Particle conformation regulates antibody access to a conserved GII.4 norovirus blockade epitope

Journal of Virology

Volumn 88, Issue 16, 2014, Pages 8826-8842

  Lindesmith, Lisa C ^a   Donaldson, Eric F ^a   Beltramello, Martina ^b   Pintus, Stefania ^b   Corti, Davide ^b,c   Swanstrom, Jesica ^a   Debbink, Kari ^a   Jones, Taylor A ^a   Lanzavecchia, Antonio ^b,d   Baric, Ralph S ^a  

^a IL   (United States)

^b INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Switzerland)

^c Humabs BioMed SA ^*  (Switzerland)

^d ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CARBOHYDRATE; EPITOPE; MONOCLONAL ANTIBODY;

ARTICLE; BINDING SITE; BIOINFORMATICS; BLOOD SAMPLING; CONFORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; GII.4 NOROVIRUS; HUMAN; NONHUMAN; NOROVIRUS; PREDICTION; PRIORITY JOURNAL; PROTEIN MOTIF; RECEPTOR BINDING ASSAY; REGULATORY MECHANISM; TEMPERATURE SENSITIVITY; VIRUS CAPSID; VIRUS LIKE AGENT; VIRUS MUTANT; VIRUS STRAIN;

ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; BINDING SITES; CALICIVIRIDAE INFECTIONS; CAPSID; CAPSID PROTEINS; EPITOPES; GASTROENTERITIS; NOROVIRUS; VIRION;

EID: 84904911886     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01192-14     Document Type: Article

References (71)

1. CDC. 2011. Updated norovirus outbreak management and disease prevention guidelines. MMWR Recommend. Rep. 60(RR-3):1-18.
2. Hoffmann S, Batz MB, Morris JG, Jr. 2012. Annual cost of illness and quality-adjusted life year losses in the United States due to 14 foodborne pathogens. J. Food Prot. 75:1292-1302. http://dx.doi.org/10.4315/0362-028X.JFP-11-417.
3. Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinje J, Parashar UD. 2008. Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg. Infect. Dis. 14:1224-1231. http://dx.doi.org/10.3201/eid1408.071114.
4. Trivedi TK, Desai R, Hall AJ, Patel M, Parashar UD, Lopman BA. 2013. Clinical characteristics of norovirus-associated deaths: a systematic literature review. Am. J. Infect. Control 41:654-657. http://dx.doi.org/10.1016/j.ajic.2012.08.002.
5. Bok K, Green KY. 2012. Norovirus gastroenteritis in immunocompromised patients. N. Engl. J. Med. 367:2126-2132. http://dx.doi.org/10.1056/NEJMra1207742.
6. Trivedi TK, DeSalvo T, Lee L, Palumbo A, Moll M, Curns A, Hall AJ, Patel M, Parashar UD, Lopman BA. 2012. Hospitalizations and mortality associated with norovirus outbreaks in nursing homes, 2009-2010. JAMA 308:1668-1675. http://dx.doi.org/10.1001/jama.2012.14023.
7. Hutson AM, Atmar RL, Estes MK. 2004. Norovirus disease: changing epidemiology and host susceptibility factors. Trends Microbiol. 12:279-287. http://dx.doi.org/10.1016/j.tim.2004.04.005.
8. Estes MK, Prasad BV, Atmar RL. 2006. Noroviruses everywhere: has something changed? Curr. Opin. Infect. Dis. 19:467-474. http://dx.doi.org/10.1097/01.qco.0000244053.69253.3d.
9. Koopmans M, Vinjé J, de Wit M, Leenen I, van der Poel W, van Duynhoven Y. 2000. Molecular epidemiology of human enteric caliciviruses in The Netherlands. J. Infect. Dis. 181(Suppl 2):S262-S269. http://dx.doi.org/10.1086/315573.
10. CDC. 2007. Norovirus activity-United States, 2006-2007. MMWR Morb. Mortal. Wkly. Rep. 56:842-846.
11. Okada M, Tanaka T, Oseto M, Takeda N, Shinozaki K. 2006. Genetic analysis of noroviruses associated with fatalities in healthcare facilities. Arch. Virol. 151:1635-1641. http://dx.doi.org/10.1007/s00705-006-0739-6.
12. Harris JP, Edmunds WJ, Pebody R, Brown DW, Lopman BA. 2008. Deaths from norovirus among the elderly, England and Wales. Emerg. Infect. Dis. 14:1546-1552. http://dx.doi.org/10.3201/eid1410.080188.
13. Schorn R, Hohne M, Meerbach A, Bossart W, Wuthrich RP, Schreier E, Muller NJ, Fehr T. 2010. Chronic norovirus infection after kidney transplantation: molecular evidence for immune-driven viral evolution. Clin. Infect. Dis. 51:307-314. http://dx.doi.org/10.1086/653939.
14. Hall AJ, Eisenbart VG, Etingue AL, Gould LH, Lopman BA, Parashar UD. 2012. Epidemiology of foodborne norovirus outbreaks, United States, 2001-2008. Emerg. Infect. Dis. 18:1566-1573. http://dx.doi.org/10.3201/eid1810.120833.
15. Atmar RL, Bernstein DI, Harro CD, Al-Ibrahim MS, Chen WH, Ferreira J, Estes MK, Graham DY, Opekun AR, Richardson C, Mendelman PM. 2011. Norovirus vaccine against experimental human Norwalk Virus illness. N. Engl. J. Med. 365:2178-2187. http://dx.doi.org/10.1056/NEJMoa1101245.
16. Richardson C, Bargatze RF, Goodwin R, Mendelman PM. 2013. Norovirus virus-like particle vaccines for the prevention of acute gastroenteritis. Expert Rev. Vaccines 12:155-167. http://dx.doi.org/10.1586/erv.12.145.
17. Noel JS, Fankhauser RL, Ando T, Monroe SS, Glass RI. 1999. Identification of a distinct common strain of "Norwalk-like viruses" having a global distribution. J. Infect. Dis. 179:1334-1344. http://dx.doi.org/10.1086/314783.
18. Vinje J, Altena S, Koopmans M. 1997. The incidence and genetic variability of small round-structured viruses in outbreaks of gastroenteritis in the Netherlands. J. Infect. Dis. 176:1374-1378. http://dx.doi.org/10.1086/517325.
19. Widdowson MA, Cramer EH, Hadley L, Bresee JS, Beard RS, Bulens SN, Charles M, Chege W, Isakbaeva E, Wright JG, Mintz E, Forney D, Massey J, Glass RI, Monroe SS. 2004. Outbreaks of acute gastroenteritis on cruise ships and on land: identification of a predominant circulating strain of norovirus-United States, 2002. J. Infect. Dis. 190:27-36. http://dx.doi.org/10.1086/420888.
20. Bull RA, Tu ET, McIver CJ, Rawlinson WD, White PA. 2006. Emergence of a new norovirus genotype II.4 variant associated with global outbreaks of gastroenteritis. J. Clin. Microbiol. 44:327-333. http://dx.doi.org/10.1128/JCM.44.2.327-333.2006.
21. Kroneman A, Vennema H, Harris J, Reuter G, von Bonsdorff CH, Hedlund KO, Vainio K, Jackson V, Pothier P, Koch J, Schreier E, Bottiger BE, Koopmans M. 2006. Increase in norovirus activity reported in Europe. Euro Surveill. 11:E061214.1.
22. Phan TG, Kuroiwa T, Kaneshi K, Ueda Y, Nakaya S, Nishimura S, Yamamoto A, Sugita K, Nishimura T, Yagyu F, Okitsu S, Muller WE, Maneekarn N, Ushijima H. 2006. Changing distribution of norovirus genotypes and genetic analysis of recombinant GIIb among infants and children with diarrhea in Japan. J. Med. Virol. 78:971-978. http://dx.doi.org/10.1002/jmv.20649.
23. Siebenga J, Kroneman A, Vennema H, Duizer E, Koopmans M. 2008. Food-borne viruses in Europe network report: the norovirus GII.4 2006b (for US named Minerva-like, for Japan Kobe034-like, for UK V6) variant now dominant in early seasonal surveillance. Euro Surveill. 13:8009.
24. Vega EBL, Gregoricus N, Williams K, Lee D, Vinjé J. 2011. Novel surveillance network for norovirus gastroenteritis outbreaks, United States. Emerg. Infect. Dis. 17:1389-1395. http://dx.doi.org/10.3201/eid1708.101837.
25. CDC. 2013. Emergence of new norovirus strain GII.4 Sydney-United States, 2012. MMWR Morb. Mortal. Wkly. Rep. 62:55.
26. van Beek J, Ambert-Balay K, Botteldoorn N, Eden JS, Fonager J, Hewitt J, Iritani N, Kroneman A, Vennema H, Vinje J, White PA, Koopmans M. 2013. Indications for worldwide increased norovirus activity associated with emergence of a new variant of genotype II.4, late 2012. Euro Surveill. 18:8-9.
27. Siebenga JJ, Vennema H, Renckens B, de Bruin E, van der Veer B, Siezen RJ, Koopmans M. 2007. Epochal evolution of GGII.4 norovirus capsid proteins from 1995 to 2006. J. Virol. 81:9932-9941. http://dx.doi.org/10.1128/JVI.00674-07.
28. Lindesmith LC, Donaldson EF, Lobue AD, Cannon JL, Zheng DP, Vinje J, Baric RS. 2008. Mechanisms of GII. 4 norovirus persistence in human populations. PLoS Med. 5:e31. http://dx.doi.org/10.1371/journal.pmed.0050031.
29. Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, Monroe SS. 2006. Norovirus classification and proposed strain nomenclature. Virology 346:312-323. http://dx.doi.org/10.1016/j.virol.2005.11.015.
30. Baric RS, Yount B, Lindesmith L, Harrington PR, Greene SR, Tseng FC, Davis N, Johnston RE, Klapper DG, Moe CL. 2002. Expression and self-assembly of Norwalk virus capsid protein from Venezuelan equine encephalitis virus replicons. J. Virol. 76:3023-3030. http://dx.doi.org/10.1128/JVI.76.6.3023-3030.2002.
31. Prasad BV, Hardy ME, Dokland T, Bella J, Rossmann MG, Estes MK. 1999. X-ray crystallographic structure of the Norwalk virus capsid. Science 286:287-290. http://dx.doi.org/10.1126/science.286.5438.287.
32. Chen R, Neill JD, Estes MK, Prasad BV. 2006. X-ray structure of a native calicivirus: structural insights into antigenic diversity and host specificity. Proc. Natl. Acad. Sci. U. S. A. 103:8048-8053. http://dx.doi.org/10.1073/pnas.0600421103.
33. Lochridge VP, Jutila KL, Graff JW, Hardy ME. 2005. Epitopes in the P2 domain of norovirus VP1 recognized by monoclonal antibodies that block cell interactions. J. Gen. Virol. 86:2799-2806. http://dx.doi.org/10.1099/vir.0.81134-0.
34. Cao S, Lou Z, Tan M, Chen Y, Liu Y, Zhang Z, Zhang XC, Jiang X, Li X, Rao Z. 2007. Structural basis for the recognition of blood group trisaccharides by norovirus. J. Virol. 81:5949-5957. http://dx.doi.org/10.1128/JVI.00219-07.
35. Debbink K, Donaldson EF, Lindesmith LC, Baric RS. 2012. Genetic mapping of a highly variable norovirus GII.4 blockade epitope: potential role in escape from human herd immunity. J. Virol. 86:1214-1226. http://dx.doi.org/10.1128/JVI.06189-11.
36. Lindesmith LC, Debbink K, Swanstrom J, Vinje J, Costantini V, Baric RS, Donaldson EF. 2012. Monoclonal antibody-based antigenic mapping of norovirus GII.4-2002. J. Virol. 86:873-883. http://dx.doi.org/10.1128/JVI.06200-11.
37. Cannon JL, Lindesmith LC, Donaldson EF, Saxe L, Baric RS, Vinje J. 2009. Herd immunity to GII.4 noroviruses is supported by outbreak patient sera. J. Virol. 83:5363-5374. http://dx.doi.org/10.1128/JVI.02518-08.
38. Harrington PR, Lindesmith L, Yount B, Moe CL, Baric RS. 2002. Binding of Norwalk virus-like particles to ABH histo-blood group antigens is blocked by antisera from infected human volunteers or experimentally vaccinated mice. J. Virol. 76:12335-12343. http://dx.doi.org/10.1128/JVI.76.23.12335-12343.2002.
39. Lindesmith LC, Donaldson E, Leon J, Moe CL, Frelinger JA, Johnston RE, Weber DJ, Baric RS. 2010. Heterotypic humoral and cellular immune responses following Norwalk virus infection. J. Virol. 84:1800-1815. http://dx.doi.org/10.1128/JVI.02179-09.
40. Bok K, Parra GI, Mitra T, Abente E, Shaver CK, Boon D, Engle R, Yu C, Kapikian AZ, Sosnovtsev SV, Purcell RH, Green KY. 2011. Chimpanzees as an animal model for human norovirus infection and vaccine development. Proc. Natl. Acad. Sci. U. S. A. 108:325-330. http://dx.doi.org/10.1073/pnas.1014577107.
41. Reeck A, Kavanagh O, Estes MK, Opekun AR, Gilger MA, Graham DY, Atmar RL. 2010. Serological correlate of protection against norovirusinduced gastroenteritis. J. Infect. Dis. 202:1212-1218. http://dx.doi.org/10.1086/656364.
42. Lindesmith LC, Costantini V, Swanstrom J, Debbink K, Donaldson EF, Vinje J, Baric RS. 2013. Emergence of a norovirus GII.4 strain correlates with changes in evolving blockade epitopes. J. Virol. 87:2803-2813. http://dx.doi.org/10.1128/JVI.03106-12.
43. Eden JS, Tanaka MM, Boni MF, Rawlinson WD, White PA. 2013. Recombination within the pandemic norovirus GII.4 lineage. J. Virol. 87:6270-6282. http://dx.doi.org/10.1128/JVI.03464-12.
44. Bull RA, Eden JS, Rawlinson WD, White PA. 2010. Rapid evolution of pandemic noroviruses of the GII.4 lineage. PLoS Pathog. 6:e1000831. http://dx.doi.org/10.1371/journal.ppat.1000831.
45. Siebenga JJ, Lemey P, Kosakovsky S, Pond L, Rambaut A, Vennema H, Koopmans M. 2010. Phylodynamic reconstruction reveals norovirus GII.4 epidemic expansions and their molecular determinants. PLoS Pathog. 6:e1000884. http://dx.doi.org/10.1371/journal.ppat.1000884.
46. Debbink K, Lindesmith LC, Donaldson EF, Costantini V, Beltramello M, Corti D, Swanstrom J, Lanzavecchia A, Vinje J, Baric RS. 2013. Emergence of new pandemic GII.4 Sydney norovirus strain correlates with escape from herd immunity. J. Infect. Dis. 208:1877-1887. http://dx.doi.org/10.1093/infdis/jit370.
47. Lindesmith LC, Beltramello M, Donaldson EF, Corti D, Swanstrom J, Debbink K, Lanzavecchia A, Baric RS. 2012. Immunogenetic mechanisms driving norovirus GII.4 antigenic variation. PLoS Pathog. 8:e1002705. http://dx.doi.org/10.1371/journal.ppat.1002705.
48. Allen DJ, Gray JJ, Gallimore CI, Xerry J, Iturriza-Gomara M. 2008. Analysis of amino acid variation in the P2 domain of the GII-4 norovirus VP1 protein reveals putative variant-specific epitopes. PLoS One 3:e1485. http://dx.doi.org/10.1371/journal.pone.0001485.
49. Donaldson EF, Lindesmith LC, Lobue AD, Baric RS. 2008. Norovirus pathogenesis: mechanisms of persistence and immune evasion in human populations. Immunol. Rev. 225:190-211. http://dx.doi.org/10.1111/j.1600-065X.2008.00680.x.
50. Belliot G, Noel JS, Li JF, Seto Y, Humphrey CD, Ando T, Glass RI, Monroe SS. 2001. Characterization of capsid genes, expressed in the baculovirus system, of three new genetically distinct strains of "Norwalk-like viruses". J. Clin. Microbiol. 39:4288-4295. http://dx.doi.org/10.1128/JCM.39.12.4288-4295.2001.
51. Lindesmith LC, Donaldson EF, Baric RS. 2011. Norovirus GII.4 strain antigenic variation. J. Virol. 85:231-242. http://dx.doi.org/10.1128/JVI.01364-10.
52. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948. http://dx.doi.org/10.1093/bioinformatics/btm404.
53. Shanker S, Choi JM, Sankaran B, Atmar RL, Estes MK, Prasad BV. 2011. Structural analysis of HBGA binding specificity in a norovirus GII.4 epidemic variant: implications for epochal evolution. J. Virol. 85:8635-8645. http://dx.doi.org/10.1128/JVI.00848-11.
54. Tian P, Yang D, Jiang X, Zhong W, Cannon JL, Burkhardt W, III, Woods JW, Hartman G, Lindesmith L, Baric RS, Mandrell R. 2010. Specificity and kinetics of norovirus binding to magnetic bead-conjugated histo-blood group antigens. J. Appl. Microbiol. 109:1753-1762. http://dx.doi.org/10.1111/j.1365-2672.2010.04812.x.
55. Swanstrom J, Lindesmith LC, Donaldson EF, Yount B, Baric RS. 2014. Characterization of blockade antibody responses in GII.2.1976 Snow Mountain virus-infected subjects. J. Virol. 88:829-837. http://dx.doi.org/10.1128/JVI.02793-13.
56. Lee PD, Mukherjee S, Edeling MA, Dowd KA, Austin SK, Manhart CJ, Diamond MS, Fremont DH, Pierson TC. 2013. The Fc region of an antibody impacts the neutralization of West Nile viruses in different maturation states. J. Virol. 87:13729-13740. http://dx.doi.org/10.1128/JVI.02340-13.
57. Corti D, Langedijk JP, Hinz A, Seaman MS, Vanzetta F, Fernandez-Rodriguez BM, Silacci C, Pinna D, Jarrossay D, Balla-Jhagjhoorsingh S, Willems B, Zekveld MJ, Dreja H, O'Sullivan E, Pade C, Orkin C, Jeffs SA, Montefiori DC, Davis D, Weissenhorn W, McKnight A, Heeney JL, Sallusto F, Sattentau QJ, Weiss RA, Lanzavecchia A. 2010. Analysis of memory B cell responses and isolation of novel monoclonal antibodies with neutralizing breadth from HIV-1-infected individuals. PLoS One 5:e8805. http://dx.doi.org/10.1371/journal.pone.0008805.
58. Sabin C, Corti D, Buzon V, Seaman MS, Lutje Hulsik D, Hinz A, Vanzetta F, Agatic G, Silacci C, Mainetti L, Scarlatti G, Sallusto F, Weiss R, Lanzavecchia A, Weissenhorn W. 2010. Crystal structure and sizedependent neutralization properties of HK20, a human monoclonal antibody binding to the highly conserved heptad repeat 1 of gp41. PLoS Pathog. 6:e1001195. http://dx.doi.org/10.1371/journal.ppat.1001195.
59. Dowd KA, Jost CA, Durbin AP, Whitehead SS, Pierson TC. 2011. A dynamic landscape for antibody binding modulates antibody-mediated neutralization of West Nile virus. PLoS Pathog. 7:e1002111. http://dx.doi.org/10.1371/journal.ppat.1002111.
60. Li Q, Yafal AG, Lee YM, Hogle J, Chow M. 1994. Poliovirus neutralization by antibodies to internal epitopes of VP4 and VP1 results from reversible exposure of these sequences at physiological temperature. J. Virol. 68:3965-3970.
61. Nelson S, Jost CA, Xu Q, Ess J, Martin JE, Oliphant T, Whitehead SS, Durbin AP, Graham BS, Diamond MS, Pierson TC. 2008. Maturation of West Nile virus modulates sensitivity to antibody-mediated neutralization. PLoS Pathog. 4:e1000060. http://dx.doi.org/10.1371/journal.ppat.1000060.
62. Hansman GS, Taylor DW, McLellan JS, Smith TJ, Georgiev I, Tame JR, Park SY, Yamazaki M, Gondaira F, Miki M, Katayama K, Murata K, Kwong PD. 2012. Structural basis for broad detection of genogroup II noroviruses by a monoclonal antibody that binds to a site occluded in the viral particle. J. Virol. 86:3635-3646. http://dx.doi.org/10.1128/JVI.06868-11.
63. VanBlargan LA, Mukherjee S, Dowd KA, Durbin AP, Whitehead SS, Pierson TC. 2013. The type-specific neutralizing antibody response elicited by a dengue vaccine candidate is focused on two amino acids of the envelope protein. PLoS Pathog. 9:e1003761. http://dx.doi.org/10.1371/journal.ppat.1003761.
64. Dowd KA, Pierson TC. 2011. Antibody-mediated neutralization of flaviviruses: a reductionist view. Virology 411:306-315. http://dx.doi.org/10.1016/j.virol.2010.12.020.
65. van Gils MJ, Sanders RW. 2013. Broadly neutralizing antibodies against HIV-1: templates for a vaccine. Virology 435:46-56. http://dx.doi.org/10.1016/j.virol.2012.10.004.
66. Corti D, Lanzavecchia A. 2013. Broadly neutralizing antiviral antibodies. Annu. Rev. Immunol. 31:705-742. http://dx.doi.org/10.1146/annurev-immunol-032712-095916.
67. Stanekova Z, Adkins I, Kosova M, Janulikova J, Sebo P, Vareckova E. 2013. Heterosubtypic protection against influenza A induced by adenylate cyclase toxoids delivering conserved HA2 subunit of hemagglutinin. Antiviral Res. 97:24-35. http://dx.doi.org/10.1016/j.antiviral.2012.09.008.
68. Ausar SF, Foubert TR, Hudson MH, Vedvick TS, Middaugh CR. 2006. Conformational stability and disassembly of Norwalk virus-like particles. Effect of pH and temperature. J. Biol. Chem. 281:19478-19488.
69. Singharoy A, Polavarapu A, Joshi H, Baik MH, Ortoleva P. 2013. Epitope fluctuations in the human papillomavirus are under dynamic allosteric control: a computational evaluation of a new vaccine design strategy. J. Am. Chem. Soc. 135:18458-18468. http://dx.doi.org/10.1021/ja407489r.
70. Chagla Z, Quirt J, Woodward K, Neary J, Rutherford C. 2013. Chronic norovirus infection in a transplant patient successfully treated with enterally administered immune globulin. J. Clin. Virol. 58:306-308. http://dx.doi.org/10.1016/j.jcv.2013.06.009.
71. Reisdorph N, Thomas JJ, Katpally U, Chase E, Harris K, Siuzdak G, Smith TJ. 2003. Human rhinovirus capsid dynamics is controlled by canyon flexibility. Virology 314:34-44. http://dx.doi.org/10.1016/S0042-6822(03)00452-5.