Influenza virus activates inflammasomes via its intracellular M2 ion channel

Nature Immunology

Volumn 11, Issue 5, 2010, Pages 404-410

  Ichinohe, Takeshi ^a,b   Pang, Iris K ^a   Iwasaki, Akiko ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CRYOPYRIN; INFLAMMASOME; ION CHANNEL; PROTEIN M2;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; GOLGI COMPLEX; INFLUENZA; INFLUENZA VIRUS; MACROPHAGE; MOLECULAR MECHANICS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN LOCALIZATION; VIRUS PATHOGENESIS;

ANIMALS; CARRIER PROTEINS; CELLS, CULTURED; CYTOKINES; DENDRITIC CELLS; GENETIC ENGINEERING; GOLGI APPARATUS; HYDROGEN-ION CONCENTRATION; ION CHANNELS; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MONENSIN; ONCOGENE PROTEINS, VIRAL; ORTHOMYXOVIRIDAE; ORTHOMYXOVIRIDAE INFECTIONS; POTASSIUM CHLORIDE; PROTEIN TRANSPORT; PROTONS; SEQUENCE DELETION; TOLL-LIKE RECEPTOR 7; VIRAL MATRIX PROTEINS; VIRUS REPLICATION;

EID: 77951295418     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.1861     Document Type: Article

References (45)

1. Ichinohe, T., Lee, H.K., Ogura, Y., Flavell, R. & Iwasaki, A. Infammasome recognition of infuenza virus is essential for adaptive immune responses. J. Exp. Med. 206, 79-87 (2009).
2. Kanneganti, T.D. et al. Critical role for cryopyrin/Nalp3 in activation of caspase-1 in response to viral infection and double-stranded RNA. J. Biol. Chem. 281, 36560-36568 (2006).
3. Allen, I.C. et al. The NLRP3 infammasome mediates in vivo innate immunity to infuenza A virus through recognition of viral RNA. Immunity 30, 556-565 (2009).
4. Thomas, P.G. et al. The intracellular sensor NLRP3 mediates key innate and healing responses to infuenza A virus via the regulation of caspase-1. Immunity 30, 566-575 (2009).
5. Martinon, F. & Tschopp, J. Infammatory caspases: linking an intracellular innate immune system to autoinfammatory diseases. Cell 117, 561-574 (2004). (Pubitemid 38692523)
6. Ogura, Y., Sutterwala, F.S. & Flavell, R.A. The infammasome: frst line of the immune response to cell stress. Cell 126, 659-662 (2006). (Pubitemid 44233635)
7. Yu, H.B. & Finlay, B.B. The caspase-1 infammasome: a pilot of innate immune responses. Cell Host Microbe 4, 198-208 (2008).
8. Dostert, C. et al. Innate immune activation through Nalp3 infammasome sensing of asbestos and silica. Science 320, 674-677 (2008). (Pubitemid 351928351)
9. Hornung, V. et al. Silica crystals and aluminum salts activate the NALP3 infammasome through phagosomal destabilization. Nat. Immunol. 9, 847-856 (2008).
10. Johnston, J.B. et al. A poxvirus-encoded pyrin domain protein interacts with ASC-1 to inhibit host infammatory and apoptotic responses to infection. Immunity 23, 587-598 (2005).
11. Muruve, D.A. et al. The infammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature 452, 103-107 (2008).
12. Fernandes-Alnemri, T., Yu, J.W., Datta, P., Wu, J. & Alnemri, E.S. AIM2 activates the infammasome and cell death in response to cytoplasmic DNA. Nature 458, 509-513 (2009).
13. Hornung, V. et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating infammasome with ASC. Nature 458, 514-518 (2009).
14. Burckstummer, T. et al. An orthogonal proteomic-genomic screen identifes AIM2 as a cytoplasmic DNA sensor for the infammasome. Nat. Immunol. 10, 266-272 (2009).
15. Roberts, T.L. et al. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323, 1057-1060 (2009).
16. Diebold, S.S., Kaisho, T., Hemmi, H., Akira, S. & Reis e Sousa, C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303, 1529-1531 (2004). (Pubitemid 38314425)
17. Lund, J.M. et al. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. USA 101, 5598-5603 (2004). (Pubitemid 38481202)
18. Hornung, V. et al. 5′-Triphosphate RNA is the ligand for RIG-I. Science 314, 994-997 (2006).
19. Pichlmair, A. et al. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science 314, 997-1001 (2006). (Pubitemid 44749946)
20. Pinto, L.H. & Lamb, R.A. The M2 proton channels of infuenza A and B viruses. J. Biol. Chem. 281, 8997-9000 (2006).
21. Takeda, M., Pekosz, A., Shuck, K., Pinto, L.H. & Lamb, R.A. Infuenza a virus M2 ion channel activity is essential for effcient replication in tissue culture. J. Virol. 76, 1391-1399 (2002). (Pubitemid 34070633)
22. Sakaguchi, T., Leser, G.P. & Lamb, R.A. The ion channel activity of the infuenza virus M2 protein affects transport through the Golgi apparatus. J. Cell Biol. 133, 733-747 (1996). (Pubitemid 26160977)
23. Holsinger, L.J., Nichani, D., Pinto, L.H. & Lamb, R.A. Infuenza A virus M2 ion channel protein: a structure-function analysis. J. Virol. 68, 1551-1563 (1994). (Pubitemid 2050323)
24. Watanabe, T., Watanabe, S., Ito, H., Kida, H. & Kawaoka, Y. Infuenza A virus can undergo multiple cycles of replication without M2 ion channel activity. J. Virol. 75, 5656-5662 (2001). (Pubitemid 32488159)
25. La Gruta, N.L., Kedzierska, K., Stambas, J. & Doherty, P.C. A question of self-preservation: immunopathology in infuenza virus infection. Immunol. Cell Biol. 85, 85-92 (2007). (Pubitemid 46398724)
26. Martinon, F., Mayor, A. & Tschopp, J. The infammasomes: guardians of the body. Annu. Rev. Immunol. 27, 229-265 (2009).
27. + channel by external ATP in mouse macrophages. FEBS Lett. 267, 281-284 (1990). (Pubitemid 20216709)
28. Venkataraman, P., Lamb, R.A. & Pinto, L.H. Chemical rescue of histidine selectivity flter mutants of the M2 ion channel of infuenza A virus. J. Biol. Chem. 280, 21463-21472 (2005). (Pubitemid 40805711)
29. Mollenhauer, H.H., Morre, D.J. & Rowe, L.D. Alteration of intracellular traffc by monensin; mechanism, specifcity and relationship to toxicity. Biochim. Biophys. Acta 1031, 225-246 (1990). (Pubitemid 20146824)
30. Lippincott-Schwartz, J., Yuan, L.C., Bonifacino, J.S. & Klausner, R.D. Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 56, 801-813 (1989). (Pubitemid 19082516)
31. Schapiro, F. et al. Golgi alkalinization by the papillomavirus E5 oncoprotein. J. Cell Biol. 148, 305-315 (2000). (Pubitemid 30078242)
32. Mariathasan, S. et al. Cryopyrin activates the infammasome in response to toxins and ATP. Nature 440, 228-232 (2006). (Pubitemid 43372102)
33. Aymeric, L. et al. Tumor cell death and ATP release prime dendritic cells and effcient anticancer immunity. Cancer Res. 70, 855-858 (2010).
34. Poeck, M. et al. Recognition of RNA virus by RIG-I results in activation of CARD9 and infammasome signaling for interleukin 1β production. Nat. Immunol. 11, 63-69 (2010).
35. Fischer, W.B. & Sansom, M.S. Viral ion channels: structure and function. Biochim. Biophys. Acta 1561, 27-45 (2002).
36. Neil, S.J., Zang, T. & Bieniasz, P.D. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451, 425-430 (2008). (Pubitemid 351158893)
37. Kuida, K. et al. Altered cytokine export and apoptosis in mice defcient in interleukin-1β converting enzyme. Science 267, 2000-2003 (1995).
38. Franchi, L. et al. Cytosolic fagellin requires Ipaf for activation of caspase-1 and interleukin 1β in salmonella-infected macrophages. Nat. Immunol. 7, 576-582 (2006). (Pubitemid 43797338)
39. Sutterwala, F.S. et al. Critical role for NALP3/CIAS1/cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24, 317-327 (2006).
40. Adachi, O. et al. Targeted disruption of the MyD88 gene results in loss of IL-1-and IL-18-mediated function. Immunity 9, 143-150 (1998). (Pubitemid 28361303)
41. Jones, C.A., Taylor, T.J. & Knipe, D.M. Biological properties of herpes simplex virus 2 replication-defective mutant strains in a murine nasal infection model. Virology 278, 137-150 (2000).
42. Rowe, H.M. et al. Immunization with a lentiviral vector stimulates both CD4 and CD8 T cell responses to an ovalbumin transgene. Mol. Ther. 13, 310-319 (2006).
43. Besnier, C., Takeuchi, Y. & Towers, G. Restriction of lentivirus in monkeys. Proc. Natl. Acad. Sci. USA 99, 11920-11925 (2002). (Pubitemid 34994499)
44. Klein, O. et al. Role of glutamine 17 of the bovine papillomavirus E5 protein in platelet-derived growth factor β receptor activation and cell transformation. J. Virol. 72, 8921-8932 (1998). (Pubitemid 28471836)
45. Axelsson, M.A. & Warren, G. Rapid, endoplasmic reticulum-independent diffusion of the mitotic Golgi haze. Mol. Biol. Cell 15, 1843-1852 (2004).