12: 171-180, 2001.
24. Kimura S, Noda T, Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 3: 452-460, 2007.
25. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, Baba M, Baehrecke EH, Bahr BA, Ballabio A, Bamber BA, Bassham DC, Bergamini E, Bi X, Biard-Piechaczyk M, Blum JS, Bredesen DE, Brodsky JL, Brumell JH, Brunk UT, Bursch W, Camougrand N, Cebollero E, Cecconi F, Chen Y, Chin LS, Choi A, Chu CT, Chung J, Clarke PG, Clark RS, Clarke SG, Clavé C, Cleveland JL, Codogno P, Colombo MI, Coto-Montes A, Cregg JM, Cuervo AM, Debnath J, Demarchi F, Dennis PB, Dennis PA, Deretic V, Devenish RJ, Di Sano F, Dice JF, Difiglia M, Dinesh-Kumar S, Distelhorst CW, Djavaheri-Mergny M, Dorsey FC, Dröge W, Dron M, Dunn WA Jr, Duszenko M, Eissa NT, Elazar Z, Esclatine A, Eskelinen EL, Fésüs L, Finley KD, Fuentes JM, Fueyo J, Fujisaki K, Galliot B, Gao FB, Gewirtz DA, Gibson SB, Gohla A, Goldberg AL, Gonzalez R, González-Estévez C, Gorski S, Gottlieb RA, Häussinger D, He YW, Heidenreich K, Hill JA, Høyer-Hansen M, Hu X, Huang WP, Iwasaki A, Jäättelä M, Jackson WT, Jiang X, Jin S, Johansen T, Jung JU, Kadowaki M, Kang C, Kelekar A, Kessel DH, Kiel JA, Kim HP, Kimchi A, Kinsella TJ, Kiselyov K, Kitamoto K, Knecht E, Komatsu M, Kominami E, Kondo S, Kovács AL, Kroemer G, Kuan CY, Kumar R, Kundu M, Landry J, Laporte M, Le W, Lei HY, Lenardo MJ, Levine B, Lieberman A, Lim KL, Lin FC, Liou W, Liu LF, Lopez-Berestein G, López-Otín C, Lu B, Macleod KF, Malorni W, Martinet W, Matsuoka K, Mautner J, Meijer AJ, Meléndez A, Michels P, Miotto G, Mistiaen WP, Mizushima N, Mograbi B, Monastyrska I, Moore MN, Moreira PI, Moriyasu Y, Motyl T, Münz C, Murphy LO, Naqvi NI, Neufeld TP, Nishino I, Nixon RA, Noda T, Nürnberg B, Ogawa M, Oleinick NL, Olsen LJ, Ozpolat B, Paglin S, Palmer GE, Papassideri I, Parkes M, Perlmutter DH, Perry G, Piacentini M, Pinkas-Kramarski R, Prescott M, Proikas-Cezanne T, Raben N, Rami A, Reggiori F, Rohrer B, Rubinsztein DC, Ryan KM, Sadoshima J, Sakagami H, Sakai Y, Sandri M, Sasakawa C, Sass M, Schneider C, Seglen PO, Seleverstov O, Settleman J, Shacka JJ, Shapiro IM, Sibirny A, Silva-Zacarin EC, Simon HU, Simone C, Simonsen A, Smith MA, Spanel-Borowski K, Srinivas V, Steeves M, Stenmark H, Stromhaug PE, Subauste CS, Sugimoto S, Sulzer D, Suzuki T, Swanson MS, Tabas I, Takeshita F, Talbot NJ, Tallóczy Z, Tanaka K, Tanaka K, Tanida I, Taylor GS, Taylor JP, Terman A, Tettamanti G, Thompson CB, Thumm M, Tolkovsky AM, Tooze SA, Truant R, Tumanovska LV, Uchiyama Y, Ueno T, Uzcátegui NL, van der Klei I, Vaquero EC, Vellai T, Vogel MW, Wang HG, Webster P, Wiley JW, Xi Z, Xiao G, Yahalom J, Yang JM, Yap G, Yin XM, Yoshimori T, Yu L, Yue Z, Yuzaki M, Zabirnyk O, Zheng X, Zhu X, Deter RL. Guidelines for the use and interpretation of assays for monitoring au-tophagy in higher eukaryotes. Autophagy 4: 151-175, 2008.
26. Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science 290: 1717-1721, 2000.
27. Lakadamyali M, Rust MJ, Zhuang X. Endocytosis of influenza viruses. Microbes Infect 6: 929-936, 2004.
28. Law AH, Lee DC, Yuen KY, Peiris M, Lau AS. Cellular response to influenza virus infection: a potential role for autophagy in CXCL10 and interferon-alpha induction. Cell Mol Immunol 7: 263-270, 2010.
29. Lee DC, Cheung CY, Law AH, Mok CK, Peiris M, Lau AS. p38 mitogen-activated protein kinase-dependent hyperinduction of tumor necrosis factor alpha expression in response to avian influenza virus H5N1. J Virol 79: 10147-10154, 2005.
30. Levine B. Eating oneself and uninvited guests: autophagy-related pathways in cellular defense. Cell 120: 159-162, 2005.
31. Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature 469: 323-335, 2011.
32. Ma J, Sun Q, Mi R, Zhang H. Avian influenza A virus H5N1 causes autophagy-mediated cell death through suppression of mTOR signaling. J Genet Genomics 38: 533-537, 2011.
33. Mackern-Oberti JP, Maccioni M, Cuffini C, Gatti G, Rivero VE. Susceptibility of prostate epithelial cells to Chlamydia muridarum infection and their role in innate immunity by recruitment of intracellular Toll-like receptors 4 and 2 and MyD88 to the inclusion. Infect Immun 74: 6973-6981, 2006.
34. Mizushima N, Yoshimori T. How to interpret LC3 immunoblotting. Autophagy 3: 542-545, 2007.
35. Mizushima N, Yoshimori T, Ohsumi Y. The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol 27: 107-132, 2011.
36. Mok KP, Wong CH, Cheung CY, Chan MC, Lee SM, Nicholls JM, Guan Y, Peiris JS. Viral genetic determinants of H5N1 influenza viruses that contribute to cytokine dysregulation. J Infect Dis 200: 1104-1112, 2009.
37. Moscat J, Diaz-Meco MT. p62 at the crossroads of autophagy, apoptosis, and cancer. Cell 137: 1001-1004, 2009.
38. Nakahira K, Choi AM. Autophagy: a potential therapeutic target in lung diseases. Am J Physiol Lung Cell Mol Physiol 305: L93-L107, 2013.
39. Nakahira K, Haspel JA, Rathinam VA, Lee SJ, Dolinay T, Lam HC, Englert JA, Rabinovitch M, Cernadas M, Kim HP, Fitzgerald KA, Ryter SW, Choi AM. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 12: 222-230, 2011.
40. Nakamura K, Kimple AJ, Siderovski DP, Johnson GL. PB1 domain interaction of p62/sequestosome 1 and MEKK3 regulates NF-kappaB activation. J Biol Chem 285: 2077-2089, 2010.
41. Orvedahl A, MacPherson S, Sumpter R Jr, Talloczy Z, Zou Z, Levine B. Autophagy protects against Sindbis virus infection of the central nervous system. Cell Host Microbe 7: 115-127, 2010.
42. Ovsyannikova IG, Haralambieva IH, Vierkant RA, Pankratz VS, Jacobson RM, Poland GA. The role of polymorphisms in Toll-like receptors and their associated intracellular signaling genes in measles vaccine immunity. Hum Genet 130: 547-561, 2011.
43. Peiris JS, Yu WC, Leung CW, Cheung CY, Ng WF, Nicholls JM, Ng TK, Chan KH, Lai ST, Lim WL, Yuen KY, Guan Y. Re-emergence of fatal human influenza A subtype H5N1 disease. Lancet 363: 617-619, 2004.
44. Pleskov VM, Bannikov AI, Zaitsev Iu V. [The receptor-mediated endo-cytosis of influenza viruses and low-density lipoproteins by tissue cells]. Vopr Virusol 39: 121-125, 1994.
45. Sakabe S, Takano R, Nagamura-Inoue T, Yamashita N, Nidom CA, Quynh Le MT, Iwatsuki-Horimoto K, Kawaoka Y. Differences in cytokine production in human macrophages and in virulence in mice are attributable to the acidic polymerase protein of highly pathogenic influenza A virus subtype H5N1. J Infect Dis 207: 262-271, 2012.
46. Schmolke M, Viemann D, Roth J, Ludwig S. Essential impact of NF-kappaB signaling on the H5N1 influenza A virus-induced transcrip-tome. J Immunol 183: 5180-5189, 2009.
47. Simmons C, Farrar J. Insights into inflammation and influenza. N Engl J Med 359: 1621-1623, 2008.
48. Sun Y, Li C, Shu Y, Ju X, Zou Z, Wang H, Rao S, Guo F, Liu H, Nan W, Zhao Y, Yan Y, Tang J, Zhao C, Yang P, Liu K, Wang S, Lu H, Li X, Tan L, Gao R, Song J, Gao X, Tian X, Qin Y, Xu KF, Li D, Jin N, Jiang C. Inhibition of autophagy ameliorates acute lung injury caused by avian influenza A H5N1 infection. Sci Signal 5: ra16, 2012.
49. Szecsi J, Boson B, Johnsson P, Dupeyrot-Lacas P, Matrosovich M, Klenk HD, Klatzmann D, Volchkov V, Cosset FL. Induction of neutralising antibodies by virus-like particles harbouring surface proteins from highly pathogenic H5N1 and H7N1 influenza viruses. Virol J 3: 70, 2006.
50. 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.
51. Tao L, Chen J, Zheng Z, Meng J, Zhang Z, Chen Y, Luo H, Li H, Chen Z, Hu Q, Wang H. H5N1 influenza virus-like particles produced by transient expression in mammalian cells induce humoral and cellular immune responses in mice. Can J Microbiol 58: 391-401, 2012.
52. Viemann D, Schmolke M, Lueken A, Boergeling Y, Friesenhagen J, Wittkowski H, Ludwig S, Roth J. H5N1 virus activates signaling pathways in human endothelial cells resulting in a specific imbalanced inflammatory response. J Immunol 186: 164-173, 2011.
53. Wang H, Jiang C. Influenza A virus H5N1 entry into host cells is through clathrin-dependent endocytosis. Sci China C Life Sci 52: 464-469, 2009.
54. Wang J, Li F, Sun R, Gao X, Wei H, Li LJ, Tian Z. Bacterial colonization dampens influenza-mediated acute lung injury via induction of M2 alveolar macrophages. Nat Commun 4: 2106, 2013.
55. Xu W, Chen M, Ge N, Xu J. Hemagglutinin from the H5N1 virus activates Janus kinase 3 to dysregulate innate immunity. PLoS One 7: e31721, 2012.
56. Zhirnov OP, Klenk HD. Influenza A virus proteins NS1 and HA along with M2 are involved in stimulation of autophagy in infected cells. J Virol 87: 13107-13114, 2013.
57. Zhou Z, Jiang X, Liu D, Fan Z, Hu X, Yan J, Wang M, Gao GF. Autophagy is involved in influenza A virus replication. Autophagy 5: 321-328, 2009.