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Phenotypic Analysis of Antigen-Specific T Lymphocytes
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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“Studies can estimate the extent of CMV “obsession” by identifying antigen-specific cells using peptide-MHC class-I or class-II multimers (Altman et al. 1996; Davis et al. 2011).”
From Is immunosenescence influenced by our lifetime “dose” of exercise? (2016) · cites this paper as Altman et al. 1996
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“To evaluate whether or not circulating TAA-specific T cells exist in patients with metastatic melanoma as evidence for systemic immune response to cancer, and to study the native biological properties of such cells, we used MHC/peptide tetramers to stain T cells in an antigen-specific manne”
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“H-2K b tetramers were produced as described previously (20, 21) and stored frozen in Tris-buffered saline/16% glycerol/0.”
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“Akatsuka (Fred Hutchinson Cancer Research Center) and were produced in a manner that was similar to the original metho”
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“The recombinant protein was purified from inclusion bodies and refolded in vitro as describe”
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“notypic characterization of antigen-specific T cells by flow cytometry (5, 85).”
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“Soluble HLA-A2–peptide tetramers were produced as described previously (26).”
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“The development of HLA tetramers (BOX 1) and higher order multimers has been transformative for the study of T cell responses, as it has facilitated the ex vivo identification and quantification of antigenspecific T cells as well, as the mapping of their epitopes 93,94 .”
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“Recently, a novel technique has been developed that uses soluble antigen presenting molecules, loaded with a specific antigen and complexed into a fluorescently labeled tetrameric form (“tetramers”), to detect and characterize antigen-specific T cells (35).”
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“(11) described a method, using tetrameric soluble MHC class I–peptide complexes, for the identification of antigen-specific CD8 1 cells in the 1 Abbreviations used in this paper: b 2 M, b 2 microglobulin; CD, cluster of”
BackgroundMethodA minimal peptide substrate in biotin holoenzyme synthetase‐catalyzed biotinylation
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“The identified sequences have been fused to either the N-terminus or the C-terminus of a variety of proteins, and can be biotinylated either in vitro or in vivo ~Altman et al., 1996; Kim & McHenry, 1996; Tatsumi et al., 1996; Tsao et al., 1996; Smith et al., 1998!.”
BackgroundANTIGEN-SPECIFIC MEMORY B CELL DEVELOPMENT
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Self-citationQuantifying Memory CD8 T Cells Reveals Regionalization of Immunosurveillance
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“However, technical innovations, such as the development of MHC I tetramers (Altman et al., 1996), revealed that antigen-specific CD8 T cell responses were 10- to 100-fold bigger than initially thought, precipitating a substantial revision in conceptualization of the immune response (Murali-Krishna et al.”
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Einsele, H., Roosnek, E. E., Rufer, N., Sinzger, C., Riegler, S., Löffler, J., Grigoleit, U., Moris, A., Rammensee, H., Kanz, L., et al. (2002) · Blood · doi:10.1182/blood.v99.11.3916 · Cited by 699
Interleukin 15 Is Required for Proliferative Renewal of Virus-specific Memory CD8 T Cells
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“The availability of TCR transgenic T cells, the development of sensitive techniques for assessing T cell function at the single cell level, and perhaps most importantly, the ability to physically identify antigen-specific CD8 T cells using MHC class I tetramers, has greatly facilitated studies addressing the important…”
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“Tetramer synthesis and validation was performed as previously describe”
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“3 , are now available [61] [62] [63] [64] .”
Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes
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“, as determined by p11C tetramer staining of freshly isolated CD8 p T lymphocyte”
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Boon, T., Coulie, P. G., den Eynde, B. J. V., & van der Bruggen, P. (2005) · Annual Review of Immunology · doi:10.1146/annurev.immunol.24.021605.090733 · Cited by 670
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“H-2D b tetramers bound to LCMV GP(33–41) were generated as describe”
MethodSpeiser, D. E., Líénard, D., Rufer, N., Rubio‐Godoy, V., Rimoldi, D., Lejeune, F. J., Krieg, A. Μ., Cerottini, J., & Romero, P. J. (2005) · Journal of Clinical Investigation · doi:10.1172/jci23373 · Cited by 647
“called tetramers) were prepared as described previously (42, 51) with Melan-A analog peptide26–35 ELAGIGILTV.”
MethodWedemeyer, H. H., He, X.-S., Nascimbeni, M., Davis, A. R., Greenberg, H. B., Hoofnagle, J. H., Liang, T. J., Alter, H. J., & Rehermann, B. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.6.3447 · Cited by 635
“Virusspecific CD8 T cells have been investigated with tetramers in several diseases including HIV (12, 13), EBV (14), and CMV infection (13), and we and others have reported the use of tetramers in studies of HCV (6, 7, 15, 16).”
BackgroundCellular immune responses to HIV
McMichael, A. J., & Rowland‐Jones, S. (2001) · Nature · doi:10.1038/35073658 · Cited by 617
Self-citationFollicular Helper T Cells: Lineage and Location
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“Polyclonal Antigen-Specific Tfh Cells Directly monitoring antigen-specific Th cells in polyclonal immune systems (McHeyzer-Williams and Davis, 1995) and the advent of pMHCII tetramer technology (Altman et al., 1996) provides experimental access to the polyclonal immune system.”
BackgroundSelf-citationReantragoon, R., Corbett, A. J., Sakala, I. G., Gherardin, N. A., Furness, J. B., Chen, Z., Eckle, S. B. G., Uldrich, A. P., Birkinshaw, R. W., Patel, O., et al. (2013) · The Journal of Experimental Medicine · doi:10.1084/jem.20130958 · Cited by 594
“Tetramers of Agpresenting molecules permit Ag-specific T cells to be isolated, quantified, tracked, and characterized from the milieu of T cells within the host (Altman et al., 1996; Davis et al., 2011).”
BackgroundEstimating the Precursor Frequency of Naive Antigen-specific CD8 T Cells
Blattman, J. N., Antia, R., Sourdive, D. J. D., Wang, X., Kaech, S. M., Murali‐Krishna, K., Altman, J. D., & Ahmed, R. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20001021 · Cited by 583
“tide (KAVYNFATM) and prepared as previously described (3, 12).”
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“Because each of these cells is also exquisitely specific for a very small subset of peptide antigens, an ability to probe the status of cells specific for a given antigen, either by stimulation with antigen or by direct identification with peptide-MHC multimers (Altman et al., 1996; Davis et al., 2011), allows insight…”
BackgroundSelf-citationReverse Vaccinology: Developing Vaccines in the Era of Genomics
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“First, the breadth of alleles for which multimeric staining reagents are commonly available is constantly expanding (Altman et al., 1996; Bakker and Schumacher, 2005; McHeyzer-Williams et al., 1996).”
BackgroundAn immunomodulatory role for CD4+CD25+ regulatory T lymphocytes in hepatitis C virus infection
Cabrera, R., Tu, Z., Xu, Y., Firpi, R. J., Rosen, H. R., Liu, C., & Nelson, D. R. (2004) · Hepatology · doi:10.1002/hep.20454 · Cited by 561
McPAS‐TCR: a manually curated catalogue of pathology‐associated T cell receptor sequences
Tickotsky, N., Sagiv, T., Prilusky, J., Shifrut, E., & Friedman, N. (2017) · Bioinform. · doi:10.1093/bioinformatics/btx286 · Cited by 547
The foundations of immune checkpoint blockade and the ipilimumab approval decennial
Korman, A. J., Garrett-Thomson, S. C., & Lönberg, N. (2021) · Nature Reviews Drug Discovery · doi:10.1038/s41573-021-00345-8 · Cited by 572
Shaping and reshaping CD8+ T-cell memory
Harty, J. T., & Badovinac, V. P. (2008) · Nature reviews. Immunology · doi:10.1038/nri2251 · Cited by 570
In Vivo Identification of Glycolipid Antigen–Specific T Cells Using Fluorescent Cd1d Tetramers
Benlagha, K., Weiss, A. H., Beavis, A. J., Teyton, L., & Bendelac, A. S. (1999) · The Journal of Experimental Medicine · doi:10.1084/jem.191.11.1895 · Cited by 555
Guidelines for the use of flow cytometry and cell sorting in immunological studies *
Cossarizza, A., Chang, H., Radbruch, A., Akdiş, M., Andrä, I., Annunziato, F., Bächer, P., Barnaba, V., Battistini, L., Bauer, W. M., et al. (2017) · European Journal of Immunology · doi:10.1002/eji.201646632 · Cited by 595
Pierson, T. C., McArthur, J. C., & Siliciano, R. F. (2000) · Annual Review of Immunology · doi:10.1146/annurev.immunol.18.1.665 · Cited by 565
Autoimmune Destruction of Skin Melanocytes by Perilesional T Cells from Vitiligo Patients
van den Boorn, J. G., Konijnenberg, D., Dellemijn, T. A. M., van der Veen, J. P. W., Bos, J. D., Melief, C. J. M., Vyth‐Dreese, F. A., & Luiten, R. M. (2009) · Journal of Investigative Dermatology · doi:10.1038/jid.2009.32 · Cited by 542
“Tetramer synthesis and T-cell specificity analysis R-phycoerythrin (PE)- or allophycocyanin (APC)-conjugated HLAA2/peptide complex tetramers were synthesized as described before (Altman et al., 1996) for the antigens tyrosinase369-377 (YMDGTMSQV), gp100280-288 (YLEPGPVTA), gp100209-217 (ITDQVPFSV), MART-126-35 (modifi…”
Altered peptide ligand vaccination with Flt3 ligand expanded dendritic cells for tumor immunotherapy
Fong, L. H., Hou, Y., Rivas, A., Benike, C. J., Yuen, A. R., Fisher, G. A., Davis, M. M., & Engleman, E. G. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.141226398 · Cited by 540
Self-citationTumor antigens recognized by T cells
Boon, T., Coulie, P. G., & den Eynde, B. J. V. (1997) · Immunology Today · doi:10.1016/s0167-5699(97)80020-5 · Cited by 541
Tumour immunity: effector response to tumour and role of the microenvironment
Mantovani, A., Romero, P. J., Palucka, A. K., & Marincola, F. M. (2008) · The Lancet · doi:10.1016/s0140-6736(08)60241-x · Cited by 539
Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition)
Cossarizza, A., Chang, H., Radbruch, A., Abrignani, S., Addo, R., Akdis, M., Andrä, I., Andreata, F., Annunziato, F., Arranz, E., et al. (2021) · European Journal of Immunology · doi:10.1002/eji.202170126 · Cited by 531
Schluns, K. S., Williams, K., Ma, A. I., Zheng, X. X., & Lefrançois, L. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.168.10.4827 · Cited by 521
“VSV-Nspecific CD8 T cells were detected using H-2K b tetramers containing the N protein-derived peptide RGYVYQGL (14) and were generated as previously described (15, 16).”
MethodRomero, P. J., Dunbar, P. R., Valmori, D., Pittet, M. J., Ogg, G. S., Rimoldi, D., Chen, J., Líénard, D., Cerottini, J., & Cerundolo, V. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.188.9.1641 · Cited by 521
In Vivo Activation of Antigen-Specific CD4 T Cells
Jenkins, M. K., Khoruts, A., Ingulli, E. G., Mueller, D. L., McSorley, S. J., Reinhardt, R. L., Itano, A. A., & Pape, K. A. (2001) · Annual Review of Immunology · doi:10.1146/annurev.immunol.19.1.23 · Cited by 512
Signal 3 Determines Tolerance versus Full Activation of Naive CD8 T Cells
Curtsinger, J., Lins, D. C., & Mescher, M. F. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20021910 · Cited by 510
Huang, H., Wang, C., Rubelt, F., Scriba, T. J., & Davis, M. M. (2020) · Nature Biotechnology · doi:10.1038/s41587-020-0505-4 · Cited by 484
Self-citationCoordinate Regulation of Complex T Cell Populations Responding to Bacterial Infection
Busch, D. H., Pilip, I. M., Vijh, S., & Pamer, E. G. (1998) · Immunity · doi:10.1016/s1074-7613(00)80540-3 · Cited by 508
Pittet, M. J., Valmori, D., Dunbar, P. R., Speiser, D. E., Líénard, D., Lejeune, F. J., Fleischhauer, K., Cerundolo, V., Cerottini, J., & Romero, P. J. (1999) · The Journal of Experimental Medicine · doi:10.1084/jem.190.5.705 · Cited by 508
“Since the majority of HLAA * 0201 individuals are sensitized against the latter immunodominant peptide (25), it served as a source of welldefined memory-type, epitope-specific CTL populations in circulating lymphocytes (26).”
BackgroundThe Critical Need for CD4 Help in Maintaining Effective Cytotoxic T Lymphocyte Responses
Kalams, S. A., & Walker, B. D. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.188.12.2199 · Cited by 660
“(20) now provide insights into how CD4 deficiency may impair CTL responses, and like other recent advances in understanding of CTLs these data have been facilitated by the direct visualization of CTL using peptide–MHC tetramers (29).”
BackgroundAbbink, P., Lemckert, A. A. C., Ewald, B. A., Lynch, D. M., Denholtz, M., Smits, S., Holterman, L., Damen, I., Vogels, R., Thorner, A. R., et al. (2007) · Journal of Virology · doi:10.1128/jvi.02696-06 · Cited by 503
“Tetrameric H-2D complexes folded around the immunodominant SIV Gag AL11 epitope (AAVKNWMTQTL) (3) were prepared and utilized to stain peptide-specific CD8 T lymphocytes from C57BL/6 mice as described previously (1, 3).”
MethodSelf-citationColonna, M., Samaridis, J., Cella, M., Ångman, L., Allen, R. L., O’Callaghan, C. A., Dunbar, P. R., Ogg, G. S., Cerundolo, V., & Rolink, A. G. (1998) · PubMed · Cited by 499
A Re-Evaluation of the Frequency of CD8+ T Cells Specific for EBV in Healthy Virus Carriers
Tan, L., Gudgeon, N. H., Annels, N. E., Hansasuta, P., O’Callaghan, C. A., Rowland‐Jones, S., McMichael, A. J., Rickinson, A. B., & Callan, M. F. C. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.3.1827 · Cited by 499
“Soluble MHC-peptide tetramers were produced using a method similar to that described previously (16).”
MethodSelf-citationc-MAF-dependent regulatory T cells mediate immunological tolerance to a gut pathobiont
Xu, M., Pokrovskii, M., Ding, Y., Yi, R., Au, C., Harrison, O. J., Galan, C., Belkaid, Y., Bonneau, R., & Littman, D. R. (2018) · Nature · doi:10.1038/nature25500 · Cited by 498
“HH-E2 tetramer was kindly produced by the NIH Tetramer Core Facility 37 .”
A Kinetic Basis For T Cell Receptor Repertoire Selection during an Immune Response
Savage, P. A., Boniface, J. J., & Davis, M. M. (1999) · Immunity · doi:10.1016/s1074-7613(00)80048-5 · Cited by 498
Self-citationSustained Dysfunction of Antiviral CD8 + T Lymphocytes after Infection with Hepatitis C Virus
Gruener, N. H., Lechner, F., Jung, M., Diepolder, H. M., Gerlach, T. J., Lauer, G. M., Walker, B. D., Sullivan, J., Phillips, R., Pape, G. R., et al. (2001) · Journal of Virology · doi:10.1128/jvi.75.12.5550-5558.2001 · Cited by 493
Andersen, M. H., Schrama, D., Straten, P. T., & Becker, J. C. (2005) · Journal of Investigative Dermatology · doi:10.1038/sj.jid.5700001 · Cited by 492
“, 2002), fluorescently labeled multimeric peptide/MHC reagents in multicolor flow cytometry (Betts et al., 2003; Altman et al., 1996), and TCR clonotype mapping (Pannetier et al.”
BackgroundSingle-cell analysis tools for drug discovery and development
Heath, J. R., Ribas, A., & Mischel, P. S. (2016) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2015.16 · Cited by 473
“To understand immune responses to cancer, it is of significant interest to develop approaches that can match the TCR genes with their specific (or cognate) antigen, which usually result from nonsynonymous somatic mutations specific for each cancer 105,133,135–138, 140, 141 .”
Yager, E. J., Ahmed, M., Lanzer, K., Randall, T. D., Woodland, D. L., & Blackman, M. A. (2008) · The Journal of Experimental Medicine · doi:10.1084/jem.20071140 · Cited by 490
WHITESIDE, T. (2005) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2005.07.008 · Cited by 492
Two-photon tissue imaging: seeing the immune system in a fresh light
Cahalan, M. D., Parker, I., Wei, S. H., & Miller, M. J. (2002) · Nature reviews. Immunology · doi:10.1038/nri935 · Cited by 486
“Antigen-specific T cells can be identified in vivo using fluorescent peptide–MHC tetramer”
BackgroundTLR2 is expressed on activated T cells as a costimulatory receptor
Komai‐Koma, M., Jones, L., Ogg, G. S., Xu, D., & Liew, F. Y. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0400171101 · Cited by 487
Vance, R. E., Leavey, J. K., Altman, J. D., Jensen, P. E., & Raulet, D. H. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.188.10.1841 · Cited by 482
“The Qa-1 b / b 2m/Qdm complex was biotinylated with the BirA enzyme as described (37), purified on a UnoQ ion exchange column (Bio-Rad Laboratories, Hercules, CA), and tetramerized with streptavidin-APC (Molecular Probes Inc.”
MethodInfluentialSelf-citationCobbold, M., Khan, N., Pourgheysari, B., Tauro, S., McDonald, D., Osman, H., Assenmacher, M., Billingham, L., Steward, C., Crawley, C., et al. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20040613 · Cited by 480
“use of standard methods (20), and the components of the HLA–peptide tetra-”
MethodSelf-citationImmune Activation and CD8+ T-Cell Differentiation towards Senescence in HIV-1 Infection
Papagno, L., Spina, C. A., Marchant, A., Salio, M., Rufer, N., Little, S., Dong, T., Chesney, G., Waters, A., Easterbrook, P., et al. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020020 · Cited by 478
“HLA–peptide tetrameric complexes (‘‘tetramers’’) were produced as previously described (Altman et al. 1996) and included the following specificity: A2 HIV p17-SLYNTVATL and pol-ILKEPVHGV, A2 CMV pp65-NLVPMVATV, A2 EBV BMLF1-GLCTLVAML, A2 influenza matrix-GILGFVFTL, A2 melanA-ELAGIGILTV, B7 HIV nef-TPGPGVRYPL and gp41-…”
MethodSelf-citationDirect access to CD4+ T cells specific for defined antigens according to CD154 expression
Frentsch, M., Arbach, O., Kirchhoff, D., Moewes, B., Worm, M., Rothe, M., Scheffold, A., & Thiel, A. (2005) · Nature Medicine · doi:10.1038/nm1292 · Cited by 475
Hadrup, S. R., Strindhall, J., Køllgaard, T., Seremet, T., Johansson, B. E. A., Pawelec, G., Straten, P. T., & Wikby, A. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.4.2645 · Cited by 471
“insight regarding the biology of Ag-specific CD8 T cells (16).”
Background
Metadata
- 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
- Venue
- Science
- Published
- 1996-10-04
- Volume
- 274
- Issue
- 5284
- Pages
- 94-96
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- 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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