Rapid cloning of antigen-specific T-cell receptors by leveraging the cis activation of T cells.
Journal
Nature biomedical engineering
ISSN: 2157-846X
Titre abrégé: Nat Biomed Eng
Pays: England
ID NLM: 101696896
Informations de publication
Date de publication:
07 2022
07 2022
Historique:
received:
22
02
2021
accepted:
24
02
2022
pubmed:
9
4
2022
medline:
20
7
2022
entrez:
8
4
2022
Statut:
ppublish
Résumé
It is commonly understood that T cells are activated via trans interactions between antigen-specific T-cell receptors (TCRs) and antigenic peptides presented on major histocompatibility complex (MHC) molecules on antigen-presenting cells. By analysing a large number of T cells at the single-cell level on a microwell array, we show that T-cell activation can occur via cis interactions (where TCRs on the T cell interact with the antigenic peptides presented on MHC class-I molecules on the same cell), and that such cis activation can be used to detect antigen-specific T cells and clone their TCR within 4 d. We used the detection-and-cloning system to clone a tumour-antigen-specific TCR from peripheral blood mononuclear cells of healthy donors. TCR cloning by leveraging the cis activation of T cells may facilitate the development of TCR-engineered T cells for cancer therapy.
Identifiants
pubmed: 35393565
doi: 10.1038/s41551-022-00874-6
pii: 10.1038/s41551-022-00874-6
doi:
Substances chimiques
Antigens, Neoplasm
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
806-818Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Held, W. & Mariuzza, R. A. Cis interactions of immunoreceptors with MHC and non-MHC ligands. Nat. Rev. Immunol. 8, 269–278 (2008).
pubmed: 18309314
pmcid: 2491490
doi: 10.1038/nri2278
Garcia, K. C. et al. An αß T cell receptor structure at 2.5 A and its orientation in the TCR-MHC complex. Science 274, 209–219 (1996).
pubmed: 8824178
doi: 10.1126/science.274.5285.209
Jin, A. et al. A rapid and efficient single-cell manipulation method for screening antigen-specific antibody-secreting cells from human peripheral blood. Nat. Med. 15, 1088–1092 (2009).
pubmed: 19684583
doi: 10.1038/nm.1966
Tokimitsu, Y. et al. Single lymphocyte analysis with a microwell array chip. Cytometry A 71, 1003–1010 (2007).
pubmed: 17972305
doi: 10.1002/cyto.a.20478
Kobayashi, E. et al. A new cloning and expression system yields and validates TCRs from blood lymphocytes of patients with cancer within 10 days. Nat. Med. 19, 1542–1546 (2013).
pubmed: 24121927
doi: 10.1038/nm.3358
Pang, S. S. et al. The structural basis for autonomous dimerization of the pre-T-cell antigen receptor. Nature 467, 844–848 (2010).
pubmed: 20944746
doi: 10.1038/nature09448
Tawara, I. et al. Safety and persistence of WT1-specific T-cell receptor gene-transduced lymphocytes in patients with AML and MDS. Blood 130, 1985–1994 (2017).
pubmed: 28860210
doi: 10.1182/blood-2017-06-791202
Chapuis, A. G. et al. T cell receptor gene therapy targeting WT1 prevents acute myeloid leukemia relapse post-transplant. Nat. Med. 25, 1064–1072 (2019).
pubmed: 31235963
pmcid: 6982533
doi: 10.1038/s41591-019-0472-9
Rapoport, A. P. et al. NY-ESO-1-specific TCR-engineered T cells mediate sustained antigen-specific antitumor effects in myeloma. Nat. Med. 21, 914–921 (2015).
pubmed: 26193344
pmcid: 4529359
doi: 10.1038/nm.3910
Clarke, S. R. et al. Characterization of the ovalbumin-specific TCR transgenic line OT-I: MHC elements for positive and negative selection. Immunol. Cell Biol. 78, 110–117 (2000).
pubmed: 10762410
doi: 10.1046/j.1440-1711.2000.00889.x
Ober, B. T. et al. Affinity of thymic self-peptides for the TCR determines the selection of CD8(+) T lymphocytes in the thymus. Int. Immunol. 12, 1353–1363 (2000).
pubmed: 10967031
doi: 10.1093/intimm/12.9.1353
Betts, M. R. et al. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 281, 65–78 (2003).
pubmed: 14580882
doi: 10.1016/S0022-1759(03)00265-5
Zehn, D., Lee, S. Y. & Bevan, M. J. Complete but curtailed T-cell response to very low-affinity antigen. Nature 458, 211–214 (2009).
pubmed: 19182777
pmcid: 2735344
doi: 10.1038/nature07657
Fu, G. et al. Themis sets the signal threshold for positive and negative selection in T-cell development. Nature 504, 441–445 (2013).
pubmed: 24226767
pmcid: 3977001
doi: 10.1038/nature12718
Mareeva, T., Lebedeva, T., Anikeeva, N., Manser, T. & Sykulev, Y. Antibody specific for the peptide.major histocompatibility complex. Is it T cell receptor-like? J. Biol. Chem. 279, 44243–44249 (2004).
pubmed: 15302863
doi: 10.1074/jbc.M407021200
Linsley, P. S. & Ledbetter, J. A. The role of the CD28 receptor during T cell responses to antigen. Annu. Rev. Immunol. 11, 191–212 (1993).
pubmed: 8386518
doi: 10.1146/annurev.iy.11.040193.001203
Yang, J. et al. Kupfer-type immunological synapse characteristics do not predict anti-brain tumor cytolytic T-cell function in vivo. Proc. Natl Acad. Sci. USA 107, 4716–4721 (2010).
pubmed: 20133734
pmcid: 2842057
doi: 10.1073/pnas.0911587107
Grakoui, A. et al. The immunological synapse: a molecular machine controlling T cell activation. Science 285, 221–227 (1999).
pubmed: 10398592
doi: 10.1126/science.285.5425.221
Santos, A. M. et al. Capturing resting T cells: the perils of PLL. Nat. Immunol. 19, 203–205 (2018).
pubmed: 29476188
pmcid: 7612954
doi: 10.1038/s41590-018-0048-8
Baniyash, M. TCR zeta-chain downregulation: curtailing an excessive inflammatory immune response. Nat. Rev. Immunol. 4, 675–687 (2004).
pubmed: 15343367
doi: 10.1038/nri1434
Desombere, I. et al. The interferon gamma secretion assay: a reliable tool to study interferon gamma production at the single cell level. J. Immunol. Methods 286, 167–185 (2004).
pubmed: 15087231
doi: 10.1016/j.jim.2004.01.001
Hu, Z. et al. A cloning and expression system to probe T-cell receptor specificity and assess functional avidity to neoantigens. Blood 132, 1911–1921 (2018).
pubmed: 30150207
pmcid: 6213317
doi: 10.1182/blood-2018-04-843763
Aleksic, M. et al. Different affinity windows for virus and cancer-specific T-cell receptors: implications for therapeutic strategies. Eur. J. Immunol. 42, 3174–3179 (2012).
pubmed: 22949370
pmcid: 3776049
doi: 10.1002/eji.201242606
Cheever, M. A. et al. The prioritization of cancer antigens: a national cancer institute pilot project for the acceleration of translational research. Clin. Cancer Res. 15, 5323–5337 (2009).
pubmed: 19723653
pmcid: 5779623
doi: 10.1158/1078-0432.CCR-09-0737
Tsuboi, A. et al. Enhanced induction of human WT1-specific cytotoxic T lymphocytes with a 9-mer WT1 peptide modified at HLA-A*2402-binding residues. Cancer Immunol. Immunother. 51, 614–620 (2002).
pubmed: 12439606
doi: 10.1007/s00262-002-0328-9
Ge, Q. et al. Soluble peptide-MHC monomers cause activation of CD8+ T cells through transfer of the peptide to T cell MHC molecules. Proc. Natl Acad. Sci. USA 99, 13729–13734 (2002).
pubmed: 12374859
pmcid: 129758
doi: 10.1073/pnas.212515299
Pearse, B. M. Clathrin: a unique protein associated with intracellular transfer of membrane by coated vesicles. Proc. Natl Acad. Sci. USA 73, 1255–1259 (1976).
pubmed: 1063406
pmcid: 430241
doi: 10.1073/pnas.73.4.1255
Anderson, R. G. The caveolae membrane system. Annu. Rev. Biochem. 67, 199–225 (1998).
pubmed: 9759488
doi: 10.1146/annurev.biochem.67.1.199
Garcia, K. C. et al. Structural basis of plasticity in T cell receptor recognition of a self peptide-MHC antigen. Science 279, 1166–1172 (1998).
pubmed: 9469799
doi: 10.1126/science.279.5354.1166
von Boehmer, H. et al. Control of T-cell development by the TCR alpha beta for antigen. Cold Spring Harb. Symp. Quant. Biol. 54, 111–118 (1989).
doi: 10.1101/SQB.1989.054.01.014
Persaud, S. P., Parker, C. R., Lo, W. L., Weber, K. S. & Allen, P. M. Intrinsic CD4+ T cell sensitivity and response to a pathogen are set and sustained by avidity for thymic and peripheral complexes of self peptide and MHC. Nat. Immunol. 15, 266–274 (2014).
pubmed: 24487322
pmcid: 3944141
doi: 10.1038/ni.2822
Lyu, F. et al. A novel and simple method to produce large amounts of recombinant soluble peptide/major histocompatibility complex monomers for analysis of antigen-specific human T cell receptors. N. Biotechnol. 49, 169–177 (2019).
pubmed: 30465909
doi: 10.1016/j.nbt.2018.11.005
Cohen, C. J. et al. Isolation of neoantigen-specific T cells from tumor and peripheral lymphocytes. J. Clin. Invest. 125, 3981–3991 (2015).
pubmed: 26389673
pmcid: 4607110
doi: 10.1172/JCI82416
Tran, E. et al. Immunogenicity of somatic mutations in human gastrointestinal cancers. Science 350, 1387–1390 (2015).
pubmed: 26516200
pmcid: 7445892
doi: 10.1126/science.aad1253
Freeman, J. D., Warren, R. L., Webb, J. R., Nelson, B. H. & Holt, R. A. Profiling the T-cell receptor beta-chain repertoire by massively parallel sequencing. Genome Res. 19, 1817–1824 (2009).
pubmed: 19541912
pmcid: 2765271
doi: 10.1101/gr.092924.109
Robins, H. S. et al. Comprehensive assessment of T-cell receptor beta-chain diversity in αβ T cells. Blood 114, 4099–4107 (2009).
pubmed: 19706884
pmcid: 2774550
doi: 10.1182/blood-2009-04-217604
Wang, C. et al. High throughput sequencing reveals a complex pattern of dynamic interrelationships among human T cell subsets. Proc. Natl Acad. Sci. USA 107, 1518–1523 (2010).
pubmed: 20080641
pmcid: 2824416
doi: 10.1073/pnas.0913939107
Linnemann, C. et al. High-throughput identification of antigen-specific TCRs by TCR gene capture. Nat. Med. 19, 1534–1541 (2013).
pubmed: 24121928
doi: 10.1038/nm.3359
Turchaninova, M. A. et al. Pairing of T-cell receptor chains via emulsion PCR. Eur. J. Immunol. 43, 2507–2515 (2013).
pubmed: 23696157
doi: 10.1002/eji.201343453
Han, A., Glanville, J., Hansmann, L. & Davis, M. M. Linking T-cell receptor sequence to functional phenotype at the single-cell level. Nat. Biotechnol. 32, 684–692 (2014).
pubmed: 24952902
pmcid: 4337815
doi: 10.1038/nbt.2938
Kondo, T. et al. Notch-mediated conversion of activated T cells into stem cell memory-like T cells for adoptive immunotherapy. Nat. Commun. 8, 15338 (2017).
pubmed: 28530241
pmcid: 5458121
doi: 10.1038/ncomms15338
Mo, F. et al. An engineered IL-2 partial agonist promotes CD8(+) T cell stemness. Nature 597, 544–548 (2021).
pubmed: 34526724
pmcid: 9172917
doi: 10.1038/s41586-021-03861-0
Weber, E. W. et al. Transient rest restores functionality in exhausted CAR-T cells through epigenetic remodeling. Science 372, eaba1786 (2021).
pubmed: 33795428
pmcid: 8049103
doi: 10.1126/science.aba1786
Ueno, T., Tomiyama, H., Fujiwara, M., Oka, S. & Takiguchi, M. Functionally impaired HIV-specific CD8 T cells show high affinity TCR-ligand interactions. J. Immunol. 173, 5451–5457 (2004).
pubmed: 15494492
doi: 10.4049/jimmunol.173.9.5451
Miyahara, Y. et al. Determination of cellularly processed HLA-A2402-restricted novel CTL epitopes derived from two cancer germ line genes, MAGE-A4 and SAGE. Clin. Cancer Res. 11, 5581–5589 (2005).
pubmed: 16061876
doi: 10.1158/1078-0432.CCR-04-2585
Hamana, H., Shitaoka, K., Kishi, H., Ozawa, T. & Muraguchi, A. A novel, rapid and efficient method of cloning functional antigen-specific T-cell receptors from single human and mouse T-cells. Biochem. Biophys. Res. Commun. 474, 709–714 (2016).
pubmed: 27155153
doi: 10.1016/j.bbrc.2016.05.015
Morita, S., Kojima, T. & Kitamura, T. Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther. 7, 1063–1066 (2000).
pubmed: 10871756
doi: 10.1038/sj.gt.3301206
Kinsella, T. M. & Nolan, G. P. Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Hum. Gene Ther. 7, 1405–1413 (1996).
pubmed: 8844199
doi: 10.1089/hum.1996.7.12-1405
Shitaoka, K. et al. Identification of tumoricidal TCRs from tumor-infiltrating lymphocytes by single-cell analysis. Cancer Immunol. Res. 6, 378–388 (2018).
pubmed: 29475880
doi: 10.1158/2326-6066.CIR-17-0489
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486–501 (2010).
pubmed: 20383002
pmcid: 2852313
doi: 10.1107/S0907444910007493