Norwalk virus-like particles as vaccines

Expert Review of Vaccines

Volumn 9, Issue 3, 2010, Pages 299-307

  Herbst Kralovetz, Melissa ^a,b   Mason, Hugh S ^a,c   Chen, Qiang ^a,d  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^c ARIZONA STATE UNIVERSITY   (United States)

^d ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Chimeric vaccines; Intranasal delivery; Mucosal antibody; Mucosal immunity; Multivalent vaccines; Norovirus; Oral delivery; Vaccine platforms; Virus like particle; VLP

Indexed keywords

AMINO ACID; ANTIGEN; CAPSID PROTEIN; CHITOSAN; CHOLERA TOXIN; EPITOPE; IMMUNOGLOBULIN A; NORWALK VIRUS LIKE PARTICLE; TOLL LIKE RECEPTOR AGONIST; UNCLASSIFIED DRUG; VIRUS ANTIBODY; VIRUS VACCINE;

ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIGEN PURIFICATION; BACULOVIRUS; CENTRIFUGATION; CHROMATOGRAPHY; CLINICAL TRIAL; DRUG ISOLATION; DRUG PURIFICATION; DRUG SAFETY; ESCHERICHIA COLI; HETEROLOGOUS EXPRESSION; HUMAN; IMMUNIZATION; IMMUNOGENICITY; INOCULATION; NONHUMAN; NOROVIRUS; PH; PLANT TISSUE; PLANT VIRUS; POTATO; PRECIPITATION; PRIORITY JOURNAL; RECEPTOR BINDING; REPLICON; REVIEW; STOMACH INTUBATION; TOMATO; TRANSGENIC PLANT; VENEZUELAN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS; VIRUS CAPSID; VIRUS EXPRESSION; VIRUS GENE; VIRUS LIKE AGENT; VIRUS NEUTRALIZATION; VIRUS STRAIN;

ADMINISTRATION, INTRANASAL; ADMINISTRATION, ORAL; ANIMALS; ANTIBODIES, VIRAL; CELL LINE; GENETIC VECTORS; HUMANS; IMMUNITY, MUCOSAL; INSECTS; MICE; NORWALK VIRUS; PLANTS; RECOMBINANT PROTEINS; VACCINES, VIROSOME; VIRAL PROTEINS; VIRAL VACCINES;

EID: 77949451352     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/erv.09.163     Document Type: Review

References (61)

1. Fankhauser RL, Noel JS, Monroe SS, Ando T, Glass RI. Molecular epidemiology of "Norwalk-like viruses" in outbreaks of gastroenteritis in the United States. J. Infect. Dis. 178(6), 1571-1578 (1998).
2. Patel MM, Hall AJ, Vinje J, Parashar UD. Noroviruses: a comprehensive review. J. Clin. Virol. 44(1), 1-8 (2009).
3. Koopmans M. Progress in understanding norovirus epidemiology. Curr. Opin Infect. Dis. 21(5), 544-552 (2008).
4. Lopman B, Vennema H, Kohli E et al. Increase in viral gastroenteritis outbreaks in Europe and epidemic spread of new norovirus variant. Lancet 363(9410), 682-688 (2004).
5. Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinje J, Parashar UD. Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg. Infect. Dis. 14(8), 1224-1231 (2008).
6. Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, Monroe SS. Norovirus classification and proposed strain nomenclature. Virology 346(2), 312-323 (2006).
7. Lindesmith LC, Donaldson EF, Lobue AD et al. Mechanisms of GII.4 norovirus persistence in human populations. PLoS Med. 5(2), e31 (2008).
8. Siebenga J, Kroneman A, Vennema H, Duizer E, Koopmans M. 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(2), 8009 (2008).
9. Siebenga JJ, Vennema H, Renckens B et al. Epochal evolution of GGII.4 norovirus capsid proteins from 1995 to 2006. J. Virol. 81(18), 9932-9941 (2007).
10. Jiang X, Wang M, Wang K, Estes MK. Sequence and genomic organization of Norwalk virus. Virology 195(1), 51-61 (1993).
11. Prasad BVV, Hardy ME, Dokland T, Bella J, Rossmann MG, Estes MK. X-ray crystallographic structure of the Norwalk virus capsid. Science 286, 287-290 (1999).
12. Prasad BVV, Hardy ME, Estes MK. Structural studies of recombinant norwalk capsids. J. Infect. Dis. 181(s2), S317-S321 (2000).
13. Hansman GS, Natori K, Shirato- Horikoshi H et al. Genetic and antigenic diversity among noroviruses. J. Gen. Virol. 87(Pt 4), 909-919 (2006).
14. Jiang X, Wang M, Graham DY, Estes MK. Expression, self-assembly, and antigenicity of the Norwalk virus capsid protein. J. Virol. 66(11), 6527-6532 (1992).
15. Santi L, Batchelor L, Huang Z et al. An efficient plant viral expression system generating orally immunogenic Norwalk virus-like particles. Vaccine 26(15), 1846-1854 (2008).
16. Huang Z, Chen Q, Hjelm B, Arntzen C, Mason H. A DNA replicon system for rapid high-level production of virus-like particles in plants. Biotechnol. Bioeng. 103(4), 706-714 (2009).
17. Hutson AM, Atmar RL, Marcus DM, Estes MK. Norwalk virus-like particle hemagglutination by binding to h histo-blood group antigens. J. Virol. 77(1), 405-415 (2003).
18. Tan M, Jiang X. Norovirus and its histo-blood group antigen receptors: an answer to a historical puzzle. Trends Microbiol. 13(6), 285-293 (2005).
19. Huang P, Farkas T, Marionneau S et al. Noroviruses bind to human ABO, Lewis, and secretor histo-blood group antigens: identification of 4 distinct strain-specific patterns. J. Infect. Dis. 188(1), 19-31 (2003).
20. Choi JM, Hutson AM, Estes MK, Prasad BV. Atomic resolution structural characterization of recognition of histo-blood group antigens by Norwalk virus. Proc. Natl Acad. Sci. USA 105(27), 9175-9180 (2008).
21. Glass RI, Parashar UD, Estes MK. Norovirus gastroenteritis. N. Engl. J. Med. 361(18), 1776-1785 (2009).
22. Barr E, Sings HL. Prophylactic HPV vaccines: new interventions for cancer control. Vaccine 26(49), 6244-6257 (2008).
23. Harper DM. Currently approved prophylactic HPV vaccines. Expert Rev. Vaccines 8(12), 1663-1679 (2009).
24. Jennings GT, Bachmann MF. The coming of age of virus-like particle vaccines. Biol. Chem. 389(5), 521-536 (2008).
25. Ball JM, Hardy ME, Atmar RL, Conner ME, Estes MK. Oral immunization with recombinant Norwalk virus-like particles induces a systemic and mucosal immune response in mice. J. Virol. 72(2), 1345-1353 (1998).
26. Guerrero RA, Ball JM, Krater SS, Pacheco SE, Clements JD, Estes MK. Recombinant Norwalk virus-like particles administered intranasally to mice induce systemic and mucosal (fecal and vaginal) immune responses. J. Virol. 75(20), 9713-9722 (2001).
27. Mason HS, Ball JM, Shi JJ, Jiang X, Estes MK, Arntzen CJ. Expression of Norwalk virus capsid protein in transgenic tobacco and potato and its oral immunogenicity in mice. Proc. Natl Acad. Sci. USA 93(11), 5335-5340 (1996).
28. Zhang X, Buehner NA, Hutson AM, Estes MK, Mason HS. Tomato is a highly effective vehicle for expression and oral immunization with Norwalk virus capsid protein. Plant Biotechnol. J. 4(4), 419-432 (2006).
29. Nilsson M, Hedlund KO, Thorhagen M et al. Evolution of human calicivirus RNA in vivo: accumulation of mutations in the protruding P2 domain of the capsid leads to structural changes and possibly a new phenotype. J. Virol. 77(24), 13117-13124 (2003).
30. LoBue AD, Thompson JM, Lindesmith L, Johnston RE, Baric RS. Alphavirus-adjuvanted norovirus-like particle vaccines: heterologous, humoral, and mucosal immune responses protect against murine norovirus challenge. J. Virol. 83(7), 3212-3227 (2009).
31. Ausar SF, Foubert TR, Hudson MH, Vedvick TS, Middaugh CR. Conformational stability and disassembly of norwalk virus like particles: effect of pH and temperature. J. Biol. Chem. 281, 19478-19488 (2006).
32. Mason HS, Ball JM, Shi J-J, Estes MK, Arntzen CJ. Expression of Norwalk virus capsid protein in transgenic tobacco and potato and its oral immunogenicity in mice. Proc. Natl Acad. Sci. USA 93, 5335-5340 (1996).
33. Rybicki EP. Plant-produced vaccines: promise and reality. Drug Discov. Today 14(1-2), 16-24 (2009).
34. Santi L, Huang Z, Mason H. Virus-like particles production in green plants. Methods 40(1), 66-76 (2006).
35. Gleba Y, Klimyuk V, Marillonnet S. Viral vectors for the expression of proteins in plants. Curr. Opin Biotechnol. 18(2), 134-141 (2007).
36. Baric RS, Yount B, Lindesmith L et al. Expression and self-assembly of Norwalk virus capsid protein from venezuelan equine encephalitis virus replicons. J. Virol. 76(6), 3023-3030 (2002).
37. Harrington PR, Yount B, Johnston RE, Davis N, Moe C, Baric RS. Systemic, mucosal, and heterotypic immune induction in mice inoculated with Venezuelan equine encephalitis replicons expressing Norwalk virus-like particles. J. Virol. 76(2), 730-742 (2002).
38. LoBue AD, Lindesmith L, Yount B et al. Multivalent norovirus vaccines induce strong mucosal and systemic blocking antibodies against multiple strains. Vaccine 24(24), 5220-5234 (2006).
39. Ball JM, Graham DY, Opekun AR, Gilger MA, Guerrero RA, Estes MK. Recombinant Norwalk virus-like particles given orally to volunteers: Phase I study. Gastroenterology 117(1), 40-48 (1999).
40. Tacket CO, Mason HS, Losonsky G, Estes MK, Levine MM, Arntzen CJ. Human immune responses to a novel norwalk virus vaccine delivered in transgenic potatoes. J. Infect. Dis. 182(1), 302-305 (2000).
41. Tacket CO, Sztein MB, Losonsky GA, SS Wasserman, Estes MK. Humoral, mucosal, and cellular immune responses to oral Norwalk virus-like particles in volunteers. Clin. Immunol. 108, 241-247 (2003).
42. Sakaguchi S, Yamaguchi T, Nomura T, Ono M. Regulatory T cells and immune tolerance. Cell 133(5), 775-787 (2008).
43. Lico C, Chen Q, Santi L. Viral vectors for production of recombinant proteins in plants. J. Cell. Physiol. 216(2), 366-377 (2008).
44. Huang Z, Phoolcharoen W, Lai H et al. High-level rapid production of full-size monoclonal antibodies in plants by a single-vector DNA replicon system. Biotechnol. Bioeng. DOI: 10.1002/ bit.22652 (2010) (Epub ahead of print).
45. Chen Q. Expression and purification of pharmaceutical proteins in plants. Biol. Eng. 1(4), 291-321 (2008).
46. Platis D, Labrou NE. Affinity chromatography for the purification of therapeutic proteins from transgenic maize using immobilized histamine. J. Sep. Sci. 31(4), 636-645 (2008).
47. Roque ACA, Lowe CR, Taipa MA. Antibodies and genetically engineered related molecules: production and purification. Biotechnol. Prog. 20(3), 639-654 (2004).
48. Estes MK. Virus like particle (VLP) vaccines. In: New Generation Vaccines. Levine MM (Ed.). Academic Press, NY, USA, 283-294 (2004).
49. Rolland D, Gauthier M, Dugua JM et al. Purification of recombinant HBc antigen expressed in Escherichia coli and Pichia pastoris: comparison of size-exclusion chromatography and ultracentrifugation. J. Chromatog. B Biomed. Sci. App. 753(1), 51-65 (2001).
50. Cook JC, Joyce JG, George HA et al. Purification of virus-like particles of recombinant human papillomavirus type 11 major capsid protein L1 from Saccharomyces cerevisiae. Protein Expr. Purif. 17(3), 477-484 (1999).
51. Pattenden LK, Middelberg APJ, Niebert M, Lipin DI. Towards the preparative and large-scale precision manufacture of virus-like particles. Trends Biotechnol. 23(10), 523-529 (2005).
52. Palomares LA, Ramírez OT. Challenges for the production of virus-like particles in insect cells: the case of rotavirus-like particles. Biochem. Eng. J. 45(3), 158-167 (2009).
53. Vicente T, Sousa MFQ, Peixoto C, Mota JPB, Alves PM, Carrondo MJT. Anion-exchange membrane chromatography for purification of rotavirus-like particles. J. Mem. Sci. 311(1-2), 270-283 (2008).
54. Goodridge L, Goodridge C, Wu J, Griffiths M, Pawliszyn J. Isoelectric point determination of norovirus virus-like particles by capillary isoelectric focusing with whole column imaging detection. Anal. Chem. 76(1), 48-52 (2004).
55. Bertolotti-Ciarlet A, White LJ, Chen R, Prasad BV, Estes MK. Structural requirements for the assembly of Norwalk virus-like particles. J. Virol. 76(8), 4044-4055 (2002).
56. Tan M, Jiang X. The P domain of norovirus capsid protein forms a subviral particle that binds to histo-blood group antigen receptors. J. Virol. 79(22), 14017-14030 (2005).
57. Tan M, Hegde RS, Jiang X. The P domain of norovirus capsid protein forms dimer and binds to histo-blood group antigen receptors. J. Virol. 78(12), 6233-6242 (2004).
58. Chen R, Neill JD, Estes MK, Prasad BV. X-ray structure of a native calicivirus: structural insights into antigenic diversity and host specificity. Proc. Natl Acad. Sci. USA 103(21), 8048-8053 (2006).
59. Cao S, Lou Z, Tan M et al. Structural basis for the recognition of blood group trisaccharides by norovirus. J. Virol. 81(11), 5949-5957 (2007).
60. El-Kamary S, Pasetti M, Tacket CO et al. Phase 1 dose escalation, safety and immunogenicity of intranasal dry powder Norovirus vaccine. Presented at: 3rd International Calicivirus Conference. Cancun, Mexico, 10-13 November 2007 (Abstract S5-3).
61. Tacket CO, Frey S, Bernstein DI et al. Phase 1 dose-comparison, safety and immunogenicity of intranasal dry powder Norwalk VLP vaccine. Presented at: 5th International Conference on Vaccines for Enteric Diseases. Malaga, Spain, 9-11 September 2009 (Session 4).