Conserved T cell receptor repertoire in primary and memory CD8 T cell responses to an acute viral infection

Journal of Experimental Medicine

Volumn 188, Issue 1, 1998, Pages 71-82

  Sourdive, David J D ^a,b,c   Murali Krishna, Kaja ^a,b   Altman, John D ^a,b   Zajac, Allan J ^a,b   Whitmire, Jason K ^a,b   Pannetier, Christophe ^c,d,f   Kourilsky, Philippe ^d   Evavold, Brian ^b   Sette, Alessandro ^e   Ahmed, Rafi ^a,b  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CENTRE D ETUDES DU BOUCHET   (France)

^d INSTITUT PASTEUR   (France)

^e Epimmune   (United States)

^f NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

CD8 T cells; Immunological memory; Lymphocytic choriomeningitis virus; T cell receptor; Viral immunity

Indexed keywords

CD8 ANTIGEN; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; HOST RESISTANCE; IMMUNOLOGICAL MEMORY; IMMUNOREACTIVITY; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MEMORY CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; VIRUS RESISTANCE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; COMPLEMENTARITY DETERMINING REGIONS; DISEASE MODELS, ANIMAL; IMMUNOGLOBULIN ALPHA-CHAINS; IMMUNOLOGIC MEMORY; INFECTION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MAJOR HISTOCOMPATIBILITY COMPLEX; MICE; MICE, INBRED BALB C; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES, CYTOTOXIC;

EID: 0032490576     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.188.1.71     Document Type: Article

References (62)

1. Ahmed, R., and D. Gray. 1996. Immunological memory and protective immunity: understanding their relation. Science. 272:54-60.
2. Wilson, R.K., E. Lai, P. Concannon, R.K. Barth, and L.E. Hood. 1988. Structure, organization and polymorphism of murine and human T-cell receptor alpha and beta chain gene families. Immunol. Rev. 101:149-172.
3. Davis, M.M. 1990. T cell receptor gene diversity and selection. Annu. Rev. Biochem. 59:475-496.
4. Goverman, J., K. Minard, N. Shastri, T. Hunkapiller, D. Hansburg, E. Sercarz, and L. Hood. 1985. Rearranged beta T cell receptor genes in a helper T cell clone specific for lysozyme: no correlation between V beta and MHC restriction. Cell. 40:859-867.
5. Goverman, J., T. Hunkapiller, and L. Hood. 1986. A speculative view of the multicomponent nature of T cell antigen recognition. Cell. 45:475-484.
6. Davis, M.M., and P.J. Bjorkman. 1988. T-cell antigen receptor genes and T-cell recognition. Nature. 334:395-402.
7. Garboczi, D.N., P. Ghosh, U. Utz, Q.R. Fan, W.E. Biddison, and D.C. Wiley. 1996. Structure of the complex between human T-cell receptor, viral peptide and HLA-A2. Nature. 384:134-141.
8. Pantaleo, G., J.F. Demarest, H. Soudeyns, C. Graziosi, F. Denis, J.W. Adelsberger, P. Borrow, M.S. Saag, G.M. Shaw, R.P. Seklay, et al. 1994. Major expansion of CD8+ T cells with a predominant V beta usage during the primary immune response to HIV. Nature. 370:463-467.
9. McHeyzer-Williams, M.G., and M.M. Davis. 1995. Antigen-specific development of primary and memory T cells in vivo. Science. 268:106-111.
10. Maryanski, J.L., C.V. Jongeneel, P. Bucher, J.L. Casanova, and P.R. Walker. 1996. Single-cell PCR analysis of TCR repertoires selected by antigen in vivo: a high magnitude CD8 response is comprised of very few clones. Immunity. 4: 47-55.
11. Moss, P.A., R.J. Moots, W.M. Rosenberg, J.S. Rowland, H.C. Bodmer, A.J. McMichael, and J.I. Bell. 1991. Extensive conservation of alpha and beta chains of the human T-cell antigen receptor recognizing HLA-A2 and influenza A matrix peptide. Proc. Natl. Acad. Sci. USA. 88:8987-8990.
12. Wills, M.R., A.J. Carmichael, K. Mynard, X. Jin, M.P. Weekes, B. Plachter, and J.G. Sissons. 1996. The human cytotoxic T-lymphocyte (CTL) response to cytomegalovirus is dominated by structural protein pp65: frequency, specificity, and T-cell receptor usage of pp65-specific CTL. J. Virol. 70: 7569-7579.
13. Kashii, Y., Y. Shimizu, S. Nambu, M. Minemura, K. Okada, K. Higuchi, and A. Watanabe. 1997. Analysis of T-cell receptor Vbeta repertoire in liver-infiltrating lymphocytes in chronic hepatitis C. J. Hepatol. 26:462-470.
14. Chen, Z.W., H. Yamamoto, D.I. Watkins, G. Levinson, and N.L. Letvin. 1992. Predominant use of a T-cell receptor V beta gene family in simian immunodeficiency virus Gag-specific cytotoxic T lymphocytes in a rhesus monkey. J. Virol. 66:3913-3917.
15. d-restricted cytotoxic T cell response against the immediate-early protein pp89 of the murine cytomegalovirus. J. Immunol. 143:4238-4243.
16. Yanagi, Y., R. Maekawa, T. Cook, O. Kanagawa, and M.B. Oldstone. 1990. Restricted V-segment usage in T-cell receptors from cytotoxic T lymphocytes specific for a major epitope of lymphocytic choriomeningitis virus. J. Virol. 64: 5919-5926.
17. b-restricted cytotoxic T cells. Eur.J. Immunol. 20:523-531.
18. Yanagi, Y., A. Tishon, H. Lewicki, B.A. Cubitt, and M.B. Oldstone. 1992. Diversity of T-cell receptors in virus-specific cytotoxic T lymphocytes recognizing three distinct viral epitopes restricted by a single major histocompatibility complex molecule. J. Virol. 66:2527-2531.
19. b-restricted response to an influenza A virus nucleoprotein epitope. J. Immunol. 151:2658-2666.
20. Cole, G.A., T.L. Hogg, and D.L. Woodland. 1994. The MHC class I-restricted T cell response to Sendai virus infection in C57BL/6 mice: a single immunodominant epitope elicits an extremely diverse repertoire of T cells. Int. Immunol. 6:1767-1775.
21. Horwitz, M.S., Y. Yanagi, and M.B. Oldstone. 1994. T-cell receptors from virus-specific cytotoxic T lymphocytes recognizing a single immunodominant nine-amino-acid viral epitope show marked diversity. J. Virol. 68:352-357.
22. Cose, S.C., J.M. Kelly, and F.R. Carbone. 1995. Characterization of diverse primary herpes simplex virus type 1 gB-specific cytotoxic T-cell response showing a preferential V beta bias. J. Virol. 69:5849-5852.
23. Chen, D., F. Lee, J.J. Cebra, and D.H. Rubin. 1997. Predominant T-cell receptor Vbeta usage of intraepithleial lymphocytes during the immune response to enteric reovirus infection. J. Virol. 71:3431-3436.
24. Cose, S.C., C.M. Jones, M.E. Wallace, W.R. Heath, and F.R. Carbone. 1997. Antigen-specific CD8+ T cell subset distribution in lymph nodes draining the site of herpes simplex virus infection. Eur. J. Immunol. 27:2310-2316.
25. Murali-Krishna, K., J.D. Altman, M. Suresh, D.J.D. Sourdive, A.J. Zajac, J.D. Miller, J. Slansky, and R. Ahmed. 1998. Counting antigen specific CD8 T cells: a re-evaluation of bystander activation during viral infection. Immunity. 8:177-187.
26. Whitton, J.L., A. Tishon, H. Lewicki, J. Gebhard, T. Cook, M. Salvato, E. Joly, and M.B. Oldstone. 1989. Molecular analyses of a five-amino-acid cytotoxic T-lymphocyte (CTL) epitope: an immunodominant region which induces nonreciprocal CTL cross-reactivity. J. Virol. 63:4303-4310.
27. Gammon, G., J. Klotz, D. Ando, and E.E. Sercarz. 1990. The T cell repertoire to a multideterminant antigen. Clonal heterogeneity of the T cell response, variation between syngeneic individuals, and in vitro selection of T cell specificities. J. Immunol. 144:1571-1577.
28. Mackensen, A., G. Carcelain, S. Viel, M.C. Raynal, H. Michalaki, F. Triebel, J. Bosq, and T. Hercend. 1994. Direct evidence to support the immunosurveillance concept in a human regressive melanoma. J. Clin. Invest. 93:1397-1402.
29. Shilyansky, J., M.I. Nishimura, J.R. Yannelli, Y. Kawakami, L.S. Jacknin, P. Charmley, and S.A. Rosenberg. 1994. T-cell receptor usage by melanoma-specific clonal and highly oligoclonal tumor-infiltrating lymphocyte lines. Proc. Natl. Acad. Sci. USA. 91:2829-2833.
30. Cibotti, R., J.P. Cabaniols, C. Pannetier, C. Delarbre, I. Vergnon, J.M. Kanellopoulos, and P. Kourilsky. 1994. Public and private V beta T cell receptor repertoires against hen egg white lysozyme (HEL) in nontransgenic versus HEL transgenic mice. J. Exp. Med. 180:861-872.
31. Lau, L.L., B.D. Jamieson, T. Somasundaram, and R. Ahmed. 1994. Cytotoxic T-cell memory without antigen. Nature. 369:648-652.
32. Vijh, S., and E.G. Pamer. 1997. Immunodominant and subdominant CTL responses to Listeria monocytogenes infection. J. Immunol. 158:3366-3371.
33. Ahmed, R., A. Salmi, L.D. Butler, J.M. Chiller, and M.B. Oldstone. 1984. Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice. Role in suppression of cytotoxic T lymphocyte response and viral persistence. J. Exp. Med. 160:521-540.
34. Taguchi, T., J.R. McGhee, R.L. Coffman, K.W. Beagley, J.H. Eldridge, K. Takatsu, and H. Kiyono. 1990. Detection of individual mouse splenic T cells producing IFN-gamma and IL-5 using the enzyme-linked immunospot (ELISPOT) assay. J. Immunol. Methods. 128:65-73.
35. van der most, R.G., A. Sette, C. Oseroff, J. Alexander, K. Muralikrishna, L.L. Lau, S. Southwood, J. Sidney, R.W. Chesnut, M. Matloubian, and R. Ahmed. 1996. Analysis of cytotoxic T cell responses to dominant and subdominant epitopes during acute and chronic lymphocytic choriomeningitis virus infection. J. Immunol. 157:5543-5554.
36. van der Most, R., R.J. Concepcion, C. Oseroff, J. Alexander, S. Southwood, J. Sidney, R.W. Chesnut, R. Ahmed, and A. Sette. 1997. Uncovering subdominant cytotoxic T-lymphocyte responses in lymphocytic choriomeningitis virus-infected BALB/c mice. J. Virol. 71:5110-5114.
37. Pannetier, C., M. Cochet, S. Darche, A. Casrouge, M. Zoller, and P. Kourilsky. 1993. The sizes of the CDR3 hypervariable regions of the murine T-cell receptor beta chains vary as a function of the recombined germ-line segments. Proc. Natl. Acad. Sci. USA. 90:4319-4323.
38. Pannetier, C., J.P. Levraud, A. Lim, J. Even, and P. Kourilsky. 1996. The Immunoscope approach for the analysis of T-cell repertoires. In The Human Antigen T-cell Receptor: Selected Protocols and Applications. J. Oksenberg, editor. R.G. Landes Company, Austin, TX. 162 pp.
39. Asano, M.S., and R. Ahmed. 1996. CD8 T cell memory in B cell-deficient mice. J. Exp. Med. 183:2165-2174.
40. Prevost, B.A., D. Chassin, D. Zeliszewski, I. Dorval, G. Sterkers, C. Pannetier, and J.G. Guillet. 1995. Preferential usage of the T-cell receptor by influenza virus hemagglutinin-specific human CD4+ T lymphocytes: in vitro life span of clonotypic T cells. J. Virol. 69:8046-8050.
41. Pannetier, C., J. Even, and P. Kourilsky. 1995. T-cell repertoire diversity and clonal expansions in normal and clinical samples. Immunol. Today. 16:176-181.
42. Prevost, B.A., M. Ostankovitch, J. Melle, C. Pannetier, E. Macintyre, F. Dreyfus, and J.G. Guillet. 1995. CDR3 size analysis of T cell receptor V beta transcripts: follow-up study in a patient with T cell acute lymphoblastic leukemia. Leukemia (Basingstoke). 9:1711-1717.
43. Wattel, E., J.P. Vartanian, C. Pannetier, and H.S. Wain. 1995. Clonal expansion of human T-cell leukemia virus type I-infected cells in asymptomatic and symptomatic carriers without malignancy. J. Virol. 69:2863-2868.
44. Levraud, J.P., C. Pannetier, D.P. Langlade, V. Brichard, and P. Kourilsky. 1996. Recurrent T cell receptor rearrangements in the cytotoxic T lymphocyte response in vivo against the p815 murine tumor. J. Exp. Med. 183:439-449.
45. Pannetier, C. 1996. Etude de la complexité et de la sélection par l'antigène du répertoire de lymphocytes T alpha-beta. Ph.D. thesis. Denis Diderot, Paris VII. 182 pp.
46. Altman, J.D., P. Moss, P. Goulder, D.H. Barouch, W.M. McHeyzer, J.I. Bell, A.J. McMichael, and M.M. Davis. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science. 274:94-96.
47. Cunningham, B.C., and J.A. Wells. 1989. High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis. Science. 244:1081-1085.
48. Bachmann, M.F., A. Oxenius, D.E. Speiser, S. Mariathasan, H. Hengartner, R.M. Zinkernagel, and P.S. Ohashi. 1997. Peptide-induced T cell receptor down-regulation on naive T cells predicts agonist/partial agonist properties and strictly correlates with T cell activation. Eur. J. Immunol. 27:2195-2203.
49. Bachmann, M.F., D.E. Speiser, and P.S. Ohashi. 1997. Functional maturation of an antiviral cytotoxic T-cell response. J. Virol. 71:5764-5768.
50. Casanova, J.L., J.C. Cerottini, M. Matthes, A. Necker, H. Gournier, C. Barra, C. Widmann, H.R. MacDonald, F. Lemonnier, B. Malissen, et al. 1992. H-2-restricted cytolytic T lymphocytes specific for HLA display T cell receptors of limited diversity. J. Exp. Med. 176:439-447.
51. Puisieux, I., J. Even, C. Pannetier, F. Jotereau, M. Favrot, and P. Kourilsky. 1994. Oligoclonality of tumor-infiltrating lymphocytes from human melanomas. J. Immunol. 153:2807-2818.
52. Taylor, A.H., A.M. Haberman, W. Gerhard, and A.J. Caton. 1990. Structure-function relationships among highly diverse T cells that recognize a determinant from influenza virus hemagglutinin. J. Exp. Med. 172:1643-1651.
53. Argaet, V.P., C.W. Schmidt, S.R., Burrows, S.L. Silins, M.G. Kurilla, D.L. Doolan, A. Suhrbier, D.J. Moss, E. Kieff, T.B. Suclley, et al. 1994. Dominant selection of an invariant T cell antigen receptor in response to persistent infection by Epstein-Barr virus. J. Exp. Med. 180:2335-2340.
54. Callan, M.F., N. Steven, P. Krausa, J.D. Wilson, P.A. Moss, G.M. Gillespie, J.I. Bell, A.B. Rickinson, and A.J. McMichael. 1996. Large clonal expansions of CD8+ T cells in acute infectious mononucleosis. Nat. Med. 2:906-911.
55. Silins, S.L., S.M. Cross, S.L. Elliott, S.J. Pye, S.R. Burrows, J.M. Burrows, D.J. Moss, V.P. Argaet, and I.S. Misko. 1996. Development of Epstein-Barr virus-specific memory T cell receptor clonotypes in acute infectious mononucleosis. J. Exp. Med. 184:1815-1824.
56. Turner, S.J., S.C. Cose, and F.R. Carbone. 1996. TCR alpha-chain usage can determine antigen-selected TCR beta-chain repertoire diversity. J. Immunol. 157:4979-4985.
57. Pham, B.N., F. Degos, J.F. Mosnier, S. Ollivier, A. Sauvanet, S. Erlinger, and J.H. Cohen. 1996. Restriction of V beta gene usage of liver-derived lymphocytes in chronic hepatitis B and C. Hum. Immunol. 49:56-63.
58. Schwab, R., P. Szabo, J.S. Manavalan, M.E. Weksler, D.N. Posnett, C. Pannetier, P. Kourilsky, and J. Even. 1997. Expanded CD4+ and CD8+ T cell clones in elderly humans. J. Immunol. 158:4493-4499.
59. Callahan, J.E., J.W. Kappler, and P. Marrack. 1993. Unexpected expansions of CD8-bearing cells in old mice. J. Immunol. 151:6657-6669.
60. Zinkernagel, R.M., M.F. Bachmann, T.M. Kundig, S. Oehen, H. Pirchet, and H. Hengartner. 1996. On immunological memory. Annu. Rev. Immunol. 14:333-367.
61. Zheng, B., S. Han, and G. Kelsoe. 1996. T helper cells in murine germinal centers are antigen-specific emigrants that downregulate Thy-1. J. Exp. Med. 184:1083-1091.
62. Alexander-Miller, M.A., G.R. Leggatt, and J.A. Berzofsky. 1996. Selective expansion of high-or low-avidity cytotoxic T lymphocytes and efficacy for adoptive immunotherapy. Proc. Natl. Acad. Sci. USA 93:4102-4107.