Apoptosis signaling in influenza virus propagation, innate host defense, and lung injury

Journal of Leukocyte Biology

Volumn 92, Issue 1, 2012, Pages 75-82

  Herold, Susanne ^a   Ludwig, Stephan ^b   Pleschka, Stephan ^c   Wolff, Thorsten ^d  

^a JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

^d ROBERT KOCH INSTITUTE   (Germany)

Author keywords

ARDS; NS1; PB1 F2; Replication; TRAIL; Viral

Indexed keywords

CASPASE 3; CRK LIKE PROTEIN; FAS LIGAND; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; NONSTRUCTURAL PROTEIN 1; PROTEIN KINASE R; RIBONUCLEOPROTEIN; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; VIRUS PROTEIN;

APOPTOSIS; CANCER CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MATURATION; CELL PERMEABILIZATION; CELL SURVIVAL; CYTOMEGALOVIRUS; DISEASE SEVERITY; DNA FRAGMENTATION; ENZYME ACTIVATION; EPITHELIUM CELL; HUMAN; IMMUNE RESPONSE; IMMUNOPATHOLOGY; INFLUENZA VIRUS; INFLUENZA VIRUS A H5N1; INNATE IMMUNITY; LUNG ALVEOLUS CELL; LUNG INJURY; MITOCHONDRIAL MEMBRANE; NONHUMAN; PATHOGENESIS; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN POLYMORPHISM; REVIEW; SIGNAL TRANSDUCTION; SPANISH INFLUENZA; UPREGULATION; VIRAL CLEARANCE; VIRUS CELL INTERACTION; VIRUS REPLICATION; VIRUS VIRULENCE;

APOPTOSIS; HUMANS; IMMUNITY, INNATE; INFLUENZA, HUMAN; LUNG INJURY; ORTHOMYXOVIRIDAE; VIRUS REPLICATION;

ORTHOMYXOVIRIDAE;

EID: 84863460855     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1011530     Document Type: Review

References (82)

1. Medina, R. A., Garcia-Sastre, A. (2011) Influenza A viruses: new research developments. Nat. Rev. Microbiol. 9, 590-603.
2. Arabi, Y., Gomersall, C. D., Ahmed, Q. A., Boynton, B. R., Memish, Z. A. (2007) The critically ill avian influenza A (H5N1) patient. Crit. Care Med. 35, 1397-1403.
3. Gannage, M., Dormann, D., Albrecht, R., Dengjel, J., Torossi, T., Ramer, P. C., Lee, M., Strowig, T., Arrey, F., Conenello, G., Pypaert, M., Andersen, J., Garcia-Sastre, A., Munz, C. (2009) Matrix protein 2 of influenza A virus blocks autophagosome fusion with lysosomes. Cell Host Microbe 6, 367-380.
4. Hedrick, S. M., Ch'en, I. L., Alves, B. N. (2010) Intertwined pathways of programmed cell death in immunity. Immunol. Rev. 236, 41-53.
5. Kerr, J. F., Wyllie, A. H., Currie, A. R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26, 239-257.
6. Igney, F. H., Krammer, P. H. (2002) Death and anti-death: tumour resistance to apoptosis. Nat. Rev. Cancer 2, 277-288.
7. Locksley, R. M., Killeen, N., Lenardo, M. J. (2001) The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104, 487-501.
8. Corazza, N., Kassahn, D., Jakob, S., Badmann, A., Brunner, T. (2009) TRAIL-induced apoptosis: between tumor therapy and immunopathol-ogy. Ann. N. Y. Acad. Sci. 1171, 50-58.
9. Monleon, I., Martinez-Lorenzo, M. J., Monteagudo, L., Lasierra, P., Taules, M., Iturralde, M., Pineiro, A., Larrad, L., Alava, M. A., Naval, J., Anel, A. (2001) Differential secretion of Fas ligand- or APO2 ligand/ TNF-related apoptosis-inducing ligand-carrying microvesicles during activation-induced death of human T cells. J. Immunol. 167, 6736-6744.
10. Falschlehner, C., Ganten, T. M., Koschny, R., Schaefer, U., Walczak, H. (2009) TRAIL and other TRAIL receptor agonists as novel cancer therapeutics. Adv. Exp. Med. Biol. 647, 195-206.
11. Cory, S., Adams, J. M. (2002) The Bcl2 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer 2, 647-656.
12. Elmore, S. (2007) Apoptosis: a review of programmed cell death. Toxi-col. Pathol. 35, 495-516.
13. Cohen, G. M. (1997) Caspases: the executioners of apoptosis. Biochem. J. 326, 1-16.
14. Thornberry, N. A., Lazebnik, Y. (1998) Caspases: enemies within. Science 281, 1312-1316.
15. Hinshaw, V. S., Olsen, C. W., Dybdahl-Sissoko, N., Evans, D. (1994) Apoptosis: a mechanism of cell killing by influenza A and B viruses. J. Virol. 68, 3667-3673.
16. Fesq, H., Bacher, M., Nain, M., Gemsa, D. (1994) Programmed cell death (apoptosis) in human monocytes infected by influenza A virus. Immunobiology 190, 175-182.
17. Korteweg, C., Gu, J. (2008) Pathology, molecular biology, and pathogen-esis of avian influenza A (H5N1) infection in humans. Am. J. Pathol. 172, 1155-1170.
18. Brydon, E. W., Morris, S. J., Sweet, C. (2005) Role of apoptosis and cytokines in influenza virus morbidity. FEMS Microbiol. Rev. 29, 837-850.
19. Mori, I., Komatsu, T., Takeuchi, K, Nakakuki, K, Sudo, M., Kimura, Y. (1995) In vivo induction of apoptosis by influenza virus. J. Gen. Virol. 76, 2869-2873.
20. Zhang, C, Yang, Y, Zhou, X., Yang, Z., Liu, X., Cao, Z., Song, H., He, Y, Huang, P. (2011) The NS1 protein of influenza A virus interacts with heat shock protein Hsp90 in human alveolar basal epithelial cells: implication for virus-induced apoptosis. Virol. J. 8, 181.
21. Krumbholz, A., Philipps, A, Oehring, H., Schwarzer, K, Eitner, A, Wut-zler, P., Zell, R. (2011) Current knowledge on PB1-F2 of influenza A viruses. Med. Microbiol. Immunol. 200, 69-75.
22. Lu, X., Masic, A, Li, Y, Shin, Y, Liu, Q., Zhou, Y (2010) The PI3K/Akt pathway inhibits influenza A virus-induced Bax-mediated apoptosis by negatively regulating the JNK pathway via ASK1. J. Gen. Virol. 91, 1439-1449.
23. Fujimoto, I., Takizawa, T., Ohba, Y, Nakanishi, Y (1998) Co-expression of Fas and Fas-ligand on the surface of influenza virus-infected cells. Cell Death Differ. 5, 426-431.
24. Balachandran, S., Roberts, P. C, Kipperman, T., Bhalla, K. N., Com-pans, R. W., Archer, D. R, Barber, G. N. (2000) α/β Interferons potentiate virus-induced apoptosis through activation of the FADD/Caspase-8 death signaling pathway. J. Virol. 74, 1513-1523.
25. Brincks, E. L., Kucaba, T. A, Legge, K. L., Griffith, T. S. (2008) Influenza-induced expression of functional tumor necrosis factor-related apoptosis-inducing ligand on human peripheral blood mononuclear cells. Hum. Immunol. 69, 634-646.
26. Ekchariyawat, P., Thitithanyanont, A, Sirisinha, S., Utaisincharoen, P. (2011) Apoptosis induced by avian H5N1 virus in human monocyte-de-rived macrophages involves TRAIL-inducing caspase-10 activation. Innate Immun., Epub ahead of print.
27. Galluzzi, L., Brenner, C, Morselli, E., Touat, Z., Kroemer, G. (2008) Viral control of mitochondrial apoptosis. PLoS Pathog. 4, e1000018.
28. Opitz, B., Rejaibi, A, Dauber, B., Eckhard, J., Vinzing, M., Schmeck, B., Hippenstiel, S., Suttorp, N., Wolff, T. (2007) IFNβinduction by influenza A virus is mediated by RIG-I which is regulated by the viral NS1 protein. Cell. Microbiol. 9, 930-938.
29. Wolff, T., Ludwig, S. (2009) Influenza viruses control the vertebrate type I interferon system: factors, mechanisms, and consequences. J. Interferon Cytokine Res. 29, 549-557.
30. Hale, B. G., Randall, R. E., Ortin, J., Jackson, D. (2008) The multifunctional NS1 protein of influenza A viruses. J. Gen. Virol. 89, 2359-2376.
31. Zhirnov, O. P., Konakova, T. E., Wolff, T., Klenk, H. D. (2002) NS1 protein of influenza A virus down-regulates apoptosis. J. Virol. 76, 1617-1625.
32. Schultz-Cherry, S., Dybdahl-Sissoko, N., Neumann, G., Kawaoka, Y, Hin-shaw, V. S. (2001) Influenza virus NS1 protein induces apoptosis in cultured cells. J. Virol. 75, 7875-7881.
33. Ehrhardt, C, Marjuki, H., Wolff, T., Nurnberg, B., Planz, O., Pleschka, S., Ludwig, S. (2006) Bivalent role of the phosphatidylinositol-3-kinase (PI3K) during influenza virus infection and host cell defence. Cell. Microbiol. 8, 1336-1348.
34. Ehrhardt, C, Wolff, T., Pleschka, S., Planz, O., Beermann, W., Bode, J. G., Schmolke, M., Ludwig, S. (2007) Influenza A virus NS1 protein activates the PI3K/Akt pathway to mediate antiapoptotic signaling responses. J. Virol. 81, 3058-3067.
35. Hale, B. G., Jackson, D., Chen, Y H., Lamb, R A, Randall, R E. (2006) Influenza A virus NS1 protein binds p85/3 and activates phosphatidylino-sitol-3-kinase signaling. Proc. Natl. Acad. Sci. USA 103, 14194-14199.
36. Ehrhardt, C, Ludwig, S. (2009) A new player in a deadly game: influenza viruses and the PI3K/Akt signalling pathway. Cell. Microbiol. 11, 863-871.
37. Heikkinen, L. S., Kazlauskas, A, Melen, K, Wagner, R, Ziegler, T., Julkunen, I., Saksela, K. (2008) Avian and 1918 Spanish influenza A virus NS1 proteins bind to Crk/CrkL Src homology 3 domains to activate host cell signaling. J. Biol. Chem. 283, 5719-5727.
38. Hrincius, E. R, Wixler, V., Wolff, T., Wagner, R, Ludwig, S., Ehrhardt, C. (2010) CRK adaptor protein expression is required for efficient replication of avian influenza A viruses and controls JNK-mediated apoptotic responses. Cell. Microbiol. 12, 831-843.
39. Liu, H., Golebiewski, L., Dow, E. C, Krug, R M., Javier, R T., Rice, A. P. (2010) The ESEV PDZ-binding motif of the avian influenza A virus NS1 protein protects infected cells from apoptosis by directly targeting Scribble. J. Virol. 84, 11164-11174.
40. Soubies, S. M., Volmer, C, Croville, G., Loupias, J., Peralta, B., Costes, P., Lacroux, C, Guerin, J. L., Volmer, R. (2010) Species-specific contribution of the four C-terminal amino acids of influenza A virus NS1 protein to virulence. J. Virol. 84, 6733-6747.
41. Zielecki, F., Semmler, I., Kalthoff, D., Voss, D., Mauel, S., Gruber, A. D., Beer, M., Wolff, T. (2010) Virulence determinants of avian H5N1 influenza A virus in mammalian and avian hosts: role of the C-terminal ESEV motif in the viral NS1 protein. J. Virol. 84, 10708-10718.
42. Dauber, B., Wolff, T. (2009) Activation of the antiviral kinase PKR and viral countermeasures. Viruses 1, 523-544.
43. Lam, W. Y., Tang, J. W., Yeung, A. C, Chiu, L. C, Sung, J. J., Chan, P. K. (2008) Avian influenza virus A/HK/483/97(H5N1) NS1 protein induces apoptosis in human airway epithelial cells. J. Virol. 82, 2741-2751.
44. Chen, W., Calvo, P. A, Malide, D., Gibbs, J., Schubert, U., Bacik, I., Basta, S., O'Neill, R., Schickli, J., Palese, P., Henklein, P., Bennink, J. R, Yewdell, J. W. (2001) A novel influenza A virus mitochondrial protein that induces cell death. Nat. Med. 7, 1306-1312.
45. Zamarin, D., Ortigoza, M. B., Palese, P. (2006) Influenza A virus PB1-F2 protein contributes to viral pathogenesis in mice. J. Virol. 80, 7976-7983.
46. McAuley, J. L., Chipuk, J. E., Boyd, K. L., Van De Velde, N., Green, D. R., McCullers, J. A. (2010) PB1-F2 proteins from H5N1 and 20 century pandemic influenza viruses cause immunopathology. PLoS Pathog. 6, e1001014.
47. McAuley, J. L., Hornung, F., Boyd, K. L., Smith, A. M., McKeon, R, Bennink, J., Yewdell, J. W., McCullers, J. A. (2007) Expression of the 1918 influenza A virus PB1-F2 enhances the pathogenesis of viral and secondary bacterial pneumonia. Cell Host Microbe 2, 240-249.
48. Zamarin, D., Garcia-Sastre, A, Xiao, X., Wang, R., Palese, P. (2005) Influenza virus PB1-F2 protein induces cell death through mitochondrial ANT3 and VDAC1. PLoS Pathog. 1, e4.
49. Chen, C. J., Chen, G. W., Wang, C. H., Huang, C. H., Wang, Y C, Shih, S. R (2010) Differential localization and function of PB1-F2 derived from different strains of influenza A virus. J. Virol. 84, 10051-10062.
50. Mazur, I., Anhlan, D., Mitzner, D., Wixler, L., Schubert, U., Ludwig, S. (2008) The proapoptotic influenza A virus protein PB1-F2 regulates viral polymerase activity by interaction with the PB1 protein. Cell. Microbiol. 10, 1140-1152.
51. McAuley, J. L., Zhang, K, McCullers, J. A. (2010) The effects of influenza A virus PB1-F2 protein on polymerase activity are strain specific and do not impact pathogenesis. J. Virol. 84, 558-564.
52. Le Goffic, R, Bouguyon, E., Chevalier, C, Vidic, J., Da Costa, B., Leyma-rie, O., Bourdieu, C, Decamps, L., Dhorne-Pollet, S., Delmas, B. (2010) Influenza A virus protein PB1-F2 exacerbates IFN-βexpression of human respiratory epithelial cells. J. Immunol. 185, 4812-4823.
53. Conenello, G. M., Zamarin, D., Perrone, L. A, Tumpey, T., Palese, P. (2007) A single mutation in the PB1-F2 of H5N1 (HK/97) and 1918 influenza A viruses contributes to increased virulence. PLoS Pathog. 3, 1414-1421.
54. Le Goffic, R, Leymarie, O., Chevalier, C, Rebours, E., Da Costa, B., Vidic, J., Descamps, D., Sallenave, J. M., Rauch, M., Samson, M., Delmas, B. (2011) Transcriptomic analysis of host immune and cell death responses associated with the influenza A virus PB1-F2 protein. PLoS Pathog, 7, e1002202.
55. Herold, S., Steinmueller, M., von Wulffen, W., Cakarova, L., Pinto, R, Pleschka, S., Mack, M., Kuziel, W. A, Corazza, N., Brunner, T., Seeger, W., Lohmeyer, J. (2008) Lung epithelial apoptosis in influenza virus pneumonia: the role of macrophage-expressed TNF-related apoptosis-inducing ligand. J. Exp. Med. 205, 3065-3077.
56. Zhirnov, O. P., Klenk, H. D. (2007) Control of apoptosis in influenza virus-infected cells by up-regulation of Akt and p53 signaling. Apoptosis 12, 1419-1432.
57. Olsen, C. W., Kehren, J. C, Dybdahl-Sissoko, N. R, Hinshaw, V. S. (1996) bcl-2 alters influenza virus yield, spread, and hemagglutinin gly-cosylation. J. Virol. 70, 663-666.
58. Wurzer, W. J., Planz, O., Ehrhardt, C, Giner, M., Silberzahn, T., Pleschka, S., Ludwig, S. (2003) Caspase 3 activation is essential for efficient influenza virus propagation. EMBOJ. 22, 2717-2728.
59. Wurzer, W. J., Ehrhardt, C, Pleschka, S., Berberich-Siebelt, F., Wolff, T., Walczak, H., Planz, O., Ludwig, S. (2004) NF-KB-dependent induction of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) and Fas/FasL is crucial for efficient influenza virus propagation. J. Biol. Chem. 279, 30931-30937.
60. Mazur, I., Wurzer, W. J., Ehrhardt, C, Pleschka, S., Puthavathana, P., Silberzahn, T., Wolff, T., Planz, O., Ludwig, S. (2007) Acetylsalicylic acid (ASA) blocks influenza virus propagation via its NF-KB-inhibiting activity. Cell. Microbiol. 9, 1683-1694.
61. Elton, D., Simpson-Holley, M., Archer, K, Medcalf, L., Hallam, R, Mc-Cauley, J., Digard, P. (2001) Interaction of the influenza virus nucleo-protein with the cellular CRM1-mediated nuclear export pathway. J. Virol. 75, 408-419.
62. Faleiro, L., Lazebnik, Y (2000) Caspases disrupt the nuclear-cytoplasmic barrier. J. Cell Biol. 151, 951-959.
63. Kramer, A, Liashkovich, I., Oberleithner, H., Ludwig, S., Mazur, I., Sha-hin, V (2008) Apoptosis leads to a degradation of vital components of active nuclear transport and a dissociation of the nuclear lamina. Proc. Natl. Acad. Sci. USA 105, 11236-11241.
64. Strasser, A, Jost, P. J., Nagata, S. (2009) The many roles of FAS receptor signaling in the immune system. Immunity 30, 180-192.
65. Topham, D. J., Tripp, R A, Doherty, P. C. (1997) CD8+ T cells clear influenza virus by perforin or Fas-dependent processes. J. Immunol. 159, 5197-5200.
66. Ishikawa, E., Nakazawa, M., Yoshinari, M., Minami, M. (2005) Role of tumor necrosis factor-related apoptosis-inducing ligand in immune response to influenza virus infection in mice. J. Virol. 79, 7658-7663.
67. Brincks, E. L., Katewa, A, Kucaba, T. A, Griffith, T. S., Legge, K. L. (2008) CD8 T cells utilize TRAIL to control influenza virus infection. J. Immunol. 181, 4918-4925.
68. Chaperot, L., Blum, A, Manches, O., Lui, G., Angel, J., Molens, J. P., Plumas, J. (2006) Virus or TLR agonists induce TRAIL-mediated cytotoxic activity of plasmacytoid dendritic cells. J. Immunol. 176, 248-255.
69. Kotelkin, A, Prikhod'ko, E. A, Cohen, J. I., Collins, P. L., Bukreyev, A. (2003) Respiratory syncytial virus infection sensitizes cells to apoptosis mediated by tumor necrosis factor-related apoptosis-inducing ligand. J. Virol. 77, 9156-9172.
70. Sedger, L. M., Shows, D. M., Blanton, R A, Peschon, J. J., Goodwin, R G., Cosman, D., Wiley, S. R (1999) IFN-7 mediates a novel antiviral activity through dynamic modulation of TRAIL and TRAIL receptor expression. J. Immunol. 163, 920-926.
71. Vidalain, P. O., Azocar, O., Lamouille, B., Astier, A., Rabourdin-Combe, C, Servet-Delprat, C. (2000) Measles virus induces functional TRAIL production by human dendritic cells. J. Virol. 74, 556-559.
72. Legge, K. L., Braciale, T.J. (2005) Lymph node dendritic cells control CD8+ T cell responses through regulated FasL expression. Immunity 23, 649-659.
73. Langlois, R A, Legge, K. L. (2010) Plasmacytoid dendritic cells enhance mortality during lethal influenza infections by eliminating virus-specific CD8 T cells. J. Immunol. 184, 4440-4446.
74. Zhou, J., Law, H. K, Cheung, C. Y, Ng, I. H., Peiris, J. S., Lau, Y L. (2006) Functional tumor necrosis factor-related apoptosis-inducing ligand production by avian influenza virus-infected macrophages. J. Infect. Dis. 193, 945-953.
75. Brincks, E. L., Gurung, P., Langlois, R A, Hemann, E. A, Legge, K. L., Griffith, T. S. (2011) The magnitude of the T cell response to a clinically significant dose of influenza virus is regulated by TRAIL. J. Immunol. 187, 4581-4588.
76. Bem, R A, Bos, A. P., Wosten-van Asperen, R M., Bruijn, M., Lutter, R, Sprick, M. R, van Woensel, J. B. (2010) Potential role of soluble TRAIL in epithelial injury in children with severe RSV infection. Am. J. Respir. Cell Mol. Biol. 42, 697-705.
77. Capelozzi, V L., Parra, E. R, Ximenes, M., Bammann, R H., Barbas, C. S., Duarte, M. I. (2011) Pathological and ultrastructural analysis of surgical lung biopsies in patients with swine-origin influenza type A/H1N1 and acute respiratory failure. Clinics (Sao Paulo) 65, 1229-1237.
78. Martin, T. R, Hagimoto, N., Nakamura, M., Matute-Bello, G. (2005) Apoptosis and epithelial injury in the lungs. Proc. Am. Thorac. Soc. 2, 214-220.
79. Herold, S., Tabar, T. S., Janssen, H., Hoegner, K, Cabanski, M., Lewe-Schlosser, P., Albrecht, J., Driever, F., Vadasz, I., Seeger, W., Steinmueller, M., Lohmeyer, J. (2011) Exudate macrophages attenuate lung injury by the release of IL-1 receptor antagonist in gram-negative pneumonia. Am. J. Respir. Crit. Care Med 183, 1380-1390.
80. Janssen, W J., Barthel, L., Muldrow, A, Oberley-Deegan, R E., Kearns, M. T., Jakubzick, C, Henson, P. M. (2011) Fas determines differential fates of resident and recruited macrophages during resolution of acute lung injury. Am. J. Respir. Crit. Care Med. 184, 547-560.
81. Skeldon, A, Saleh, M. (2011) The inflammasomes: molecular effectors of host resistance against bacterial, viral, parasitic, and fungal infections. Front. Microbiol. 2, 15.
82. Pang, I. K, Iwasaki, A. (2011) Inflammasomes as mediators of immunity against influenza virus. Trends Immunol. 32, 34-41.