Norovirus-specific memory T cell responses in adult human donors

Frontiers in Microbiology

Volumn 7, Issue OCT, 2016, Pages

  Malm, Maria ^a   Tamminen, Kirsi ^a   Vesikari, Timo ^a   Blazevic, Vesna ^a  

^a TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

Author keywords

Cellular immunity; ELISPOT IFN gamma; Norovirus; PBMC; Peptide pools; T cell epitope; VLP

Indexed keywords

DIMETHYL SULFOXIDE; EPITOPE; GAMMA INTERFERON; HLA A ANTIGEN; INTERLEUKIN 2; PROTEIN VP1; RECOMBINANT PROTEIN; SYNTHETIC PEPTIDE; TUMOR NECROSIS FACTOR;

ADULT; AMINO ACID SEQUENCE; ANTIBODY RESPONSE; ARTICLE; BLOOD DONOR; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; EPSTEIN BARR VIRUS; FLOW CYTOMETRY; GENOTYPE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CYTOMEGALOVIRUS; INFLUENZA VIRUS; MEMORY T LYMPHOCYTE; MONONUCLEAR CELL; NONHUMAN; NORMAL HUMAN; NOROVIRUS; SEROLOGY; SPODOPTERA FRUGIPERDA; STAINING; VIRUS LIKE AGENT;

EID: 84996939009     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.01570     Document Type: Article

References (74)

1. Atmar, R. L., Bernstein, D. I., Lyon, G. M., Treanor, J. J., Al-Ibrahim, M. S., Graham, D. Y., et al. (2015). Serological correlates of protection against a GII.4 Norovirus. Clin. Vaccine Immunol. 22, 923-929. doi: 10.1128/CVI.00196-15
2. Blazevic, V., Lappalainen, S., Nurminen, K., Huhti, L., and Vesikari, T. (2011). Norovirus VLPs and rotavirus VP6 protein as combined vaccine for childhood gastroenteritis. Vaccine 29, 8126-8133. doi: 10.1016/j.vaccine.2011.08.026
3. Blazevic, V., Malm, M., Honkanen, H., Knip, M., Hyoty, H., and Vesikari, T. (2015a). Development and maturation of norovirus antibodies in childhood. Microbes Infect. 18, 263-269. doi: 10.1016/j.micinf.2015.12.004
4. Blazevic, V., Malm, M., Salminen, M., Oikarinen, S., Hyoty, H., Veijola, R., et al. (2015b). Multiple consecutive norovirus infections in the first 2 years of life. Eur. J. Pediatr. 174, 1679-1683. doi: 10.1007/s00431-015-2591-8
5. Blazevic, V., Malm, M., and Vesikari, T. (2015c). Induction of homologous and cross-reactive GII.4-specific blocking antibodies in children after GII.4 new orleans norovirus infection. J. Med. Virol. 87, 1656-1661. doi: 10.1002/jmv.24237
6. Blazevic, V., Ranki, A., and Krohn, K. J. (1995). Helper and cytotoxic T cell responses of HIV type 1-infected individuals to synthetic peptides of HIV type 1 Rev. AIDS Res. Hum. Retroviruses 11, 1335-1342. doi: 10.1089/aid.1995.11.1335
7. Blazevic, V., Sahgal, N., Kessler, H. A., Landay, A. L., and Shearer, G. M. (2000). T cell responses to recall antigens, alloantigen, and mitogen of HIV-infected patients receiving long-term combined antiretroviral therapy. AIDS Res. Hum. Retroviruses 16, 1887-1893. doi: 10.1089/08892220050195847
8. Bok, K., Abente, E. J., Realpe-Quintero, M., Mitra, T., Sosnovtsev, S. V., Kapikian, A. Z., et al. (2009). Evolutionary dynamics of GII.4 noroviruses over a 34-year period. J. Virol. 83, 11890-11901. doi: 10.1128/JVI.00864-09
9. Bull, R. A., and White, P. A. (2011). Mechanisms of GII.4 norovirus evolution. Trends Microbiol. 19, 233-240. doi: 10.1016/j.tim.2011.01.002
10. Cao, S., Lou, Z., Tan, M., Chen, Y., Liu, Y., Zhang, Z., et al. (2007). Structural basis for the recognition of blood group trisaccharides by norovirus. J. Virol. 81, 5949-5957. doi: 10.1128/JVI.00219-07
11. Carmona-Vicente, N., Fernandez-Jimenez, M., Ribes, J. M., Tellez-Castillo, C. J., Khodayar-Pardo, P., Rodriguez-Diaz, J., et al. (2015). Norovirus infections and seroprevalence of genotype GII.4-specific antibodies in a Spanish population. J. Med. Virol. 87, 675-682. doi: 10.1002/jmv.24112
12. Chachu, K. A., LoBue, A. D., Strong, D. W., Baric, R. S., and Virgin, H. W. (2008). Immune mechanisms responsible for vaccination against and clearance of mucosal and lymphatic norovirus infection. PLoS Pathog. 4:e1000236. doi: 10.1371/journal.ppat.1000236
13. Currier, J. R., Kuta, E. G., Turk, E., Earhart, L. B., Loomis-Price, L., Janetzki, S., et al. (2002). A panel of MHC class I restricted viral peptides for use as a quality control for vaccine trial ELISPOT assays. J. Immunol. Methods 260, 157-172. doi: 10.1016/S0022-1759(01)00535-X
14. Eden, J. S., Hewitt, J., Lim, K. L., Boni, M. F., Merif, J., Greening, G., et al. (2014). The emergence and evolution of the novel epidemic norovirus GII.4 variant Sydney 2012. Virology 450-451, 106-113. doi: 10.1016/j.virol.2013.12.005
15. Ferrari, G., Neal, W., Ottinger, J., Jones, A. M., Edwards, B. H., Goepfert, P., et al. (2004). Absence of immunodominant anti-Gag p17 (SL9) responses among Gag CTL-positive, HIV-uninfected vaccine recipients expressing the HLA-A*0201 allele. J. Immunol. 173, 2126-2133. doi: 10.4049/jimmunol.173.3.2126
16. Freer, G., and Rindi, L. (2013). Intracellular cytokine detection by fluorescence-activated flow cytometry: basic principles and recent advances. Methods 61, 30-38. doi: 10.1016/j.ymeth.2013.03.035
17. Hall, A. J., Glass, R. I., and Parashar, U. D. (2016). New insights into the global burden of noroviruses and opportunities for prevention. Expert Rev. Vaccines 15, 949-951. doi: 10.1080/14760584.2016.1178069
18. Havelaar, A. H., Kirk, M. D., Torgerson, P. R., Gibb, H. J., Hald, T., Lake, R. J., et al. (2015). World Health Organization global estimates and regional comparisons of the burden of foodborne disease in 2010. PLoS Med. 12:e1001923. doi: 10.1371/journal.pmed.1001923
19. Hinkula, J., Ball, J. M., Lofgren, S., Estes, M. K., and Svensson, L. (1995). Antibody prevalence and immunoglobulin IgG subclass pattern to Norwalk virus in Sweden. J. Med. Virol. 47, 52-57. doi: 10.1002/jmv.1890470111
20. Huang, P., Farkas, T., Marionneau, S., Zhong, W., Ruvoen-Clouet, N., Morrow, A. L., et al. (2003). Noroviruses bind to human ABO, Lewis, and secretor histo-blood group antigens: identification of 4 distinct strain-specific patterns. J. Infect. Dis. 188, 19-31. doi: 10.1086/375742
21. Huhti, L., Blazevic, V., Nurminen, K., Koho, T., Hytonen, V. P., and Vesikari, T. (2010). A comparison of methods for purification and concentration of norovirus GII-4 capsid virus-like particles. Arch. Virol. 155, 1855-1858. doi: 10.1007/s00705-010-0768-z
22. Hutson, A. M., Atmar, R. L., Graham, D. Y., and Estes, M. K. (2002). Norwalk virus infection and disease is associated with ABO histo-blood group type. J. Infect. Dis. 185, 1335-1337. doi: 10.1086/339883
23. Jing, Y., Qian, Y., Huo, Y., Wang, L. P., and Jiang, X. (2000). Seroprevalence against Norwalk-like human caliciviruses in beijing. China. J. Med. Virol. 60, 97-101. doi: 10.1002/(SICI)1096-9071(200001)60:1<97::AID-JMV16>3.0.CO;2-D
24. Johnson, P. C., Mathewson, J. J., DuPont, H. L., and Greenberg, H. B. (1990). Multiple-challenge study of host susceptibility to Norwalk gastroenteritis in US adults. J. Infect. Dis. 161, 18-21. doi: 10.1093/infdis/161.1.18
25. Jones, M. K., Grau, K. R., Costantini, V., Kolawole, A. O., de Graaf, M., Freiden, P., et al. (2015). Human norovirus culture in B cells. Nat. Protoc. 10, 1939-1947. doi: 10.1038/nprot.2015.121
26. Kaufhold, R. M., Field, J. A., Caulfield, M. J., Wang, S., Joseph, H., Wooters, M. A., et al. (2005). Memory T-cell response to rotavirus detected with a gamma interferon enzyme-linked immunospot assay. J. Virol. 79, 5684-5694. doi: 10.1128/JVI.79.9.5684-5694.2005
27. Kern, F., Faulhaber, N., Frommel, C., Khatamzas, E., Prosch, S., Schonemann, C., et al. (2000). Analysis of CD8 T cell reactivity to cytomegalovirus using protein-spanning pools of overlapping pentadecapeptides. Eur. J. Immunol. 30, 1676-1682. doi: 10.1002/1521-4141(200006)30:6<1676::AID-IMMU1676>3.0.CO;2-V
28. Kiecker, F., Streitz, M., Ay, B., Cherepnev, G., Volk, H. D., Volkmer-Engert, R., et al. (2004). Analysis of antigen-specific T-cell responses with synthetic peptides-what kind of peptide for which purpose? Hum. Immunol. 65, 523-536. doi: 10.1016/j.humimm.2004.02.017
29. Kroneman, A., Vega, E., Vennema, H., Vinje, J., White, P. A., Hansman, G., et al. (2013). Proposal for a unified norovirus nomenclature and genotyping. Arch. Virol. 158, 2059-2068. doi: 10.1007/s00705-013-1708-5
30. Kutscher, S., Dembek, C. J., Allgayer, S., Heltai, S., Stadlbauer, B., Biswas, P., et al. (2008). The intracellular detection of MIP-1beta enhances the capacity to detect IFN-gamma mediated HIV-1-specific CD8 T-cell responses in a flow cytometric setting providing a sensitive alternative to the ELISPOT. AIDS Res. Ther. 5:22. doi: 10.1186/1742-6405-5-22
31. Kutscher, S., Dembek, C. J., Deckert, S., Russo, C., Korber, N., Bogner, J. R., et al. (2013). Overnight resting of PBMC changes functional signatures of antigen specific T-cell responses: impact for immune monitoring within clinical trials. PLoS ONE 8:e76215. doi: 10.1371/journal.pone.0076215
32. La Gruta, N. L., and Turner, S. J. (2014). T cell mediated immunity to influenza: mechanisms of viral control. Trends Immunol. 35, 396-402. doi: 10.1016/j.it.2014.06.004
33. Lartey, S., Pathirana, R. D., Zhou, F., Jul-Larsen, A., Montomoli, E., Wood, J., et al. (2015). Single dose vaccination of the ASO3-adjuvanted A(H1N1)pdm09 monovalent vaccine in health care workers elicits homologous and cross-reactive cellular and humoral responses to H1N1 strains. Hum. Vaccin. Immunother. 11, 1654-1662. doi: 10.1080/21645515.2015.1048939
34. Lindesmith, L., Moe, C., Lependu, J., Frelinger, J. A., Treanor, J., and Baric, R. S. (2005). Cellular and humoral immunity following Snow Mountain virus challenge. J. Virol. 79, 2900-2909. doi: 10.1128/JVI.79.5.2900-2909.2005
35. Lindesmith, L., Moe, C., Marionneau, S., Ruvoen, N., Jiang, X., Lindblad, L., et al. (2003). Human susceptibility and resistance to Norwalk virus infection. Nat. Med. 9, 548-553. doi: 10.1038/nm860
36. Lindesmith, L. C., Costantini, V., Swanstrom, J., Debbink, K., Donaldson, E. F., Vinje, J., et al. (2013). Emergence of a norovirus GII.4 strain correlates with changes in evolving blockade epitopes. J. Virol. 87, 2803-2813. doi: 10.1128/JVI.03106-12
37. Lindesmith, L. C., Donaldson, E., Leon, J., Moe, C. L., Frelinger, J. A., Johnston, R. E., et al. (2010). Heterotypic humoral and cellular immune responses following Norwalk virus infection. J. Virol. 84, 1800-1815. doi: 10.1128/JVI.02179-09
38. Lindesmith, L. C., Ferris, M. T., Mullan, C. W., Ferreira, J., Debbink, K., Swanstrom, J., et al. (2015). Broad blockade antibody responses in human volunteers after immunization with a multivalent norovirus VLP candidate vaccine: immunological analyses from a phase I clinical trial. PLoS Med. 12:e1001807. doi: 10.1371/journal.pmed.1001807
39. Lundegaard, C., Lamberth, K., Harndahl, M., Buus, S., Lund, O., and Nielsen, M. (2008). NetMHC-3.0: accurate web accessible predictions of human, mouse and monkey MHC class I affinities for peptides of length 8-11. Nucleic Acids Res. 36, W509-W512. doi: 10.1093/nar/gkn202
40. Mallard, E., Vernel-Pauillac, F., Velu, T., Lehmann, F., Abastado, J. P., Salcedo, M., et al. (2004). IL-2 production by virus-and tumor-specific human CD8 T cells is determined by their fine specificity. J. Immunol. 172, 3963-3970. doi: 10.4049/jimmunol.172.6.3963
41. Malm, M., Tamminen, K., Lappalainen, S., Uusi-Kerttula, H., Vesikari, T., and Blazevic, V. (2015). Genotype considerations for virus-like particle-based bivalent norovirus vaccine composition. Clin. Vaccine Immunol. 22, 656-663. doi: 10.1128/CVI.00015-15
42. Malm, M., Uusi-Kerttula, H., Vesikari, T., and Blazevic, V. (2014). High serum levels of norovirus genotype-specific blocking antibodies correlate with protection from infection in children. J. Infect. Dis. 210, 1755-1762. doi: 10.1093/infdis/jiu361
43. Matthews, J. E., Dickey, B. W., Miller, R. D., Felzer, J. R., Dawson, B. P., Lee, A. S., et al. (2012). The epidemiology of published norovirus outbreaks: a review of risk factors associated with attack rate and genogroup. Epidemiol. Infect. 140, 1161-1172. doi: 10.1017/S0950268812000234
44. McFarland, B. J., Sant, A. J., Lybrand, T. P., and Beeson, C. (1999). Ovalbumin(323-339) peptide binds to the major histocompatibility complex class II I-A(d) protein using two functionally distinct registers. Biochemistry 38, 16663-16670. doi: 10.1021/bi991393l
45. Meddows-Taylor, S., Shalekoff, S., Kuhn, L., Gray, G. E., and Tiemessen, C. T. (2007). Development of a whole blood intracellular cytokine staining assay for mapping CD4(+) and CD8(+) T-cell responses across the HIV-1 genome. J. Virol. Methods 144, 115-121. doi: 10.1016/j.jviromet.2007.04.004
46. Murphy, K., Travers, P., and Walport, M. (2007). "Chapter 3. Antigen recognition by B-cell and T-cell receptors," in Janeway's Immunobiology, 7th Edn, ed. E. Lawrence (New York, NY: Garland Science), 110-142.
47. Nielsen, M., Lundegaard, C., Worning, P., Lauemoller, S. L., Lamberth, K., Buus, S., et al. (2003). Reliable prediction of T-cell epitopes using neural networks with novel sequence representations. Protein Sci. 12, 1007-1017. doi: 10.1110/ps.0239403
48. Nurminen, K., Blazevic, V., Huhti, L., Rasanen, S., Koho, T., Hytonen, V. P., et al. (2011). Prevalence of norovirus GII-4 antibodies in Finnish children. J. Med. Virol. 83, 525-531. doi: 10.1002/jmv.21990
49. Pepperl, S., Benninger-Doring, G., Modrow, S., Wolf, H., and Jilg, W. (1998). Immediate-early transactivator Rta of Epstein-Barr virus (EBV) shows multiple epitopes recognized by EBV-specific cytotoxic T lymphocytes. J. Virol. 72, 8644-8649.
50. Peters, B., and Sette, A. (2005). Generating quantitative models describing the sequence specificity of biological processes with the stabilized matrix method. BMC Bioinformatics 6:132. doi: 10.1186/1471-2105-6-132
51. Prasad, B. V., Hardy, M. E., Dokland, T., Bella, J., Rossmann, M. G., and Estes, M. K. (1999). X-ray crystallographic structure of the Norwalk virus capsid. Science 286, 287-290. doi: 10.1126/science.286.5438.287
52. Ramani, S., Estes, M. K., and Atmar, R. L. (2016). Correlates of protection against Norovirus infection and disease-where are we now, where do we go? PLoS Pathog. 12:e1005334. doi: 10.1371/journal.ppat.1005334
53. Ramani, S., Neill, F. H., Opekun, A. R., Gilger, M. A., Graham, D. Y., Estes, M. K., et al. (2015). Mucosal and cellular immune responses to Norwalk virus. J. Infect. Dis. 212, 397-405. doi: 10.1093/infdis/jiv053
54. Reeck, A., Kavanagh, O., Estes, M. K., Opekun, A. R., Gilger, M. A., Graham, D. Y., et al. (2010). Serological correlate of protection against norovirus-induced gastroenteritis. J. Infect. Dis. 202, 1212-1218. doi: 10.1086/656364
55. Rockx, B., Baric, R. S., de Grijs, I., Duizer, E., and Koopmans, M. P. (2005). Characterization of the homo-and heterotypic immune responses after natural norovirus infection. J. Med. Virol. 77, 439-446. doi: 10.1002/jmv.20473
56. Rosenberg, E. S., Billingsley, J. M., Caliendo, A. M., Boswell, S. L., Sax, P. E., Kalams, S. A., et al. (1997). Vigorous HIV-1-specific CD4+ T cell responses associated with control of viremia. Science 278, 1447-1450. doi: 10.1126/science.278.5342.1447
57. Saito, M., Goel-Apaza, S., Espetia, S., Velasquez, D., Cabrera, L., Loli, S., et al. (2014). Multiple norovirus infections in a birth cohort in a Peruvian Periurban community. Clin. Infect. Dis. 58, 483-491. doi: 10.1093/cid/cit763
58. Schmittel, A., Keilholz, U., Bauer, S., Kuhne, U., Stevanovic, S., Thiel, E., et al. (2001). Application of the IFN-gamma ELISPOT assay to quantify T cell responses against proteins. J. Immunol. Methods 247, 17-24. doi: 10.1016/S0022-1759(00)00305-7
59. Seder, R. A., Darrah, P. A., and Roederer, M. (2008). T-cell quality in memory and protection: implications for vaccine design. Nat. Rev. Immunol. 8, 247-258. doi: 10.1038/nri2274
60. Siebenga, J. J., Vennema, H., Zheng, D. P., Vinje, J., Lee, B. E., Pang, X. L., et al. (2009). Norovirus illness is a global problem: emergence and spread of norovirus GII.4 variants, 2001-2007. J. Infect. Dis. 200, 802-812. doi: 10.1086/605127
61. Simmons, K., Gambhir, M., Leon, J., and Lopman, B. (2013). Duration of immunity to norovirus gastroenteritis. Emerg. Infect. Dis. 19, 1260-1267. doi: 10.3201/eid1908.130472
62. Stanley, M. (2006). Immune responses to human papillomavirus. Vaccine 24(Suppl. 1), S16-S22. doi: 10.1016/j.vaccine.2005.09.002
63. Streeck, H., Frahm, N., and Walker, B. D. (2009). The role of IFN-gamma Elispot assay in HIV vaccine research. Nat. Protoc. 4, 461-469. doi: 10.1038/nprot.2009.7
64. Tacket, C. O., Sztein, M. B., Losonsky, G. A., Wasserman, S. S., and Estes, M. K. (2003). Humoral, mucosal, and cellular immune responses to oral Norwalk virus-like particles in volunteers. Clin. Immunol. 108, 241-247. doi: 10.1016/S1521-6616(03)00120-7
65. Tamminen, K., Malm, M., Vesikari, T., and Blazevic, V. (2016). Mucosal antibodies induced by intranasal but not intramuscular immunization block Norovirus GII.4 virus-like particle receptor binding. Viral Immunol. 29, 315-319. doi: 10.1089/vim.2015.0141
66. Tassignon, J., Burny, W., Dahmani, S., Zhou, L., Stordeur, P., Byl, B., et al. (2005). Monitoring of cellular responses after vaccination against tetanus toxoid: comparison of the measurement of IFN-gamma production by ELISA, ELISPOT, flow cytometry and real-time PCR. J. Immunol. Methods 305, 188-198. doi: 10.1016/j.jim.2005.07.014
67. Tobery, T. W., Dubey, S. A., Anderson, K., Freed, D. C., Cox, K. S., Lin, J., et al. (2006). A comparison of standard immunogenicity assays for monitoring HIV type 1 gag-specific T cell responses in Ad5 HIV Type 1 gag vaccinated human subjects. AIDS Res. Hum. Retroviruses 22, 1081-1090. doi: 10.1089/aid.2006.22.1081
68. Tomov, V. T., Osborne, L. C., Dolfi, D. V., Sonnenberg, G. F., Monticelli, L. A., Mansfield, K., et al. (2013). Persistent enteric murine norovirus infection is associated with functionally suboptimal virus-specific CD8 T cell responses. J. Virol. 87, 7015-7031. doi: 10.1128/JVI.03389-12
69. Uusi-Kerttula, H., Tamminen, K., Malm, M., Vesikari, T., and Blazevic, V. (2014). Comparison of human saliva and synthetic histo-blood group antigens usage as ligands in norovirus-like particle binding and blocking assays. Microbes Infect. 16, 472-480. doi: 10.1016/j.micinf.2014.02.010
70. Vinje, J. (2015). Advances in laboratory methods for detection and typing of norovirus. J. Clin. Microbiol. 53, 373-381. doi: 10.1128/JCM.01535-14
71. Wilkinson, T. M., Li, C. K., Chui, C. S., Huang, A. K., Perkins, M., Liebner, J. C., et al. (2012). Preexisting influenza-specific CD4+ T cells correlate with disease protection against influenza challenge in humans. Nat. Med. 18, 274-280. doi: 10.1038/nm.2612
72. Wobus, C. E., Thackray, L. B., and Virgin, H. W. (2006). Murine norovirus: a model system to study norovirus biology and pathogenesis. J. Virol. 80, 5104-5112. doi: 10.1128/JVI.02346-05
73. Wyatt, R. G., Dolin, R., Blacklow, N. R., DuPont, H. L., Buscho, R. F., Thornhill, T. S., et al. (1974). Comparison of three agents of acute infectious nonbacterial gastroenteritis by cross-challenge in volunteers. J. Infect. Dis. 129, 709-714. doi: 10.1093/infdis/129.6.709
74. Zheng, D. P., Ando, T., Fankhauser, R. L., Beard, R. S., Glass, R. I., and Monroe, S. S. (2006). Norovirus classification and proposed strain nomenclature. Virology 346, 312-323. doi: 10.1016/j.virol.2005.11.015