Global k
Avidity
T-cell population
TCR
koff-rate
Journal
European journal of immunology
ISSN: 1521-4141
Titre abrégé: Eur J Immunol
Pays: Germany
ID NLM: 1273201
Informations de publication
Date de publication:
04 2022
04 2022
Historique:
revised:
07
12
2021
received:
21
08
2021
accepted:
24
01
2022
pubmed:
1
2
2022
medline:
8
4
2022
entrez:
31
1
2022
Statut:
ppublish
Résumé
The avidity of TCRs for peptide-major histocompatibility complexes (pMHCs) is a governing factor in how T cells respond to antigen. TCR avidity is generally linked to T-cell functionality and there is growing evidence for distinct roles of low and high avidity T cells in different phases of immune responses. While physiological immune responses and many therapeutic T-cell products targeting infections or cancers consist of polyclonal T-cell populations with a wide range of individual avidities, the role of T-cell avidity is usually investigated only in monoclonal experimental settings. In this report, we induced polyclonal T-cell responses with a wide range of avidities toward a model epitope by altered peptide ligands, and benchmarked global avidity of physiological polyclonal populations by investigation of TCR-pMHC k
Identifiants
pubmed: 35099805
doi: 10.1002/eji.202149597
doi:
Substances chimiques
Antigens
0
Peptides
0
Receptors, Antigen, T-Cell
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
582-596Informations de copyright
© 2022 The Authors. European Journal of Immunology published by Wiley-VCH GmbH.
Références
van der Merwe, P. A. and Davis, S. J., Molecular interactions mediating T cell antigen recognition. Annu. Rev. Immunol. 2003. 21: 659-684.
Trambas, C. M. and Griffiths, G. M., Delivering the kiss of death. Nat. Immunol. 2003. 4: 399-403.
Zhong, S., Malecek, K., Johnson, L. A., Yu, Z., Vega-Saenz de Miera, E., Darvishian, F., McGary, K. et al., T-cell receptor affinity and avidity defines antitumor response and autoimmunity in T-cell immunotherapy. Proc. Natl. Acad. Sci. USA 2013. 110: 6973-6978.
Hombrink, P., Raz, Y., Kester, M. G. D., de Boer, R., Weißbrich, B., von dem Borne, P. A., Busch, D. H. et al., Mixed functional characteristics correlating with tcr-ligand koff -rate of MHC-tetramer reactive t cells within the naive T-cell repertoire. Eur. J. Immunol. 2013. 43: 3038-3050.
Nauerth, M., Weißbrich, B., Knall, R., Franz, T., Dössinger, G., Bet, J., Paszkiewicz, P. J., et al., TCR-ligand koff rate correlates with the protective capacity of antigen-specific Cd8+ T cells for adoptive transfer. Sci. Transl. Med. 2013. 5: 192ra87.
Schober, K., Voit, F., Grassmann, S., Müller, T. R., Eggert, J., Jarosch, S., Weißbrich, B. et al., Reverse TCR repertoire evolution toward dominant low-affinity clones during chronic CMV infection. Nat. Immunol. 2020. 21: 434-441.
Martinez, R. J., Andargachew, R., Martinez, H. A. and Evavold, B. D., Low-affinity CD4+ T cells are major responders in the primary immune response. Nat. Commun. 2016. 7: 13848.
Zehn, D., Lee, S. Y. and Bevan, M. J., Complete but curtailed T cell response to very low affinity antigen. Nature 2009. 458: 211-214.
Lever, M., Maini, P. K., van der Merwe, P. A. and Dushek, O., Phenotypic models of T cell activation. Nat. Rev. Immunol. 2014. 14: 619-629.
Kalergis, A. M., Boucheron, N., Doucey, M. A., Palmieri, E., Goyarts, E. C., Vegh, Z., Luescher, I. F. and Nathenson, S. G., Efficient T cell activation requires an optimal dwell-time of interaction between the TCR and the PMHC complex. Nat. Immunol. 2001. 2: 229-234.
Corr, M., Slanetz, A. E., Boyd, L. F., Jelonek, M. T., Khilko, S., al-Ramadi, B. K., Kim, Y. S. et al., T cell receptor-mhc class i peptide interactions: Affinity, kinetics, and specificity. Science 1994. 265: 946-949.
Huppa, J. B., Axmann, M., Mörtelmaier, M. A., Lillemeier, B. F., Newell, E. W., Brameshuber, M., Klein, L. O. et al., TCR-peptide-MHC interactions in situ show accelerated kinetics and increased affinity. Nature 2010. 463: 963-967.
Huang, J., Zarnitsyna, V. I., Liu, B., Edwards, L. J., Jiang, N., Evavold, B. D. and Zhu, C., The kinetics of two-dimensional TCR and PMHC interactions determine T-cell responsiveness. Nature 2010. 464: 932-936.
Hebeisen, M., Schmidt, J., Guillaume, P., Baumgaertner, P., Speiser, D. E., Luescher, I. and Rufer, N., Identification of rare high-avidity, tumor-reactive CD8+ T cells by monomeric TCR-ligand off-rates measurements on living cells. Cancer Res. 2015. 75: 1983-1991.
Dutoit, V., Rubio-Godoy, V., Doucey, M. - A., Batard, P., Liénard, D., Rimoldi, D., Speiser, D. et al., Functional avidity of tumor antigen-specific ctl recognition directly correlates with the stability of MHC/peptide multimer binding to TCR. J. Immunol. 2002. 168: 1167-1171.
Yee, C., Savage, P. A., Lee, P. P., Davis, M. M. and Greenberg, P. D., Isolation of high avidity melanoma-reactive CTL from heterogeneous populations using peptide-MHC tetramers. J. Immunol. 1999. 162: 2227-2234.
Busch, D. H. and Pamer, E. G., T cell affinity maturation by selective expansion during infection. J. Exp. Med. 1999. 189: 701-710.
Sherwood, A. M., Emerson, R. O., Scherer, D., Habermann, N., Buck, K., Staffa, J., Desmarais, C. et al., Tumor-infiltrating lymphocytes in colorectal tumors display a diversity of T cell receptor sequences that differ from the T cells in adjacent mucosal tissue. Cancer Immunol. Immunother 2013. 62: 1453-1461.
Neuenhahn, M., Albrecht, J., Odendahl, M., Schlott, F., Dössinger, G., Schiemann, M., Lakshmipathi, S. et al., Transfer of minimally manipulated CMV-specific T cells from stem cell or third-party donors to treat cmv infection after allo-HSCT. Leukemia 2017. 31: 2161-2171.
Verfuerth, S., Peggs, K., Vyas, P., Barnett, L., O'Reilly, R. J. and Mackinnon, S., Longitudinal monitoring of immune reconstitution by CDR3 size spectratyping after T-cell-depleted allogeneic bone marrow transplant and the effect of donor lymphocyte infusions on T-cell repertoire. Blood 2000. 95: 3990-3995.
Twyman-Saint Victor, C., Rech, A. J., Maity, A., Rengan, R., Pauken, K. E., Stelekati, E., Benci, J. L. et al., Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature 2015. 520: 373-377.
Allard, M., Couturaud, B., Carretero-Iglesia, L., Duong, M. N., Schmidt, J., Monnot, G. C., Romero, P. et al., TCR-ligand dissociation rate is a robust and stable biomarker of cd8+ t cell potency. JCI Insight 2017. 2: e92570.
Nauerth, M., Stemberger, C., Mohr, F., Weißbrich, B., Schiemann, M., Germeroth, L. and Busch, D. H., Flow cytometry-based TCR-ligand koff -rate assay for fast avidity screening of even very small antigen-specific T cell populations ex vivo. Cytometry. Part A J Int Socr Analyticl Cytol 2016. 89: 816-825.
Gannon, P. O., Wieckowski, S., Baumgaertner, P., Hebeisen, M., Allard, M., Speiser, D. E. and Rufer, N., Quantitative TCR:pMHC dissociation rate assessment by ntamers reveals antimelanoma T cell repertoires enriched for high functional competence. J. Immunol. 2015. 195: 356-366.
Martin-Blanco, N., Blanco, R., Alda-Catalinas, C., Bovolenta, E. R., Oeste, C. L., Palmer, E., Schamel, W. W. et al., A window of opportunity for cooperativity in the T cell receptor. Nat. Commun. 2018. 9: 2618.
Fuertes Marraco, S. A., Soneson, C., Cagnon, L., Gannon, P. O., Allard, M., Abed Maillard, S., Montandon, N. et al., Long-lasting stem cell-like memory CD8+ T cells with a naïve-like profile upon yellow fever vaccination. Sci. Transl. Med. 2015. 7: 282ra48.
Stone, J. D., Chervin, A. S. and Kranz, D. M., T-cell receptor binding affinities and kinetics: Impact on t-cell activity and specificity. Immunology 2009. 126: 165-176.
Matsui, K., Boniface, J. J., Steffner, P., Reay, P. A. and Davis, M. M., Kinetics of T-cell receptor binding to peptide/i-ek complexes: correlation of the dissociation rate with T-cell responsiveness. Proc. Natl. Acad. Sci. USA. 1994. 91: 12862-12866.
Bullock, T. N., Mullins, D. W., Colella, T. A. and Engelhard, V. H., Manipulation of avidity to improve effectiveness of adoptively transferred CD8(+) T cells for melanoma immunotherapy in human MHC class i-transgenic mice. J. Immunol. 2001. 167: 5824-5831.
Wilde, S., Sommermeyer, D., Leisegang, M., Frankenberger, B., Mosetter, B., Uckert, W. and Schendel, D. J., Human antitumor CD8+ T cells producing Th1 polycytokines show superior antigen sensitivity and tumor recognition. J. Immunol. 2012. 189: 598-605.
Tian, S., Maile, R., Collins, E. J. and Frelinger, J. A., Cd8+ T cell activation is governed by TCR-peptide/MHC affinity, not dissociation rate. J. Immunol. 2007. 179: 2952-2960.
Laugel, B., van den Berg, H. A., Gostick, E., Cole, D. K., Wooldridge, L., Boulter, J., Milicic, A. et al., Different t cell receptor affinity thresholds and CD8 coreceptor dependence govern cytotoxic t lymphocyte activation and tetramer binding properties. J. Biol. Chem. 2007. 282: 23799-23810.
Rius, C., Attaf, M., Tungatt, K., Bianchi, V., Legut, M., Bovay, A., Donia, M. et al., Peptide-MHC class i tetramers can fail to detect relevant functional T cell clonotypes and underestimate antigen-reactive T-cell populations. J. Immunol. 2018. 200: 2263-2279.
Savage, P. A., Boniface, J. J. and Davis, M. M., A kinetic basis for T cell receptor repertoire selection during an immune response. Immunity. 1999. 10: 485-492.
Schmid, D. A., Irving, M. B., Posevitz, V., Hebeisen, M., Posevitz-Fejfar, A., Sarria, J.-C. F., Gomez-Eerland, R. et al., Evidence for a TCR affinity threshold delimiting maximal Cd8 T cell function. J. Immunol. 2010. 184: 4936-4946.
Tan, M. P., Gerry, A. B., Brewer, J. E., Melchiori, L., Bridgeman, J. S., Bennett, A. D., Pumphrey, N. J. et al., T cell receptor binding affinity governs the functional profile of cancer-specific Cd8+ T cells. Clin. Exp. Immunol. 2015. 180: 255-270.
Cafri, G., Yossef, R., Pasetto, A., Deniger, D. C., Lu, Y. - C., Parkhurst, M., Gartner, J. J. et al., Memory T cells targeting oncogenic mutations detected in peripheral blood of epithelial cancer patients. Nat. Commun. 2019. 10: 449.
D'Ippolito, E., Schober, K., Nauerth, M. and Busch, D. H., T cell engineering for adoptive T cell therapy: safety and receptor avidity. Cancer Immunol. Immunother. 2019. 68: 1701-1712.
Cossarizza, A., Chang, H. - D., Radbruch, A., Abrignani, S., Addo, R., Akdis, M., Andrä, I. et al., Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition). Eur. J. Immunol. 2021. 51: 2708-3145.