Contribution of intertwined loop to membrane association revealed by Zika virus full-length NS1 structure

EMBO Journal

Volumn 35, Issue 20, 2016, Pages 2170-2178

  Xu, Xiaoying ^a,b   Song, Hao ^b,c   Qi, Jianxun ^b,d   Liu, Yuqian ^b,e   Wang, Haiyuan ^b,f   Su, Chao ^b,g   Shi, Yi ^b,c,d   Gao, George F ^a,b,c,d,h  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b INSTITUTE OF MICROBIOLOGY   (China)

^c INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^d UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^e ANHUI UNIVERSITY   (China)

^f GUANGXI UNIVERSITY   (China)

^g CHINA AGRICULTURAL UNIVERSITY   (China)

^h CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

Author keywords

crystal structure; membrane association; NS1; Zika virus

Indexed keywords

AMINO ACID; DIMER; HYDROGEN; NONSTRUCTURAL PROTEIN 1; NONSTRUCTURAL PROTEIN 1, WEST NILE VIRUS; NS1 PROTEIN, DENGUE VIRUS TYPE 2; NS1 PROTEIN, FLAVIVIRUS; VIRAL PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DENGUE VIRUS 2; EXTRACELLULAR SPACE; HYDROGEN BOND; HYDROPHOBICITY; INTERTWINED LOOP; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN GLYCOSYLATION; PROTEIN SECONDARY STRUCTURE; STATIC ELECTRICITY; SURFACE PROPERTY; VIRUS ENVELOPE; VIRUS REPLICATION; WEST NILE VIRUS; ZIKA VIRUS; CHEMISTRY; CRYSTALLIZATION; GENETICS; PROTEIN CONFORMATION;

CRYSTALLIZATION; PROTEIN CONFORMATION; VIRAL NONSTRUCTURAL PROTEINS; ZIKA VIRUS;

EID: 84983806029     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201695290     Document Type: Article

References (53)

1. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213–221
2. Akey DL, Brown WC, Dutta S, Konwerski J, Jose J, Jurkiw TJ, DelProposto J, Ogata CM, Skiniotis G, Kuhn RJ, Smith JL (2014) Flavivirus NS1 structures reveal surfaces for associations with membranes and the immune system. Science 343: 881–885
3. Alcon S, Talarmin A, Debruyne M, Falconar A, Deubel V, Flamand M (2002) Enzyme-linked immunosorbent assay specific to dengue virus type 1 nonstructural protein NS1 reveals circulation of the antigen in the blood during the acute phase of disease in patients experiencing primary or secondary infections. J Clin Microbiol 40: 376–381
4. Amorim JH, Alves RP, Boscardin SB, Ferreira LC (2014) The dengue virus non-structural 1 protein: risks and benefits. Virus Res 181: 53–60
5. Ashkenazy H, Abadi S, Martz E, Chay O, Mayrose I, Pupko T, Ben-Tal N (2016) ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules. Nucleic Acids Res 44: W344–W350
6. Avirutnan P, Zhang L, Punyadee N, Manuyakorn A, Puttikhunt C, Kasinrerk W, Malasit P, Atkinson JP, Diamond MS (2007) Secreted NS1 of dengue virus attaches to the surface of cells via interactions with heparan sulfate and chondroitin sulfate E. PLoS Pathog 3: e183
7. Avirutnan P, Fuchs A, Hauhart RE, Somnuke P, Youn S, Diamond MS, Atkinson JP (2010) Antagonism of the complement component C4 by flavivirus nonstructural protein NS1. J Exp Med 207: 793–806
8. Avirutnan P, Hauhart RE, Somnuke P, Blom AM, Diamond MS, Atkinson JP (2011) Binding of flavivirus nonstructural protein NS1 to C4b binding protein modulates complement activation. J Immunol 187: 424–433
9. Beatty PR, Puerta-Guardo H, Killingbeck SS, Glasner DR, Hopkins K, Harris E (2015) Dengue virus NS1 triggers endothelial permeability and vascular leak that is prevented by NS1 vaccination. Sci Transl Med 7: 304ra141
10. Brandt WE, Chiewslip D, Harris DL, Russell PK (1970) Partial purification and characterization of a dengue virus soluble complement-fixing antigen. J Immunol 105: 1565–1568
11. Brown WC, DelProposto J, Rubin JR, Lamiman K, Carless J, Smith JL (2011) New ligation-independent cloning vectors compatible with a high-throughput platform for parallel construct expression evaluation using baculovirus-infected insect cells. Protein Expr Purif 77: 34–45
12. †
13. Cao-Lormeau VM, Blake A, Mons S, Lastere S, Roche C, Vanhomwegen J, Dub T, Baudouin L, Teissier A, Larre P, Vial AL, Decam C, Choumet V, Halstead SK, Willison HJ, Musset L, Manuguerra JC, Despres P, Fournier E, Mallet HP et al (2016) Guillain-Barre Syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. Lancet 387: 1531–1539
14. Carteaux G, Maquart M, Bedet A, Contou D, Brugières P, Fourati S, Cleret de Langavant L, de Broucker T, Brun-Buisson C, Leparc-Goffart I, Mekontso Dessap A (2016) Zika virus associated with meningoencephalitis. New Engl J Med 374: 1595–1596
15. Cheng HJ, Lin CF, Lei HY, Liu HS, Yeh TM, Luo YH, Lin YS (2009) Proteomic analysis of endothelial cell autoantigens recognized by anti-dengue virus nonstructural protein 1 antibodies. Exp Biol Med 234: 63–73
16. Chung KM, Liszewski MK, Nybakken G, Davis AE, Townsend RR, Fremont DH, Atkinson JP, Diamond MS (2006a) West Nile virus nonstructural protein NS1 inhibits complement activation by binding the regulatory protein factor H. Proc Natl Acad Sci USA 103: 19111–19116
17. Chung KM, Nybakken GE, Thompson BS, Engle MJ, Marri A, Fremont DH, Diamond MS (2006b) Antibodies against West Nile virus nonstructural protein NS1 prevent lethal infection through Fc gamma receptor-dependent and -independent mechanisms. J Virol 80: 1340–1351
18. Chuang YC, Lei HY, Lin YS, Liu HS, Wu HL, Yeh TM (2011) Dengue virus-induced autoantibodies bind to plasminogen and enhance its activation. J Immunol 187: 6483–6490
19. Chuang YC, Lin YS, Liu HS, Yeh TM (2014) Molecular mimicry between dengue virus and coagulation factors induces antibodies to inhibit thrombin activity and enhance fibrinolysis. J Virol 88: 13759–13768
20. D'Ortenzio E, Matheron S, Yazdanpanah Y, de Lamballerie X, Hubert B, Piorkowski G, Maquart M, Descamps D, Damond F, Leparc-Goffart I (2016) Evidence of sexual transmission of Zika virus. N Engl J Med 374: 2195–2198
21. Edeling MA, Diamond MS, Fremont DH (2014) Structural basis of Flavivirus NS1 assembly and antibody recognition. Proc Natl Acad Sci USA 111: 4285–4290
22. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126–2132
23. Flamand M, Megret F, Mathieu M, Lepault J, Rey FA, Deubel V (1999) Dengue virus type 1 nonstructural glycoprotein NS1 is secreted from mammalian cells as a soluble hexamer in a glycosylation-dependent fashion. J Virol 73: 6104–6110
24. Gutsche I, Coulibaly F, Voss JE, Salmon J, d'Alayer J, Ermonval M, Larquet E, Charneau P, Krey T, Megret F, Guittet E, Rey FA, Flamand M (2011) Secreted dengue virus nonstructural protein NS1 is an atypical barrel-shaped high-density lipoprotein. Proc Natl Acad Sci USA 108: 8003–8008
25. Khromykh AA, Sedlak PL, Westaway EG (2000) cis- and trans-acting elements in flavivirus RNA replication. J Virol 74: 3253–3263
26. Ledermann JP, Guillaumot L, Yug L, Saweyog SC, Tided M, Machieng P, Pretrick M, Marfel M, Griggs A, Bel M, Duffy MR, Hancock WT, Ho-Chen T, Powers AM (2014) Aedes hensilli as a potential vector of Chikungunya and Zika viruses. PLoS Negl Trop Dis 8: e3188
27. Lindenbach BD, Rice CM (1997) Trans-complementation of yellow fever virus NS1 reveals a role in early RNA replication. J Virol 71: 9608–9617
28. Lindenbach BD, Rice CM (1999) Genetic interaction of flavivirus nonstructural proteins NS1 and NS4A as a determinant of replicase function. J Virol 73: 4611–4621
29. Liu IJ, Chiu CY, Chen YC, Wu HC (2011) Molecular mimicry of human endothelial cell antigen by autoantibodies to nonstructural protein 1 of dengue virus. J Biol Chem 286: 9726–9736
30. Mlakar J, Korva M, Tul N, Popović M, Poljšak-Prijatelj M, Mraz J, Kolenc M, Resman Rus K, Vesnaver Vipotnik T, Fabjan Vodušek V, Vizjak A, Pižem J, Petrovec M, Avšič Županc T (2016) Zika virus associated with microcephaly. New Engl J Med 374: 951–958
31. Modhiran N, Watterson D, Muller DA, Panetta AK, Sester DP, Liu L, Hume DA, Stacey KJ, Young PR (2015) Dengue virus NS1 protein activates cells via Toll-like receptor 4 and disrupts endothelial cell monolayer integrity. Sci Transl Med 7: 304ra142
32. Muller DA, Landsberg MJ, Bletchly C, Rothnagel R, Waddington L, Hankamer B, Young PR (2012) Structure of the dengue virus glycoprotein non-structural protein 1 by electron microscopy and single-particle analysis. J Gen Virol 93: 771–779
33. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240–255
34. Musso D, Roche C, Robin E, Nhan T, Teissier A, Cao-Lormeau VM (2015) Potential sexual transmission of Zika virus. Emerg Infect Dis 21: 359–361
35. Musso D, Gubler DJ (2016) Zika virus. Clin Microbiol Rev 29: 487–524
36. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307–326
37. Read RJ (2001) Pushing the boundaries of molecular replacement with maximum likelihood. Acta Crystallogr D 57: 1373–1382
38. Russell PK, Chiewsilp D, Brandt WE (1970) Immunoprecipitation analysis of soluble complement-fixing antigens of dengue viruses. J Immunol 105: 838–845
39. Scaturro P, Cortese M, Chatel-Chaix L, Fischl W, Bartenschlager R (2015) Dengue virus non-structural protein 1 modulates infectious particle production via interaction with the structural proteins. PLoS Pathog 11: e1005277
40. Schlesinger JJ, Brandriss MW, Walsh EE (1987) Protection of mice against dengue 2 virus encephalitis by immunization with the dengue 2 virus non-structural glycoprotein NS1. J Gen Virol 68(Pt 3): 853–857
41. Song H, Qi J, Haywood J, Shi Y, Gao GF (2016a) Zika virus NS1 structure reveals diversity of electrostatic surfaces among flaviviruses. Nat Struct Mol Biol 23: 456–458
42. Song H, Qi J, Khedri Z, Diaz S, Yu H, Chen X, Varki A, Shi Y, Gao GF (2016b) An open receptor-binding cavity of hemagglutinin-esterase-fusion glycoprotein from newly-identified influenza D virus: basis for its broad cell tropism. PLoS Pathog 12: e1005411
43. Stettler K, Beltramello M, Espinosa DA, Graham V, Cassotta A, Bianchi S, Vanzetta F, Minola A, Jaconi S, Mele F, Foglierini M, Pedotti M, Simonelli L, Dowall S, Atkinson B, Percivalle E, Simmons CP, Varani L, Blum J, Baldanti F et al (2016) Specificity, cross-reactivity and function of antibodies elicited by Zika virus infection. Science 353: 823–826
44. Sun DS, King CC, Huang HS, Shih YL, Lee CC, Tsai WJ, Yu CC, Chang HH (2007) Antiplatelet autoantibodies elicited by dengue virus non-structural protein 1 cause thrombocytopenia and mortality in mice. J Thromb Haemost 5: 2291–2299
45. Sun DS, Chang YC, Lien TS, King CC, Shih YL, Huang HS, Wang TY, Li CR, Lee CC, Hsu PN, Chang HH (2015) Endothelial cell sensitization by death receptor fractions of an anti-dengue nonstructural protein 1 antibody induced plasma leakage, coagulopathy, and mortality in mice. J Immunol 195: 2743–2753
46. Ventura CV, Maia M, Bravo-Filho V, Gois AL, Belfort R Jr (2016) Zika virus in Brazil and macular atrophy in a child with microcephaly. Lancet 387: 228
47. Wang Q, Yang Y, Zheng H, Bi Y, Song J, Li L, Gu D, Wang P, Li S, Liu S, Zhao Y, Liu L, Gao GF, Liu Y (2016) Genetic and biological characterization of Zika virus from human cases imported through Shenzhen Port (in Chinese). Chin Sci Bull 61: 2463–2474
48. Watterson D, Modhiran N, Young PR (2016) The many faces of the flavivirus NS1 protein offer a multitude of options for inhibitor design. Antiviral Res 130: 7–18
49. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AGW, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D 67: 235–242
50. Yin Y, Jiang L, Fang D, Jiang L, Zhou J (2013) Differentially expressed genes of human microvascular endothelial cells in response to anti-dengue virus NS1 antibodies by suppression subtractive hybridization. Viral Immunol 26: 185–191
51. Youn S, Li T, McCune BT, Edeling MA, Fremont DH, Cristea IM, Diamond MS (2012) Evidence for a genetic and physical interaction between nonstructural proteins NS1 and NS4B that modulates replication of West Nile virus. J Virol 86: 7360–7371
52. Zhang Y, Chen W, Wong G, Bi Y, Yan J, Sun Y, Chen E, Yan H, Lou X, Mao H, Xia S, Gao GF, Shi W, Chen Z (2016) Highly diversified Zika viruses imported to China, 2016. Protein Cell 7: 461–464
53. Zhu Z, Chan JF, Tee KM, Choi GK, Lau SK, Woo PC, Tse H, Yuen KY (2016) Comparative genomic analysis of pre-epidemic and epidemic Zika virus strains for virological factors potentially associated with the rapidly expanding epidemic. Emerg Microbes Infect 5: e22