T-cell receptor affinity and avidity defines antitumor response and autoimmunity in T-cell immunotherapy

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 17, 2013, Pages 6973-6978

  Zhong, Shi ^a   Malecek, Karolina ^a,d   Johnson, Laura A ^b   Yu, Zhiya ^b   De Miera, Eleazar Vega Saenz ^a   Darvishian, Farbod ^a   McGary, Katelyn ^a   Huang, Kevin ^a,e   Boyer, Josh ^a,f   Corse, Emily ^a   Shao, Yongzhao ^a,c   Rosenberg, Steven A ^b   Restifo, Nicholas P ^b   Osman, Iman ^a   Krogsgaard, Michelle ^a  

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

^b NATIONAL CANCER INSTITUTE   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^f UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Adoptive cell transfer; Kinetic threshold; Ocular autoimmunity; Tumor immunity

Indexed keywords

CD8 ANTIGEN; T LYMPHOCYTE RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOTHERAPY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

ANALYSIS OF VARIANCE; AUTOIMMUNITY; CYTOTOXICITY TESTS, IMMUNOLOGIC; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE; GP100 MELANOMA ANTIGEN; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOTHERAPY, ADOPTIVE; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL; TRANSDUCTION, GENETIC;

EID: 84876859096     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1221609110     Document Type: Article

References (64)

1. June CH, Blazar BR, Riley JL (2009) Engineering lymphocyte subsets: Tools, trials and tribulations. Nat Rev Immunol 9(10):704-716.
2. Rosenberg SA, Restifo NP, Yang JC, Morgan RA, Dudley ME (2008) Adoptive cell transfer: A clinical path to effective cancer immunotherapy. Nat Rev Cancer 8(4):299-308.
3. Weber J, et al.; Immunotherapy Task Force of the NCI Investigational Drug Steering Committee (2011) White paper on adoptive cell therapy for cancer with tumor-infiltrating lymphocytes: A report of the CTEP subcommittee on adoptive cell therapy. Clin Cancer Res 17(7):1664-1673.
4. Dudley ME, et al. (2002) Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298(5594):850-854.
5. Dudley ME, et al. (2008) Adoptive cell therapy for patients with metastatic melanoma: Evaluation of intensive myeloablative chemoradiation preparative regimens. J Clin Oncol 26(32):5233-5239.
6. Johnson LA, et al. (2009) Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 114(3):535-546.
7. Morgan RA, Dudley ME, Rosenberg SA (2010) Adoptive cell therapy: Genetic modification to redirect effector cell specificity. Cancer J 16(4):336-341.
8. Rosenberg SA, Dudley ME (2009) Adoptive cell therapy for the treatment of patients with metastatic melanoma. Curr Opin Immunol 21(2):233-240.
9. Morgan RA, et al. (2006) Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314(5796):126-129.
10. Alexander-Miller MA, Leggatt GR, Berzofsky JA (1996) Selective expansion of high-or low-avidity cytotoxic T lymphocytes and efficacy for adoptive immunotherapy. Proc Natl Acad Sci USA 93(9):4102-4107.
11. Zeh HJ, 3rd, Perry-Lalley D, Dudley ME, Rosenberg SA, Yang JC (1999) High avidity CTLs for two self-antigens demonstrate superior in vitro and in vivo antitumor efficacy. J Immunol 162(2):989-994.
12. Tian S, Maile R, Collins EJ, Frelinger JA (2007) CD8+ T cell activation is governed by TCR-peptide/MHC affinity, not dissociation rate. J Immunol 179(5):2952-2960.
13. Corse E, Gottschalk RA, Allison JP (2011) Strength of TCR-peptide/MHC interactions and in vivo T cell responses. J Immunol 186(9):5039-5045.
14. Krogsgaard M, et al. (2003) Evidence that structural rearrangements and/or flexibility during TCR binding can contribute to T cell activation. Mol Cell 12(6):1367-1378.
15. Zehn D, Lee SY, Bevan MJ (2009) Complete but curtailed T-cell response to very low-affinity antigen. Nature 458(7235):211-214.
16. Laugel B, et al. (2007) Different T cell receptor affinity thresholds and CD8 coreceptor dependence govern cytotoxic T lymphocyte activation and tetramer binding properties. J Biol Chem 282(33):23799-23810.
17. Schmid DA, et al. (2010) Evidence for a TCR affinity threshold delimiting maximal CD8 T cell function. J Immunol 184(9):4936-4946.
18. Holler PD, Kranz DM (2003) Quantitative analysis of the contribution of TCR/pepMHC affinity and CD8 to T cell activation. Immunity 18(2):255-264.
19. Robbins PF, et al. (2008) Single and dual amino acid substitutions in TCR CDRs can enhance antigen-specific T cell functions. J Immunol 180(9):6116-6131.
20. Chinnasamy N, et al. (2011) A TCR targeting the HLA-A*0201- restricted epitope of MAGE-A3 recognizes multiple epitopes of the MAGE-A antigen superfamily in several types of cancer. J Immunol 186(2):685-696.
21. Robbins PF, et al. (2011) Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol 29(7):917-924.
22. Varela-Rohena A, et al. (2008) Control of HIV-1 immune escape by CD8 T cells expressing enhanced T-cell receptor. Nat Med 14(12):1390-1395.
23. McMahan RH, et al. (2006) Relating TCR-peptide-MHC affinity to immunogenicity for the design of tumor vaccines. J Clin Invest 116(9):2543-2551.
24. Irving M, et al. (2012) Interplay between T cell receptor binding kinetics and the level of cognate peptide presented by major histocompatibility complexes governs CD8+ T cell responsiveness. J Biol Chem 287(27):23068-23078.
25. Corse E, Gottschalk RA, Krogsgaard M, Allison JP (2010) Attenuated T cell responses to a high-potency ligand in vivo. PLoS Biol 8(9):e1000481.
26. Palmer DC, et al. (2008) Effective tumor treatment targeting a melanoma/melanocyte-associated antigen triggers severe ocular autoimmunity. Proc Natl Acad Sci USA 105 (23):8061-8066.
27. Yeh S, et al. (2009) Ocular and systemic autoimmunity after successful tumor-infiltrating lymphocyte immunotherapy for recurrent, metastatic melanoma. Ophthalmology 116(5):981-989.
28. Gronski MA, et al. (2004) TCR affinity and negative regulation limit autoimmunity. Nat Med 10(11):1234-1239.
29. Stone JD, Chervin AS, Kranz DM (2009) T-cell receptor binding affinities and kinetics: Impact on T-cell activity and specificity. Immunology 126(2):165-176.
30. Savage PA, Boniface JJ, Davis MM (1999) A kinetic basis for T cell receptor repertoire selection during an immune response. Immunity 10(4):485-492.
31. Johnson LA, et al. (2006) 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 177(9):6548-6559.
32. Boon T, Coulie PG, Van den Eynde BJ, van der Bruggen P (2006) Human T cell responses against melanoma. Annu Rev Immunol 24:175-208.
33. Parkhurst MR, et al. (1996) Improved induction of melanoma-reactive CTL with peptides from the melanoma antigen gp100 modified at HLA-A*0201- binding residues. J Immunol 157(6):2539-2548.
34. Borbulevych OY, Baxter TK, Yu Z, Restifo NP, Baker BM (2005) Increased immunogenicity of an anchor-modified tumor-associated antigen is due to the enhanced stability of the peptide/MHC complex: Implications for vaccine design. J Immunol 174(8):4812-4820.
35. Yu Z, et al. (2004) Poor immunogenicity of a self/tumor antigen derives from peptide-MHC-I instability and is independent of tolerance. J Clin Invest 114(4):551-559.
36. Rosenberg SA, et al. (1999) Impact of cytokine administration on the generation of antitumor reactivity in patients with metastatic melanoma receiving a peptide vaccine. J Immunol 163(3):1690-1695.
37. Walker EB, et al. (2004) gp100(209-2M) peptide immunization of human lymphocyte antigen-A2+ stage I-III melanoma patients induces significant increase in antigen-specific effector and long-term memory CD8+ T cells. Clin Cancer Res 10(2):668-680.
38. Vitiello A, Marchesini D, Furze J, Sherman LA, Chesnut RW (1991) Analysis of the HLA-restricted influenza-specific cytotoxic T lymphocyte response in transgenic mice carrying a chimeric human-mouse class I major histocompatibility complex. JExp Med 173(4):1007-1015.
39. Frankel TL, et al. (2010) Both CD4 and CD8 T cells mediate equally effective in vivo tumor treatment when engineered with a highly avid TCR targeting tyrosinase. J Immunol 184(11):5988-5998.
40. Zhong S, Malecek K, Perez-Garcia A, Krogsgaard M (2010) Retroviral transduction of T-cell receptors in mouse T-cells. J Vis Exp (44):2307.
41. Jiang N, et al. (2011) Two-stage cooperative T cell receptor-peptide major histocompatibility complex-CD8 trimolecular interactions amplify antigen discrimination. Immunity 34(1):13-23.
42. Huang J, et al. (2010) The kinetics of two-dimensional TCR and pMHC interactions determine T-cell responsiveness. Nature 464(7290):932-936.
43. Smith-Garvin JE, Koretzky GA, Jordan MS (2009) T cell activation. Annu Rev Immunol 27:591-619.
44. Irvine KR, et al. (1999) Recombinant virus vaccination against "self" antigens using anchor-fixed immunogens. Cancer Res 59(11):2536-2540.
45. Overwijk WW, et al. (2003) Tumor regression and autoimmunity after reversal of a functionally tolerant state of self-reactive CD8+ T cells. J Exp Med 198(4):569-580.
46. Smith FO, Klapper JA, Wunderlich JR, Rosenberg SA, Dudley ME (2009) Impact of a recombinant fowlpox vaccine on the efficacy of adoptive cell therapy with tumor infiltrating lymphocytes in a patient with metastatic melanoma. J Immunother 32(8):870-874.
47. Hinrichs CS, et al. (2009) Adoptively transferred effector cells derived from naive rather than central memory CD8+ T cells mediate superior antitumor immunity. Proc Natl Acad Sci USA 106(41):17469-17474.
48. Gattinoni L, et al. (2009) Wnt signaling arrests effector T cell differentiation and generates CD8+ memory stem cells. Nat Med 15(7):808-813.
49. Rosenberg SA, et al. (2003) Recombinant fowlpox viruses encoding the anchor-modified gp100 melanoma antigen can generate antitumor immune responses in patients with metastatic melanoma. Clin Cancer Res 9(8):2973-2980.
50. Borbulevych OY, Santhanagopolan SM, Hossain M, Baker BM (2011) TCRs used in cancer gene therapy cross-react with MART-1/Melan-A tumor antigens via distinct mechanisms. J Immunol 187(5):2453-2463.
51. Huppa JB, Gleimer M, Sumen C, Davis MM (2003) Continuous T cell receptor signaling required for synapse maintenance and full effector potential. NatImmunol4(8):749-755.
52. Purbhoo MA, Irvine DJ, Huppa JB, Davis MM (2004) T cell killing does not require the formation of a stable mature immunological synapse. Nat Immunol 5(5):524-530.
53. Wiedemann A, Depoil D, Faroudi M, Valitutti S (2006) Cytotoxic T lymphocytes kill multiple targets simultaneously via spatiotemporal uncoupling of lytic and stimulatory synapses. Proc Natl Acad Sci USA 103(29):10985-10990.
54. Stone JD, Cochran JR, Stern LJ (2001) T-cell activation by soluble MHC oligomers can be described by a two-parameter binding model. Biophys J 81(5):2547-2557.
55. Krogsgaard M, et al. (2005) Agonist/endogenous peptide-MHC heterodimers drive T cell activation and sensitivity. Nature 434(7030):238-243.
56. Slansky JE, Jordan KR (2010) The Goldilocks model forTCR-too much attraction might not be best for vaccine design. PLoS Biol 8(9):e1000482.
57. Hebeisen M, et al. (2013) SHP-1 phosphatase activity counteracts increased T cell receptor affinity. J Clin Invest 123(3):1044-56.
58. Eck SC, Turka LA (2001) Adoptive transfer enables tumor rejection targeted against a self-antigen without the induction of autoimmunity. Cancer Res 61(7):3077-3083.
59. Morgan DJ, et al. (1998) Activation of low avidity CTL specific for a self epitope results in tumor rejection but not autoimmunity. J Immunol 160(2):643-651.
60. Bowne WB, et al. (1999) Coupling and uncoupling of tumor immunity and autoimmunity. J Exp Med 190(11):1717-1722.
61. Cohen CJ, Zhao Y, Zheng Z, Rosenberg SA, Morgan RA (2006) 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 66(17):8878-8886.
62. Zhao Y, et al. (2005) Primary human lymphocytes transduced with NY-ESO-1 antigen-specific TCR genes recognize and kill diverse human tumor cell lines. J Immunol 174(7):4415-4423.
63. Kerkar SP, et al. (2011) Genetic engineering of murine CD8+ and CD4+ T cells for preclinical adoptive immunotherapy studies. J Immunother 34(4):343-352.
64. Feinerman O, Veiga J, Dorfman JR, Germain RN, Altan-Bonnet G (2008) Variability and robustness in T cell activation from regulated heterogeneity in protein levels. Science 321(5892):1081-1084.