1887

Journal of General Virology header logo

Volume 85, Issue 10

The glycoprotein of a fish rhabdovirus profiles the virus-specific T-cell repertoire in rainbow trout Free

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.

  • Received:
  • Accepted:
  • Published Online:
SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.80135-0
2004-10-01
2024-04-20
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 Roberts R. J. London: Academic Press;
     [Google Scholar]
  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, CD8 α , 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 Manning F. J., Tatner M. F. London: Academic Press;
     [Google Scholar]
  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
The glycoprotein of a fish rhabdovirus profiles the virus-specific T-cell repertoire in rainbow trout
J. Gen. Virol. 85, 3099 (2004); https://doi.org/10.1099/vir.0.80135-0
/content/journal/jgv/10.1099/vir.0.80135-0
/content/journal/jgv/10.1099/vir.0.80135-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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