NLRP3 inflammasome activation by viroporins of animal viruses

Viruses

Volumn 7, Issue 7, 2015, Pages 3380-3391

  Guo, Hui Chen ^a   Jin, Ye ^a   Zhi, Xiao Yin ^a   Yan, Dan ^a   Sun, Shi Qi ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Animal virus; Inflammasome; NLRP3; Viroporin

Indexed keywords

AGNOPROTEIN; CALCIUM; CALCIUM SENSING RECEPTOR; CRYOPYRIN; CYTOKINE; INFLAMMASOME; INTERLEUKIN 1BETA CONVERTING ENZYME; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; VIROPORIN; VIRUS PROTEIN; CARRIER PROTEIN; VIRAL PROTEIN;

ANIMAL VIRUS; APOPTOSIS; AUTOPHAGY; CELL DIFFERENTIATION; CELL STRESS; GENE REPLICATION; GENETIC TRANSCRIPTION; INFLAMMATION; INNATE IMMUNITY; ION TRANSPORT; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN SYNTHESIS REGULATION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; VIRUS INFECTION; ANIMAL; GENETICS; HUMAN; IMMUNOLOGY; VIROLOGY; VIRUS;

ANIMALIA;

ANIMALS; CARRIER PROTEINS; HUMANS; INFLAMMASOMES; VIRAL PROTEINS; VIRUS DISEASES; VIRUSES;

EID: 84936980740     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v7072777     Document Type: Review

References (58)

1. Grice, A.L.; Kerr, I.D.; Sansom, M.S. Ion channels formed by HIV-1 VPU: A modelling and simulation study. FEBS Lett. 1997, 405, 299-304.
2. Masante, C.; el Najjar, F.; Chang, A.; Jones, A.; Moncman, C.L.; Dutch, R.E. The human metapneumovirus small hydrophobic protein has properties consistent with those of a viroporin and can modulate viral fusogenic activity. J. Virol. 2014, 88, 6423-6433.
3. Raghava, S.; Giorda, K.M.; Romano, F.B.; Heuck, A.P.; Hebert, D.N. The SV40 late protein VP4 is a viroporin that forms pores to disrupt membranes for viral release. PLoS Pathog. 2011, 7, e1002116.
4. Suzuki, T.; Orba, Y.; Makino, Y.; Okada, Y.; Sunden, Y.; Hasegawa, H.; Hall, W.W.; Sawa, H. Viroporin activity of the JC polyomavirus is regulated by interactions with the adaptor protein complex 3. Proc. Natl. Acad. Sci. USA 2013, 110, 18668-18673.
5. Ao, D.; Guo, H.-C.; Sun, S.-Q.; Sun, D.-H.; Fung, T.S.; Wei, Y.-Q.; Han, S.-C.; Yao, X.-P.; Cao, S.-Z.; Liu, D.X.; et al. Viroporin activity of the foot-and-mouth disease virus non-structural 2B protein. PLoS ONE 2015, 10, e0125828.
6. Pinto, L.H.; Dieckmann, G.R.; Gandhi, C.S.; Papworth, C.G.; Braman, J.; Shaughnessy, M.A.; Lear, J.D.; Lamb, R.A.; DeGrado, W.F. A functionally defined model for the M2 proton channel of influenza a virus suggests a mechanism for its ion selectivity. Proc. Natl. Acad. Sci. USA 1997, 94, 11301-11306.
7. Agirre, A.; Barco, A.; Carrasco, L.; Nieva, J.L. Viroporin-mediated membrane permeabilization. Pore formation by nonstructural poliovirus 2B protein. J. Biol. Chem. 2002, 277, 40434-40441.
8. Carrasco, L. Modification of membrane permeability by animal viruses. Adv. Virus Res. 1995, 45, 61-112.
9. Gonzalez, M.E.; Carrasco, L. Viroporins. FEBS Lett. 2003, 552, 28-34.
10. Hyser, J.M.; Utama, B.; Crawford, S.E.; Broughman, J.R.; Estes, M.K. Activation of the endoplasmic reticulum calcium sensor stim1 and store-operated calcium entry by rotavirus requires NSP4 viroporin activity. J. Virol. 2013, 87, 13579-13588.
11. Wozniak, A.L.; Griffin, S.; Rowlands, D.; Harris, M.; Yi, M.; Lemon, S.M.; Weinman, S.A. Intracellular proton conductance of the hepatitis C virus p7 protein and its contribution to infectious virus production. PLoS Pathog. 2010, 6, e1001087.
12. Wang, K.; Xie, S.; Sun, B. Viral proteins function as ion channels. Biochim. Biophys. Acta 2011, 1808, 510-515.
13. Madan, V.; Castello, A.; Carrasco, L. Viroporins from rna viruses induce caspase-dependent apoptosis. Cell. Microbiol. 2008, 10, 437-451.
14. Crawford, S.E.; Hyser, J.M.; Utama, B.; Estes, M.K. Autophagy hijacked through viroporin-activated calcium/calmodulin-dependent kinase kinase-β signaling is required for rotavirus replication. Proc. Natl. Acad. Sci. USA 2012, 109, E3405-E3413.
15. Nieva, J.L.; Madan, V.; Carrasco, L. Viroporins: Structure and biological functions. Nat. Rev. Microbiol. 2012, 10, 563-574.
16. Sanchez-Martinez, S.; Huarte, N.; Maeso, R.; Madan, V.; Carrasco, L.; Nieva, J.L. Functional and structural characterization of 2B viroporin membranolytic domains. Biochemistry 2008, 47, 10731-10739.
17. Ali, M.H.; Imperiali, B. Protein oligomerization: How and why. Bioorganic Med. Chem. 2005, 13, 5013-5020.
18. Nieva, J.L.; Sanz, M.A.; Carrasco, L. Membrane-permeabilizing motif in semliki forest virus E1 glycoprotein. FEBS Lett. 2004, 576, 417-422.
19. Kasermann, F.; Kempf, C. Low pH-induced pore formation by spike proteins of enveloped viruses. J. Gen. Virol. 1996, 77, 3025-3032.
20. Madan, V.; Redondo, N.; Carrasco, L. Cell permeabilization by poliovirus 2B viroporin triggers bystander permeabilization in neighbouring cells through a mechanism involving GAP junctions. Cell. Microbiol. 2010, 12, 1144-1157.
21. 2+ and virus. Cell Calcium 2009, 46, 1-17.
22. Triantafilou, K.; Triantafilou, M. Ion flux in the lung: Virus-induced inflammasome activation. Trends Microbiol. 2014, 22, 580-588.
23. Medzhitov, R.; Janeway, C.A., Jr. Innate immunity: Impact on the adaptive immune response. Curr. Opin. Immunol. 1997, 9, 4-9.
24. Medzhitov, R.; Janeway, C.A., Jr. Innate immunity: The virtues of a nonclonal system of recognition. Cell 1997, 91, 295-298.
25. Medzhitov, R.; Janeway, C.A., Jr. Decoding the patterns of self and nonself by the innate immune system. Science 2002, 296, 298-300.
26. Janeway, C.A., Jr.; Medzhitov, R. Innate immune recognition. Annu. Rev. Immunol. 2002, 20, 197-216.
27. Kawai, T.; Akira, S. TLR signaling. Semin Immunol. 2007, 19, 24-32.
28. Kato, H.; Sato, S.; Yoneyama, M.; Yamamoto, M.; Uematsu, S.; Matsui, K.; Tsujimura, T.; Takeda, K.; Fujita, T.; Takeuchi, O.; et al. Cell type-specific involvement of rig-i in antiviral response. Immunity 2005, 23, 19-28.
29. Ratsimandresy, R.A.; Dorfleutner, A.; Stehlik, C. An update on pyrin domain-containing pattern recognition receptors: From immunity to pathology. Front. Immunol. 2013, 4, doi:10.3389/fimmu.2013.00440
30. Kapetanovic, R.; Bokil, N.J.; Sweet, M.J. Innate immune perturbations, accumulating damps and inflammasome dysregulation: A ticking time bomb in ageing. Ageing Res. Rev. 2015, doi:10.1016/j.arr.2015.02.005.
31. Kufer, T.A.; Fritz, J.H.; Philpott, D.J. NACHT-LRR proteins (NLRS) in bacterial infection and immunity. Trends Microbiol. 2005, 13, 381-388.
32. Petrilli, V.; Dostert, C.; Muruve, D.A.; Tschopp, J. The inflammasome: A danger sensing complex triggering innate immunity. Curr. Opin. Immunol. 2007, 19, 615-622.
33. Chen, I.Y.; Ichinohe, T. Response of host inflammasomes to viral infection. Trends Microbiol. 2015, 23, 55-63.
34. Thomas, P.G.; Dash, P.; Aldridge, J.R., Jr.; Ellebedy, A.H.; Reynolds, C.; Funk, A.J.; Martin, W.J.; Lamkanfi, M.; Webby, R.J.; Boyd, K.L.; et al. The intracellular sensor NLRP3 mediates key innate and healing responses to influenza a virus via the regulation of caspase-1. Immunity 2009, 30, 566-575.
35. Owen, D.M.; Gale, M., Jr. Fighting the flu with inflammasome signaling. Immunity 2009, 30, 476-478.
36. Kanneganti, T.D. Central roles of nlrs and inflammasomes in viral infection. Nat. Rev. Immunol. 2010, 10, 688-698.
37. Keller, M.; Ruegg, A.; Werner, S.; Beer, H.D. Active caspase-1 is a regulator of unconventional protein secretion. Cell 2008, 132, 818-831.
38. Sutterwala, F.S.; Haasken, S.; Cassel, S.L. Mechanism of NLRP3 inflammasome activation. Ann. N. Y. Acad. Sci. 2014, 1319, 82-95.
39. Martinon, F.; Mayor, A.; Tschopp, J. The inflammasomes: Guardians of the body. Annu. Rev. Immunol. 2009, 27, 229-265.
40. Schroder, K.; Zhou, R.; Tschopp, J. The NLRP3 inflammasome: A sensor for metabolic danger? Science 2010, 327, 296-300.
41. Martinon, F. Signaling by ros drives inflammasome activation. Eur. J. Immunol. 2010, 40, 616-619.
42. Dostert, C.; Petrilli, V.; van Bruggen, R.; Steele, C.; Mossman, B.T.; Tschopp, J. Innate immune activation through NALP3 inflammasome sensing of asbestos and silica. Science 2008, 320, 674-677.
43. Ichinohe, T.; Pang, I.K.; Iwasaki, A. Influenza virus activates inflammasomes via its intracellular M2 ion channel. Nat. Immunol. 2010, 11, 404-410.
44. 2+ is a danger signal activating the NLRP3 inflammasome through G protein-coupled calcium sensing receptors. Nat. Commun. 2012, 3, doi:10.1038/ncomms2339.
45. 2+ and camp. Nature 2012, 492, 123-127.
46. 2+ puffs. Cell Calcium 2015, 57, 109-119.
47. Hyser, J.M.; Collinson-Pautz, M.R.; Utama, B.; Estes, M.K. Rotavirus disrupts calcium homeostasis by NSP4 viroporin activity. mBio 2010, 1, doi:10.1128/mBio.00265-10.
48. Guo, H.-C.; Sun, S.-Q.; Sun, D.-H.; Wei, Y.-Q.; Xu, J.; Huang, M.; Liu, X.-T.; Liu, Z.-X.; Luo, J.-X.; Yin, H.; et al. Viroporin activity and membrane topology of classic swine fever virus P7 protein. Int. J. Biochem. Cell Biol. 2013, 45, 1186-1194.
49. Vieyres, G.; Brohm, C.; Friesland, M.; Gentzsch, J.; Wolk, B.; Roingeard, P.; Steinmann, E.; Pietschmann, T. Subcellular localization and function of an epitope-tagged P7 viroporin in hepatitis C virus-producing cells. J. Virol. 2013, 87, 1664-1678.
50. Ito, M.; Yanagi, Y.; Ichinohe, T. Encephalomyocarditis virus viroporin 2B activates NLRP3 inflammasome. PLoS Pathog. 2012, 8, e1002857.
51. Suzuki, T.; Orba, Y.; Okada, Y.; Sunden, Y.; Kimura, T.; Tanaka, S.; Nagashima, K.; Hall, W.W.; Sawa, H. The human polyoma JC virus agnoprotein acts as a viroporin. PLoS Pathog. 2010, 6, e1000801.
52. Triantafilou, K.; Kar, S.; van Kuppeveld, F.J.; Triantafilou, M. Rhinovirus-induced calcium flux triggers NLRP3 and NLRC5 activation in bronchial cells. Am. J. Respir. Cell Mol. Biol. 2013, 49, 923-934.
53. Shrivastava, S.; Mukherjee, A.; Ray, R.; Ray, R.B. Hepatitis c virus induces interleukin-1β (IL-1β)/IL-18 in circulatory and resident liver macrophages. J. Virol. 2013, 87, 12284-12290.
54. Segovia, J.; Sabbah, A.; Mgbemena, V.; Tsai, S.Y.; Chang, T.H.; Berton, M.T.; Morris, I.R.; Allen, I.C.; Ting, J.P.; Bose, S. TLR2/MYD88/NF-κb pathway, reactive oxygen species, potassium efflux activates NLRP3/ASC inflammasome during respiratory syncytial virus infection. PLoS ONE 2012, 7, e29695.
55. Triantafilou, K.; Kar, S.; Vakakis, E.; Kotecha, S.; Triantafilou, M. Human respiratory syncytial virus viroporin sh: A viral recognition pathway used by the host to signal inflammasome activation. Thorax 2013, 68, 66-75.
56. Allen, I.C.; Scull, M.A.; Moore, C.B.; Holl, E.K.; McElvania-TeKippe, E.; Taxman, D.J.; Guthrie, E.H.; Pickles, R.J.; Ting, J.P. The nlrp3 inflammasome mediates in vivo innate immunity to influenza a virus through recognition of viral rna. Immunity 2009, 30, 556-565.
57. Negash, A.A.; Ramos, H.J.; Crochet, N.; Lau, D.T.; Doehle, B.; Papic, N.; Delker, D.A.; Jo, J.; Bertoletti, A.; Hagedorn, C.H.; et al. IL-1β production through the nlrp3 inflammasome by hepatic macrophages links hepatitis c virus infection with liver inflammation and disease. PLoS Pathog. 2013, 9, e1003330.
58. Chen, W.; Xu, Y.; Li, H.; Tao, W.; Xiang, Y.; Huang, B.; Niu, J.; Zhong, J.; Meng, G. HCV genomic RNA activates the NLRP3 inflammasome in human myeloid cells. PLoS ONE 2014, 9, e84953.