DOI: 10.1084/jem.188.1.71. Conserved T Cell Receptor Repertoire in Primary and Memory CD8 T Cell Responses to an Acute Viral Infection

Conserved T Cell Receptor Repertoire in Primary and Memory CD8 T Cell Responses to an Acute Viral Infection

10.1084/jem.188.1.71

Crossref journal-article

Rockefeller University Press

The Journal of Experimental Medicine (291)

Abstract

Viral infections often induce potent CD8 T cell responses that play a key role in antiviral immunity. After viral clearance, the vast majority of the expanded CD8 T cells undergo apoptosis, leaving behind a stable number of memory cells. The relationship between the CD8 T cells that clear the acute viral infection and the long-lived CD8 memory pool remaining in the individual is not fully understood. To address this issue, we examined the T cell receptor (TCR) repertoire of virus-specific CD8 T cells in the mouse model of infection with lymphocytic choriomeningitis virus (LCMV) using three approaches: (a) in vivo quantitative TCR β chain V segment and complementarity determining region 3 (CDR3) length repertoire analysis by spectratyping (immunoscope); (b) identification of LCMV-specific CD8 T cells with MHC class I tetramers containing viral peptide and costaining with TCR Vβ–specific antibodies; and (c) functional TCR fingerprinting based on recognition of variant peptides. We compared the repertoire of CD8 T cells responding to acute primary and secondary LCMV infections, together with that of virus-specific memory T cells in immune mice. Our analysis showed that CD8 T cells from several Vβ families participated in the anti-LCMV response directed to the dominant cytotoxic T lymphocyte (CTL) epitope (NP118–126). However, the bulk (∼70%) of this CTL response was due to three privileged T cell populations systematically expanding during LCMV infection. Approximately 30% of the response consisted of Vβ10+ CD8 T cells with a β chain CDR3 length of nine amino acids, and 40% consisted of Vβ8.1+ (β CDR3 = eight amino acids) and Vβ8.2+ cells (β CDR3 = six amino acids). Finally, we showed that the TCR repertoire of the primary antiviral CD8 T cell response was similar both structurally and functionally to that of the memory pool and the secondary CD8 T cell effectors. These results suggest a stochastic selection of memory cells from the pool of CD8 T cells activated during primary infection.

Bibliography

Sourdive, D. J. D., Murali-Krishna, K., Altman, J. D., Zajac, A. J., Whitmire, J. K., Pannetier, C., Kourilsky, P., Evavold, B., Sette, A., & Ahmed, R. (1998). Conserved T Cell Receptor Repertoire in Primary and Memory CD8 T Cell Responses to an Acute Viral Infection. The Journal of Experimental Medicine, 188(1), 71â82.

Authors 10

David J.D. Sourdive (first)
Kaja Murali-Krishna (additional)
John D. Altman (additional)
Allan J. Zajac (additional)
Jason K. Whitmire (additional)
Christophe Pannetier (additional)
Philippe Kourilsky (additional)
Brian Evavold (additional)
Alessandro Sette (additional)
Rafi Ahmed (additional)

References 62 Referenced 177

10.1126/science.272.5258.54 / Science / Immunological memory and protective immunity: understanding their relation by Ahmed (1996)
10.1111/j.1600-065X.1988.tb00736.x / Immunol Rev / Structure, organization and polymorphism of murine and human T-cell receptor alpha and beta chain gene families by Wilson (1988)
10.1146/annurev.bi.59.070190.002355 / Annu Rev Biochem / T cell receptor gene diversity and selection by Davis (1990)
10.1016/0092-8674(85)90345-9 / Cell / Rearranged beta T cell receptor genes in a helper T cell clone specific for lysozyme: no correlation between V beta and MHC restriction by Goverman (1985)
10.1016/0092-8674(86)90279-5 / Cell / A speculative view of the multicomponent nature of T cell antigen recognition by Goverman (1986)
10.1038/334395a0 / Nature / T-cell antigen receptor genes and T-cell recognition by Davis (1988)
10.1038/384134a0 / Nature / Structure of the complex between human T-cell receptor, viral peptide and HLA-A2 by Garboczi (1996)
10.1038/370463a0 / Nature / Major expansion of CD8+ T cells with a predominant V beta usage during the primary immune response to HIV by Pantaleo (1994)
10.1126/science.7535476 / Science / Antigen-specific development of primary and memory T cells in vivo by McHeyzer-Williams (1995)
10.1016/S1074-7613(00)80297-6 / Immunity / Single-cell PCR analysis of TCR repertoires selected by antigen in vivo: a high magnitude CD8 response is comprised of very few clones by Maryanski (1996)
10.1073/pnas.88.20.8987 / Proc Natl Acad Sci USA / Extensive conservation of alpha and beta chains of the human T-cell antigen receptor recognizing HLA-A2 and influenza A matrix peptide by Moss (1991)
10.1128/jvi.70.11.7569-7579.1996 / J Virol / 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 by Wills (1996)
10.1016/S0168-8278(97)80408-4 / J Hepatol / Analysis of T-cell receptor Vbeta repertoire in liver-infiltrating lymphocytes in chronic hepatitis C by Kashii (1997)
10.1128/jvi.66.6.3913-3917.1992 / J Virol / Predominant use of a T-cell receptor V beta gene family in simian immunodeficiency virus Gag-specific cytotoxic T lymphocytes in a rhesus monkey by Chen (1992)
10.4049/jimmunol.143.12.4238 / J Immunol / Predominant utilization of V beta 8+ T cell receptor genes in the H-2Ld-restricted cytotoxic T cell response against the immediate-early protein pp89 of the murine cytomegalovirus by Rodewald (1989)
10.1128/jvi.64.12.5919-5926.1990 / J Virol / Restricted V-segment usage in T-cell receptors from cytotoxic T lymphocytes specific for a major epitope of lymphocytic choriomeningitis virus by Yanagi (1990)
10.1002/eji.1830200310 / Eur J Immunol / Preferential usage of V alpha 4 and V beta 10 T cell receptor genes by lymphocytic choriomeningitis virus glycoprotein-specific H-2Db-restricted cytotoxic T cells by Aebischer (1990)
10.1128/jvi.66.4.2527-2531.1992 / J Virol / Diversity of T-cell receptors in virus-specific cytotoxic T lymphocytes recognizing three distinct viral epitopes restricted by a single major histocompatibility complex molecule by Yanagi (1992)
10.4049/jimmunol.151.5.2658 / J Immunol / Prominent usage of V beta 8.3 T cells in the H-2Db-restricted response to an influenza A virus nucleoprotein epitope by Deckhut (1993)
10.1093/intimm/6.11.1767 / Int Immunol / 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 by Cole (1994)
10.1128/jvi.68.1.352-357.1994 / J Virol / T-cell receptors from virus-specific cytotoxic T lymphocytes recognizing a single immunodominant nine-amino-acid viral epitope show marked diversity by Horwitz (1994)
10.1128/jvi.69.9.5849-5852.1995 / J Virol / Characterization of diverse primary herpes simplex virus type 1 gB-specific cytotoxic T-cell response showing a preferential V beta bias by Cose (1995)
10.1128/jvi.71.5.3431-3436.1997 / J Virol / Predominant T-cell receptor Vbeta usage of intraepithelial lymphocytes during the immune response to enteric reovirus infection by Chen (1997)
10.1002/eji.1830270927 / Eur J Immunol / Antigen-specific CD8+ T cell subset distribution in lymph nodes draining the site of herpes simplex virus infection by Cose (1997)
10.1016/S1074-7613(00)80470-7 / Immunity / Counting antigen specific CD8 T cells: a re-evaluation of bystander activation during viral infection by Murali-Krishna (1998)
10.1128/jvi.63.10.4303-4310.1989 / J Virol / Molecular analyses of a five-amino-acid cytotoxic T-lymphocyte (CTL) epitope: an immunodominant region which induces nonreciprocal CTL cross-reactivity by Whitton (1989)
10.4049/jimmunol.144.5.1571 / J Immunol / 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 by Gammon (1990)
10.1172/JCI117116 / J Clin Invest / Direct evidence to support the immunosurveillance concept in a human regressive melanoma by Mackensen (1994)
10.1073/pnas.91.7.2829 / Proc Natl Acad Sci USA / T-cell receptor usage by melanoma-specific clonal and highly oligoclonal tumor-infiltrating lymphocyte lines by Shilyansky (1994)
10.1084/jem.180.3.861 / J Exp Med / Public and private V beta T cell receptor repertoires against hen egg white lysozyme (HEL) in nontransgenic versus HEL transgenic mice by Cibotti (1994)
10.1038/369648a0 / Nature / Cytotoxic T-cell memory without antigen by Lau (1994)
10.4049/jimmunol.158.7.3366 / J Immunol / Immunodominant and subdominant CTL responses to Listeria monocytogenesinfection by Vijh (1997)
10.1084/jem.160.2.521 / J Exp Med / 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 by Ahmed (1984)
10.1016/0022-1759(90)90464-7 / J Immunol Methods / Detection of individual mouse splenic T cells producing IFN-gamma and IL-5 using the enzyme-linked immunospot (ELISPOT) assay by Taguchi (1990)
10.4049/jimmunol.157.12.5543 / J Immunol / Analysis of cytotoxic T cell responses to dominant and subdominant epitopes during acute and chronic lymphocytic choriomeningitis virus infection by 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)
10.1128/jvi.71.7.5110-5114.1997 / J Virol / Uncovering subdominant cytotoxic T-lymphocyte responses in lymphocytic choriomeningitis virus-infected BALB/c mice by van der Most (1997)
10.1073/pnas.90.9.4319 / Proc Natl Acad Sci USA / 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 by Pannetier (1993)
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10.1084/jem.183.5.2165 / J Exp Med / CD8 T cell memory in B cell–deficient mice by Asano (1996)
10.1128/jvi.69.12.8046-8050.1995 / J Virol / Preferential usage of the T-cell receptor by influenza virus hemagglutinin-specific human CD4+ T lymphocytes: in vitro life span of clonotypic T cells by Prevost (1995)
10.1016/0167-5699(95)80117-0 / Immunol Today / T-cell repertoire diversity and clonal expansions in normal and clinical samples by Pannetier (1995)
{'key': '2023072508082939900_B42', 'first-page': '1711', 'article-title': 'CDR3 size analysis of T cell receptor V beta transcripts: follow-up study in a patient with T cell acute lymphoblastic leukemia', 'volume': '9', 'author': 'Prevost', 'year': '1995', 'journal-title': 'Leukemia (Basingstoke)'} / Leukemia (Basingstoke) / CDR3 size analysis of T cell receptor V beta transcripts: follow-up study in a patient with T cell acute lymphoblastic leukemia by Prevost (1995)
10.1128/jvi.69.5.2863-2868.1995 / J Virol / Clonal expansion of human T-cell leukemia virus type I-infected cells in asymptomatic and symptomatic carriers without malignancy by Wattel (1995)
10.1084/jem.183.2.439 / J Exp Med / Recurrent T cell receptor rearrangements in the cytotoxic T lymphocyte response in vivo against the p815 murine tumor by Levraud (1996)
{'key': '2023072508082939900_B45'}
10.1126/science.274.5284.94 / Science / Phenotypic analysis of antigen-specific T lymphocytes by Altman (1996)
10.1126/science.2471267 / Science / High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis by Cunningham (1989)
10.1002/eji.1830270912 / Eur J Immunol / Peptide-induced T cell receptor down-regulation on naive T cells predicts agonist/partial agonist properties and strictly correlates with T cell activation by Bachmann (1997)
10.1128/jvi.71.8.5764-5768.1997 / J Virol / Functional maturation of an antiviral cytotoxic T-cell response by Bachmann (1997)
10.1084/jem.176.2.439 / J Exp Med / H-2–restricted cytolytic T lymphocytes specific for HLA display T cell receptors of limited diversity by Casanova (1992)
10.4049/jimmunol.153.6.2807 / J Immunol / Oligoclonality of tumor-infiltrating lymphocytes from human melanomas by Puisieux (1994)
10.1084/jem.172.6.1643 / J Exp Med / Structure–function relationships among highly diverse T cells that recognize a determinant from influenza virus hemagglutinin by Taylor (1990)
10.1084/jem.180.6.2335 / J Exp Med / Dominant selection of an invariant T cell antigen receptor in response to persistent infection by Epstein-Barr virus by Argaet (1994)
10.1038/nm0896-906 / Nat Med / Large clonal expansions of CD8+ T cells in acute infectious mononucleosis by Callan (1996)
10.1084/jem.184.5.1815 / J Exp Med / Development of Epstein-Barr virus–specific memory T cell receptor clonotypes in acute infectious mononucleosis by Silins (1996)
10.4049/jimmunol.157.11.4979 / J Immunol / TCR alpha-chain usage can determine antigen-selected TCR beta-chain repertoire diversity by Turner (1996)
10.1016/0198-8859(96)00053-5 / Hum Immunol / Restriction of V beta gene usage of liver-derived lymphocytes in chronic hepatitis B and C by Pham (1996)
10.4049/jimmunol.158.9.4493 / J Immunol / Expanded CD4+ and CD8+ T cell clones in elderly humans by Schwab (1997)
10.4049/jimmunol.151.12.6657 / J Immunol / Unexpected expansions of CD8-bearing cells in old mice by Callahan (1993)
10.1146/annurev.immunol.14.1.333 / Annu Rev Immunol / On immunological memory by Zinkernagel (1996)
10.1084/jem.184.3.1083 / J Exp Med / T helper cells in murine germinal centers are antigen-specific emigrants that downregulate Thy-1 by Zheng (1996)
10.1073/pnas.93.9.4102 / Proc Natl Acad Sci USA / Selective expansion of high- or low-avidity cytotoxic T lymphocytes and efficacy for adoptive immunotherapy by Alexander-Miller (1996)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 12:49 p.m.)
Deposited	2 years, 1 month ago (July 25, 2023, 5:14 a.m.)
Indexed	4 months, 2 weeks ago (April 19, 2025, 12:25 a.m.)
Issued	27 years, 2 months ago (July 1, 1998)
Published	27 years, 2 months ago (July 1, 1998)
Published Online	27 years, 2 months ago (July 1, 1998)
Published Print	27 years, 2 months ago (July 1, 1998)

Funders 0

None

BibTeX

@article{Sourdive_1998, title={Conserved T Cell Receptor Repertoire in Primary and Memory CD8 T Cell Responses to an Acute Viral Infection}, volume={188}, ISSN={1540-9538}, url={http://dx.doi.org/10.1084/jem.188.1.71}, DOI={10.1084/jem.188.1.71}, number={1}, journal={The Journal of Experimental Medicine}, publisher={Rockefeller University Press}, author={Sourdive, David J.D. and Murali-Krishna, Kaja and Altman, John D. and Zajac, Allan J. and Whitmire, Jason K. and Pannetier, Christophe and Kourilsky, Philippe and Evavold, Brian and Sette, Alessandro and Ahmed, Rafi}, year={1998}, month=jul, pages={71–82} }

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  "abstract": "<jats:p>Viral infections often induce potent CD8 T cell responses that play a key role in antiviral immunity. After viral clearance, the vast majority of the expanded CD8 T cells undergo apoptosis, leaving behind a stable number of memory cells. The relationship between the CD8 T cells that clear the acute viral infection and the long-lived CD8 memory pool remaining in the individual is not fully understood. To address this issue, we examined the T cell receptor (TCR) repertoire of virus-specific CD8 T cells in the mouse model of infection with lymphocytic choriomeningitis virus (LCMV) using three approaches: (a) in vivo quantitative TCR \u03b2 chain V segment and complementarity determining region 3 (CDR3) length repertoire analysis by spectratyping (immunoscope); (b) identification of LCMV-specific CD8 T cells with MHC class I tetramers containing viral peptide and costaining with TCR V\u03b2\u2013specific antibodies; and (c) functional TCR fingerprinting based on recognition of variant peptides. We compared the repertoire of CD8 T cells responding to acute primary and secondary LCMV infections, together with that of virus-specific memory T cells in immune mice. Our analysis showed that CD8 T cells from several V\u03b2 families participated in the anti-LCMV response directed to the dominant cytotoxic T lymphocyte (CTL) epitope (NP118\u2013126). However, the bulk (\u223c70%) of this CTL response was due to three privileged T cell populations systematically expanding during LCMV infection. Approximately 30% of the response consisted of V\u03b210+ CD8 T cells with a \u03b2 chain CDR3 length of nine amino acids, and 40% consisted of V\u03b28.1+ (\u03b2 CDR3 = eight amino acids) and V\u03b28.2+ cells (\u03b2 CDR3 = six amino acids). Finally, we showed that the TCR repertoire of the primary antiviral CD8 T cell response was similar both structurally and functionally to that of the memory pool and the secondary CD8 T cell effectors. These results suggest a stochastic selection of memory cells from the pool of CD8 T cells activated during primary infection.</jats:p>",
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        },
        {
          "name": "From the *Emory Vaccine Center, Rollins Research Center, and the \u2021Department of Microbiology and Immunology, Emory University, Atlanta, Georgia 30322; the \u00a7Centre d'Etudes du Bouchet, 91710 Vert-le-Petit, France; the \u2016Unit\u00e9 de Biologie Mol\u00e9culaire du G\u00e8ne, Institut Pasteur, 75724 Paris cedex 15, France; and \u00b6Epimmune, San Diego, California 92121"
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          "name": "From the *Emory Vaccine Center, Rollins Research Center, and the \u2021Department of Microbiology and Immunology, Emory University, Atlanta, Georgia 30322; the \u00a7Centre d'Etudes du Bouchet, 91710 Vert-le-Petit, France; the \u2016Unit\u00e9 de Biologie Mol\u00e9culaire du G\u00e8ne, Institut Pasteur, 75724 Paris cedex 15, France; and \u00b6Epimmune, San Diego, California 92121"
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        {
          "name": "From the *Emory Vaccine Center, Rollins Research Center, and the \u2021Department of Microbiology and Immunology, Emory University, Atlanta, Georgia 30322; the \u00a7Centre d'Etudes du Bouchet, 91710 Vert-le-Petit, France; the \u2016Unit\u00e9 de Biologie Mol\u00e9culaire du G\u00e8ne, Institut Pasteur, 75724 Paris cedex 15, France; and \u00b6Epimmune, San Diego, California 92121"
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        },
        {
          "name": "From the *Emory Vaccine Center, Rollins Research Center, and the \u2021Department of Microbiology and Immunology, Emory University, Atlanta, Georgia 30322; the \u00a7Centre d'Etudes du Bouchet, 91710 Vert-le-Petit, France; the \u2016Unit\u00e9 de Biologie Mol\u00e9culaire du G\u00e8ne, Institut Pasteur, 75724 Paris cedex 15, France; and \u00b6Epimmune, San Diego, California 92121"
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        {
          "name": "From the *Emory Vaccine Center, Rollins Research Center, and the \u2021Department of Microbiology and Immunology, Emory University, Atlanta, Georgia 30322; the \u00a7Centre d'Etudes du Bouchet, 91710 Vert-le-Petit, France; the \u2016Unit\u00e9 de Biologie Mol\u00e9culaire du G\u00e8ne, Institut Pasteur, 75724 Paris cedex 15, France; and \u00b6Epimmune, San Diego, California 92121"
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        },
        {
          "name": "From the *Emory Vaccine Center, Rollins Research Center, and the \u2021Department of Microbiology and Immunology, Emory University, Atlanta, Georgia 30322; the \u00a7Centre d'Etudes du Bouchet, 91710 Vert-le-Petit, France; the \u2016Unit\u00e9 de Biologie Mol\u00e9culaire du G\u00e8ne, Institut Pasteur, 75724 Paris cedex 15, France; and \u00b6Epimmune, San Diego, California 92121"
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          "name": "From the *Emory Vaccine Center, Rollins Research Center, and the \u2021Department of Microbiology and Immunology, Emory University, Atlanta, Georgia 30322; the \u00a7Centre d'Etudes du Bouchet, 91710 Vert-le-Petit, France; the \u2016Unit\u00e9 de Biologie Mol\u00e9culaire du G\u00e8ne, Institut Pasteur, 75724 Paris cedex 15, France; and \u00b6Epimmune, San Diego, California 92121"
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  "reference": [
    {
      "key": "2023072508082939900_B1",
      "doi-asserted-by": "crossref",
      "first-page": "54",
      "DOI": "10.1126/science.272.5258.54",
      "article-title": "Immunological memory and protective immunity: understanding their relation",
      "volume": "272",
      "author": "Ahmed",
      "year": "1996",
      "journal-title": "Science"
    },
    {
      "key": "2023072508082939900_B2",
      "doi-asserted-by": "crossref",
      "first-page": "149",
      "DOI": "10.1111/j.1600-065X.1988.tb00736.x",
      "article-title": "Structure, organization and polymorphism of murine and human T-cell receptor alpha and beta chain gene families",
      "volume": "101",
      "author": "Wilson",
      "year": "1988",
      "journal-title": "Immunol Rev"
    },
    {
      "key": "2023072508082939900_B3",
      "doi-asserted-by": "crossref",
      "first-page": "475",
      "DOI": "10.1146/annurev.bi.59.070190.002355",
      "article-title": "T cell receptor gene diversity and selection",
      "volume": "59",
      "author": "Davis",
      "year": "1990",
      "journal-title": "Annu Rev Biochem"
    },
    {
      "key": "2023072508082939900_B4",
      "doi-asserted-by": "crossref",
      "first-page": "859",
      "DOI": "10.1016/0092-8674(85)90345-9",
      "article-title": "Rearranged beta T cell receptor genes in a helper T cell clone specific for lysozyme: no correlation between V beta and MHC restriction",
      "volume": "40",
      "author": "Goverman",
      "year": "1985",
      "journal-title": "Cell"
    },
    {
      "key": "2023072508082939900_B5",
      "doi-asserted-by": "crossref",
      "first-page": "475",
      "DOI": "10.1016/0092-8674(86)90279-5",
      "article-title": "A speculative view of the multicomponent nature of T cell antigen recognition",
      "volume": "45",
      "author": "Goverman",
      "year": "1986",
      "journal-title": "Cell"
    },
    {
      "key": "2023072508082939900_B6",
      "doi-asserted-by": "crossref",
      "first-page": "395",
      "DOI": "10.1038/334395a0",
      "article-title": "T-cell antigen receptor genes and T-cell recognition",
      "volume": "334",
      "author": "Davis",
      "year": "1988",
      "journal-title": "Nature"
    },
    {
      "key": "2023072508082939900_B7",
      "doi-asserted-by": "crossref",
      "first-page": "134",
      "DOI": "10.1038/384134a0",
      "article-title": "Structure of the complex between human T-cell receptor, viral peptide and HLA-A2",
      "volume": "384",
      "author": "Garboczi",
      "year": "1996",
      "journal-title": "Nature"
    },
    {
      "key": "2023072508082939900_B8",
      "doi-asserted-by": "crossref",
      "first-page": "463",
      "DOI": "10.1038/370463a0",
      "article-title": "Major expansion of CD8+ T cells with a predominant V beta usage during the primary immune response to HIV",
      "volume": "370",
      "author": "Pantaleo",
      "year": "1994",
      "journal-title": "Nature"
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    {
      "key": "2023072508082939900_B9",
      "doi-asserted-by": "crossref",
      "first-page": "106",
      "DOI": "10.1126/science.7535476",
      "article-title": "Antigen-specific development of primary and memory T cells in vivo",
      "volume": "268",
      "author": "McHeyzer-Williams",
      "year": "1995",
      "journal-title": "Science"
    },
    {
      "key": "2023072508082939900_B10",
      "doi-asserted-by": "crossref",
      "first-page": "47",
      "DOI": "10.1016/S1074-7613(00)80297-6",
      "article-title": "Single-cell PCR analysis of TCR repertoires selected by antigen in vivo: a high magnitude CD8 response is comprised of very few clones",
      "volume": "4",
      "author": "Maryanski",
      "year": "1996",
      "journal-title": "Immunity"
    },
    {
      "key": "2023072508082939900_B11",
      "doi-asserted-by": "crossref",
      "first-page": "8987",
      "DOI": "10.1073/pnas.88.20.8987",
      "article-title": "Extensive conservation of alpha and beta chains of the human T-cell antigen receptor recognizing HLA-A2 and influenza A matrix peptide",
      "volume": "88",
      "author": "Moss",
      "year": "1991",
      "journal-title": "Proc Natl Acad Sci USA"
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      "key": "2023072508082939900_B12",
      "doi-asserted-by": "crossref",
      "first-page": "7569",
      "DOI": "10.1128/jvi.70.11.7569-7579.1996",
      "article-title": "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",
      "volume": "70",
      "author": "Wills",
      "year": "1996",
      "journal-title": "J Virol"
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      "key": "2023072508082939900_B13",
      "doi-asserted-by": "crossref",
      "first-page": "462",
      "DOI": "10.1016/S0168-8278(97)80408-4",
      "article-title": "Analysis of T-cell receptor Vbeta repertoire in liver-infiltrating lymphocytes in chronic hepatitis C",
      "volume": "26",
      "author": "Kashii",
      "year": "1997",
      "journal-title": "J Hepatol"
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      "doi-asserted-by": "crossref",
      "first-page": "3913",
      "DOI": "10.1128/jvi.66.6.3913-3917.1992",
      "article-title": "Predominant use of a T-cell receptor V beta gene family in simian immunodeficiency virus Gag-specific cytotoxic T lymphocytes in a rhesus monkey",
      "volume": "66",
      "author": "Chen",
      "year": "1992",
      "journal-title": "J Virol"
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      "first-page": "4238",
      "DOI": "10.4049/jimmunol.143.12.4238",
      "article-title": "Predominant utilization of V beta 8+ T cell receptor genes in the H-2Ld-restricted cytotoxic T cell response against the immediate-early protein pp89 of the murine cytomegalovirus",
      "volume": "143",
      "author": "Rodewald",
      "year": "1989",
      "journal-title": "J Immunol"
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      "doi-asserted-by": "crossref",
      "first-page": "5919",
      "DOI": "10.1128/jvi.64.12.5919-5926.1990",
      "article-title": "Restricted V-segment usage in T-cell receptors from cytotoxic T lymphocytes specific for a major epitope of lymphocytic choriomeningitis virus",
      "volume": "64",
      "author": "Yanagi",
      "year": "1990",
      "journal-title": "J Virol"
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      "key": "2023072508082939900_B17",
      "doi-asserted-by": "crossref",
      "first-page": "523",
      "DOI": "10.1002/eji.1830200310",
      "article-title": "Preferential usage of V alpha 4 and V beta 10 T cell receptor genes by lymphocytic choriomeningitis virus glycoprotein-specific H-2Db-restricted cytotoxic T cells",
      "volume": "20",
      "author": "Aebischer",
      "year": "1990",
      "journal-title": "Eur J Immunol"
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      "doi-asserted-by": "crossref",
      "first-page": "2527",
      "DOI": "10.1128/jvi.66.4.2527-2531.1992",
      "article-title": "Diversity of T-cell receptors in virus-specific cytotoxic T lymphocytes recognizing three distinct viral epitopes restricted by a single major histocompatibility complex molecule",
      "volume": "66",
      "author": "Yanagi",
      "year": "1992",
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      "first-page": "2658",
      "DOI": "10.4049/jimmunol.151.5.2658",
      "article-title": "Prominent usage of V beta 8.3 T cells in the H-2Db-restricted response to an influenza A virus nucleoprotein epitope",
      "volume": "151",
      "author": "Deckhut",
      "year": "1993",
      "journal-title": "J Immunol"
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      "first-page": "1767",
      "DOI": "10.1093/intimm/6.11.1767",
      "article-title": "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",
      "volume": "6",
      "author": "Cole",
      "year": "1994",
      "journal-title": "Int Immunol"
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      "first-page": "352",
      "DOI": "10.1128/jvi.68.1.352-357.1994",
      "article-title": "T-cell receptors from virus-specific cytotoxic T lymphocytes recognizing a single immunodominant nine-amino-acid viral epitope show marked diversity",
      "volume": "68",
      "author": "Horwitz",
      "year": "1994",
      "journal-title": "J Virol"
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      "first-page": "5849",
      "DOI": "10.1128/jvi.69.9.5849-5852.1995",
      "article-title": "Characterization of diverse primary herpes simplex virus type 1 gB-specific cytotoxic T-cell response showing a preferential V beta bias",
      "volume": "69",
      "author": "Cose",
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      "first-page": "3431",
      "DOI": "10.1128/jvi.71.5.3431-3436.1997",
      "article-title": "Predominant T-cell receptor Vbeta usage of intraepithelial lymphocytes during the immune response to enteric reovirus infection",
      "volume": "71",
      "author": "Chen",
      "year": "1997",
      "journal-title": "J Virol"
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      "first-page": "2310",
      "DOI": "10.1002/eji.1830270927",
      "article-title": "Antigen-specific CD8+ T cell subset distribution in lymph nodes draining the site of herpes simplex virus infection",
      "volume": "27",
      "author": "Cose",
      "year": "1997",
      "journal-title": "Eur J Immunol"
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      "doi-asserted-by": "crossref",
      "first-page": "177",
      "DOI": "10.1016/S1074-7613(00)80470-7",
      "article-title": "Counting antigen specific CD8 T cells: a re-evaluation of bystander activation during viral infection",
      "volume": "8",
      "author": "Murali-Krishna",
      "year": "1998",
      "journal-title": "Immunity"
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      "doi-asserted-by": "crossref",
      "first-page": "4303",
      "DOI": "10.1128/jvi.63.10.4303-4310.1989",
      "article-title": "Molecular analyses of a five-amino-acid cytotoxic T-lymphocyte (CTL) epitope: an immunodominant region which induces nonreciprocal CTL cross-reactivity",
      "volume": "63",
      "author": "Whitton",
      "year": "1989",
      "journal-title": "J Virol"
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      "doi-asserted-by": "crossref",
      "first-page": "1571",
      "DOI": "10.4049/jimmunol.144.5.1571",
      "article-title": "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",
      "volume": "144",
      "author": "Gammon",
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      "DOI": "10.1172/JCI117116",
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      "volume": "93",
      "author": "Mackensen",
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      "journal-title": "J Clin Invest"
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      "first-page": "2829",
      "DOI": "10.1073/pnas.91.7.2829",
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      "volume": "91",
      "author": "Shilyansky",
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      "journal-title": "Proc Natl Acad Sci USA"
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      "first-page": "861",
      "DOI": "10.1084/jem.180.3.861",
      "article-title": "Public and private V beta T cell receptor repertoires against hen egg white lysozyme (HEL) in nontransgenic versus HEL transgenic mice",
      "volume": "180",
      "author": "Cibotti",
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      "journal-title": "J Exp Med"
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      "first-page": "648",
      "DOI": "10.1038/369648a0",
      "article-title": "Cytotoxic T-cell memory without antigen",
      "volume": "369",
      "author": "Lau",
      "year": "1994",
      "journal-title": "Nature"
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      "first-page": "3366",
      "DOI": "10.4049/jimmunol.158.7.3366",
      "article-title": "Immunodominant and subdominant CTL responses to Listeria monocytogenesinfection",
      "volume": "158",
      "author": "Vijh",
      "year": "1997",
      "journal-title": "J Immunol"
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      "first-page": "521",
      "DOI": "10.1084/jem.160.2.521",
      "article-title": "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",
      "volume": "160",
      "author": "Ahmed",
      "year": "1984",
      "journal-title": "J Exp Med"
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      "first-page": "65",
      "DOI": "10.1016/0022-1759(90)90464-7",
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      "volume": "128",
      "author": "Taguchi",
      "year": "1990",
      "journal-title": "J Immunol Methods"
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      "key": "2023072508082939900_B35",
      "doi-asserted-by": "crossref",
      "first-page": "5543",
      "DOI": "10.4049/jimmunol.157.12.5543",
      "article-title": "Analysis of cytotoxic T cell responses to dominant and subdominant epitopes during acute and chronic lymphocytic choriomeningitis virus infection",
      "volume": "157",
      "author": "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",
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      "first-page": "5110",
      "DOI": "10.1128/jvi.71.7.5110-5114.1997",
      "article-title": "Uncovering subdominant cytotoxic T-lymphocyte responses in lymphocytic choriomeningitis virus-infected BALB/c mice",
      "volume": "71",
      "author": "van der Most",
      "year": "1997",
      "journal-title": "J Virol"
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      "first-page": "4319",
      "DOI": "10.1073/pnas.90.9.4319",
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      "volume": "90",
      "author": "Pannetier",
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      "first-page": "2165",
      "DOI": "10.1084/jem.183.5.2165",
      "article-title": "CD8 T cell memory in B cell\u2013deficient mice",
      "volume": "183",
      "author": "Asano",
      "year": "1996",
      "journal-title": "J Exp Med"
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      "doi-asserted-by": "crossref",
      "first-page": "8046",
      "DOI": "10.1128/jvi.69.12.8046-8050.1995",
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      "volume": "69",
      "author": "Prevost",
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      "first-page": "176",
      "DOI": "10.1016/0167-5699(95)80117-0",
      "article-title": "T-cell repertoire diversity and clonal expansions in normal and clinical samples",
      "volume": "16",
      "author": "Pannetier",
      "year": "1995",
      "journal-title": "Immunol Today"
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      "first-page": "1711",
      "article-title": "CDR3 size analysis of T cell receptor V beta transcripts: follow-up study in a patient with T cell acute lymphoblastic leukemia",
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      "author": "Prevost",
      "year": "1995",
      "journal-title": "Leukemia (Basingstoke)"
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      "first-page": "2863",
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      "volume": "69",
      "author": "Wattel",
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      "first-page": "439",
      "DOI": "10.1084/jem.183.2.439",
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      "volume": "183",
      "author": "Levraud",
      "year": "1996",
      "journal-title": "J Exp Med"
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      "article-title": "Phenotypic analysis of antigen-specific T lymphocytes",
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      "author": "Altman",
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      "journal-title": "Science"
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      "first-page": "1081",
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      "article-title": "High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis",
      "volume": "244",
      "author": "Cunningham",
      "year": "1989",
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      "first-page": "2195",
      "DOI": "10.1002/eji.1830270912",
      "article-title": "Peptide-induced T cell receptor down-regulation on naive T cells predicts agonist/partial agonist properties and strictly correlates with T cell activation",
      "volume": "27",
      "author": "Bachmann",
      "year": "1997",
      "journal-title": "Eur J Immunol"
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      "first-page": "5764",
      "DOI": "10.1128/jvi.71.8.5764-5768.1997",
      "article-title": "Functional maturation of an antiviral cytotoxic T-cell response",
      "volume": "71",
      "author": "Bachmann",
      "year": "1997",
      "journal-title": "J Virol"
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      "first-page": "439",
      "DOI": "10.1084/jem.176.2.439",
      "article-title": "H-2\u2013restricted cytolytic T lymphocytes specific for HLA display T cell receptors of limited diversity",
      "volume": "176",
      "author": "Casanova",
      "year": "1992",
      "journal-title": "J Exp Med"
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      "doi-asserted-by": "crossref",
      "first-page": "2807",
      "DOI": "10.4049/jimmunol.153.6.2807",
      "article-title": "Oligoclonality of tumor-infiltrating lymphocytes from human melanomas",
      "volume": "153",
      "author": "Puisieux",
      "year": "1994",
      "journal-title": "J Immunol"
    },
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      "key": "2023072508082939900_B52",
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      "first-page": "1643",
      "DOI": "10.1084/jem.172.6.1643",
      "article-title": "Structure\u2013function relationships among highly diverse T cells that recognize a determinant from influenza virus hemagglutinin",
      "volume": "172",
      "author": "Taylor",
      "year": "1990",
      "journal-title": "J Exp Med"
    },
    {
      "key": "2023072508082939900_B53",
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      "first-page": "2335",
      "DOI": "10.1084/jem.180.6.2335",
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