Norovirus P Particle Efficiently Elicits Innate, Humoral and Cellular Immunity

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Fang, Hao ^a   Tan, Ming ^a,b   Xia, Ming ^a   Wang, Leyi ^a   Jiang, Xi ^a,b  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NOROVIRUS P DIMER; NOROVIRUS P PARTICLE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VIRUS VACCINE; VIRUS ANTIBODY; VIRUS ANTIGEN; VIRUS LIKE PARTICLE VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY TITER; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; FLOW CYTOMETRY; HUMORAL IMMUNITY; INNATE IMMUNITY; LYMPHOCYTE PROLIFERATION; MOUSE; MYELOID DENDRITIC CELL; NONHUMAN; NOROVIRUS; PHENOTYPE; UPREGULATION; VACCINATION; VIRUS LIKE AGENT; VIRUS PARTICLE; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; BONE MARROW CELL; CELL PROLIFERATION; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; DENDRITIC CELL; IMMUNOLOGY; METABOLISM; PROTEIN TERTIARY STRUCTURE; SPECIES DIFFERENCE;

ESCHERICHIA COLI; MUS; NOROVIRUS;

ANIMALS; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; BONE MARROW CELLS; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; DENDRITIC CELLS; FEMALE; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; IMMUNITY, INNATE; INTERFERON-GAMMA; INTERLEUKIN-2; MICE; MICE, INBRED BALB C; MODELS, MOLECULAR; NOROVIRUS; PROTEIN STRUCTURE, TERTIARY; SPECIES SPECIFICITY; TUMOR NECROSIS FACTOR-ALPHA; VACCINES, VIRUS-LIKE PARTICLE;

EID: 84876931013     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063269     Document Type: Article

References (47)

1. Glass RI, Parashar UD, Estes MK, (2009) Norovirus gastroenteritis. N Engl J Med 361: 1776-1785.
2. 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.
3. Prasad BV, Hardy ME, Dokland T, Bella J, Rossmann MG, et al. (1999) X-ray crystallographic structure of the Norwalk virus capsid. Science 286: 287-290.
4. Bertolotti-Ciarlet A, White LJ, Chen R, Prasad BV, Estes MK, (2002) Structural requirements for the assembly of Norwalk virus-like particles. J Virol 76: 4044-4055.
5. Tan M, Hegde RS, Jiang X, (2004) The P domain of norovirus capsid protein forms dimer and binds to histo-blood group antigen receptors. J Virol 78: 6233-6242.
6. Tan M, Jiang X, (2007) Norovirus-host interaction: implications for disease control and prevention. Expert Rev Mol Med 9: 1-22.
7. Tan M, Jiang X, (2011) Norovirus-host interaction: Multi-selections by human histo-blood group antigens. Trends Microbiol 19: 382-388.
8. Tan M, Jiang X, (2010) Norovirus gastroenteritis, carbohydrate receptors, and animal models. PLoS Pathog 6: e1000983.
9. Tan M, Jiang X, (2005) The p domain of norovirus capsid protein forms a subviral particle that binds to histo-blood group antigen receptors. J Virol 79: 14017-14030.
10. Tan M, Jiang X (2010) Virus-Host Interaction and Celluar Receptors of Caliciviruses. In: Hansman G, Jiang X, Green K, editors. Caliciruses. Norwich: Caister Academic Press. 111-130.
11. Bu W, Mamedova A, Tan M, Xia M, Jiang X, et al. (2008) Structural basis for the receptor binding specificity of Norwalk virus. J Virol 82: 5340-5347.
12. Cao S, Lou Z, Tan M, Chen Y, Liu Y, et al. (2007) Structural basis for the recognition of blood group trisaccharides by norovirus. J Virol 81: 5949-5957.
13. Chen Y, Tan M, Xia M, Hao N, Zhang XC, et al. (2011) Crystallography of a lewis-binding norovirus, elucidation of strain-specificity to the polymorphic human histo-blood group antigens. PLoS Pathog 7: e1002152.
14. 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.
15. Tan M, Fang PA, Xia M, Chachiyo T, Jiang W, et al. (2011) Terminal modifications of norovirus P domain resulted in a new type of subviral particles, the small P particles. Virology 410: 345-352.
16. Tan M, Fang P, Chachiyo T, Xia M, Huang P, et al. (2008) Noroviral P particle: Structure, function and applications in virus-host interaction. Virology 382: 115-123.
17. Tan M, Jiang X, (2012) Norovirus P particle, a subviral nanoparticle for vaccine development against norovirus, rotavirus and influenza virus. Nanomedicine 7: 1-9.
18. Bereszczak JZ, Barbu IM, Tan M, Xia M, Jiang X, et al. (2012) Structure, stability and dynamics of norovirus P domain derived protein complexes studied by native mass spectrometry. J Struct Biol 177: 273-282.
19. Yang Y, Xia M, Tan M, Huang P, Zhong W, et al. (2010) Genetic and Phenotypic Characterization of GII-4 Noroviruses That Circulated during 1987 to 2008. J Virol 84: 9595-9607.
20. Tan M, Meller J, Jiang X, (2006) C-terminal arginine cluster is essential for receptor binding of norovirus capsid protein. J Virol 80: 7322-7331.
21. Greenberg HB, Valdesuso JR, Kalica AR, Wyatt RG, McAuliffe VJ, et al. (1981) Proteins of Norwalk virus. J Virol 37: 994-999.
22. Hardy ME, White LJ, Ball JM, Estes MK, (1995) Specific proteolytic cleavage of recombinant Norwalk virus capsid protein. J Virol 69: 1693-1698.
23. Atmar RL, Bernstein DI, Harro CD, Al-Ibrahim MS, Chen WH, et al. (2011) Norovirus vaccine against experimental human Norwalk Virus illness. N Engl J Med 365: 2178-2187.
24. Bok K, Parra GI, Mitra T, Abente E, Shaver CK, et al. (2011) Chimpanzees as an animal model for human norovirus infection and vaccine development. Proc Natl Acad Sci U S A 108: 325-330.
25. Parra GI, Bok K, Taylor R, Haynes JR, Sosnovtsev SV, et al. (2012) Immunogenicity and specificity of norovirus Consensus GII.4 virus-like particles in monovalent and bivalent vaccine formulations. Vaccine 30: 3580-3586.
26. Reeck A, Kavanagh O, Estes MK, Opekun AR, Gilger MA, et al. (2010) Serological correlate of protection against norovirus-induced gastroenteritis. J Infect Dis 202: 1212-1218.
27. Tan M, Huang P, Xia M, Fang PA, Zhong W, et al. (2011) Norovirus P particle, a novel platform for vaccine development and antibody production. J Virol 85: 753-764.
28. Tan M, Xia M, Huang P, Wang L, Zhong W, et al. (2011) Norovirus P Particle as a Platform for Antigen Presentation. Procedia in Vaccinology 4: 19-26.
29. El-Kamary SS, Pasetti MF, Mendelman PM, Frey SE, Bernstein DI, et al. (2010) Adjuvanted intranasal Norwalk virus-like particle vaccine elicits antibodies and antibody-secreting cells that express homing receptors for mucosal and peripheral lymphoid tissues. J Infect Dis 202: 1649-1658.
30. Xia M, Tan M, Wei C, Zhong W, Wang L, et al. (2011) A candidate dual vaccine against influenza and noroviruses. Vaccine 29: 7670-7677.
31. Tan M, Jiang X, (2012) The formation of P particle increased immunogenicity of norovirus P protein. Immunology 136: 28-29.
32. Ahlers JD, Belyakov IM, (2010) Memories that last forever: strategies for optimizing vaccine T-cell memory. Blood 115: 1678-1689.
33. Lees JR, Farber DL, (2010) Generation, persistence and plasticity of CD4 T-cell memories. Immunology 130: 463-470.
34. Aosai F, Rodriguez Pena MS, Mun HS, Fang H, Mitsunaga T, et al. (2006) Toxoplasma gondii-derived heat shock protein 70 stimulates maturation of murine bone marrow-derived dendritic cells via Toll-like receptor 4. Cell Stress Chaperones 11: 13-22.
35. Inaba K, Swiggard WJ, Steinman RM, Romani N, Schuler G, et al. (2009) Isolation of dendritic cells. Curr Protoc Immunol Chapter 3: Unit 3 7.
36. Fang H, Welte T, Zheng X, Chang GJ, Holbrook MR, et al. (2010) gammadelta T cells promote the maturation of dendritic cells during West Nile virus infection. FEMS Immunol Med Microbiol 59: 71-80.
37. Tacket CO, Sztein MB, Losonsky GA, Wasserman SS, Estes MK, (2003) Humoral, mucosal, and cellular immune responses to oral Norwalk virus-like particles in volunteers. Clin Immunol 108: 241-247.
38. Herbst-Kralovetz M, Mason HS, Chen Q, (2010) Norwalk virus-like particles as vaccines. Expert Rev Vaccines 9: 299-307.
39. 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.
40. Kubota T, Kumagai A, Ito H, Furukawa S, Someya Y, et al. (2012) Structural basis for the recognition of Lewis antigens by genogroup I norovirus. J Virol 86: 11138-11150.
41. LoBue AD, Lindesmith LC, Baric RS, (2010) Identification of cross-reactive norovirus CD4+ T cell epitopes. J Virol 84: 8530-8538.
42. Lindesmith L, Moe C, Marionneau S, Ruvoen N, Jiang X, et al. (2003) Human susceptibility and resistance to Norwalk virus infection. Nat Med 9: 548-553.
43. Tamminen K, Huhti L, Koho T, Lappalainen S, Hytonen VP, et al. (2012) A comparison of immunogenicity of norovirus GII-4 virus-like particles and P-particles. Immunology 135: 89-99.
44. Villadangos JA, Schnorrer P, (2007) Intrinsic and cooperative antigen-presenting functions of dendritic-cell subsets in vivo. Nat Rev Immunol 7: 543-555.
45. Platt CD, Ma JK, Chalouni C, Ebersold M, Bou-Reslan H, et al. (2010) Mature dendritic cells use endocytic receptors to capture and present antigens. Proc Natl Acad Sci U S A 107: 4287-4292.
46. Savina A, Amigorena S, (2007) Phagocytosis and antigen presentation in dendritic cells. Immunol Rev 219: 143-156.
47. Lim JP, Gleeson PA, (2011) Macropinocytosis: an endocytic pathway for internalising large gulps. Immunol Cell Biol 89: 836-843.