Influenza virus PB1-F2 protein induces cell death through mitochondrial ANT3 and VDAC1

PLoS Pathogens

Volumn 1, Issue 1, 2005, Pages 0040-0054

  Zamarin, Dmitriy ^a   García Sastre, Adolfo ^a   Xiao, Xiaoyao ^a   Wang, Rong ^a   Palese, Peter ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77951059450     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.0010004     Document Type: Article

References (52)

1. Garcia-Sastre A (2001) Inhibition of interferon-mediated antiviral responses by influenza A viruses and other negative-strand RNA viruses. Virology 279: 375-384.
2. Garcia-Sastre A, Egorov A, Matassov D, Brandt S, Levy DE, et al. (1998) Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252: 324-330.
3. Chen W, Calvo PA, Malide D, Gibbs J, Schubert U, et al. (2001) A novel influenza A virus mitochondrial protein that induces cell death. Nat Med 7: 1306-1312.
4. Gibbs JS, Malide D, Hornung F, Bennink JR, Yewdell JW (2003) The influenza A virus PB1-F2 protein targets the inner mitochondrial membrane via a predicted basic amphipathic helix that disrupts mitochondrial function. J Virol 77: 7214-7224.
5. Yamada H, Chounan R, Higashi Y, Kurihara N, Kido H (2004) Mitochondrial targeting sequence of the influenza A virus PB1-F2 protein and its function in mitochondria. FEBS Lett 578: 331-336.
6. Chanturiya AN, Basanez G, Schubert U, Henklein P, Yewdell JW, et al. (2004) PB1-F2, an influenza A virus-encoded proapoptotic mitochondrial protein, creates variably sized pores in planar lipid membranes. J Virol 78: 6304-6312.
7. Henklein P, Bruns K, Nimtz M, Wray V, Tessmer U, et al. (2005) Influenza A virus protein PB1-F2: Synthesis and characterization of the biologically active full length protein and related peptides. J Pept Sci 11: 481-490.
8. Vieira HL, Boya P, Cohen I, El Hamel C, Haouzi D, et al. (2002) Cell permeable BH3-peptides overcome the cytoprotective effect of Bcl-2 and Bcl-X(L). Oncogene 21: 1963-1977.
9. Basanez G, Zhang J, Chau BN, Maksaev GI, Frolov VA, et al. (2001) Proapoptotic cleavage products of Bcl-xL form cytochrome c-conducting pores in pure lipid membranes. J Biol Chem 276: 31083-31091.
10. Boya P, Roumier T, Andreau K, Gonzalez-Polo RA, Zamzami N, et al. (2003) Mitochondrion-targeted apoptosis regulators of viral origin. Biochem Biophys Res Commun 304: 575-581.
11. Boya P, Roques B, Kroemer G (2001) New EMBO members' review: Viral and bacterial proteins regulating apoptosis at the mitochondrial level. EMBO J 20: 4325-4331.
12. Nencioni L, Iuvara A, Aquilano K, Ciriolo MR, Cozzolino F, et al. (2003) Influenza A virus replication is dependent on an antioxidant pathway that involves GSH and Bcl-2. FASEB J 17: 758-760.
13. Olsen CW, Kehren JC, Dybdahl-Sissoko NR, Hinshaw VS (1996) Bcl-2 alters influenza virus yield, spread, and hemagglutinin glycosylation. J Virol 70: 663-666.
14. 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: 3667-3673.
15. van Gurp M, Festjens N, van Loo G, Saelens X, Vandenabeele P (2003) Mitochondrial intermembrane proteins in cell death. Biochem Biophys Res Commun 304: 487-497.
16. Zamzami N, Kroemer G (2001) The mitochondrion in apoptosis: How Pandora's box opens. Nat Rev Mol Cell Biol 2: 67-71.
17. Martinou JC, Green DR (2001) Breaking the mitochondrial barrier. Nat Rev Mol Cell Biol 2: 63-67.
18. Beutner G, Ruck A, Riede B, Brdiczka D (1998) Complexes between porin, hexokinase, mitochondrial creatine kinase and adenylate translocator display properties of the permeability transition pore. Implication for regulation of permeability transition by the kinases. Biochim Biophys Acta 1368: 7-18.
19. Vyssokikh MY, Brdiczka D (2003) The function of complexes between the outer mitochondrial membrane pore (VDAC) and the adenine nucleotide translocase in regulation of energy metabolism and apoptosis. Acta Biochim Pol 50: 389-404.
20. Valentijn AJ, Gilmore AP (2004) Translocation of full-length Bid to mitochondria during anoikis. J Biol Chem 279: 32848-32857.
21. Puthalakath H, VillungerA, O'Reilly LA, Beaumont JG, Coultas L, et al. (2001) Bmf: A proapoptotic BH3-only protein regulated by interaction with the myosin V actin motor complex, activated by anoikis. Science 293: 1829-1832.
22. Frisch SM (1999) Evidence for a function of death-receptor-related, death-domain-containing proteins in anoikis. Curr Biol 9: 1047-1049.
23. Shimizu S, Tsujimoto Y (2000) Proapoptotic BH3-only Bcl-2 family members induce cytochrome c release, but not mitochondrial membrane potential loss, and do not directly modulate voltage-dependent anion channel activity. Proc Natl Acad Sci U S A 97: 577-582.
24. Halestrap AP, Brennerb C (2003) The adenine nucleotide translocase: A central component of the mitochondrial permeability transition pore and key player in cell death. Curr Med Chem 10: 1507-1525.
25. Vyssokikh M, Brdiczka D (2004) VDAC and peripheral channelling complexes in health and disease. Mol Cell Biochem 256-257(1-2): 117-126.
26. Shimizu S, Narita M, Tsujimoto Y (1999) Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399: 483-487.
27. Rizzuto R, Brini M, Pizzo P, Murgia M, Pozzan T (1995) Chimeric green fluorescent protein as a tool for visualizing subcellular organelles in living cells. Curr Biol 5: 635-642.
28. Henderson PJ, Lardy HA (1970) Bongkrekic acid. An inhibitor of the adenine nucleotide translocase of mitochondria. J Biol Chem 245: 1319-1326.
29. Danial NN, Korsmeyer SJ (2004) Cell death: Critical control points. Cell 116: 205-219.
30. Kroemer G (1997) The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat Med 3: 614-620.
31. Massari P, Ho Y, Wetzler LM (2000) Neisseria meningitidis porin PorB interacts with mitochondria and protects cells from apoptosis. Proc Natl Acad Sci U S A 97: 9070-9075.
32. Muller A, Gunther D, Brinkmann V, Hurwitz R, Meyer TF, et al. (2000) Targeting of the pro-apoptotic VDAC-like porin (PorB) of Neisseria gonorrhoeae to mitochondria of infected cells. EMBO J 19: 5332-5343.
33. Rahmani Z, Huh KW, Lasher R, Siddiqui A (2000) Hepatitis B virus X protein colocalizes to mitochondria with a human voltage-dependent anion channel, HVDAC3, and alters its transmembrane potential. J Virol 74: 2840-2846.
34. Goldmacher VS, Bartle LM, Skaletskaya A, Dionne CA, Kedersha NL, et al. (1999) A cytomegalovirus-encoded mitochondria-localized inhibitor of apoptosis structurally unrelated to Bcl-2. Proc Natl Acad Sci U S A 96: 12536-12541.
35. Jacotot E, Ferri KF, El Hamel C, Brenner C, Druillennec S, et al. (2001) Control of mitochondrial membrane permeabilization by adenine nucleotide translocator interacting with HIV-1 viral protein rR and Bcl-2. J Exp Med 193: 509-519.
36. Everett H, Barry M, Sun X, Lee SF, Frantz C, et al. (2002) The myxoma poxvirus protein, M11L, prevents apoptosis by direct interaction with the mitochondrial permeability transition pore. J Exp Med 196: 1127-1139.
37. Su F, Schneider RJ (1997) Hepatitis B virus HBx protein sensitizes cells to apoptotic killing by tumor necrosis factor alpha. Proc Natl Acad Sci U S A 94: 8744-8749.
38. Rytomaa M, Martins LM, Downward J (1999) Involvement of FADD and caspase-8 signalling in detachment-induced apoptosis. Curr Biol 9: 1043-1046.
39. Kokoszka JE, Waymire KG, Levy SE, Sligh JE, Cai J, et al. (2004) The ADP/ ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 427: 461-465.
40. Jacotot E, Ravagnan L, Loeffler M, Ferri KF, Vieira HL, et al. (2000) The HIV-1 viral protein R induces apoptosis via a direct effect on the mitochondrial permeability transition pore. J Exp Med 191: 33-46.
41. Cheng EH, Sheiko TV, Fisher JK, Craigen WJ, Korsmeyer SJ (2003) VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 301: 513-517.
42. Wurzer WJ, Planz O, Ehrhardt C, Giner M, Silberzahn T, et al. (2003) Caspase 3 activation is essential for efficient influenza virus propagation. EMBO J 22: 2717-2728.
43. Lowy RJ (2003) Influenza virus induction of apoptosis by intrinsic and extrinsic mechanisms. Int Rev Immunol 22: 425-449.
44. Seo SH, Webster RG (2002) Tumor necrosis factor alpha exerts powerful anti-influenza virus effects in lung epithelial cells. J Virol 76: 1071-1076.
45. Levy DE, Garcia-Sastre A (2001) The virus battles: IFN induction of the antiviral state and mechanisms of viral evasion. Cytokine Growth Factor Rev 12: 143-156.
46. Brydon EW, Smith H, Sweet C (2003) Influenza A virus-induced apoptosis in bronchiolar epithelial (NCI-H292) cells limits pro-inflammatory cytokine release. J Gen Virol 84: 2389-2400.
47. Doerner A, Pauschinger M, Badorff A, Noutsias M, Giessen S, et al. (1997) Tissue-specific transcription pattern of the adenine nucleotide translocase isoforms in humans. FEBS Lett 414: 258-262.
48. Stepien G, Torroni A, Chung AB, Hodge JA, Wallace DC (1992) Differential expression of adenine nucleotide translocator isoforms in mammalian tissues and during muscle cell differentiation. J Biol Chem 267: 14592-14597.
49. Kayser H, Kratzin HD, Thinnes FP, Gotz H, Schmidt WE, et al. (1989) [Identification of human porins. II. Characterization and primary structure of a 31-lDa porin from human B lymphocytes (Porin 31HL).]. Biol Chem Hoppe Seyler 370: 1265-1278.
50. Blachly-Dyson E, Zambronicz EB, Yu WH, Adams V, McCabe ER, et al. (1993) Cloning and functional expression in yeast of two human isoforms of the outer mitochondrial membrane channel, the voltage-dependent anion channel. J Biol Chem 268: 1835-1841.
51. Niwa H, Yamamura K, Miyazaki J (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108: 193-199.
52. Wei MC, Lindsten T, Mootha VK, Weiler S, Gross A, et al. (2000) tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 14: 2060-2071.