Engineering improved T cell receptors using an alanine-scan guided T cell display selection system

Journal of Immunological Methods

Volumn 392, Issue 1-2, 2013, Pages 1-11

  Malecek, Karolina ^a   Zhong, Shi ^a   McGary, Katelyn ^a   Yu, Connie ^a   Huang, Kevin ^a   Johnson, Laura A ^b   Rosenberg, Steven A ^b   Krogsgaard, Michelle ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

CDR3 alanine scanning mutagenesis; Combinatorial library design; Mammalian TCR display system; T cell clones; T cell receptor

Indexed keywords

ALANINE; CD8 ANTIGEN; GLYCOPROTEIN; GLYCOPROTEIN GP209 2M; HLA A2 ANTIGEN; INTERLEUKIN 2; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; AMINO ACID; CYTOKINE; PEPTIDE;

ADOPTIVE IMMUNOTHERAPY; AMINO ACID ANALYSIS; AMINO ACID SUBSTITUTION; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; ARTICLE; BINDING AFFINITY; BIOENGINEERING; CODON; COMBINATORIAL LIBRARY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISPLAY SYSTEM; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GEL PERMEATION CHROMATOGRAPHY; HALF LIFE TIME; HUMAN; HUMAN CELL; HYBRIDOMA CELL CULTURE; IN VITRO STUDY; MAJOR HISTOCOMPATIBILITY COMPLEX; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; RECEPTOR AFFINITY; SURFACE PLASMON RESONANCE; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TUMOR REJECTION; WILD TYPE; ANIMAL CELL; ANTIGEN BINDING; BACTERIOPHAGE; IMMUNE RESPONSE; LIBRARY; MAMMAL; NONHUMAN; RECEPTOR BINDING; YEAST;

ALANINE; ANTIGENS; CYTOKINES; HLA-A2 ANTIGEN; HUMANS; LYMPHOCYTE ACTIVATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MUTAGENESIS; PROTEIN BINDING; RECEPTORS, ANTIGEN, T-CELL; RETROVIRIDAE; T-LYMPHOCYTES;

MAMMALIA;

EID: 84880002705     PISSN: 00221759     EISSN: 18727905     Source Type: Journal    
DOI: 10.1016/j.jim.2013.02.018     Document Type: Article

References (80)

1. Adams J.J., Narayanan S., et al. T cell receptor signaling is limited by docking geometry to peptide-major histocompatibility complex. Immunity 2011, 35(5):681.
2. Aleksic M., Dushek O., et al. Dependence of T cell antigen recognition on T cell receptor-peptide MHC confinement time. Immunity 2010, 32(2):163.
3. Altman J.D., Moss P.A., et al. Phenotypic analysis of antigen-specific T lymphocytes. Science 1996, 274(5284):94.
4. Boniface J.J., Rabinowitz J.D., et al. Initiation of signal transduction through the T cell receptor requires the multivalent engagement of peptide/MHC ligands [corrected]. Immunity 1998, 9(4):459.
5. Boon T., Coulie P.G., et al. Tumor antigens recognized by T cells. Immunol. Today 1997, 18(6):267.
6. Brioen P., Sijens R.J., et al. Hybridoma antibodies to poliovirus N and H antigen. Arch. Virol. 1982, 74(4):325.
7. Chervin A.S., Aggen D.H., et al. Engineering higher affinity T cell receptors using a T cell display system. J. Immunol. Methods 2008.
8. Chervin A.S., Stone J.D., et al. The impact of TCR-binding properties and antigen presentation format on T cell responsiveness. J. Immunol. 2009, 183(2):1166.
9. Choi Y.W., Kotzin B., et al. A method for production of antibodies to human T-cell receptor beta-chain variable regions. Proc. Natl. Acad. Sci. U. S. A. 1991, 88(19):8357.
10. Choi E.M., Chen J.L., et al. High avidity antigen-specific CTL identified by CD8-independent tetramer staining. J. Immunol. 2003, 171(10):5116.
11. Cohen C.J., Zhao Y., et al. Enhanced antitumor activity of murine-human hybrid T-cell receptor (TCR) in human lymphocytes is associated with improved pairing and TCR/CD3 stability. Cancer Res. 2006, 66(17):8878.
12. Corse E., Gottschalk R.A., et al. Strength of TCR-peptide/MHC interactions and in vivo T cell responses. J. Immunol. 2011, 186(9):5039.
13. Dai S., Huseby E.S., et al. Crossreactive T cells spotlight the germline rules for alphabeta T cell-receptor interactions with MHC molecules. Immunity 2008, 28(3):324.
14. Davis M.M., Bjorkman P.J. T-cell antigen receptor genes and T-cell recognition. Nature 1988, 334(6181):395.
15. Davis M.M., Boniface J.J., et al. Ligand recognition by alpha beta T cell receptors. Annu. Rev. Immunol. 1998, 16:523.
16. Dudley M.E., Wunderlich J., et al. Adoptive transfer of cloned melanoma-reactive T lymphocytes for the treatment of patients with metastatic melanoma. J. Immunother. 2001, 24(4):363.
17. Dunn S.M., Rizkallah P.J., et al. Directed evolution of human T cell receptor CDR2 residues by phage display dramatically enhances affinity for cognate peptide-MHC without increasing apparent cross-reactivity. Protein Sci. 2006, 15(4):710.
18. Gascoigne N.R., Zal T., et al. T-cell receptor binding kinetics in T-cell development and activation. Expert Rev. Mol. Med. 2001, 2001:1.
19. Gattinoni L., Powell D.J., et al. Adoptive immunotherapy for cancer: building on success. Nat. Rev. Immunol. 2006, 6(5):383.
20. Germain R.N., Stefanova I. The dynamics of T cell receptor signaling: complex orchestration and the key roles of tempo and cooperation. Annu. Rev. Immunol. 1999, 17:467.
21. Goldrath A.W., Bevan M.J. Selecting and maintaining a diverse T-cell repertoire. Nature 1999, 402(6759):255.
22. Holler P.D., Kranz D.M. Quantitative analysis of the contribution of TCR/pepMHC affinity and CD8 to T cell activation. Immunity 2003, 18(2):255.
23. Holler P.D., Holman P.O., et al. In vitro evolution of a T cell receptor with high affinity for peptide/MHC. Proc. Natl. Acad. Sci. U. S. A. 2000, 97(10):5387.
24. Holler P.D., Chlewicki L.K., et al. TCRs with high affinity for foreign pMHC show self-reactivity. Nat. Immunol. 2003, 4(1):55.
25. Huang J., Zarnitsyna V.I., et al. The kinetics of two-dimensional TCR and pMHC interactions determine T-cell responsiveness. Nature 2010, 464(7290):932.
26. Huppa J.B., Axmann M., et al. TCR-peptide-MHC interactions in situ show accelerated kinetics and increased affinity. Nature 2010, 463(7283):963.
27. Jiang N., Huang J., et al. Two-stage cooperative T cell receptor-peptide major histocompatibility complex-CD8 trimolecular interactions amplify antigen discrimination. Immunity 2011, 34(1):13.
28. Johnson L.A., Heemskerk B., et al. Gene transfer of tumor-reactive TCR confers both high avidity and tumor reactivity to nonreactive peripheral blood mononuclear cells and tumor-infiltrating lymphocytes. J. Immunol. 2006, 177(9):6548.
29. Johnson L.A., Morgan R.A., et al. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 2009, 114(3):535.
30. Juang J., Ebert P.J., et al. Peptide-MHC heterodimers show that thymic positive selection requires a more restricted set of self-peptides than negative selection. J. Exp. Med. 2010, 207(6):1223.
31. Kane L.P., Lin J., et al. Signal transduction by the TCR for antigen. Curr. Opin. Immunol. 2000, 12(3):242.
32. Kawakami Y., Eliyahu S., et al. Identification of a human melanoma antigen recognized by tumor-infiltrating lymphocytes associated with in vivo tumor rejection. Proc. Natl. Acad. Sci. U. S. A. 1994, 91(14):6458.
33. + T cells for preclinical adoptive immunotherapy studies. J. Immunother. 2011, 34(4):343.
34. Kersh G.J., Kersh E.N., et al. High- and low-potency ligands with similar affinities for the TCR: the importance of kinetics in TCR signaling. Immunity 1998, 9(6):817.
35. Kessels H.W., van Den Boom M.D., et al. Changing T cell specificity by retroviral T cell receptor display. Proc. Natl. Acad. Sci. U. S. A. 2000, 97(26):14578.
36. Kitamura T., Koshino Y., et al. Retrovirus-mediated gene transfer and expression cloning: powerful tools in functional genomics. Exp. Hematol. 2003, 31(11):1007.
37. Krogsgaard M., Davis M.M. How T cells 'see' antigen. Nat. Immunol. 2005, 6(3):239.
38. Krogsgaard M., Prado N., et al. Evidence that structural rearrangements and/or flexibility during TCR binding can contribute to T cell activation. Mol. Cell 2003, 12(6):1367.
39. Krogsgaard M., Li Q.J., et al. Agonist/endogenous peptide-MHC heterodimers drive T cell activation and sensitivity. Nature 2005, 434(7030):238.
40. Kubota E., Ishikawa H., et al. Evidence for a cloned hybridoma (HO-13-4-9) producing 2 kinds of antibody molecules different in specificity, one directed to Thy 1.2 gene products and the other to antigen on a subpopulation of Thy 1.1 thymocytes. J. Immunol. 1981, 127(4):1498.
41. Lanzavecchia A., Lezzi G., et al. From TCR engagement to T cell activation: a kinetic view of T cell behavior. Cell 1999, 96(1):1.
42. Laugel B., van den Berg H.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(33):23799.
43. Laugel B., Cole D.K., et al. The multiple roles of the CD8 coreceptor in T cell biology: opportunities for the selective modulation of self-reactive cytotoxic T cells. J. Leukoc. Biol. 2011, 90(6):1089.
44. Letourneur F., Malissen B. Derivation of a T cell hybridoma variant deprived of functional T cell receptor alpha and beta chain transcripts reveals a nonfunctional alpha-mRNA of BW5147 origin. Eur. J. Immunol. 1989, 19(12):2269.
45. Li Y., Moysey R., et al. Directed evolution of human T-cell receptors with picomolar affinities by phage display. Nat. Biotechnol. 2005, 23(3):349.
46. Manning T.C., Schlueter C.J., et al. Alanine scanning mutagenesis of an alphabeta T cell receptor: mapping the energy of antigen recognition. Immunity 1998, 8(4):413.
47. McKeithan T.W. Kinetic proofreading in T-cell receptor signal transduction. Proc. Natl. Acad. Sci. U. S. A. 1995, 92(11):5042.
48. Minguet S., Swamy M., et al. Full activation of the T cell receptor requires both clustering and conformational changes at CD3. Immunity 2007, 26(1):43.
49. Mitchell D.A., Karikari I., et al. Selective modification of antigen-specific T cells by RNA electroporation. Hum. Gene Ther. 2008, 19(5):511.
50. Morgan R.A., Dudley M.E., et al. High efficiency TCR gene transfer into primary human lymphocytes affords avid recognition of melanoma tumor antigen glycoprotein 100 and does not alter the recognition of autologous melanoma antigens. J. Immunol. 2003, 171(6):3287.
51. Morgan R.A., Dudley M.E., et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 2006, 314(5796):126.
52. Narimatsu S., Yoshioka Y., et al. Structure-activity relationship of T-cell receptors based on alanine scanning. Biochem. Biophys. Res. Commun. 2011, 415(4):558.
53. Newell E.W., Ely L.K., et al. Structural basis of specificity and cross-reactivity in T cell receptors specific for cytochrome c-I-E(k). J. Immunol. 2011, 186(10):5823.
54. Overwijk W.W., Theoret M.R., et al. Tumor regression and autoimmunity after reversal of a functionally tolerant state of self-reactive CD8+ T cells. J. Exp. Med. 2003, 198(4):569.
55. Persaud S.P., Donermeyer D.L., et al. High-affinity T cell receptor differentiates cognate peptide-MHC and altered peptide ligands with distinct kinetics and thermodynamics. Mol. Immunol. 2010, 47(9):1793.
56. Purbhoo M.A., Boulter J.M., et al. The human CD8 coreceptor effects cytotoxic T cell activation and antigen sensitivity primarily by mediating complete phosphorylation of the T cell receptor zeta chain. J. Biol. Chem. 2001, 276(35):32786.
57. Rabinowitz J.D., Beeson C., et al. Kinetic discrimination in T-cell activation. Proc. Natl. Acad. Sci. U. S. A. 1996, 93(4):1401.
58. Richman S.A., Kranz D.M. Display, engineering, and applications of antigen-specific T cell receptors. Biomol. Eng. 2007, 24(4):361.
59. Robbins P.F., Li Y.F., et al. Single and dual amino acid substitutions in TCR CDRs can enhance antigen-specific T cell functions. J. Immunol. 2008, 180(9):6116.
60. Robins H.S., Campregher P.V., et al. Comprehensive assessment of T-cell receptor beta-chain diversity in alphabeta T cells. Blood 2009, 114(19):4099.
61. Robins H.S., Srivastava S.K., et al. Overlap and effective size of the human CD8+ T cell receptor repertoire. Sci. Transl. Med. 2010, 2(47):47ra64.
62. Rosenberg S.A., Yang J.C., et al. Cancer immunotherapy: moving beyond current vaccines. Nat. Med. 2004, 10(9):909.
63. Rudolph M.G., Stanfield R.L., et al. How TCRs bind MHCs, peptides, and coreceptors. Annu. Rev. Immunol. 2006, 24:419.
64. Savage P.A., Boniface J.J., et al. A kinetic basis for T cell receptor repertoire selection during an immune response. Immunity 1999, 10(4):485.
65. Schodin B.A., Tsomides T.J., et al. Correlation between the number of T cell receptors required for T cell activation and TCR-ligand affinity. Immunity 1996, 5(2):137.
66. Shusta E.V., Kieke M.C., et al. Yeast polypeptide fusion surface display levels predict thermal stability and soluble secretion efficiency. J. Mol. Biol. 1999, 292(5):949.
67. Smith-Garvin J.E., Koretzky G.A., et al. T cell activation. Annu. Rev. Immunol. 2009, 27:591.
68. Sprent J., Kishimoto H. T cell tolerance and the thymus. Ann. N. Y. Acad. Sci. 1998, 841:236.
69. Stockinger B. T lymphocyte tolerance: from thymic deletion to peripheral control mechanisms. Adv. Immunol. 1999, 71:229.
70. Stone J.D., Chervin A.S., et al. T-cell receptor binding affinities and kinetics: impact on T-cell activity and specificity. Immunology 2009, 126(2):165.
71. Szymczak A.L., Vignali D.A. Development of 2A peptide-based strategies in the design of multicistronic vectors. Expert Opin. Biol. Ther. 2005, 5(5):627.
72. Tian S., Maile R., et al. CD8+ T cell activation is governed by TCR-peptide/MHC affinity, not dissociation rate. J. Immunol. 2007, 179(5):2952.
73. Valitutti S., Muller S., et al. Serial triggering of many T-cell receptors by a few peptide-MHC complexes. Nature 1995, 375(6527):148.
74. van der Merwe P.A., Davis S.J. Molecular interactions mediating T cell antigen recognition. Annu. Rev. Immunol. 2003, 21:659.
75. Warren R.L., Freeman J.D., et al. Exhaustive T-cell repertoire sequencing of human peripheral blood samples reveals signatures of antigen selection and a directly measured repertoire size of at least 1 million clonotypes. Genome Res. 2011, 21(5):790.
76. Weber K.S., Donermeyer D.L., et al. Class II-restricted T cell receptor engineered in vitro for higher affinity retains peptide specificity and function. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(52):19033.
77. Zhao Y., Zheng Z., et al. High-efficiency transfection of primary human and mouse T lymphocytes using RNA electroporation. Mol. Ther. 2006, 13(1):151.
78. Zhao Y., Bennett A.D., et al. High-affinity TCRs generated by phage display provide CD4+ T cells with the ability to recognize and kill tumor cell lines. J. Immunol. 2007, 179(9):5845.
79. Zhong, S., K. Malecek, et al. (in press). T cell receptor affinity and avidity defines antitumor response and autoimmunity in T cell immunotherapy. PNAS.
80. Zhong S., Malecek K., et al. Retroviral transduction of T-cell receptors in mouse T-cells. J. Vis. Exp. 2010, (44).