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Erschienen in: Archives of Virology 3/2017

16.11.2016 | Original Article

Influenza virus infection induces translocation of apoptosis-inducing factor (AIF) in A549 cells: role of AIF in apoptosis and viral propagation

verfasst von: Xinyan Qu, Xiaoran Ding, Ming Duan, Jing Yang, Ruxian Lin, Zhe Zhou, Shengqi Wang

Erschienen in: Archives of Virology | Ausgabe 3/2017

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Abstract

It is recognized that influenza virus induces caspase-dependent apoptosis by activating caspase-3. Apoptosis-inducing factor (AIF) is a caspase-independent cell death effector, and its mitochondrial-nuclear translocation plays an important role in apoptosis. It is demonstrated in this study how influenza virus infection can induce caspase-independent apoptosis in the human alveolar epithelial cell line A549. AIF is translocated from the mitochondria to the nucleus in a caspase-independent manner in response to infection with influenza virus. Knockdown of AIF expression by small interfering RNA (siRNA) led to a reduction in virus-infection-induced apoptosis and virus yield. These results indicate that AIF translocation has a role in influenza-virus-induced apoptosis.
Literatur
1.
Zurück zum Zitat Arnoult D, Parone P, Martinou JC, Antonsson B, Estaquier J, Ameisen JC (2002) Mitochondrial release of apoptosis-inducing factor occurs downstream of cytochrome c release in response to several proapoptotic stimuli. J Cell Biol 159:923–929CrossRefPubMedPubMedCentral Arnoult D, Parone P, Martinou JC, Antonsson B, Estaquier J, Ameisen JC (2002) Mitochondrial release of apoptosis-inducing factor occurs downstream of cytochrome c release in response to several proapoptotic stimuli. J Cell Biol 159:923–929CrossRefPubMedPubMedCentral
2.
Zurück zum Zitat Arnoult D, Gaume B, Karbowski M, Sharpe JC, Cecconi F, Youle RJ (2003) Mitochondrial release of AIF and EndoG requires caspase activation downstream of Bax/Bak-mediated permeabilization. EMBO J 22:4385–4399CrossRefPubMedPubMedCentral Arnoult D, Gaume B, Karbowski M, Sharpe JC, Cecconi F, Youle RJ (2003) Mitochondrial release of AIF and EndoG requires caspase activation downstream of Bax/Bak-mediated permeabilization. EMBO J 22:4385–4399CrossRefPubMedPubMedCentral
3.
Zurück zum Zitat Chen W, Calvo PA, Malide D, Gibbs J, Schubert U, Bacik I, Basta S, O’Neill R, Schickli J, Palese P, Henklein P, Bennink JR, Yewdell JW (2001) A novel influenza A virus mitochondrial protein that induces cell death. Nat Med 7:1306–1312CrossRefPubMed Chen W, Calvo PA, Malide D, Gibbs J, Schubert U, Bacik I, Basta S, O’Neill R, Schickli J, Palese P, Henklein P, Bennink JR, Yewdell JW (2001) A novel influenza A virus mitochondrial protein that induces cell death. Nat Med 7:1306–1312CrossRefPubMed
4.
Zurück zum Zitat Daugas E, Nochy D, Ravagnan L, Loeffler M, Susin SA, Zamzami N, Kroemer G (2000) Apoptosis-inducing factor (AIF): a ubiquitous mitochondrial oxidoreductase involved in apoptosis. FEBS Lett 476:118–123CrossRefPubMed Daugas E, Nochy D, Ravagnan L, Loeffler M, Susin SA, Zamzami N, Kroemer G (2000) Apoptosis-inducing factor (AIF): a ubiquitous mitochondrial oxidoreductase involved in apoptosis. FEBS Lett 476:118–123CrossRefPubMed
5.
Zurück zum Zitat 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 5:426–431CrossRefPubMed 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 5:426–431CrossRefPubMed
6.
Zurück zum Zitat Guo Y, Srinivasula SM, Druilhe A, Fernandes-Alnemri T, Alnemri ES (2002) Caspase-2 induces apoptosis by releasing proapoptotic proteins from mitochondria. J Biol Chem 277:13430–13437CrossRefPubMed Guo Y, Srinivasula SM, Druilhe A, Fernandes-Alnemri T, Alnemri ES (2002) Caspase-2 induces apoptosis by releasing proapoptotic proteins from mitochondria. J Biol Chem 277:13430–13437CrossRefPubMed
7.
Zurück zum Zitat Hinshaw VS, Olsen CW, Dybdahl-Sissoko N, Evans D (1994) Apoptosis: a mechanism of cell killing by influenza A and B viruses. J Virol 68:3667–3673PubMedPubMedCentral Hinshaw VS, Olsen CW, Dybdahl-Sissoko N, Evans D (1994) Apoptosis: a mechanism of cell killing by influenza A and B viruses. J Virol 68:3667–3673PubMedPubMedCentral
8.
Zurück zum Zitat Joza N, Susin SA, Daugas E, Stanford WL, Cho SK, Li CY, Sasaki T, Elia AJ, Cheng HY, Ravagnan L, Ferri KF, Zamzami N, Wakeham A, Hakem R, Yoshida H, Kong YY, Mak TW, Zuniga-Pflucker JC, Kroemer G, Penninger JM (2001) Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410:549–554CrossRefPubMed Joza N, Susin SA, Daugas E, Stanford WL, Cho SK, Li CY, Sasaki T, Elia AJ, Cheng HY, Ravagnan L, Ferri KF, Zamzami N, Wakeham A, Hakem R, Yoshida H, Kong YY, Mak TW, Zuniga-Pflucker JC, Kroemer G, Penninger JM (2001) Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410:549–554CrossRefPubMed
9.
Zurück zum Zitat Kang YH, Yi MJ, Kim MJ, Park MT, Bae S, Kang CM, Cho CK, Park IC, Park MJ, Rhee CH, Hong SI, Chung HY, Lee YS, Lee SJ (2004) Caspase-independent cell death by arsenic trioxide in human cervical cancer cells: reactive oxygen species-mediated poly(ADP-ribose) polymerase-1 activation signals apoptosis-inducing factor release from mitochondria. Cancer Res 64:8960–8967CrossRefPubMed Kang YH, Yi MJ, Kim MJ, Park MT, Bae S, Kang CM, Cho CK, Park IC, Park MJ, Rhee CH, Hong SI, Chung HY, Lee YS, Lee SJ (2004) Caspase-independent cell death by arsenic trioxide in human cervical cancer cells: reactive oxygen species-mediated poly(ADP-ribose) polymerase-1 activation signals apoptosis-inducing factor release from mitochondria. Cancer Res 64:8960–8967CrossRefPubMed
10.
Zurück zum Zitat Kawahara A, Ohsawa Y, Matsumura H, Uchiyama Y, Nagata S (1998) Caspase-independent cell killing by Fas-associated protein with death domain. J Cell Biol 143:1353–1360CrossRefPubMedPubMedCentral Kawahara A, Ohsawa Y, Matsumura H, Uchiyama Y, Nagata S (1998) Caspase-independent cell killing by Fas-associated protein with death domain. J Cell Biol 143:1353–1360CrossRefPubMedPubMedCentral
11.
Zurück zum Zitat Kim JY, Choi JA, Kim TH, Yoo YD, Kim JI, Lee YJ, Yoo SY, Cho CK, Lee YS, Lee SJ (2002) Involvement of p38 mitogen-activated protein kinase in the cell growth inhibition by sodium arsenite. J Cell Physiol 190:29–37CrossRefPubMed Kim JY, Choi JA, Kim TH, Yoo YD, Kim JI, Lee YJ, Yoo SY, Cho CK, Lee YS, Lee SJ (2002) Involvement of p38 mitogen-activated protein kinase in the cell growth inhibition by sodium arsenite. J Cell Physiol 190:29–37CrossRefPubMed
12.
13.
Zurück zum Zitat Lin C, Zimmer SG, Lu Z, Holland RE Jr, Dong Q, Chambers TM (2001) The involvement of a stress-activated pathway in equine influenza virus-mediated apoptosis. Virology 287:202–213CrossRefPubMed Lin C, Zimmer SG, Lu Z, Holland RE Jr, Dong Q, Chambers TM (2001) The involvement of a stress-activated pathway in equine influenza virus-mediated apoptosis. Virology 287:202–213CrossRefPubMed
14.
Zurück zum Zitat Ludwig S, Ehrhardt C, Neumeier ER, Kracht M, Rapp UR, Pleschka S (2001) Influenza virus-induced AP-1-dependent gene expression requires activation of the JNK signaling pathway. J Biol Chem 276:10990–10998CrossRef Ludwig S, Ehrhardt C, Neumeier ER, Kracht M, Rapp UR, Pleschka S (2001) Influenza virus-induced AP-1-dependent gene expression requires activation of the JNK signaling pathway. J Biol Chem 276:10990–10998CrossRef
15.
Zurück zum Zitat Mao WP, Ye JL, Guan ZB, Zhao JM, Zhang C, Zhang NN, Jiang P, Tian T (2007) Cadmium induces apoptosis in human embryonic kidney (HEK) 293 cells by caspase-dependent and -independent pathways acting on mitochondria. Toxicology In Vitro 21:343–354CrossRefPubMed Mao WP, Ye JL, Guan ZB, Zhao JM, Zhang C, Zhang NN, Jiang P, Tian T (2007) Cadmium induces apoptosis in human embryonic kidney (HEK) 293 cells by caspase-dependent and -independent pathways acting on mitochondria. Toxicology In Vitro 21:343–354CrossRefPubMed
16.
Zurück zum Zitat Marchetti C, Jouy N, Leroy-Martin B, Defossez A, Formstecher P, Marchetti P (2004) Comparison of four fluorochromes for the detection of the inner mitochondrial membrane potential in human spermatozoa and their correlation with sperm motility. Hum Reprod 19:2267–2276CrossRefPubMed Marchetti C, Jouy N, Leroy-Martin B, Defossez A, Formstecher P, Marchetti P (2004) Comparison of four fluorochromes for the detection of the inner mitochondrial membrane potential in human spermatozoa and their correlation with sperm motility. Hum Reprod 19:2267–2276CrossRefPubMed
17.
Zurück zum Zitat McCarthy NJ, Whyte MK, Gilbert CS, Evan GI (1997) Inhibition of Ced-3/ICE-related proteases does not prevent cell death induced by oncogenes, DNA damage, or the Bcl-2 homologue Bak. J Cell Biol 136:215–227CrossRefPubMedPubMedCentral McCarthy NJ, Whyte MK, Gilbert CS, Evan GI (1997) Inhibition of Ced-3/ICE-related proteases does not prevent cell death induced by oncogenes, DNA damage, or the Bcl-2 homologue Bak. J Cell Biol 136:215–227CrossRefPubMedPubMedCentral
18.
Zurück zum Zitat Meggyeshazi N, Andocs G, Balogh L, Balla P, Kiszner G, Teleki I, Jeney A, Krenacs T (2014) DNA fragmentation and caspase-independent programmed cell death by modulated electrohyperthermia. Strahlentherapie und Onkologie Organ der Deutschen Rontgengesellschaft 190:815–822CrossRef Meggyeshazi N, Andocs G, Balogh L, Balla P, Kiszner G, Teleki I, Jeney A, Krenacs T (2014) DNA fragmentation and caspase-independent programmed cell death by modulated electrohyperthermia. Strahlentherapie und Onkologie Organ der Deutschen Rontgengesellschaft 190:815–822CrossRef
19.
Zurück zum Zitat Mori I, Komatsu T, Takeuchi K, Nakakuki K, Sudo M, Kimura Y (1995) In vivo induction of apoptosis by influenza virus. J Gen Virol 76:2869–2873CrossRefPubMed Mori I, Komatsu T, Takeuchi K, Nakakuki K, Sudo M, Kimura Y (1995) In vivo induction of apoptosis by influenza virus. J Gen Virol 76:2869–2873CrossRefPubMed
20.
Zurück zum Zitat Nimmerjahn F, Dudziak D, Dirmeier U, Hobom G, Riedel A, Schlee M, Staudt LM, Rosenwald A, Behrends U, Bornkamm GW, Mautner J (2004) Active NF-kappaB signalling is a prerequisite for influenza virus infection. J Gen Virol 85:2347–2356CrossRefPubMed Nimmerjahn F, Dudziak D, Dirmeier U, Hobom G, Riedel A, Schlee M, Staudt LM, Rosenwald A, Behrends U, Bornkamm GW, Mautner J (2004) Active NF-kappaB signalling is a prerequisite for influenza virus infection. J Gen Virol 85:2347–2356CrossRefPubMed
21.
Zurück zum Zitat Shin YK, Liu Q, Tikoo SK, Babiuk LA, Zhou Y (2007) Effect of the phosphatidylinositol 3-kinase/Akt pathway on influenza A virus propagation. J Gen Virol 88:942–950CrossRefPubMed Shin YK, Liu Q, Tikoo SK, Babiuk LA, Zhou Y (2007) Effect of the phosphatidylinositol 3-kinase/Akt pathway on influenza A virus propagation. J Gen Virol 88:942–950CrossRefPubMed
22.
Zurück zum Zitat Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441–446CrossRefPubMed Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441–446CrossRefPubMed
23.
24.
Zurück zum Zitat Turpin E, Luke K, Jones J, Tumpey T, Konan K, Schultz-Cherry S (2005) Influenza virus infection increases p53 activity: role of p53 in cell death and viral replication. J Virol 79:8802–8811CrossRefPubMedPubMedCentral Turpin E, Luke K, Jones J, Tumpey T, Konan K, Schultz-Cherry S (2005) Influenza virus infection increases p53 activity: role of p53 in cell death and viral replication. J Virol 79:8802–8811CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Wurzer WJ, Planz O, Ehrhardt C, Giner M, Silberzahn T, Pleschka S, Ludwig S (2003) Caspase 3 activation is essential for efficient influenza virus propagation. EMBO J 22:2717–2728CrossRefPubMedPubMedCentral Wurzer WJ, Planz O, Ehrhardt C, Giner M, Silberzahn T, Pleschka S, Ludwig S (2003) Caspase 3 activation is essential for efficient influenza virus propagation. EMBO J 22:2717–2728CrossRefPubMedPubMedCentral
26.
Zurück zum Zitat Yu F, Chen Z, Wang B, Jin Z, Hou Y, Ma S, Liu X (2015) The role of lysosome in cell death regulation. Tumour Biol 37:1427–1436CrossRefPubMed Yu F, Chen Z, Wang B, Jin Z, Hou Y, Ma S, Liu X (2015) The role of lysosome in cell death regulation. Tumour Biol 37:1427–1436CrossRefPubMed
Metadaten
Titel
Influenza virus infection induces translocation of apoptosis-inducing factor (AIF) in A549 cells: role of AIF in apoptosis and viral propagation
verfasst von
Xinyan Qu
Xiaoran Ding
Ming Duan
Jing Yang
Ruxian Lin
Zhe Zhou
Shengqi Wang
Publikationsdatum
16.11.2016
Verlag
Springer Vienna
Erschienen in
Archives of Virology / Ausgabe 3/2017
Print ISSN: 0304-8608
Elektronische ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-016-3151-x

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