1887

Abstract

T-cell responses to viruses are still poorly investigated in lower vertebrates. In rainbow trout, a specific clonal expansion of T cells in response to infection with viral haemorrhagic septicaemia virus (VHSV) was recently identified. Expanded T-cell clones expressed a unique 8 aa V4-J1 junction (SSGDSYSE) in different individuals, reminiscent of a typical public response. To get further insight into the nature of this response the modifications of the T-cell repertoire following immunization with plasmid expressing the VHSV external glycoprotein (G), which is the only protein involved in protective immunity, was analysed. After G-based DNA immunization, CDR3-length spectratypes were skewed for several V-J combinations, including V4-J1. In V4-J1, biases consisted of 6 and 8 aa junctions that were detected from day 52, and were still present 3 months after DNA immunization. Sequence analysis of the V4-J1 junctions showed that the 8 aa junction (SSGDSYSE) was clearly expanded, indicating that viral G protein was probably the target of the anti-VHSV public response. Additional 6 and 8 aa V4-J1 junctions were also expanded in G-DNA-vaccinated fish, showing that significant clonotypic diversity was selected in response to the plasmid-delivered G protein. This higher clonotypic diversity may be related to the demonstrated higher efficiency of G-based DNA vaccines over whole virus immunization. The use of infectious hematopietic necrosis virus (IHNV) recombinant viruses, expressing the VHSV G protein, further substantiated the VHSV G-protein specificity of the 8 aa V4-J1 response and designated the 6 aa V4-J1 response as potentially directed to a T-cell epitope common to VHSV and IHNV.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.80135-0
2004-10-01
2020-01-21
Loading full text...

Full text loading...

/deliver/fulltext/jgv/85/10/vir853099.html?itemId=/content/journal/jgv/10.1099/vir.0.80135-0&mimeType=html&fmt=ahah

References

  1. Anderson, E. D., Mourich, D. V., Fahrenkrug, S. C., LaPatra, S., Shepherd, J. & Leong, J. A. ( 1996; ). Genetic immunization of rainbow trout (Oncorhynchus mykiss) against infectious hematopoietic necrosis virus. Mol Mar Biol Biotechnol 5, 114–122.
    [Google Scholar]
  2. Basurco, B. & Benmansour, A. ( 1995; ). Distant strains of the fish rhabdovirus VHSV maintain a sixth functional cistron which codes for a nonstructural protein of unknown function. Virology 212, 741–745.[CrossRef]
    [Google Scholar]
  3. Benmansour, A., Paubert, G., Bernard, J. & de Kinkelin, P. ( 1994; ). The polymerase-associated protein (M1) and the matrix protein (M2) from a virulent and an avirulent strain of viral hemorrhagic septicemia virus (VHSV), a fish rhabdovirus. Virology 198, 602–612.[CrossRef]
    [Google Scholar]
  4. Bernard, J., Lecocq-Xhonneux, F., Rossius, M., Thiry, M. E. & de Kinkelin, P. ( 1990; ). Cloning and sequencing the messenger RNA of the N gene of viral haemorrhagic septicaemia virus. J Gen Virol 71, 1669–1674.[CrossRef]
    [Google Scholar]
  5. Biacchesi, S., Thoulouze, M. I., Bearzotti, M., Yu, Y. X. & Bremont, M. ( 2000a; ). Recovery of NV knockout infectious hematopoietic necrosis virus expressing foreign genes. J Virol 74, 11247–11253.[CrossRef]
    [Google Scholar]
  6. Biacchesi, S., Yu, Y. X., Bearzotti, M., Tafalla, C., Fernandez-Alonso, M. & Bremont, M. ( 2000b; ). Rescue of synthetic salmonid rhabdovirus minigenomes. J Gen Virol 81, 1941–1945.
    [Google Scholar]
  7. Biacchesi, S., Bearzotti, M., Bouguyon, E. & Bremont, M. ( 2002; ). Heterologous exchanges of the glycoprotein and the matrix protein in a Novirhabdovirus. J Virol 76, 2881–2889.[CrossRef]
    [Google Scholar]
  8. Blattman, J. N., Sourdive, D. J., Murali-Krishna, K., Ahmed, R. & Altman, J. D. ( 2000; ). Evolution of the T cell repertoire during primary, memory, and recall responses to viral infection. J Immunol 165, 6081–6090.[CrossRef]
    [Google Scholar]
  9. Boudinot, P., Blanco, M., de Kinkelin, P. & Benmansour, A. ( 1998; ). Combined DNA immunization with the glycoprotein gene of viral hemorrhagic septicemia virus and infectious hematopoietic necrosis virus induces double-specific protective immunity and nonspecific response in rainbow trout. Virology 249, 297–306.[CrossRef]
    [Google Scholar]
  10. Boudinot, P., Boubekeur, S. & Benmansour, A. ( 2001; ). Rhabdovirus infection induces public and private T cell responses in teleost fish. J Immunol 167, 6202–6209.[CrossRef]
    [Google Scholar]
  11. Bousso, P., Casrouge, A., Altman, J. D., Haury, M., Kanellopoulos, J., Abastado, J. P. & Kourilsky, P. ( 1998; ). Individual variations in the murine T cell response to a specific peptide reflect variability in naive repertoires. Immunity 9, 169–178.[CrossRef]
    [Google Scholar]
  12. Chen, W., Anton, L. C., Bennink, J. R. & Yewdell, J. W. ( 2000; ). Dissecting the multifactorial causes of immunodominance in class I-restricted T cell responses to viruses. Immunity 12, 83–93.[CrossRef]
    [Google Scholar]
  13. Collette, A. & Six, A. ( 2002; ). ISEApeaks: an Excel platform for GeneScan and Immunoscope data retrieval, management and analysis. Bioinformatics 18, 329–330.[CrossRef]
    [Google Scholar]
  14. Corbeil, S., LaPatra, S. E., Anderson, E. D., Jones, J., Vincent, B., Hsu, Y. L. & Kurath, G. ( 1999; ). Evaluation of the protective immunogenicity of the N, P, M, NV and G proteins of infectious hematopoietic necrosis virus in rainbow trout Oncorhynchus mykiss using DNA vaccines. Dis Aquat Org 39, 29–36.[CrossRef]
    [Google Scholar]
  15. de Kinkelin, P., Bearzotti-Le Berre, M. & Bernard, J. ( 1980; ). Viral hemorrhagic septicemia of rainbow trout: selection of a thermoresistant virus variant and comparison of polypeptide synthesis with the wild-type virus strain. J Virol 36, 652–658.
    [Google Scholar]
  16. Diter, A., Quillet, E. & Chourrout, D. ( 1993; ). Suppression of first egg mitosis induced by heat shocks in the rainbow trout. J Fish Biol 42, 777–786.[CrossRef]
    [Google Scholar]
  17. Donnelly, J. J., Ulmer, J. B. & Liu, M. A. ( 1997; ). DNA vaccines. Life Sci 60, 163–172.
    [Google Scholar]
  18. Ellis, A. E. ( 1982; ). Differences between the immune mechanisms of fish and higher vertebrates. In Microbial Diseases of Fish, pp. 1–29. Edited by R. J. Roberts. London: Academic Press.
  19. Engelking, H. M. & Leong, J. C. ( 1989; ). The glycoprotein of infectious hematopoietic necrosis virus elicits neutralizing antibody and protective responses. Virus Res 13, 213–230.[CrossRef]
    [Google Scholar]
  20. Fischer, U., Ototake, M. & Nakanishi, T. ( 1998; ). In vitro cell-mediated cytotoxicity against allogeneic erythrocytes in ginbuna crucian carp and goldfish using a non-radioactive assay. Dev Comp Immunol 22, 195–206.[CrossRef]
    [Google Scholar]
  21. Fischer, U., Utke, K., Ototake, M., Dijkstra, J. M. & Kollner, B. ( 2003; ). Adaptive cell-mediated cytotoxicity against allogeneic targets by CD8-positive lymphocytes of rainbow trout (Oncorhynchus mykiss). Dev Comp Immunol 27, 323–337.[CrossRef]
    [Google Scholar]
  22. Hansen, J. D. & Strassburger, P. ( 2000; ). Description of an ectothermic TCR coreceptor, CD8α, in rainbow trout. J Immunol 164, 3132–3139.[CrossRef]
    [Google Scholar]
  23. Heppell, J., Lorenzen, N., Armstrong, N. K., Tong, W., Lorenzen, E., Einer-Jensen, K., Schorr, J. & Davis, H. L. ( 1998; ). Development of DNA vaccines for fish: vector design, intramuscular injection and antigen expression using viral haemorrhagic septicaemia virus genes as model. Fish Shellfish Immunol 8, 271–286.[CrossRef]
    [Google Scholar]
  24. Ingram, G. A. ( 1985; ). The immune response of brown trout, Salmo trutta, to sheep and human ‘O’ erythrocytes. In Fish Immunology, pp. 157–170. Edited by F. J. Manning & M. F. Tatner. London: Academic Press.
  25. Kang, J. A., Mohindru, M., Kang, B. S., Park, S. H. & Kim, B. S. ( 2000; ). Clonal expansion of infiltrating T cells in the spinal cords of SJL/J mice infected with Theiler's virus. J Immunol 165, 583–590.[CrossRef]
    [Google Scholar]
  26. Kharbanda, M., Than, S., Chitnis, V., Sun, M., Chavan, S., Bakshi, S. & Pahwa, S. ( 2000; ). Patterns of CD8 T cell clonal dominance in response to change in antiretroviral therapy in HIV-infected children. AIDS 14, 2229–2238.[CrossRef]
    [Google Scholar]
  27. Kim, C. H., Johnson, M. C., Drennan, J. D., Simon, B. E., Thomann, E. & Leong, J. A. ( 2000; ). DNA vaccines encoding viral glycoproteins induce nonspecific immunity and Mx protein synthesis in fish. J Virol 74, 7048–7054.[CrossRef]
    [Google Scholar]
  28. Kostense, S., Raaphorst, F. M., Joling, J. & 7 other authors ( 2001; ). T cell expansions in lymph nodes and peripheral blood in HIV-1-infected individuals: effect of antiretroviral therapy. AIDS 15, 1097–1107.[CrossRef]
    [Google Scholar]
  29. Kou, Z. C., Puhr, J. S., Wu, S. S., Goodenow, M. M. & Sleasman, J. W. ( 2003; ). Combination antiretroviral therapy results in a rapid increase in T cell receptor variable region β repertoire diversity within CD45RA CD8 T cells in human immunodeficiency virus-infected children. J Infect Dis 187, 385–397.[CrossRef]
    [Google Scholar]
  30. Kurath, G. & Leong, J. C. ( 1985; ). Characterization of infectious hematopoietic necrosis virus mRNA species reveals a nonvirion rhabdovirus protein. J Virol 53, 462–468.
    [Google Scholar]
  31. Kurath, G., Ahern, K. G., Pearson, G. D. & Leong, J. C. ( 1985; ). Molecular cloning of the six mRNA species of infectious hematopoietic necrosis virus, a fish rhabdovirus, and gene order determination by R-loop mapping. J Virol 53, 469–476.
    [Google Scholar]
  32. Lin, M. Y. & Welsh, R. M. ( 1998; ). Stability and diversity of T cell receptor repertoire usage during lymphocytic choriomeningitis virus infection of mice. J Exp Med 188, 1993–2005.[CrossRef]
    [Google Scholar]
  33. Lorenzen, N., Olesen, N. J. & Jorgensen, P. E. ( 1990; ). Neutralization of Egtved virus pathogenicity to cell cultures and fish by monoclonal antibodies to the viral G protein. J Gen Virol 71, 561–567.[CrossRef]
    [Google Scholar]
  34. Lorenzen, N., Lorenzen, E., Einer-Jensen, K., Heppell, J., Wu, T. & Davis, H. ( 1998; ). Protective immunity to VHS in rainbow trout (Oncorhynchus mykiss, Walbaum) following DNA vaccination. Fish Shellfish Immunol 8, 261–270.[CrossRef]
    [Google Scholar]
  35. Lorenzen, N., Lorenzen, E., Einer-Jensen, K. & LaPatra, S. E. ( 2002; ). DNA vaccines as a tool for analysing the protective immune response against rhabdoviruses in rainbow trout. Fish Shellfish Immunol 12, 439–453.[CrossRef]
    [Google Scholar]
  36. Messaoudi, I., Guevara Patino, J. A., Dyall, R., LeMaoult, J. & Nikolich-Zugich, J. ( 2002; ). Direct link between mhc polymorphism, T cell avidity, and diversity in immune defense. Science 298, 1797–1800.[CrossRef]
    [Google Scholar]
  37. Miller, N. W., Deuter, A. & Clem, L. W. ( 1986; ). Phylogeny of lymphocyte heterogeneity: the cellular requirements for the mixed leucocyte reaction with channel catfish. Immunology 59, 123–128.
    [Google Scholar]
  38. Oldstone, M. B., Lewicki, H., Homann, D., Nguyen, C., Julien, S. & Gairin, J. E. ( 2001; ). Common antiviral cytotoxic T-lymphocyte epitope for diverse arenaviruses. J Virol 75, 6273–6278.[CrossRef]
    [Google Scholar]
  39. Palmowski, M. J., Choi, E. M., Hermans, I. F. & 10 other authors ( 2002; ). Competition between CTL narrows the immune response induced by prime-boost vaccination protocols. J Immunol 168, 4391–4398.[CrossRef]
    [Google Scholar]
  40. Pannetier, C., Even, J. & Kourilsky, P. ( 1995; ). T-cell repertoire diversity and clonal expansions in normal and clinical samples. Immunol Today 16, 176–181.[CrossRef]
    [Google Scholar]
  41. Peacock, C. D., Lin, M. Y., Ortaldo, J. R. & Welsh, R. M. ( 2000; ). The virus-specific and allospecific cytotoxic T-lymphocyte response to lymphocytic choriomeningitis virus is modified in a subpopulation of CD8+ T cells coexpressing the inhibitory major histocompatibility complex class I receptor Ly49G2. J Virol 74, 7032–7038.[CrossRef]
    [Google Scholar]
  42. Saito, M., Higuchi, I., Saito, A., Izumo, S., Usuku, K., Bangham, C. R. & Osame, M. ( 2002; ). Molecular analysis of T cell clonotypes in muscle-infiltrating lymphocytes from patients with human T lymphotropic virus type 1 polymyositis. J Infect Dis 186, 1231–1241.[CrossRef]
    [Google Scholar]
  43. Schütze, H., Enzmann, P. -J., Kuchling, R., Mundt, E., Niemann, H. & Mettenleiter, T. C. ( 1995; ). Complete genomic sequence of the fish rhabdovirus infectious haematopoietic necrosis virus. J Gen Virol 76, 2519–2527.[CrossRef]
    [Google Scholar]
  44. Schütze, H., Mundt, E. & Mettenleiter, T. C. ( 1999; ). Complete genomic sequence of viral hemorrhagic septicemia virus, a fish rhabdovirus. Virus Genes 19, 59–65.[CrossRef]
    [Google Scholar]
  45. Selin, L. K., Lin, M. Y., Kraemer, K. A., Pardoll, D. M., Schneck, J. P., Varga, S. M., Santolucito, P. A., Pinto, A. K. & Welsh, R. M. ( 1999; ). Attrition of T cell memory: selective loss of LCMV epitope-specific memory CD8 T cells following infections with heterologous viruses. Immunity 11, 733–742.[CrossRef]
    [Google Scholar]
  46. Sing, G. K., Li, D., Chen, X., Macnaughton, T., Lichanska, A. M., Butterworth, L., Ladhams, A. & Cooksley, G. ( 2001; ). A molecular comparison of T lymphocyte populations infiltrating the liver and circulating in the blood of patients with chronic hepatitis B: evidence for antigen-driven selection of a public complementarity-determining region 3 (CDR3) motif. Hepatology 33, 1288–1298.[CrossRef]
    [Google Scholar]
  47. Sourdive, D. J., Murali-Krishna, K., Altman, J. D. & 7 other authors ( 1998; ). Conserved T cell receptor repertoire in primary and memory CD8 T cell responses to an acute viral infection. J Exp Med 188, 71–82.[CrossRef]
    [Google Scholar]
  48. Stuge, T. B., Wilson, M. R., Zhou, H., Barker, K. S., Bengten, E., Chinchar, G., Miller, N. W. & Clem, L. W. ( 2000; ). Development and analysis of various clonal alloantigen-dependent cytotoxic cell lines from channel catfish. J Immunol 164, 2971–2977.[CrossRef]
    [Google Scholar]
  49. Thiry, M., Lecocq-Xhonneux, F., Dheur, I., Renard, A. & de Kinkelin, P. ( 1990; ). Molecular cloning of the mRNA coding for the G protein of the viral haemorrhagic septicaemia (VHS) of salmonids. Vet Microbiol 23, 221–226.[CrossRef]
    [Google Scholar]
  50. Umemura, T., Yoshizawa, K., Ota, M., Katsuyama, Y., Inada, H., Tanaka, E. & Kiyosawa, K. ( 2000; ). Analysis of T cell repertoire in the liver of patients with chronic hepatitis C. Clin Exp Immunol 121, 120–126.[CrossRef]
    [Google Scholar]
  51. Vogel, T. U., Horton, H., Fuller, D. H. & 10 other authors ( 2002; ). Differences between T cell epitopes recognized after immunization and after infection. J Immunol 169, 4511–4521.[CrossRef]
    [Google Scholar]
  52. Xiang, Z. Q., Spitalnik, S., Tran, M., Wunner, W. H., Cheng, J. & Ertl, H. C. ( 1994; ). Vaccination with a plasmid vector carrying the rabies virus glycoprotein gene induces protective immunity against rabies virus. Virology 199, 132–140.[CrossRef]
    [Google Scholar]
  53. Yewdell, J. W. & Bennink, J. R. ( 1999; ). Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annu Rev Immunol 17, 51–88.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.80135-0
Loading
/content/journal/jgv/10.1099/vir.0.80135-0
Loading

Data & Media loading...

Most cited articles

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error