EV71 3D Protein Binds with NLRP3 and Enhances the Assembly of Inflammasome Complex

PLoS Pathogens

Volumn 13, Issue 1, 2017, Pages

  Wang, Wenbiao ^a   Xiao, Feng ^a   Wan, Pin ^a   Pan, Pan ^a   Zhang, Yecheng ^a   Liu, Fang ^a   Wu, Kailang ^a   Liu, Yingle ^a   Wu, Jianguo ^a  

^a WUHAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AURINTRICARBOXYLIC ACID; CASPASE; CRYOPYRIN; CYCLOHEXIMIDE; GREEN FLUORESCENT PROTEIN; INFLAMMASOME; INTERLEUKIN 1BETA; ISOPROPYL THIOGALACTOSIDE; LIPOPOLYSACCHARIDE; NIGERICIN; RNA DIRECTED RNA POLYMERASE; SHORT HAIRPIN RNA; CYTOSKELETON PROTEIN; IL1B PROTEIN, HUMAN; INTERLEUKIN 1BETA CONVERTING ENZYME; NLRP3 PROTEIN, HUMAN; PROTEIN BINDING; PYCARD PROTEIN, HUMAN; VIRAL PROTEIN;

ARTICLE; CELL ACTIVATION; CELL LYSATE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENTEROVIRUS A71; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; GENE EXPRESSION; GENE SILENCING; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INFLAMMATION; LENTIVIRINAE; MACROPHAGE; OLIGOMERIZATION; PERIPHERAL BLOOD MONONUCLEAR CELL; PLASMID; PROTEIN CONTENT; PROTEIN SYNTHESIS; REAL TIME POLYMERASE CHAIN REACTION; VIRUS REPLICATION; WESTERN BLOTTING; ENTEROVIRUS A; ENTEROVIRUS INFECTION; ENZYME ACTIVATION; IMMUNOLOGY; METABOLISM; MONONUCLEAR CELL; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; SECRETION (PROCESS); TUMOR CELL LINE; VIROLOGY;

CASPASE 1; CELL LINE, TUMOR; CYTOSKELETAL PROTEINS; ENTEROVIRUS A, HUMAN; ENTEROVIRUS INFECTIONS; ENZYME ACTIVATION; HEK293 CELLS; HUMANS; INFLAMMASOMES; INTERLEUKIN-1BETA; LEUKOCYTES, MONONUCLEAR; MACROPHAGES; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; PROTEIN BINDING; RNA REPLICASE; VIRAL NONSTRUCTURAL PROTEINS;

EID: 85011000168     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1006123     Document Type: Article

References (53)

1. Akira S, Uematsu S, Takeuchi O, (2006) Pathogen recognition and innate immunity. Cell124: 783–801. doi: 10.1016/j.cell.2006.02.01516497588
2. Takeuchi O, Akira S, (2010) Pattern recognition receptors and inflammation. Cell140: 805–820. doi: 10.1016/j.cell.2010.01.02220303872
3. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, et al. (2004) The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral response. Nat Immunol5: 730–737. doi: 10.1038/ni108715208624
4. Ting JP, Lovering RC, Alnemri ES, Bertin J, Boss JM, et al. (2008) The NLR gene family: a standard nomenclature. Immunity28: 285–287. doi: 10.1016/j.immuni.2008.02.00518341998
5. Hardison SE, Brown GD, (2012) C-type lectin receptors orchestrate antifungal immunity. Nat Immunol13(9): 817–822. doi: 10.1038/ni.236922910394
6. Martinon F, Mayor A, Tschopp J, (2009) The inflammasomes: Guardians of the body. Annu Rev Immunol27: 229–2265. doi: 10.1146/annurev.immunol.021908.13271519302040
7. Schroder K, Tschopp J, (2010) The inflammasomes. Cell140: 821–832. doi: 10.1016/j.cell.2010.01.04020303873
8. Mariathasan S, Weiss DS, Newton K, McBride J, O’Rourke K, et al. (2006) Cryopyrin activates the inflammasome in response to toxins and ATP. Nature440: 228–232. doi: 10.1038/nature0451516407890
9. Kanneganti TD, Body-Malapel M, Amer A, Park JH, Whitfield J, et al. (2006) Critical role for Cryopyrin/Nalp3 in activation of caspase-1 in response to viral infection and double-stranded RNA. J Biol Chem281: 36560–36568. doi: 10.1074/jbc.M60759420017008311
10. Muruve DA, Pétrilli V, Zaiss AK, White LR, Clark SA, et al. (2008) The inflammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature452: 103–107. doi: 10.1038/nature0666418288107
11. Zhou R, Tardivel A, Thorens B, Choi I, Tschopp J, (2010) Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol11: 136–140. doi: 10.1038/ni.183120023662
12. Karmakar M, Katsenelson MA, et al.(2016).Neutrophil P2X7 receptors mediate NLRP3 inflammasome-dependent IL-1β secretion in response to ATP. Nature Communications7:1–13.
13. Yamasaki K, Muto J, Taylor KR, Cogen AL, Audish D, et al. (2009) NLRP3/cryopyrin is necessary for interleukin-1beta (IL-1beta) release in response to hyaluronan, an endogenous trigger of inflammation in response to injury. J Biol Chem284: 12762–12771. doi: 10.1074/jbc.M80608420019258328
14. Martinon F, Agostini L, Meylan E, Tschopp J, (2009) Identification of bacterial muramyl dipeptide as activator of the NALP3/cryopyrin inflammasome. Curr Biol14(21): 1929–1934.
15. Dinarello CA, (2009) Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol27: 519–550. doi: 10.1146/annurev.immunol.021908.13261219302047
16. Wang H, Lei X, Ciao X, Yang C, Lu W, et al. (2015) Reciprocal regulation between enterovirus 71 and the NLRP3 inflammasome. Cell Rep12: 1–7.
17. Huang PN, Shih SR, (2014) Update on enterovirus 71 infection. Curr Opin Virol5: 98–104. doi: 10.1016/j.coviro.2014.03.00724727707
18. Gong X, Zhou J, Zhu W, Liu N, Li J, et al. (2012) Excessive proinflammatory cytokine and chemokine responses of human monocyte-derived macrophages to enterovirus 71 infection. BMC Infect Dis12: 224. doi: 10.1186/1471-2334-12-22422994237
19. Racaniello VR, Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE, Picornaviridae: the viruses and their replication. In, editors. (ed), Fields Virology, 4th edLippincott Williams & Wilkins, Philadelphia, PA, 2001: 685–722.
20. Huang HI, Weng KF, Shih SR, (2012) Viral and host factors that contribute to pathogenicity of enterovirus 71. Future Microbiol7(4): 467–479. doi: 10.2217/fmb.12.2222439724
21. Griffiths MJ, Ooi MH, Wong SC, Mohan A, Podin Y, et al. (2012) In enterovirus 71 encephalitis with cardio-respiratory compromise, elevated interleukin 1β, interleukin 1 receptor antagonist, and granulocyte colony-stimulating factor levels are markers of poor prognosis. J Infect Dis206: 881–892. doi: 10.1093/infdis/jis44622829643
22. Tung WH, Sun CC, Hsieh HL, Wang SW, Horng JT, et al. (2007) EV71 induces VCAM-1 expression via PDGF receptor, PI3-K/Akt, p38 MAPK, JNK and NF-κB in vascular smooth muscle cells. Cell Signal19: 2127–2137. doi: 10.1016/j.cellsig.2007.06.00917669626
23. Tung WH, Hsieh HL, Yang CM,. (2010) Enterovirus 71 induces COX-2 expression via MAPK, NF-κB, and AP-1 in SK-N-SH cells: Role of PGE2 in viral replication. Cell Signal22: 234–246. doi: 10.1016/j.cellsig.2009.09.01819800403
24. Shenoy AR, Wellington DA, Kumar P, Kassa H, Booth CJ, et al. (2012) GBP5 promotes NLRP3 inflammasome assembly and immunity in mammals. Science336: 481–485. doi: 10.1126/science.121714122461501
25. Allen IC, Scull MA, Moore CB, Holl EK, McElvania-TeKippe E, et al (2009) The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity30(4): 556–565. doi: 10.1016/j.immuni.2009.02.00519362020
26. Chen Wei, Xu Yongfen, Li H, Tao W, Xiang Y, et al. (2014) HCV genomic RNA activates the NLRP3 inflammasome in human myeloid cells. PLoS One9(1): e84953. doi: 10.1371/journal.pone.008495324400125
27. Lin Keng-Mean, Hu Wei, Jennings M, Brewer T, et al. (2014) IRAK-1 bypasses priming and directly links TLRs to rapid NLRP3 inflammasome activation. Proc Natl Acad Sci U S A111(2): 775–780. doi: 10.1073/pnas.132029411124379360
28. Ito M, Yanagi Y, Ichinohe T, (2012) Encephalomyocarditis virus viroporin 2B activates NLRP3 inflammasome. PLoS Pathog8(8): e1002857. doi: 10.1371/journal.ppat.100285722916014
29. Wang B, Xi X, Lei X, Zhang X, Cui S, et al. (2013) Enterovirus 71 protease 2Apro targets MAVS to inhibit anti-viral type I interferon responses. PLoS Pathog9: 1–18
30. Hung HC, Chen TC, Fang MY, Yen KJ, Shih SR, et al. (2010) Inhibition of enterovirus 71 replication and the viral 3D polymerase by aurintricarboxylic acid. J Antimicrob Chemother65: 676–683. doi: 10.1093/jac/dkp50220089540
31. Compan V, Baroja-Mazo A, Lopez-Castejon G, Gomez AI, Martínez CM, et al. (2012) Cell volume regulation modulates NLRP3 inflammasomes activation. Immunity37: 487–500. doi: 10.1016/j.immuni.2012.06.01322981536
32. Faustin B, Lartigue L, Bruey JM, Luciano F, Sergienko E, et al. (2007) Reconstituted NALP inflammasome reveals two-step mechanism of caspase-1 activation. Mol Cell25: 713–724. doi: 10.1016/j.molcel.2007.01.03217349957
33. Allen IC, Scull MA, Moore CB, Holl EK, McElvania-TeKippe E, et al. (2009) The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity30(4): 556–565. doi: 10.1016/j.immuni.2009.02.00519362020
34. Rajan JV, Rodriguez D, Miao EV, Aderem A, (2011) The NLRP3 inflammasome detects encephalomyocarditis virus and vesicular stomatitis virus infection. J Virol85(9): 4167–4172. doi: 10.1128/JVI.01687-1021289120
35. Komune N, Ichinohe T, Ito M, Yanagi Y, (2011) Measles virus V protein inhibits NLRP3 inflammasome-mediated interleukin-1β secretion. J Virol85: 13019–13026. doi: 10.1128/JVI.05942-1121994456
36. Rahman MM, Mcfadden G, (2011) Myxoma virus lacking the pyrin-like protein M013 is sensed in human myeloid cells by both NLRP3 and multiple Toll-Like receptors, which independently activate the inflammasome and NF-kappa B innate response pathways. J Virol85: 12505–12517. doi: 10.1128/JVI.00410-1121957307
37. Barlan AU, Danthi P, Wiethoff CM, (2011) Lysosomal localization and mechanism of membrane penetration influence nonenveloped virus activation of the NLRP3 inflammsome. Virology412: 306–314. doi: 10.1016/j.virol.2011.01.01921315400
38. Kumar M, Roe K, Orillo B, Muruve DA, Nerurkar VR, (2013) Inflammasome adaptor protein apoptosis-associated speck-like protein containing CARD (ASC) is critical for the immune response and survival in west Nile virus encephalitis. J Virol87: 3655–3667. doi: 10.1128/JVI.02667-1223302887
39. Lawrence TM, Hudacek AW, de Zoete MR, Flavell RA, Schnell MJ, (2013) Rabies virus is recognized by the NLRP3 inflammasome and activates interleukin-1β release in murine dendritic cells. J Virol87: 5848–5857. doi: 10.1128/JVI.00203-1323487464
40. Johnson KE, Chikoti L, Chandran B, (2013) Herpes simplex virus 1 infection induces activation and subsequent inhibition of the IFI16 and NLRP3 inflammasomes. J Virol87: 5005–5018. doi: 10.1128/JVI.00082-1323427152
41. Ermler ME, Traylor Z, Patel K, Schattgen SA, Vanaja SK, et al. (2014) Rift valley fever virus infection induces activation of the NLRP3 inflammsome. Virology449: 174–180. doi: 10.1016/j.virol.2013.11.01524418550
42. Kamada AJ, Pontillo A, Guimaraes RL, Loureiro P, Crovella S, et al. (2014) NLRP3 polymorphism is associated with protection against human T-lymphotropic virus 1 infection. Men Inst Oswaldo Cruz109: 960–963.
43. Moriyama M, Chen IY, Kawaguchi A, Koshiba T, Nagata K, et al. (2016) The RNA- and TRIM25-binding domains of influenza virus NS1 protein are essential for suppression of NLRP3 inflammasome-mediated interleukin-1β secretion. J Virol90: 4105–4114. doi: 10.1128/JVI.00120-1626865721
44. Ichinohe T, Pang IK, Iwasaki A, (2010) Influenza virus activates inflammasomes via its intracellular M2 ion channel. Nat Immunol11: 404–410. doi: 10.1038/ni.186120383149
45. Chen C, Wang Y, Shan C, Sun Y, Xu P, et al. (2013) Crystal structure of enterovirus 71 RNA-dependent RNA polymerase complexed with its protein primer VPg: implication for a trans mechanism of VPg uridylylation. J Virol87(10): 5575–5768.
46. Sun Y, Wang Y, Shan C, Chen C, Xu P, et al. (2012) Enterovirus 71 VPg uridylation uses a two-molecular mechanism of 3D polymerase. J Virol86: 13662–13671. doi: 10.1128/JVI.01712-1223055549
47. Velu AB, Chen GW, Hsieh PT, et al.(2014).BPR-3P0128 inhibits RNA-dependent RNA polymerase elongation and VPg uridylylation activities of Enterovirus 71.Antiviral Research112:18–25. doi: 10.1016/j.antiviral.2014.10.00325448086
48. Chen TC, Chang HY, Lin PF, et al.(2009).Novel Antiviral Agent DTriP-22 Targets RNA-Dependent RNA polymerase of Enterovirus 71.ANTIMICROBIAL AGENTS AND CHEMOTHERAPY53:2740–2747.
49. Yu J, Zhang L, Ren P, Zhong T, Li Z, et al. (2015) Enterovirus 71 mediates cell cycle arrest in S phase through non-structural protein 3D. Cell Cycle14(3): 425–436. doi: 10.4161/15384101.2014.98063125659038
50. Wang LC, Chen SO, Chang SP, Lee YP, Yu CK, et al. (2015) Enterovirus 71 protein 2A and 3D antagonize the antiviral activity of IFN-γ via signaling attenuation. J Virol89(14): 7028–7037. doi: 10.1128/JVI.00205-1525926657
51. Mao K, Chen S, Chen M, Ma Y, Wang Y, et al. (2013) Nitric oxide suppresses NLRP3 inflammasome activation and protects against LPS-induced septic shock. Cell Res23(2): 201–212. doi: 10.1038/cr.2013.623318584
52. Liu WY, Wu SM, Xiong Y, Li T, Wen Z, et al. (2014) Co-circulation and genomic recombination of coxsackievirus A16 and enterovirus 71 during a large outbreak of hand, foot, and mouth disease in central China. PLoS One9(4): e96051. doi: 10.1371/journal.pone.009605124776922
53. Song Y, Cheng X, Yang X, Zhao R, Wang P, et al. (2015) Early growth response-1 facilitates Enterovirus 71 replication by direct binding to the viral genome RNA. Int J Biochem Cell Biol62:36–46. doi: 10.1016/j.biocel.2015.02.01225724735