Pattern of activation of human antigen presenting cells by genotype GII.4 norovirus virus-like particles

Journal of Translational Medicine

Franco Maria Ruggeri²  Luigi Buonaguro¹  Franco Maria Buonaguro¹  Ilaria Di Bartolo²  Annacarmen Petrizzo¹  Eleonora Ponterio² 

[1] Laboratory of Molecular Biology and Viral Oncology, Department of Experimental Oncology, Istituto Nazionale per lo Studio e la Cura dei Tumori “Fondazione Pascale” - IRCCS, Via Mariano Semmola 142, Naples, 80131, Italy;Department of Veterinary Public Health and Food Safety, Istituto Superiore di Sanità, V.le Regina Elena, 299, 00161, Rome, Italy

关键词: VLPs;    PBMCs;    Immunology;    Norovirus;   

Others  :  827535
DOI  :  10.1186/1479-5876-11-127

 received in 2013-02-07, accepted in 2013-05-20,  发布年份 2013

【 摘 要 】

Background

Virus-like particles (VLPs) from an Italian GII.4 norovirus strain were used to investigate activation and maturation of circulating antigen presenting cells (APCs) of human origin.

Methods

Peripheral blood mononuclear cells (PBMCs) isolated from five healthy subjects were pulsed ex vivo with VLPs, and stained with a set of monoclonal antibodies (MAbs) for phenotypic analysis by flow cytometry. Cytokine release in cell supernatants was investigated by ELISA.

Results

Norovirus VLPs induced activation and maturation of circulating APCs derived from the five donors, as well as production of IL-6, IFN-γ and TNF-α cytokines.

Conclusions

The present results suggest that VLPs can activate antigen presenting cells for an efficient induction of the adaptive immune response.

【 授权许可】

   
2013 Ponterio et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

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【 参考文献 】

• [1]Estes MK, Prasad BV, Atmar RL: Noroviruses everywhere: has something changed? Curr Opin Infect Dis 2006, 19:467-474.
• [2]Bull RA, Eden JS, Luciani F, McElroy K, Rawlinson WD, White PA: Contribution of intra- and interhost dynamics to norovirus evolution. J Virol 2012, 86:3219-3229.
• [3]EFSAPanelonBiologicalHazards(BIOHAZ): Norovirus (NoV) in oysters: methods, limits and control options. EFSA J 2012, 10(1):2500. Available online: http://www.efsa.europa.eu/en/efsajournal/pub/2500.htm webcite
• [4]Glass RI, Parashar UD, Estes MK: Norovirus gastroenteritis. N Engl J Med 2009, 361:1776-1785.
• [5]Donaldson EF, Lindesmith LC, Lobue AD, Baric RS: Viral shape-shifting: norovirus evasion of the human immune system. Nat Rev Microbiol 2010, 8:231-241.
• [6]Gray JJ, Kohli E, Ruggeri FM, Vennema H, Sanchez-Fauquier A, Schreier E, Gallimore CI, Iturriza-Gomara M, Giraudon H, Pothier P: European multicenter evaluation of commercial enzyme immunoassays for detecting norovirus antigen in fecal samples. Clin Vaccine Immunol 2007, 14:1349-1355.
• [7]Estes MK, Ball JM, Guerrero RA, Opekun AR, Gilger MA, Pacheco SS, Graham DY: Norwalk virus vaccines: challenges and progress. J Infect Dis 2000, 181(Suppl 2):S367-373.
• [8]Lochridge VP, Jutila KL, Graff JW, Hardy ME: Epitopes in the P2 domain of norovirus VP1 recognized by monoclonal antibodies that block cell interactions. J Gen Virol 2005, 86:2799-2806.
• [9]Debbink K, Donaldson EF, Lindesmith LC, Baric RS: Genetic mapping of a highly variable norovirus GII.4 blockade epitope: potential role in escape from human herd immunity. J Virol 2012, 86:1214-1226.
• [10]Tan M, Jiang X: Association of histo-blood group antigens with susceptibility to norovirus infection may be strain-specific rather than genogroup dependent. J Infect Dis 2008, 198:940-941. author reply 942–943
• [11]Tan M, Jiang X: Norovirus gastroenteritis, carbohydrate receptors, and animal models. PLoS Pathog 2010, 6:e1000983.
• [12]Noad R, Roy P: Virus-like particles as immunogens. Trends Microbiol 2003, 11:438-444.
• [13]Buonaguro L, Tornesello ML, Tagliamonte M, Gallo RC, Wang LX, Kamin-Lewis R, Abdelwahab S, Lewis GK, Buonaguro FM: Baculovirus-derived human immunodeficiency virus type 1 virus-like particles activate dendritic cells and induce ex vivo T-cell responses. J Virol 2006, 80:9134-9143.
• [14]Harper DM: Preliminary HPV vaccine results for women older than 25 years. Lancet 2009, 373:1921-1922.
• [15]Zhou H, Guo L, Wang M, Qu J, Zhao Z, Wang J, Hung T: Prime immunization with rotavirus VLP 2/6 followed by boosting with an adenovirus expressing VP6 induces protective immunization against rotavirus in mice. Virol J 2011, 8:3.
• [16]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 2001, 75:9713-9722.
• [17]Tacket CO, Sztein MB, Losonsky GA, Wasserman SS, Estes MK: Humoral, mucosal, and cellular immune responses to oral Norwalk virus-like particles in volunteers. Clin Immunol 2003, 108:241-247.
• [18]Souza M, Cheetham SM, Azevedo MS, Costantini V, Saif LJ: Cytokine and antibody responses in gnotobiotic pigs after infection with human norovirus genogroup II.4 (HS66 strain). J Virol 2007, 81:9183-9192.
• [19]Atmar RL, Bernstein DI, Harro CD, Al-Ibrahim MS, Chen WH, Ferreira J, Estes MK, Graham DY, Opekun AR, Richardson C, Mendelman PM: Norovirus vaccine against experimental human Norwalk Virus illness. N Engl J Med 2011, 365:2178-2187.
• [20]Freer G, Matteucci D: Influence of dendritic cells on viral pathogenicity. PLoS Pathog 2009, 5:e1000384.
• [21]Steinman RM, Banchereau J: Taking dendritic cells into medicine. Nature 2007, 449:419-426.
• [22]Buonaguro L, Monaco A, Arico E, Wang E, Tornesello ML, Lewis GK, Marincola FM, Buonaguro FM: Gene expression profile of peripheral blood mononuclear cells in response to HIV-VLPs stimulation. BMC Bioinformatics 2008, 9(2):S5.
• [23]Arico E, Wang E, Tornesello ML, Tagliamonte M, Lewis GK, Marincola FM, Buonaguro FM, Buonaguro L: Immature monocyte derived dendritic cells gene expression profile in response to Virus-Like Particles stimulation. J Transl Med 2005, 3:45.
• [24]Buonaguro L, Petrizzo A, Tornesello M, Napolitano M, Martorelli D, Castello G, Beneduce G, De Renzo A, Perrella O, Romagnoli L: Immune signatures in human PBMCs of idiotypic vaccine for HCV-related lymphoproliferative disorders. J Transl Med 2010, 8:18.
• [25]Gaucher D, Therrien R, Kettaf N, Angermann BR, Boucher G, Filali-Mouhim A, Moser JM, Mehta RS, Drake DR 3rd, Castro E: Yellow fever vaccine induces integrated multilineage and polyfunctional immune responses. J Exp Med 2008, 205:3119-3131.
• [26]Monaco A, Marincola FM, Sabatino M, Pos Z, Tornesello ML, Stroncek DF, Wang E, Lewis GK, Buonaguro FM, Buonaguro L: Molecular immune signatures of HIV-1 vaccines in human PBMCs. FEBS Lett 2009, 583:3004-3008.
• [27]Boccia D, Tozzi AE, Cotter B, Rizzo C, Russo T, Buttinelli G, Caprioli A, Marziano ML, Ruggeri FM: Waterborne outbreak of Norwalk-like virus gastroenteritis at a tourist resort, Italy. Emerg Infect Dis 2002, 8:563-568.
• [28]Jiang X, Wang M, Graham DY, Estes MK: Expression, self-assembly, and antigenicity of the Norwalk virus capsid protein. J Virol 1992, 66:6527-6532.
• [29]Kenney SP, Pudupakam RS, Huang YW, Pierson FW, LeRoith T, Meng XJ: The PSAP motif within the ORF3 protein of an avian strain of the hepatitis E virus is not critical for viral infectivity in vivo but plays a role in virus release. J Virol 2012, 86:5637-5646.
• [30]Wheeler CM, Bautista OM, Tomassini JE, Nelson M, Sattler CA, Barr E: Protocol 11 study I: Safety and immunogenicity of co-administered quadrivalent human papillomavirus (HPV)-6/11/16/18 L1 virus-like particle (VLP) and hepatitis B (HBV) vaccines. Vaccine 2008, 26:686-696.
• [31]Kitamoto N, Tanaka T, Natori K, Takeda N, Nakata S, Jiang X, Estes MK: Cross-reactivity among several recombinant calicivirus virus-like particles (VLPs) with monoclonal antibodies obtained from mice immunized orally with one type of VLP. J Clin Microbiol 2002, 40:2459-2465.
• [32]Tanaka T, Kitamoto N, Jiang X, Estes MK: High efficiency cross-reactive monoclonal antibody production by oral immunization with recombinant norwalk virus-like particles. Microbiol Immunol 2006, 50:883-888.
• [33]Tamminen K, Huhti L, Koho T, Lappalainen S, Hytonen VP, Vesikari T, Blazevic V: A comparison of immunogenicity of norovirus GII-4 virus-like particles and P-particles. Immunology 2012, 135:89-99.
• [34]Lindesmith LC, Debbink K, Swanstrom J, Vinje J, Costantini V, Baric RS, Donaldson EF: Monoclonal antibody-based antigenic mapping of norovirus GII.4-2002. J Virol 2012, 86:873-883.
• [35]Lichtenegger FS, Mueller K, Otte B, Beck B, Hiddemann W, Schendel DJ, Subklewe M: CD86 and IL-12p70 are key players for T helper 1 polarization and natural killer cell activation by Toll-like receptor-induced dendritic cells. PLoS One 2012, 7:e44266.
• [36]Crow MK: Costimulatory molecules and T-cell-B-cell interactions. Rheum Dis Clin North Am 2004, 30:175-191. vii-viii
• [37]O'Sullivan B, Thomas R: CD40 and dendritic cell function. Crit Rev Immunol 2003, 23:83-107.
• [38]Braciale TJ, Morrison LA, Sweetser MT, Sambrook J, Gething MJ, Braciale VL: Antigen presentation pathways to class I and class II MHC-restricted T lymphocytes. Immunol Rev 1987, 98:95-114.
• [39]Lindesmith L, Moe C, Lependu J, Frelinger JA, Treanor J, Baric RS: Cellular and humoral immunity following Snow Mountain virus challenge. J Virol 2005, 79:2900-2909.
• [40]Souza M, Costantini V, Azevedo MS, Saif LJ: A human norovirus-like particle vaccine adjuvanted with ISCOM or mLT induces cytokine and antibody responses and protection to the homologous GII.4 human norovirus in a gnotobiotic pig disease model. Vaccine 2007, 25:8448-8459.
• [41]Nicollier-Jamot B, Pico V, Pothier P, Kohli E: Molecular cloning, expression, self-assembly, antigenicity, and seroepidemiology of a genogroup II norovirus isolated in France. J Clin Microbiol 2003, 41:3901-3904.
• [42]Periwal SB, Kourie KR, Ramachandaran N, Blakeney SJ, DeBruin S, Zhu D, Zamb TJ, Smith L, Udem S, Eldridge JH: A modified cholera holotoxin CT-E29H enhances systemic and mucosal immune responses to recombinant Norwalk virus-virus like particle vaccine. Vaccine 2003, 21:376-385.