Evidence for the persistence of monoclonal expansions of CD8+ T cells following primary simian immunodeficiency virus infection
Jamie D. K. Wilson
Molecular Immunology Group, Institute of Molecular Medicine, John Radcliffe Hospital, Oxford, GB
Search for more papers by this authorMartin Cranage
Centre for Applied Microbiology & Research (CAMR), Porton Down, Salisbury, GB
Search for more papers by this authorNicola Cook
Centre for Applied Microbiology & Research (CAMR), Porton Down, Salisbury, GB
Search for more papers by this authorSharon Leech
Centre for Applied Microbiology & Research (CAMR), Porton Down, Salisbury, GB
Search for more papers by this authorAndrew J. McMichael
Molecular Immunology Group, Institute of Molecular Medicine, John Radcliffe Hospital, Oxford, GB
Search for more papers by this authorMargaret F. C. Callan
Molecular Immunology Group, Institute of Molecular Medicine, John Radcliffe Hospital, Oxford, GB
Search for more papers by this authorJamie D. K. Wilson
Molecular Immunology Group, Institute of Molecular Medicine, John Radcliffe Hospital, Oxford, GB
Search for more papers by this authorMartin Cranage
Centre for Applied Microbiology & Research (CAMR), Porton Down, Salisbury, GB
Search for more papers by this authorNicola Cook
Centre for Applied Microbiology & Research (CAMR), Porton Down, Salisbury, GB
Search for more papers by this authorSharon Leech
Centre for Applied Microbiology & Research (CAMR), Porton Down, Salisbury, GB
Search for more papers by this authorAndrew J. McMichael
Molecular Immunology Group, Institute of Molecular Medicine, John Radcliffe Hospital, Oxford, GB
Search for more papers by this authorMargaret F. C. Callan
Molecular Immunology Group, Institute of Molecular Medicine, John Radcliffe Hospital, Oxford, GB
Search for more papers by this authorAbstract
A longitudinal study of the CD8+ TCR variable (Vβ) chain repertoire was performed in rhesus macaques experimentally infected with simian immunodeficiency virus (SIV) using both TCR Vβ chain-specific monoclonal antibodies and TCR β chain CDR3 length analysis. Expansions of subpopulations of CD8+ T cells were detected during the acute phase of SIV infection. In all monkeys studied, monoclonal expansions persisted for at least 18 months and increasingly dominated the repertoire of CD8+ T cells expressing the relevant Vβ chain. This study shows that persistent CD8+ T cell expansions develop in response to a virus infection. This is important not only for our understanding of the T cell response to viruses but also for understanding the factors that determine the normal CD8+ TCR repertoire.
References
- 1 Koup, R. A., Safrit, J. T., Cao, Y., Andres, C. A., Wu, Y., McLeod, G., Borkowsky, W., Farthing, C. and Ho, D. D., Temporal association of cellular immune response with the initial control of viremia in primary HIV-1 syndrome. J. Virol. 1994. 67: 1707–1711.
- 2 Moss, P. A. H., Rowland-Jones, S. L., Frodsham, P. M., McAdam, S., Giangrande, P., McMichael, A. J. and Bell, J. I., Persistent high frequency of human immunodeficiency virus-specific cytotoxic T cells in peripheral blood of infected donors. Proc. Natl. Acad. Sci. USA 1995. 92: 5773–5777.
- 3 Price, D. A., Goulder, P. J., Klenerman, P., Sewell, A. K., Easterbrook, P. J., Troop, M. and Bangham, C. R., Positive selection of HIV-1 cytotoxic T lymphocyte escape variants during primary infection. Proc. Natl. Acad. Sci. USA 1997. 94: 1890–1895.
- 4 Goulder, P. J., Phillips, R. E., Colbert, R. A., McAdam, S., Ogg, G., Nowak, M. A., Giangrande, P., Luzzi, G., Morgan, B., Edwards, A., McMichael, A. J. and Rowland-Jones, S., Late escape from an immunodominant cytotoxic T lymphocyte response associated with progression to AIDS. Nature Med. 1997. 3: 212–217.
- 5 Rowland-Jones, S., Sutton, J., Ariyoshi, K., Dong, T., Gotch, F., McAdam, S., Whitby, D., Sabally, S., Gallimore, A., Corrah, T., Takiguchi, M., Schultz, T., McMichael, A. J. and Whittle, H., HIV-specific cytotoxic T cells in HIV exposed but unifected Gambian women. Nature Med. 1995. 1: 59–64.
- 6 Pantaleo, G., Demarest, J. F., Soudeyns, H., Grazios, C., Denis, F., Adelsberger, J. W., Borrow, P., Saag, M. S., Shaw, G. M., Sekaly, R. P. and Fauci, A. S., Major expansion of CD8+ T cells with a predominant Vβ usage during the primary immune response to HIV. Nature 1994. 370: 463–467.
- 7 Callan, M. F. C., Steven, N., Krausa, P., Wilson, J. D. K., Moss, P. A. H., Gillespie, G. M., Bell, J. I., Rickinson, A. B. and McMichael, A. J., Large clonal expansions of CD8+ T cells in acute infectious mononucleosis. Nature Med. 1996. 2: 906–911.
- 8 Pantaleo, G., Soudeyns, H., Demarest, J. F., Vaccarezza, M., Graziosi, C., Paolucci, S., Daucher, M., Cohen, O. J., Denis, F., Biddison, W. E., Sekaly, R. P. and Fauci, A. S., Evidence for the rapid disappearance of initially expanded HIV-specific CD8+ T cell clones during primary HIV infection. Proc. Natl. Acad. Sci. USA 1997. 94: 9848–9853.
- 9 Chen, Z. W., Kou, Z. C., Lekutis, C., Shen, L., Zhou, D., Halloran, M., Li, J., Sodroski, J., Lee-Parritz, D. and Letvin, N. L., T cell receptor Vβ repertoire in an acute infection of Rhesus Monkeys with Simian Immunodeficiency Viruses and a Chimeric Simian-Human Immunodeficiency Virus. J. Exp. Med. 1995. 182: 21–31.
- 10 Monteiro, J., Hingorani, R., Choi, I.-H., Silvler, J., Pergolizzi, R. and Gregersen, P. K., Oligoclonality in the human CD8+ T cell repertoire in normal subjects and monozygotic twins: Implications for studies of infectious and autoimmune diseases. Mol. Med. 1995. 1: 614–624.
- 11 Batliwalla, F., Hingorani, R. and Gregersen, P. K., Reactivity of TCR mAbs with primate cells. The Immunologist 1996. 4: 111–112.
- 12 Garcia, K. C., Degan, M., Stanfield, R. L., Brunmark, A., Jackson, M. R., Peterson, P. A., Teyton, L. and Wilson, I. A., An alpha-beta T cell receptor structure at 2.5 A and its orientation in the TCR-MHC complex. Science 1996. 274: 209–219.
- 13 Garboczi, D. N., Ghosh, P., Utz, U., Fan, Q. R., Biddison, W. E. and Wiley, D. C., Structure of the complex between human T cell receptor, viral peptide and HLA-A2. Nature 1996. 384: 134–141.
- 14 McHeyzer-Williams, M. G. and Davis, M. M., Antigen specific development of primary and memory T cells in vivo. Science 1995. 268: 106–111.
- 15 Moss, P. A. H., Moots, R. J., Rosenberg, W. M. C., Rowland-Jones, S. J., Bodmer, H. C., McMichael, A. J. and Bell, J. I., Extensive conservation of alpha and beta chains of the human T-cell antigen receptor recognising HLA A-2 and influenza A matrix peptide. Proc. Natl. Acad. Sci. USA 1991. 88: 8987–8990.
- 16 Callan, M. F. C., Reyburn, H. T., Bowness, P., Rowland-Jones, S., Bell, J. I. and McMichael, A. J., Selection of T cell receptor variable gene-encoded amino acids on the third binding site loop: a factor influencing variable chain selection in a T cell response. Eur. J. Immunol. 1995. 25: 1529–1534.
- 17 Pannetier, C., Even, J. and Kourilsky, P., T-cell repertoire and clonal expansions in normal and clinical samples. Immunol. Today 1995. 16: 176–181.
- 18 Miyawaki, T., Uehara, T., Nivu, R., Tsuji, T., Yachie, A., Yonehara, S. and Taniguchi, N., Differential expression of apoptosis-related fas antigen on lymphocyte subpopulations in human peripheral blood. J. Immunol. 1992. 149: 3753–3758.
- 19 Tamaru, Y., Miyawaki, T., Iwai, K., Tsuji, T., Nivu, R., Yachie, A., Koizumi, S. and Taniguchi, N., Absence of bcl-2 expression by activated CD45RO+ T lymphocytes in acute infectious mononucleosis supporting their susceptibility to programmed cell death. Blood 1993. 82: 521–527.
- 20 Akbar, A. N., Borthwick, N., Salmon, M., Gombert, W., Shamsadeen, M., Pilling, D., Pett, S., Grundy, J. E. and Janossy, G., The significance of low bcl-2 expression by CD45RO T cells in normal individuals and patients with acute viral infections. The role of apoptosis in T cell memory. J. Exp. Med. 1993. 178: 427–438.
- 21 Kalams, S. A., Johnson, R. P., Trocha, A. K., Dynan, M. J., Ngo, H. S., D'Aquila, A. K., Kurnick, J. T. and Walker, B. D., Longitudinal analysis of T cell receptor (TCR) gene usage by Human Immunodeficiency Virus 1 envelope-specific cytotoxic T lymphocyte clones reveals a limited TCR repertoire. J. Exp. Med. 1994. 179: 1261–1271.
- 22 Dupuy, D'Agneac., Moier, A. S., Pilling, D., Travaglio-Encinoza, A., Reme, T. and Salmon, M., CD57+ T lymphocytes are derived from CD57-precursors by differentiation occurring in late immune responses. Eur. J. Immunol. 1994. 24: 1503–1511.
- 23 Posnett, D. N., Sinha, R., Kabak, S. and Russo, C., Clonal populations of T cells in normal elderly humans: The T cell equivalent to “benign monoclonal gammopathy”. J. Exp. Med. 1994. 179: 609–618.
- 24 Hingorani, R., Choi, I. H., Alkolar, P., Gulwani-Akolkar, B., Silver, J. and Gregersen, P. K., Clonal predominance of T cell receptors within the CD8+, CD45RO+ subset in normal human subjects. J. Immunol. 1993. 151: 5726–5769.
- 25 Monteiro, J., Batliwalla, F., Ostrer, H. and Gregersen, P. K., Shortened telomeres in clonally expanded CD28-CD8+ T cells imply a replicative history that is distinct from their CD28+CD8+ counterparts. J. Immunol. 1996. 156: 3587–3590.
- 26 Roueau, M., Bernard, A., Lantz, O., Vernant, J. P., Charpentier, B. and Senik, A., Apoptosis of activated CDS positive/CD57 positive T cells in induced by some combinations of anti-CDE2 mAb. J. Immunol. 1993. 151: 3547–3556.
- 27 Morley, J. K., Batliwalla, F. M., Hingorani, R. and Gregersen, P. K., Oligoclonal CD8+ T cells are preferentially expanded in the CD57+ subset. J. Immunol. 1995. 154: 6182–6190.
- 28 Polyanskaya, N., Sharpe, S., Cook, N., Leech, S., Banks, J., Dennis, M., Hall, G., Stott, J. and Cranage, M., Anti-major histocompatibility complex antibody responses to simian B cells do not protect macaques against SIVmac infection. AIDS Res. Hum. Retroviruses 1997. 13: 923–931.
- 29 Cranage, M. P., Whatmore, A. M., Sharpe, S. A., Cook, N., Polyanskaya, N., Leech, S., Smith, J. D., Rud, E. W., Dennis, M. J. and Hall, G. A., Macaques infected with live attenuated SIVmac are protected against superinfection via the rectal mucosa. Virology 1997. 229: 143–154.
- 30
Kärber, G.,
Beitrag zur kollektiven Behandlung pharma-kologischer Reihenversuche.
Arch. Exp. Pathol. Pharmakol.
1931.
162: 956–959.
10.1007/BF01863914 Google Scholar
- 31 Posnett, D. N., Romagne, F., Necker, A., Kotzin, B. L. and Sekaly, R.-P., First human TCR monoclonal antibody workshop. The Immunologist 1996. 4: 5–8.
- 32 Levinson, G., Hughes, A. L. and Letvin, N. L., Sequence and diversity of rhesus monkey T cell receptor p chain genes. Immunogenetics 1992. 35: 75–88.
- 33 Cheynier, R., Henrichward, S. and Wain-Hobson, S., Sequence of the rhesus monkey T cell receptor β chain diversity and joining loci. Immunogenetics 1995. 43: 83–87.