High-throughput identification of antigen-specific TCRs by TCR gene capture

Nature Medicine

Volumn 19, Issue 11, 2013, Pages 1534-1541

  Linnemann, Carsten ^a   Heemskerk, Bianca ^a   Kvistborg, Pia ^a   Kluin, Roelof J C ^a   Bolotin, Dmitriy A ^b   Chen, Xiaojing ^c,d   Bresser, Kaspar ^a   Nieuwland, Marja ^a   Schotte, Remko ^a,e   Michels, Samira ^a   Gomez Eerland, Raquel ^a   Jahn, Lorenz ^f   Hombrink, Pleun ^f   Legrand, Nicolas ^e,g,i,j   Shu, Chengyi Jenny ^a   Mamedov, Ilgar Z ^b   Velds, Arno ^a   Blank, Christian U ^a   Haanen, John B A G ^a   Turchaninova, Maria A ^b   Kerkhoven, Ron M ^a   Spits, Hergen ^e,g   Hadrup, Sine Reker ^h   Heemskerk, Mirjam H M ^f   Blankenstein, Thomas ^c,d   Chudakov, Dmitriy M ^b   Bendle, Gavin M ^a,i   Schumacher, Ton N M ^a   more..

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e UNIVERSITY OF AMSTERDAM   (Netherlands)

^f LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^g AIMM Therapeutics   (Netherlands)

^h GENTOFTE UNIVERSITY HOSPITAL   (Denmark)

ⁱ INSTITUT PASTEUR   (France)

^j UNIVERSITY OF BIRMINGHAM   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GENOMIC DNA; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANTIGEN SPECIFICITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE LOCUS; GENE THERAPY; GENE TRANSFER; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; LYMPHOCYTE SUBPOPULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; T LYMPHOCYTE RECEPTOR GENE; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; ANTIGENS, NEOPLASM; GENE LIBRARY; GENES, T-CELL RECEPTOR; GENETIC THERAPY; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MICE; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES;

MUS;

EID: 84887453773     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3359     Document Type: Article

References (49)

1. Restifo, N.P., Dudley, M.E. & Rosenberg, S.A. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat. Rev. Immunol. 12, 269-281 (2012).
2. Dudley, M.E. et al. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298, 850-854 (2002).
3. Besser, M.J. et al. Clinical responses in a phase II study using adoptive transfer of short-term cultured tumor infiltration lymphocytes in metastatic melanoma patients. Clin. Cancer Res. 16, 2646-2655 (2010).
4. Schumacher, T.N. T-cell-receptor gene therapy. Nat. Rev. Immunol. 2, 512-519 (2002).
5. Linnemann, C., Schumacher, T.N. & Bendle, G.M. T-cell receptor gene therapy: critical parameters for clinical success. J. Invest. Dermatol. 131, 1806-1816 (2011).
6. Morgan, R.A. et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314, 126-129 (2006).
7. Johnson, L.A. et al. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 114, 535-546 (2009).
8. Robbins, P.F. et al. Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J. Clin. Oncol. 29, 917-924 (2011).
9. Simpson, A.J., Caballero, O.L., Jungbluth, A., Chen, Y.T. & Old, L.J. Cancer/testis antigens, gametogenesis and cancer. Nat. Rev. Cancer 5, 615-625 (2005).
10. Scanlan, M.J., Simpson, A.J. & Old, L.J. The cancer/testis genes: review, standardization, and commentary. Cancer Immun. 4, 1 (2004).
11. Reddy, S.T. et al. Monoclonal antibodies isolated without screening by analyzing the variable-gene repertoire of plasma cells. Nat. Biotechnol. 28, 965-969 (2010).
12. Kwakkenbos, M.J. et al. Generation of stable monoclonal antody-producing B cell receptor-positive human memory B cells by genetic programming. Nat. Med. 16, 123-128 (2010).
13. Wrammert, J. et al. Rapid cloning of high-affinity human monoclonal antibodies against influenza virus. Nature 453, 667-671 (2008).
14. Heemskerk, M.H. et al. Efficiency of T cell receptor expression in dual-specific T cells is controlled by the intrinsic qualities of the TCR chains within the TCR-CD3 complex. Blood 109, 235-243 (2007).
15. Mamedov, I.Z. et al. Quantitative tracking of T cell clones after haematopoietic stem cell transplantation. EMBO Mol. Med. 3, 201-207 (2011).
16. Bolotin, D.A. et al. Next generation sequencing for TCR repertoire profiling: Platform-specific features and correction algorithms. Eur. J. Immunol. 42, 3073-3083 (2012).
17. Andersen, R.S. et al. Dissection of T cell antigen specificity in human melanoma. Cancer Res. 72, 1642-1650 (2012).
18. Kvistborg, P. et al. TIL therapy broadens the tumor-reactive CD8+ T cell compartment in melanoma patients. OncoImmunology 1, 409-418 (2012).
19. Derbinski, J. & Kyewski, B. How thymic antigen presenting cells sample the body's self-antigens. Curr. Opin. Immunol. 22, 592-600 (2010).
20. Sadovnikova, E. & Stauss, H.J. Peptide-specific cytotoxic T lymphocytes restricted by nonself major histocompatibility complex class I molecules: reagents for tumor immunotherapy. Proc. Natl. Acad. Sci. USA 93, 13114-13118 (1996).
21. Amir, A.L. et al. PRAME-specific allo-HLA-restricted T cells with potent antitumor reactivity useful for therapeutic T-cell receptor gene transfer. Clin. Cancer Res. 17, 5615-5625 (2011).
22. Li, Y. et al. Directed evolution of human T-cell receptors with picomolar affinities by phage display. Nat. Biotechnol. 23, 349-354 (2005).
23. Li, L.P. et al. Transgenic mice with a diverse human T cell antigen receptor repertoire. Nat. Med. 16, 1029-1034 (2010).
24. Stanislawski, T. et al. Circumventing tolerance to a human MDM2-derived tumor antigen by TCR gene transfer. Nat. Immunol. 2, 962-970 (2001).
25. Wilde, S. et al. Dendritic cells pulsed with RNA encoding allogeneic MHC and antigen induce T cells with superior antitumor activity and higher TCR functional avidity. Blood 114, 2131-2139 (2009).
26. Traggiai, E. et al. Development of a human adaptive immune system in cord blood cell-transplanted mice. Science 304, 104-107 (2004).
27. Gimeno, R. et al. Monitoring the effect of gene silencing by RNA interference in human CD34+ cells injected into newborn RAG2?/? ?c?/? mice: functional inactivation of p53 in developing T cells. Blood 104, 3886-3893 (2004).
28. Hombrink, P. et al. High-throughput identification of potential minor histocompatibility antigens by MHC tetramer-based screening: feasibility and limitations. PLoS ONE 6, e22523 (2011).
29. Jorritsma, A. et al. Selecting highly affine and well-expressed TCRs for gene therapy of melanoma. Blood 110, 3564-3572 (2007).
30. Hodis, E. et al. A landscape of driver mutations in melanoma. Cell 150, 251-263 (2012).
31. Pleasance, E.D. et al. A small-cell lung cancer genome with complex signatures of tobacco exposure. Nature 463, 184-190 (2010).
32. Wang, G.C., Dash, P., McCullers, J.A., Doherty, P.C. & Thomas, P.G. T cell receptor diversity inversely correlates with pathogen-specific antibody levels in human cytomegalovirus infection. Sci. Transl. Med. 4, 128ra142 (2012).
33. Seitz, S. et al. Reconstitution of paired T cell receptor ?-and ?-chains from microdissected single cells of human inflammatory tissues. Proc. Natl. Acad. Sci. USA 103, 12057-12062 (2006).
34. Matsushita, H. et al. Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature 482, 400-404 (2012).
35. Castle, J.C. et al. Exploiting the mutanome for tumor vaccination. Cancer Res. 72, 1081-1091 (2012).
36. van Rooij, N. et al. Tumor exome analysis reveals neo-antigen-specific T cell reactivity in an ipilimumab-responsive melanoma. J. Clin. Oncol. doi:10.1200/JCO.2012.47.7521 (16 September 2013).
37. de Witte, M.A. et al. An inducible caspase 9 safety switch can halt cell therapy-induced autoimmune disease. J. Immunol. 180, 6365-6373 (2008).
38. Kieback, E., Charo, J., Sommermeyer, D., Blankenstein, T. & Uckert, W. A safeguard eliminates T cell receptor gene-modified autoreactive T cells after adoptive transfer. Proc. Natl. Acad. Sci. USA 105, 623-628 (2008).
39. Kalos, M. et al. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced Leukemia. Sci. Transl. Med. 3, 95ra73 (2011).
40. Kebriaei, P. et al. Infusing CD19-directed T cells to augment disease control in patients undergoing autologous hematopoietic stem-cell transplantation for advanced B-lymphoid malignancies. Hum. Gene Ther. 23, 444-450 (2012).
41. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).
42. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
43. Krzywinski, M. et al. Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639-1645 (2009).
44. Friedman, K.M. et al. Tumor-specific CD4+ melanoma tumor-infiltrating lymphocytes. J. Immunother. 35, 400-408 (2012).
45. van Lent, A.U. et al. In vivo modulation of gene expression by lentiviral transduction in ?human immune system? Rag2?/? ?c?/? mice. Methods Mol. Biol. 595, 87-115 (2010).
46. Legrand, N. et al. Functional CD47/signal regulatory protein ? (SIRP?) interaction is required for optimal human T-and natural killer-(NK) cell homeostasis in vivo. Proc. Natl. Acad. Sci. USA 108, 13224-13229 (2011).
47. Yssel, H., De Vries, J.E., Koken, M., Van Blitterswijk, W. & Spits, H. Serum-free medium for generation and propagation of functional human cytotoxic and helper T cell clones. J. Immunol. Methods 72, 219-227 (1984).
48. Spits, H. & Yssel, H. Cloning of human T and natural killer cells. Methods 9, 416-421 (1996).
49. Schiavetti, F., Thonnard, J., Colau, D., Boon, T. & Coulie, P.G. A human endogenous retroviral sequence encoding an antigen recognized on melanoma by cytolytic T lymphocytes. Cancer Res. 62, 5510-5516 (2002)