Cited by 3,544T-cell and B-cell ImmunologyImmunotherapy and Immune Responsesvaccines and immunoinformatics approaches

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Phenotypic Analysis of Antigen-Specific T Lymphocytes

Altman, John D., Moss, Paul A. H., Goulder, Philip J. R., Barouch, Dan H., McHeyzer-Williams, Michael G., Bell, John I., McMichael, Andrew J., Davis, Mark M.·1996·Science

DOI 10.1126/science.274.5284.94

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Abstract

Identification and characterization of antigen-specific T lymphocytes during the course of an immune response is tedious and indirect. To address this problem, the peptide-major histocompatability complex (MHC) ligand for a given population of T cells was multimerized to make soluble peptide-MHC tetramers. Tetramers of human lymphocyte antigen A2 that were complexed with two different human immunodeficiency virus (HIV)-derived peptides or with a peptide derived from influenza A matrix protein bound to peptide-specific cytotoxic T cells in vitro and to T cells from the blood of HIV-infected individuals. In general, tetramer binding correlated well with cytotoxicity assays. This approach should be useful in the analysis of T cells specific for infectious agents, tumors, and autoantigens.

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Self-citation
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Method
Multiple Innate Immune Pathways Contribute to the Immunogenicity of Recombinant Adenovirus Vaccine Vectors
Rhee, E. G., Blattman, J. N., Kasturi, S. P., Kelley, R., Kaufman, D. R., Lynch, D. M., Porte, A. L., Simmons, N. L., Clark, S., Pulendran, B., et al. (2010) · Journal of Virology · doi:10.1128/jvi.01597-10 · Cited by 79
Self-citation
A Fractal Clonotype Distribution in the CD8+ Memory T Cell Repertoire Could Optimize Potential for Immune Responses
Naumov, Y. N., Naumova, E. N., Hogan, K. T., Selin, L. K., & Gorski, J. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.8.3994 · Cited by 79
DNA fusion gene vaccines against cancer: from the laboratory to the clinic
Stevenson, F. K., Rice, J., Ottensmeier, C. H. H., Thirdborough, S. M., & Zhu, D. (2004) · Immunological Reviews · doi:10.1111/j.0105-2896.2004.00145.x · Cited by 78
“The use of tetramer-binding assays has changed the ease with which CD8þ T cells specific for a particular peptide in the context of an MHC class I restriction element can be detected (164).”
Background
Costimulatory mechanisms in the elderly
Effros, R. B. (2000) · Vaccine · doi:10.1016/s0264-410x(99)00503-4 · Cited by 79
Survivin-specific T-cell reactivity correlates with tumor response and patient survival: a phase-II peptide vaccination trial in metastatic melanoma
Becker, J. C., Andersen, M. H., Hofmeister, V., Wobser, M., Frey, L. M., Sandig, C., Walter, S., Singh‐Jasuja, H., Kämpgen, E., Opitz, A., et al. (2012) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-012-1266-9 · Cited by 77
“Biotinylated recombinant peptide–HLAA*0201-monomers and multimers were produced as previously described [22].”
Method
Immune Activation and Collateral Damage in AIDS Pathogenesis
Miedema, F. F., Hazenberg, M. D., Tesselaar, K., van Baarle, D., de Boer, R. J., & Borghans, J. A. M. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00298 · Cited by 79
Immune responses to viruses
Mueller, S. N., & Rouse, B. T. (2008) · Elsevier eBooks · doi:10.1016/b978-0-323-04404-2.10027-2 · Cited by 79
Expanding Role of T Cells in Human Autoimmune Diseases of the Central Nervous System
Pilli, D., Zou, A., Tea, F., Dale, R. C., & Brilot, F. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00652 · Cited by 81
“This rapidly evolving technology involves the formation of a complex of peptide-loaded MHC monomers via biotinylation with a fluorescently labeled streptavidin (Figure 1), which increases binding avidity (234) and overcomes the issue of low affinity binding and fast dissociation rate between TCRs and pMHC monomers (23…”
Background
Rebooting Human Immunology
Davis, M. M., & Brodin, P. (2018) · Annual Review of Immunology · doi:10.1146/annurev-immunol-042617-053206 · Cited by 76
Self-citation
Multidisciplinary approach for post-liver transplant recurrence of hepatocellular carcinoma: A proposed management algorithm
Au, K. P., & Chok, K. (2018) · World Journal of Gastroenterology · doi:10.3748/wjg.v24.i45.5081 · Cited by 79
T-Cell Mechanobiology: Force Sensation, Potentiation, and Translation
Harrison, D. L., Fang, Y. H., & Huang, J. (2019) · Frontiers in Physics · doi:10.3389/fphy.2019.00045 · Cited by 83
The oncogenic fusion protein DNAJB1-PRKACA can be specifically targeted by peptide-based immunotherapy in fibrolamellar hepatocellular carcinoma
Bauer, J., Köhler, N., Maringer, Y., Bucher, P., Bilich, T., Zwick, M., Dicks, S., Nelde, A., Dubbelaar, M. L., Scheid, J., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33746-3 · Cited by 77
Immunodominance and Immunodomination: Critical Factors in Developing Effective CD8+ T‐Cell–Based Cancer Vaccines
Chen, W., & McCluskey, J. (2006) · Advances in cancer research · doi:10.1016/s0065-230x(06)95006-4 · Cited by 78
Peripheral T cell tolerance occurs early during spontaneous prostate cancer development and can be rescued by dendritic cell immunization
Degl'Innocenti, E., Grioni, M., Boni, A., Camporeale, A., Bertilaccio, M. T. S., Freschi, M., Monno, A., Arcelloni, C., Greenberg, N. M., & Bellone, M. (2004) · European Journal of Immunology · doi:10.1002/eji.200425531 · Cited by 78
IL-21 Restricts Virus-driven Treg Cell Expansion in Chronic LCMV Infection
Schmitz, I., Schneider, C., Fröhlich, A., Frebel, H., Christ, D., Leonard, W., Sparwasser, T., Oxenius, A., Freigang, S., & Kopf, M. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003362 · Cited by 88
“PE- and APC-conjugated peptide-MHC class I tetramers (H-2D/gp33-41) were generated as described [74] or kindly provided the NIH tetramer core facility.”
Method
Early reconstitution of effector memory CD4+ CMV-specific T cells protects against CMV reactivation following allogeneic SCT
Pourgheysari, B., Piper, K. P., McLarnon, A., Arrazi, J., Bruton, R. K., Clark, F. J., Cook, M. A., Mahendra, P., Craddock, C., & Moss, P. A. H. (2008) · Bone Marrow Transplantation · doi:10.1038/bmt.2008.403 · Cited by 78
“Cell staining with tetramers CMV tetramers derived from pp65, immediate early Ag (IE-1) and pp50 proteins were produced using a previously described method”
MethodSelf-citation
Phase I clinical trial of survivin‐derived peptide vaccine therapy for patients with advanced or recurrent oral cancer
Miyazaki, A., Kobayashi, J., Torigoe, T., Hirohashi, Y., Yamamoto, T., Yamaguchi, A., Asanuma, H., Takahashi, A., Michifuri, Y., Nakamori, K., et al. (2010) · Cancer Science · doi:10.1111/j.1349-7006.2010.01789.x · Cited by 78
Simultaneous quantification of human cytomegalovirus (HCMV)-specific CD4+ and CD8+T cells by a novel method using monocyte-derived HCMV-infected immature dendritic cells
Lozza, L., Lilleri, D., Percivalle, E., Fornara, C., Comolli, G., Revello, M. G., & Gerna, G. (2005) · European Journal of Immunology · doi:10.1002/eji.200526023 · Cited by 78
Latent Infection with Herpes Simplex Virus Is Associated with Ongoing CD8+T-Cell Stimulation by Parenchymal Cells within Sensory Ganglia
van Lint, A. L., Kleinert, L., Clarke, S. R. M., Stock, A. T., Heath, W. R., & Carbone, F. (2005) · Journal of Virology · doi:10.1128/jvi.79.23.14843-14851.2005 · Cited by 78
“described (3) and provided by Martha Kotsifas (University of Melbourne).”
Background
Comparative Analysis of Cytotoxic T Lymphocytes in Lymph Nodes and Peripheral Blood of Simian Immunodeficiency Virus-Infected Rhesus Monkeys
Kuroda, M. J., Schmitz, J. E., Charini, W. A., Nickerson, C. E., Lord, C. I., Forman, M. A., & Letvin, N. L. (1999) · Journal of Virology · doi:10.1128/jvi.73.2.1573-1579.1999 · Cited by 78
“In the present study, CTL specific for SIVmac have been characterized in lymph nodes of infected, Mamu-A*01(1) rhesus monkeys using both Gag peptide-specific functional CTL assays and tetrameric peptide-MHC class I molecule complex staining techniques (2, 6, 12, 18, 24, 27).”
Method
Frequencies of Neuroantigen-Specific T Cells in the Central Nervous System Versus the Immune Periphery During the Course of Experimental Allergic Encephalomyelitis
Targoni, O. S., Baus, J., Hofstetter, H. H., Hesse, M. D., Karulin, A. Y., Boehm, B. O., Forsthuber, T. G., & Lehmann, P. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.7.4757 · Cited by 77
Identification of multiple HLA-A*0201-restricted cruzipain and FL-160 CD8+ epitopes recognized by T cells from chronically Trypanosoma cruzi-infected patients
Fonseca, S. G., Moins‐Teisserenc, H., Clave, E., Ianni, B. M., Nunes, V. L., Mady, C., Iwai, L. K., Sette, A., Sidney, J., Marin, M. L. C., et al. (2005) · Microbes and Infection · doi:10.1016/j.micinf.2005.01.001 · Cited by 77
Precision and linearity targets for validation of an IFNγ ELISPOT, cytokine flow cytometry, and tetramer assay using CMV peptides
Maecker, H. T., Hassler, J., Payne, J. K., Summers, A. N., Comatas, K., Ghanayem, M., Morse, M. A., Clay, T. M., Lyerly, H. K., Bhatia, S., et al. (2008) · BMC Immunology · doi:10.1186/1471-2172-9-9 · Cited by 77
“Less well-characterized are cellular immunity assays, of which the single-cell assays like tetramer staining [4], cytokine flow cytometry (CFC) [5,6], and ELISPOT [7] are among the most popular.”
Background
Frequency of circulating autoreactive T cells committed to myelin determinants in relapsing–remitting multiple sclerosis patients
Ngono, A. E., Pettré, S., Salou, M., Bahbouhi, B., Soulillou, J., Brouard, S., & Laplaud, D. A. (2012) · Clinical Immunology · doi:10.1016/j.clim.2012.05.009 · Cited by 79
Vpu Increases Susceptibility of Human Immunodeficiency Virus Type 1-Infected Cells to Fas Killing
Casella, C. R., Rapaport, E. L., & Finkel, T. H. (1999) · Journal of Virology · doi:10.1128/jvi.73.1.92-100.1999 · Cited by 76
“HIV-specific CTLs and macrophages which are low to absent in in vitro cultures of infected cells might be a source of FasL in vivo.”
BackgroundInfluential
Antigen-Specific T Cells Maintain an Effector Memory Phenotype during Persistent Trypanosoma cruzi Infection
Martin, D. L., & Tarleton, R. L. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.3.1594 · Cited by 77
“The use of MHC I tetramers has allowed for the phenotypic and functional analysis of peptide-specific T cells in a wide array of infections (29, 38, 39).”
Background
The role of hepatitis B virus-specific memory CD8 T cells in the control of viral replication
Sobao, Y., Tomiyama, H., Sugi, K., Tokunaga, M., Ueno, T., Saito, S., Fujiyama, S., Morimoto, M., Tanaka, K., & Takiguchi, M. (2002) · Journal of Hepatology · doi:10.1016/s0168-8278(01)00264-1 · Cited by 77
HLA-restricted epitope identification and detection of functional T cell responses by using MHC–peptide and costimulatory microarrays
Stone, J. D., Demkowicz, W. E., & Stern, L. J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407019102 · Cited by 77
Commercial high speed machines open new opportunities in high throughput flow cytometry (HTFC)
Ashcroft, R. G., & Lopez, P. (2000) · Journal of Immunological Methods · doi:10.1016/s0022-1759(00)00219-2 · Cited by 77
Reversal in the Immunodominance Hierarchy in Secondary CD8+ T Cell Responses to Influenza A Virus: Roles for Cross-Presentation and Lysis-Independent Immunodomination
Chen, W., Pang, K. C., Masterman, K., Kennedy, G., Basta, S., Dimopoulos, N., Hornung, F., Smyth, M. J., Bennink, J. R., & Yewdell, J. W. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.8.5021 · Cited by 77
“(9) based on the numbers of responding T CD8 as quantitated using MHC-class I peptide complex tetramers (10) or”
Method
Functionally Heterogeneous CD8+T-Cell Memory Is Induced by Sendai Virus Infection of Mice
Usherwood, E. J., Hogan, R. J., Crowther, G., Surman, S. L., Hogg, T. L., Altman, J. D., & Woodland, D. L. (1999) · Journal of Virology · doi:10.1128/jvi.73.9.7278-7286.1999 · Cited by 77
“Recently, the development of major histocompatibility complex (MHC) class I tetramers has made it possible to directly identify antigenspecific T cells ex vivo (3).”
BackgroundSelf-citation
Strategies for an HIV vaccine
Letvin, N. L. (2002) · Journal of Clinical Investigation · doi:10.1172/jci15985 · Cited by 77
Commensal Bacteria-Specific CD4+ T Cell Responses in Health and Disease
Sorini, C., Cardoso, R. F., Gagliani, N., & Villablanca, E. J. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02667 · Cited by 77
“Tetramers • Soluble MHC/peptide multimers with the capability of binding selected TCRs, useful for the ex vivo study of low-frequency endogenous antigen-specific CD4 or CD8 T cell populations (37, 38)”
Background
TIGIT limits immune pathology during viral infections
Schorer, M., Rakebrandt, N., Lambert, K., Hunziker, A., Pallmer, K., Oxenius, A., Kipar, A., Stertz, S., & Joller, N. (2020) · Nature Communications · doi:10.1038/s41467-020-15025-1 · Cited by 76
Clonotype Selection and Composition of Human CD8 T Cells Specific for Persistent Herpes Viruses Varies with Differentiation but Is Stable Over Time
Iancu, E. M., Corthésy, P., Baumgaertner, P., Devêvre, E., Voelter, V., Romero, P. J., Speiser, D. E., & Rufer, N. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0803647 · Cited by 76
“Immune responses to viruses (influenza, EBV, CMV, and HIV) are characterized by massive expansions of CD8 T lymphocytes (17, 42, 44) and by the preferential selection of a particular TCR-BV gene, as well as for the expansion of public clonotypes bearing common motifs in the amino acid sequence of the CDR3 region (26–2…”
Background
Streptabody, a high avidity molecule made by tetramerization of in vivo biotinylated, phage display-selected scFv fragments on streptavidin
Cloutier, S. M., Couty, S., Terskikh, A. V., Marguerat, L., Crivelli, V., Pugnière, M., Mani, J. C., Leisinger, H., Mach, J. P., & Deperthes, D. (2000) · Molecular Immunology · doi:10.1016/s0161-5890(01)00023-2 · Cited by 76
“The concept of site-specific in vivo biotinylation, originally described by Schatz (1993), has become very popular in recent years due to its application in the assembling of MHC class I tetramers on phycoerythrin–streptavidin for fluorometry analysis of T lymphocyte responses (Altman et al., 1996).”
Background
Human CTLs to Wild-Type and Enhanced Epitopes of a Novel Prostate and Breast Tumor-Associated Protein, TARP, Lyse Human Breast Cancer Cells
Oh, S., Terabe, M., Pendleton, C. D., Bhattacharyya, A., Bera, T. K., Epel, M., Reiter, Y., Phillips, J., Linehan, W. M., Kasten-Sportès, C., et al. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-2183 · Cited by 76
“synthesized as described previously (29, 30) using a single-chain HLA-A2”
Method
Determination of equid herpesvirus 1-specific, CD8+, cytotoxic T lymphocyte precursor frequencies in ponies
O'Neill, T., Kydd, J. H., Allen, G. P., Wattrang, E., Mumford, J. A., & Hannant, D. (1999) · Veterinary Immunology and Immunopathology · doi:10.1016/s0165-2427(99)00037-9 · Cited by 69
Cytotoxic-t-lymphocyte-mediated elimination of target cells transduced with engineered adeno-associated virus type 2 vector in vivo
Li, C., Hirsch, M., DiPrimio, N., Asokan, A., Goudy, K., Tisch, R., & Samulski, R. J. (2009) · Journal of Virology · doi:10.1128/jvi.00278-09 · Cited by 42
Development of a T-cell Receptor Mimic Antibody against Wild-Type p53 for Cancer Immunotherapy
Li, D., Bentley, C., Anderson, A., Wiblin, S., Cleary, K. L. S., Koustoulidou, S., Hassanali, T., Yates, J., Greig, J., Nordkamp, M. O., et al. (2017) · Cancer Research · doi:10.1158/0008-5472.can-16-3247 · Cited by 38
“12 HLA-A2 tetramers were generated as previously described(16, 17).”
Method
Longevity of T-Cell Memory following Acute Viral Infection
Walker, J. M., & Slifka, M. K. (2010) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4419-6451-9_8 · Cited by 30
Phage display enables machine learning discovery of cancer antigen–specific TCRs
Croce, G., Lani, R., Tardivon, D., Bobisse, S., de Tiani, M., Bragina, M., Perez, M. A. S., Michaux, J., Pak, H. S., Michel, A., et al. (2025) · Science Advances · doi:10.1126/sciadv.ads5589 · Cited by 23
Monitoring specific T-cell responses to melanoma vaccines: ELISPOT, tetramers, and beyond
Gajewski, T. F. (2000) · Clinical Diagnostic Laboratory Immunology · doi:10.1128/cdli.7.2.141-144.2000 · Cited by 21
“The starting T cells again can be unfractionated or purified CD81 cells, and the stimulator cell population can be an autologous tumor cell line or peptide-loaded autologous APCs.”
BackgroundInfluential

Authors: Altman, J. D., Moss, P. A. H., Goulder, P. J. R., Barouch, D. H., McHeyzer-Williams, M. G., Bell, J. I., McMichael, A. J., & Davis, M. M.
Affiliations: Stanford Medicine (US)
John Radcliffe Hospital (GB)
J. D. Altman and M. G. McHeyzer-Williams, Department of Microbiology and Immunology, Stanford University School of Medicine, Stanford, CA 94305-5428, USA.
Howard Hughes Medical Institute (US)
Corresponding author: Davis, Mark M.
ORCID: Altman, John D.
Moss, Paul A. H.
Goulder, Philip J. R.
Barouch, Dan H.
Bell, John I.
McMichael, Andrew J.
Davis, Mark M.
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 1996-10-04
Volume: 274
Issue: 5284
Pages: 94-96
ISSN: 0036-8075 (ISSN-L)
1095-9203
DOI: 10.1126/science.274.5284.94
OpenAlex: W2067069532
Cited by: 3,544
References: 39
Citations by year: 2026: 44 · 2025: 41 · 2024: 45 · 2023: 59 · 2022: 43 · 2021: 68 · 2020: 59 · 2019: 71 · 2018: 70 · 2017: 42 · 2016: 62 · 2015: 73 · 2014: 69 · 2013: 101 · 2012: 93
FWCI: 35.24
Type: journal article
Language: en
Open access: closed
Locations: Science (publishedVersion)
PubMed (publishedVersion)
Funders: Wellcome Trust
Topics: Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › vaccines and immunoinformatics approaches
Keywords: antigen-specific T cells, peptide-MHC tetramers, HLA-A2, cytotoxic T lymphocytes, cytotoxicity assay, T cell phenotyping, HIV infection, tumor-specific T cells, autoantigen-specific T cells
MeSH terms: Amino Acid Sequence, Epitopes, Antigens, Viral, Base Sequence, Cell Line, Coloring Agents, Flow Cytometry, HIV Seropositivity, Humans, Molecular Sequence Data, Peptide Fragments, Phenotype, RNA-Directed DNA Polymerase, T-Lymphocytes, Cytotoxic, Viral Matrix Proteins, Gene Products, gag, HLA-A2 Antigen, CD8-Positive T-Lymphocytes

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Phenotypic Analysis of Antigen-Specific T Lymphocytes

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