Chimeric GII.4 norovirus virus-like-particle-based vaccines induce broadly blocking immune responses

Journal of Virology

Volumn 88, Issue 13, 2014, Pages 7256-7266

  Debbink, Kari ^a   Lindesmith, Lisa C ^b   Donaldson, Eric F ^b   Swanstrom, Jesica ^b   Baric, Ralph S ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b University of North Carolina at Chapel Hill   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; EPITOPE; VIRUS LIKE PARTICLE VACCINE; HYBRID PROTEIN; VIRUS ANTIBODY;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANTIGENIC VARIATION; ARTICLE; CAPSID GENE; CONTROLLED STUDY; DRUG DESIGN; EPITOPE MAPPING; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNOGENICITY; LIGAND BINDING; MOUSE; NONHUMAN; NOROVIRUS; NOROVIRUS INFECTION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; VACCINE PRODUCTION; VIRUS NEUTRALIZATION; ANIMAL; BAGG ALBINO MOUSE; CALICIVIRIDAE INFECTIONS; GENETICS; HUMAN; IMMUNOCOMPROMIZED PATIENT; IMMUNOLOGY; ISOLATION AND PURIFICATION; MOLECULAR GENETICS; PROTEIN CONFORMATION; VIROLOGY;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, VIRAL; ANTIGENIC VARIATION; CALICIVIRIDAE INFECTIONS; CAPSID PROTEINS; EPITOPES; HUMANS; IMMUNOCOMPROMISED HOST; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; NOROVIRUS; PROTEIN CONFORMATION; RECOMBINANT FUSION PROTEINS; VACCINES, VIRUS-LIKE PARTICLE;

EID: 84902001344     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00785-14     Document Type: Article

References (50)

1. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM. 2011. Foodborne illness acquired in the United States-major pathogens. Emerg. Infect. Dis. 17:7-15. http://dx.doi.org/10 .3201/eid1701.09-1101p1.
2. 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.
3. Bartsch SM, Lopman BA, Hall AJ, Parashar UD, Lee BY. 2012. The potential economic value of a human norovirus vaccine for the United States. Vaccine 30:7097-7104. http://dx.doi.org/10.1016/j.vaccine.2012 .09.040.
4. Kroneman A, Vega E, Vennema H, Vinje J, White PA, Hansman G, Green K, Martella V, Katayama K, Koopmans M. 2013. Proposal for a unified norovirus nomenclature and genotyping. Arch. Virol. 158:2059-2068. http://dx.doi.org/10.1007/s00705-013-1708-5.
5. 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.
6. 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.
7. 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.
8. 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.
9. Choi JM, Hutson AM, Estes MK, Prasad BV. 2008. Atomic resolution structural characterization of recognition of histo-blood group antigens by Norwalk virus. Proc. Natl. Acad. Sci. U. S. A. 105:9175-9180. http://dx .doi.org/10.1073/pnas.0803275105.
10. 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.
11. Shanker S, Choi JM, Sankaran B, Atmar RL, Estes MK, Prasad BV.2011. Structural analysis of histo-blood group antigen 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.
12. de Rougemont A, Ruvoen-Clouet N, Simon B, Estienney M, Elie-Caille C, Aho S, Pothier P, Le Pendu J, Boireau W, Belliot G. 2011. Qualitative and quantitative analysis of the binding of GII.4 norovirus variants onto human blood group antigens. J. Virol. 85:4057-4070. http://dx.doi.org/10 .1128/JVI.02077-10.
13. 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.
14. Marionneau S, Ruvoen N, Le Moullac-Vaidye B, Clement M, Cailleau-Thomas A, Ruiz-Palacois G, Huang P, Jiang X, Le Pendu J. 2002. Norwalk virus binds to histo-blood group antigens present on gastroduodenal epithelial cells of secretor individuals. Gastroenterology 122: 1967-1977. http://dx.doi.org/10.1053/gast.2002.33661.
15. 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.
16. 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.
17. 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.
18. 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.
19. 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.
20. 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.
21. 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.
22. 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.
23. 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.
24. Boon D, Mahar JE, Abente EJ, Kirkwood CD, Purcell RH, Kapikian AZ, Green KY, Bok K. 2011. Comparative evolution of GII.3 and GII.4 norovirus over a 31-year period. J. Virol. 85:8656-8666. http://dx.doi.org/10 .1128/JVI.00472-11.
25. 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.
26. Fankhauser RL, Monroe SS, Noel JS, Humphrey CD, Bresee JS, Parashar UD, Ando T, Glass RI. 2002. Epidemiologic and molecular trends of "Norwalk-like viruses" associated with outbreaks of gastroenteritis in the United States. J. Infect. Dis. 186:1-7. http://dx.doi.org/10.1086/341085.
27. Jing Y, Qian Y, Huo Y, Wang LP, Jiang X. 2000. Seroprevalence against Norwalk-like human caliciviruses in Beijing, China. J. Med. Virol. 60:97-101. http://dx.doi.org/10.1002/(SICI)1096-9071(200001)60:1<97::AID-JMV16>3.0.CO;2-D.
28. Parrino TA, Schreiber DS, Trier JS, Kapikian AZ, Blacklow NR. 1977. Clinical immunity in acute gastroenteritis caused by Norwalk agent. N. Engl. J. Med. 297:86-89. http://dx.doi.org/10.1056/NEJM197707142970204.
29. Teunis PF, Moe CL, Liu P, Miller SE, Lindesmith L, Baric RS, Le Pendu J, Calderon RL. 2008. Norwalk virus: how infectious is it? J. Med. Virol. 80:1468-1476. http://dx.doi.org/10.1002/jmv.21237.
30. Atmar RL, Opekun AR, Gilger MA, Estes MK, Crawford SE, Neill FH, Ramani S, Hill H, Ferreira J, Graham DY. 18 November 2013. Determination of the human infectious dose-50% for Norwalk virus. J. Infect. Dis. http://dx.doi.org/10.1093/infdis/jit620.
31. Simmons K, Gambhir M, Leon J, Lopman B. 2013. Duration of immunity to norovirus gastroenteritis. Emerg. Infect. Dis. 19:1260-1267. http: //dx.doi.org/10.3201/eid1908.130472.
32. Lindesmith L, Moe C, Marionneau S, Ruvoen N, Jiang X, Lindblad L, Stewart P, LePendu J, Baric R. 2003. Human susceptibility and resistance to Norwalk virus infection. Nat. Med. 9:548-553. http://dx.doi.org/10 .1038/nm860.
33. Siebenga JJ, Lemey P, Kosakovsky Pond SL, 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.
34. LoBue AD, Lindesmith L, Yount B, Harrington PR, Thompson JM, Johnston RE, Moe CL, Baric RS. 2006. Multivalent norovirus vaccines induce strong mucosal and systemic blocking antibodies against multiple strains. Vaccine 24:5220-5234. http://dx.doi.org/10.1016/j.vaccine.2006 .03.080.
35. 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.
36. + T cell responses to co-delivered antigen. Vaccine 26:4267-4275. http://dx.doi.org/10.1016 /j.vaccine.2008.05.046.
37. LoBue AD, Thompson JM, Lindesmith L, Johnston RE, Baric RS. 2009. Alphavirus-adjuvanted norovirus-like particle vaccines: heterologous, humoral, and mucosal immune responses protect against murine norovirus challenge. J. Virol. 83:3212-3227. http://dx.doi.org/10.1128/JVI .01650-08.
38. Harrington PR, Yount B, Johnston RE, Davis N, Moe C, Baric RS. 2002. Systemic, mucosal, and heterotypic immune induction in mice inoculated with Venezuelan equine encephalitis replicons expressing Norwalk viruslike particles. J. Virol. 76:730-742. http://dx.doi.org/10.1128/JVI.76.2.730-742.2002.
39. Tian P, Yang D, Jiang X, Zhong W, Cannon JL, WBurkhardt 3rd, 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.
40. Messer WB, de Alwis R, Yount BL, Royal SR, Huynh JP, Smith SA, Crowe JE, Jr, Doranz BJ, Kahle KM, Pfaff JM, White LJ, Sariol CA, de Silva AM, Baric RS. 2 January 2014. Dengue virus envelope protein domain I/II hinge determines long-lived serotype-specific dengue immunity. Proc. Natl. Acad. Sci. U. S. A. http://dx.doi.org/10.1073/pnas .1317350111.
41. Correia BE, Bates JT, Loomis RJ, Baneyx G, Carrico C, Jardine JG, Rupert P, Correnti C, Kalyuzhniy O, Vittal V, Connell MJ, Stevens E, Schroeter A, Chen M, Macpherson S, Serra AM, Adachi Y, Holmes MA, Li Y, Klevit RE, Graham BS, Wyatt RT, Baker D, Strong RK, Crowe JE, Johnson PR, Schief WR. 2014. Proof of principle for epitope-focused vaccine design. Nature 507: 201-206. http://dx.doi.org/10.1038/nature12966.
42. Parra GI, Bok K, Taylor R, Haynes JR, Sosnovtsev SV, Richardson C, Green KY. 2012. Immunogenicity and specificity of norovirus consensus GII.4 virus-like particles in monovalent and bivalent vaccine formulations. Vaccine 30:3580-3586. http://dx.doi.org/10.1016/j.vaccine.2012.03 .050.
43. Zhang T, Xu Y, Qiao L, Wang Y, Wu X, Fan D, Peng Q, Xu X. 2010. Trivalent human papillomavirus (HPV) VLP vaccine covering HPV type 58 can elicit high level of humoral immunity but also induce immune interference among component types. Vaccine 28:3479-3487. http://dx .doi.org/10.1016/j.vaccine.2010.02.057.
44. Berger R, Just M, Gluck R. 1988. Interference between strains in live virus vaccines. I: Combined vaccination with measles, mumps and rubella vaccine. J. Biol. Stand. 16:269-273.
45. Guy B, Barban V, Mantel N, Aguirre M, Gulia S, Pontvianne J, Jourdier TM, Ramirez L, Gregoire V, Charnay C, Burdin N, Dumas R, Lang J.2009. Evaluation of interferences between dengue vaccine serotypes in a monkey model. Am. J. Trop. Med. Hyg. 80:302-311. http://www.ajtmh .org/content/80/2/302.long.
46. Frey S, Dagan R, Ashur Y, Chen XQ, Ibarra J, Kollaritsch H, Mazur MH, Poland GA, Reisinger K, Walter E, Van Damme P, Braconier JH, Uhnoo I, Wahl M, Blatter MM, Clements D, Greenberg D, Jacobson RM, Norrby SR, Rowe M, Shouval D, Simmons SS, van Hattum J, Wennerholm S, Gress JO, Chan I, Kuter B. 1999. Interference of antibody production to hepatitis B surface antigen in a combination hepatitis A/hepatitis B vaccine. J. Infect. Dis. 180:2018-2022. http://dx.doi.org/10 .1086/315119.
47. Kitler ME, Gavinio P, Lavanchy D. 2002. Influenza and the work of the World Health Organization. Vaccine 20(Suppl 2):S5-S14. http://dx.doi .org/10.1016/S0264-410X(02)00121-4.
48. Vega E, Barclay L, Gregoricus N, Williams K, Lee D, Vinje 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.
49. van Beek J, Ambert-Balay K, Botteldoorn N, Eden J, Fonager J, Hewitt J, Iritani N, Kroneman A, Vennema H, Vinje J, White P, 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. http: //www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20345.
50. Vega E, Barclay L, Gregoricus N, Shirley SH, Lee D, Vinje J. 2014. Genotypic and epidemiologic trends of norovirus outbreaks in the United States, 2009 to 2013. J. Clin. Microbiol. 52:147-155. http://dx.doi.org/10 .1128/JCM.02680-13.