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Original Research

Affinity-enhanced T-cell receptors for adoptive T-cell therapy targeting MAGE-A10: strategy for selection of an optimal candidate

ORCID Icon, ORCID Icon, , &
Article: e1532759 | Received 12 Jun 2018, Accepted 30 Aug 2018, Published online: 20 Nov 2018

References

  • Aranda F, Buque A, Bloy N, Castoldi F, Eggermont A, Cremer I, Starmann J, Tjwa M, Plate KH, Sültmann H, et al. Trial watch: adoptive cell transfer for oncological indications. Oncoimmunology. 2015;4:e1046673. doi:10.1080/2162402X.2015.1008371.
  • Wang M, Yin B, Wang HY, Wang RF. Current advances in T-cell-based cancer immunotherapy. Immunotherapy. 2014;6:1265–1278. doi:10.2217/imt.14.86.
  • Rosenberg SA, Yang JC, Sherry RM, Kammula US, Hughes MS, Phan GQ, Citrin DE, Restifo NP, Robbins PF, Wunderlich JR, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res: An Off J Am Assoc Cancer Res. 2011;17:4550–4557. doi:10.1158/1078-0432.CCR-11-0116.
  • Aleksic M, Liddy N, Molloy PE, Pumphrey N, Vuidepot A, Chang KM, Jakobsen BK. Different affinity windows for virus and cancer-specific T-cell receptors: implications for therapeutic strategies. Eur J Immunol. 2012;42:3174–3179. doi:10.1002/eji.201242606.
  • van der Merwe PA, Davis SJ. Molecular interactions mediating T cell antigen recognition. Annu Rev Immunol. 2003;21:659–684. doi:10.1146/annurev.immunol.21.120601.141036.
  • Bridgeman JS, Sewell AK, Miles JJ, Price DA, Cole DK. Structural and biophysical determinants of αβ T-cell antigen recognition. Immunology. 2012;135:9–18. doi:10.1111/j.1365-2567.2011.03515.x.
  • Garrido F, Cabrera T, Aptsiauri N. “Hard” and “soft” lesions underlying the HLA class I alterations in cancer cells: implications for immunotherapy. Int J Cancer. 2010;127:249–256. doi:10.1002/ijc.25270.
  • Tan MP, Gerry AB, Brewer JE, Melchiori L, Bridgeman JS, Bennett AD, Pumphrey NJ, Jakobsen BK, Price DA, Ladell K, et al. T cell receptor binding affinity governs the functional profile of cancer-specific CD8+ T cells. Clin Exp Immunol. 2015;180:255–270. doi:10.1111/cei.12570.
  • Hebeisen M, Oberle SG, Presotto D, Speiser DE, Zehn D, Rufer N. Molecular insights for optimizing T cell receptor specificity against cancer. Front Immunol. 2013;4:154. doi:10.3389/fimmu.2013.00154.
  • Zhong S, Malecek K, Johnson LA, Yu Z, Vega-Saenz de Miera E, Darvishian F, McGary K, Huang K, Boyer J, Corse E, et al. T-cell receptor affinity and avidity defines antitumor response and autoimmunity in T-cell immunotherapy. Proc Natl Acad Sci U S A. 2013;110:6973–6978. doi:10.1073/pnas.1221609110.
  • Hebeisen M, Allard M, Gannon PO, Schmidt J, Speiser DE, Rufer N. Identifying individual T cell receptors of optimal avidity for tumor antigens. Front Immunol. 2015;6:582. doi:10.3389/fimmu.2015.00582.
  • Cameron BJ, Gerry AB, Dukes J, Harper JV, Kannan V, Bianchi FC, Grand F, Brewer JE, Gupta M, Plesa G, et al. Identification of a Titin-derived HLA-A1-presented peptide as a cross-reactive target for engineered MAGE A3-directed T cells. Sci Transl Med. 2013;5:197ra03. doi:10.1126/scitranslmed.3006034.
  • Johnson LA, Morgan RA, Dudley ME, Cassard L, Yang JC, Hughes MS, Kammula US, Royal RE, Sherry RM, Wunderlich JR, et al. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood. 2009;114:535–546. doi:10.1182/blood-2009-03-211714.
  • Hinrichs CS, Rosenberg SA. Exploiting the curative potential of adoptive T-cell therapy for cancer. Immunol Rev. 2014;257:56–71. doi:10.1111/imr.12132.
  • Parkhurst MR, Yang JC, Langan RC, Dudley ME, Nathan DA, Feldman SA, Davis JL, Morgan RA, Merino MJ, Sherry RM, et al. T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol Ther: J Am Soc Gene Ther. 2011;19:620–626. doi:10.1038/mt.2010.272.
  • Morgan RA, Chinnasamy N, Abate-Daga D, Gros A, Robbins PF, Zheng Z, Feldman SA, Yang JC, Sherry RM, Phan GQ, et al. Cancer regression and neurological toxicity following anti-MAGE-A3 TCR gene therapy. J Immunother. 2013;36:133–151. doi:10.1097/CJI.0b013e3182829903.
  • Linette GP, Stadtmauer EA, Maus MV, Rapoport AP, Levine BL, Emery L, Litzky L, Bagg A, Carreno BM, Cimino PJ, et al. Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma. Blood. 2013;122:863–871. doi:10.1182/blood-2013-03-490565.
  • Amos SM, Duong CP, Westwood JA, Ritchie DS, Junghans RP, Darcy PK, Kershaw MH. Autoimmunity associated with immunotherapy of cancer. Blood. 2011;118:499–509. doi:10.1182/blood-2011-01-325266.
  • Kunert A, Obenaus M, Lamers CHJ, Blankenstein T, Debets R. T-cell receptors for clinical therapy: in vitro assessment of toxicity risk. Clin Cancer Res: An Off J Am Assoc Cancer Res. 2017;23:6012–6020. doi:10.1158/1078-0432.CCR-17-1012.
  • van Loenen MM, de Boer R, Amir AL, Hagedoorn RS, Volbeda GL, Willemze R, van Rood JJ, Falkenburg JHF, Heemskerk MHM. Mixed T cell receptor dimers harbor potentially harmful neoreactivity. Proceedings of the National Academy of Sciences of the United States of America 2010; 107:10972–10977. doi:10.1073/pnas.1005802107.
  • Caballero OL, Chen YT. Cancer/testis (CT) antigens: potential targets for immunotherapy. Cancer Sci. 2009;100:2014–2021. doi:10.1111/j.1349-7006.2009.01303.x.
  • Hickman ES, Lomax ME, Jakobsen BK. Antigen selection for enhanced affinity T-cell receptor-based cancer therapies. J Biomol Screen. 2016;21:769–785. doi:10.1177/1087057116637837.
  • Weon JL, Potts PR. The MAGE protein family and cancer. Curr Opin Cell Biol. 2015;37:1–8. doi:10.1016/j.ceb.2015.08.002.
  • Raman MC, Rizkallah PJ, Simmons R, Donnellan Z, Dukes J, Bossi G, Le Provost GS, Todorov P, Baston E, Hickman E, et al. Direct molecular mimicry enables off-target cardiovascular toxicity by an enhanced affinity TCR designed for cancer immunotherapy. Sci Rep. 2016;6:18851. doi:10.1038/srep18851.
  • Fremont DH, Rees WA, Kozono H. Biophysical studies of T-cell receptors and their ligands. Curr Opin Immunol. 1996;8:93–100.
  • De Plaen E, Arden K, Traversari C, Gaforio JJ, Szikora JP, De Smet C, Brasseur F, van der Bruggen P, Lethe B, Lurquin C, et al. Structure, chromosomal localization, and expression of 12 genes of the MAGE family. Immunogenetics. 1994;40:360–369.
  • Rimoldi D, Salvi S, Reed D, Coulie P, Jongeneel VC, De Plaen E, Brasseur F, Rodriguez AM, Boon T, Cerottini JC. cDNA and protein characterization of human MAGE-10. Int J Cancer. 1999;82:901–907.
  • Kim Y, Sidney J, Pinilla C, Sette A, Peters B. Derivation of an amino acid similarity matrix for peptide: MHC binding and its application as a Bayesian prior. BMC Bioinformatics. 2009;10:394. doi:10.1186/1471-2105-10-394.
  • Lesk A. Introduction to Bioinformatics. Oxford, UK: Oxford University Press; 2013. .
  • Birnbaum ME, Mendoza JL, Sethi DK, Dong S, Glanville J, Dobbins J, Özkan E,  Davis MM, Wucherpfennig KW, Garcia KC. Deconstructing the peptide-MHC specificity of T cell recognition. Cell. 2014;157:1073–1087. doi:10.1016/j.cell.2014.03.047.
  • Zhang H, Lim HS, Knapp B, Deane CM, Aleksic M, Dushek O, van der Merwe PA. The contribution of major histocompatibility complex contacts to the affinity and kinetics of T cell receptor binding. Sci Rep. 2016;6:35326. doi:10.1038/srep35326.
  • Attaf M, Holland SJ, Bartok I, Dyson J. alphabeta T cell receptor germline CDR regions moderate contact with MHC ligands and regulate peptide cross-reactivity. Sci Rep. 2016;6:35006. doi:10.1038/srep35006.
  • Mason D. A very high level of crossreactivity is an essential feature of the T-cell receptor. Immunol Today. 1998;19:395–404.
  • Sewell AK. Why must T cells be cross-reactive? Nat Rev Immunol. 2012;12:669–677. doi:10.1038/nri3279.
  • Wooldridge L, Ekeruche-Makinde J, van den Berg HA, Skowera A, Miles JJ, Tan MP, Dolton G, Clement M, Llewellyn-Lacey S, Price DA, et al. A single autoimmune T cell receptor recognizes more than a million different peptides. J Biol Chem. 2012;287:1168–1177. doi:10.1074/jbc.M111.289488.
  • Bijen HM, van der Steen DM, Hagedoorn RS, Wouters AK, Wooldridge L, Falkenburg JHF, Heemskerk MHM. Preclinical strategies to identify off-target toxicity of high-affinity TCRs. Mol Ther: J Am Soc Gene Ther. 2018. doi:10.1016/j.ymthe.2018.02.017.
  • Cole DK, van den Berg HA, Lloyd A, Crowther MD, Beck K, Ekeruche-Makinde J, Miles JJ, Bulek AM, Dolton G, Schauenburg AJ, et al. Structural mechanism underpinning cross-reactivity of a CD8+ T-cell clone that recognizes a peptide derived from human telomerase reverse transcriptase. J Biol Chem. 2017;292:802–813. doi:10.1074/jbc.M116.741603.
  • Huang YH, Terabe M, Pendleton CD, Stewart Khursigara D, Bera TK, Pastan I, Berzofsky JA. Identification and enhancement of HLA-A2.1-restricted CTL epitopes in a new human cancer antigen-POTE. PLoS One. 2013;8:e64365. doi:10.1371/journal.pone.0064365.
  • Moysey R, Vuidepot AL, Boulter JM. Amplification and one-step expression cloning of human T cell receptor genes. Anal Biochem. 2004;326:284–286. doi:10.1016/j.ab.2003.12.011.
  • Boulter JM, Glick M, Todorov PT, Baston E, Sami M, Rizkallah P, Jakobsen BK. Stable, soluble T-cell receptor molecules for crystallization and therapeutics. Protein Eng. 2003;16:707–711.
  • Cole DK, Pumphrey NJ, Boulter JM, Sami M, Bell JI, Gostick E, Price DA, Gao GF, Sewell AK, Jakobsen BK. Human TCR-binding affinity is governed by MHC class restriction. J Immunol. 2007;178:5727–5734.
  • Garboczi DN, Hung DT, Wiley DC. HLA-A2-peptide complexes: refolding and crystallization of molecules expressed in Escherichia coli and complexed with single antigenic peptides. Proc Natl Acad Sci U S A. 1992;89:3429–3433.
  • O’Callaghan C A, Byford MF, Wyer JR, Willcox BE, Jakobsen BK, McMichael AJ, Bell JI. BirA enzyme: production and application in the study of membrane receptor-ligand interactions by site-specific biotinylation. Anal Biochem. 1999;266:9–15. doi:10.1006/abio.1998.2930.
  • Parry RV, Rumbley CA, Vandenberghe LH, June CH, Riley JL. CD28 and inducible costimulatory protein Src homology 2 binding domains show distinct regulation of phosphatidylinositol 3-kinase, Bcl-xL, and IL-2 expression in primary human CD4 T lymphocytes. J Immunol. 2003;171:166–174.
  • McCormack E, Adams KJ, Hassan NJ, Kotian A, Lissin NM, Sami M, Mujić M, Osdal T, Gjertsen BT, Baker D, et al. Bi-specific TCR-anti CD3 redirected T-cell targeting of NY-ESO-1- and LAGE-1-positive tumors. Cancer Immunol, Immunother. 2013;62:773–785. doi:10.1007/s00262-012-1384-4.