Preclinical evaluation of an affinity-enhanced MAGE-A4-specific T-cell receptor for adoptive T-cell therapy

References

• Fournier C, Martin F, Zitvogel L, Kroemer G, Galluzzi L, Apetoh L. Trial watch: adoptively transferred cells for anticancer immunotherapy. Oncoimmunology. 2017;6:e1363139. doi:10.1080/2162402X.2017.1363139.
   PubMed Web of Science ®Google Scholar
• Ping Y, Liu C, Zhang Y. T-cell receptor-engineered T cells for cancer treatment: current status and future directions. Protein Cell. 2018;9:254–11. doi:10.1007/s13238-016-0367-1.
   PubMed Web of Science ®Google Scholar
• Aleksic M, Liddy N, Molloy PE, Pumphrey N, Vuidepot A, Chang K-M, Jakobsen BK, Robbins PF, Morgan RA, Feldman SA, et al. 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Bossi G, Gerry AB, Paston SJ, Sutton DH, Hassan NJ, Jakobsen BK. Examining the presentation of tumor-associated antigens on peptide-pulsed T2 cells. Oncoimmunology. 2013;2:e26840.
   PubMed Web of Science ®Google Scholar
• Manning TC, Parke EA, Teyton L, Kranz DM. Effects of complementarity determining region mutations on the affinity of an alpha/beta T cell receptor: measuring the energy associated with CD4/CD8 repertoire skewing. J Exp Med. 1999;189:461–470. doi:10.1084/jem.189.3.461.
   PubMed Web of Science ®Google Scholar
• Border EC, Sanderson JP, Weissensteiner T, Gerry AB, Pumphrey NJ. Affinity-enhanced T-cell receptors for adoptive T-cell therapy targeting MAGE-A10: strategy for selection of an optimal candidate. Oncoimmunology. 2018;8: e1532759.
   PubMed Web of Science ®Google Scholar
• Manning TC, Schlueter CJ, Brodnicki TC, Parke EA, Speir JA, Garcia KC, Teyton L, Wilson IA, Kranz DM. Alanine scanning mutagenesis of an αβ T cell receptor: mapping the energy of antigen recognition. Immunity. 1998;8:413–425. doi:10.1016/S1074-7613(00)80547-6.
   PubMed Web of Science ®Google Scholar
• Robbins PF, Li YF, El-Gamil M, Zhao Y, Wargo JA, Zheng Z, Xu H, Morgan RA, Feldman SA, Johnson LA, et al. Single and dual amino acid substitutions in TCR CDRs can enhance antigen-specific T cell functions. J Immunol. 2008;180:6116–6131. doi:10.4049/jimmunol.180.9.6116.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Weber KS, Donermeyer DL, Allen PM, Kranz DM. 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;102:19033–19038. doi:10.1073/pnas.0507554102.
   PubMed Web of Science ®Google Scholar
• Li Y, Moysey R, Molloy PE, Vuidepot, A.L., Mahon, T., Baston, E., Dunn, S., Liddy, N., Jacob, J., Jakobsen, B.K., et al. Directed evolution of human T-cell receptors with picomolar affinities by phage display. Nat Biotechnol. 2005;23:349–354. doi:10.1038/nbt1070.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Docta RY, Ferronha T, Sanderson JP,  Weissensteiner T, Pope GR, Bennett AD, Pumphrey NJ, Ferjentsik Z, Quinn LL, Wiedermann GE, et al. Tuning T cell receptor affinity to optimize clinical risk-benefit when targeting alpha-fetoprotein-positive liver cancer. Hepatology. 2019;69:2061-2075.
   Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• D’Angelo SP, Melchiori L, Merchant MS, Bernstein D, Glod J, Kaplan R, Grupp S, Tap WD, Chagin K, Binder GK, et al. Antitumor Activity Associated with Prolonged Persistence of Adoptively Transferred NY-ESO-1c259T cells in Synovial Sarcoma. Cancer Discov. 2018;8:944–957.
   Google Scholar
• Rapoport AP, Stadtmauer EA, Binder-Scholl GK, Goloubeva O, Vogl DT, Lacey SF, Badros AZ, Garfall A, Weiss B, Finklestein J, et al. NY-ESO-1-specific TCR-engineered T cells mediate sustained antigen-specific antitumor effects in myeloma. Nat Med. 2015;21:914–921. doi:10.1038/nm.3910.
   PubMed Web of Science ®Google Scholar
• Robbins PF, Morgan RA, Feldman SA, Yang JC, Sherry RM, Dudley ME, Wunderlich JR, Nahvi AV, Helman LJ, Mackall CL, 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. 2011;29:917–924. doi:10.1200/JCO.2010.32.2537.
   PubMed Web of Science ®Google Scholar
• Robbins PF, Kassim SH, Tran TL, Crystal JS, Morgan RA, Feldman SA, Yang JC, Dudley ME, Wunderlich JR, Sherry RM, et al. A pilot trial using lymphocytes genetically engineered with an NY-ESO-1-reactive T-cell receptor: long-term follow-up and correlates with response. Clin Cancer Res. 2015;21:1019–1027. doi:10.1158/1078-0432.CCR-14-2708.
   PubMed Web of Science ®Google Scholar
• 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;5:197ra103. doi:10.1126/scitranslmed.3006034.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Morgan RA, Chinnasamy N, Abate-Daga D,  Gros A, Robbins PF, Zheng Z, Dudley ME, Feldman SA, Yang JC, Sherry RM, 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.
   PubMed Web of Science ®Google Scholar
• Parkhurst MR, Yang JC, Langan RC, Dudley ME, Nathan D-AN, 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. 2011;19:620–626. doi:10.1038/mt.2010.272.
   PubMed Web of Science ®Google Scholar
• Meek DW, Marcar L. MAGE-A antigens as targets in tumour therapy. Cancer Lett. 2012;324:126–132. doi:10.1016/j.canlet.2012.05.011.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Daudi S, Eng KH, Mhawech-Fauceglia P, Morrison C, Miliotto A, Beck A, Matsuzaki J, Tsuji T, Groman A, Gnjatic S, et al. Expression and immune responses to MAGE antigens predict survival in epithelial ovarian cancer. PLoS One. 2014;9:e104099. doi:10.1371/journal.pone.0104099.
   PubMed Web of Science ®Google Scholar
• Fratta E, Coral S, Covre A, Parisi G, Colizzi F, Danielli R, Marie Nicolay HJ, Sigalotti L, Maio M. The biology of cancer testis antigens: putative function, regulation and therapeutic potential. Mol Oncol. 2011;5:164–182. doi:10.1016/j.molonc.2011.02.001.
   PubMed Web of Science ®Google Scholar
• Alves PM, Levy N, Bouzourene H, Viatte S, Bricard G, Ayyoub M, Vuilleumier H, Givel J-CR, Halkic N, Speiser DE, et al. Molecular and immunological evaluation of the expression of cancer/testis gene products in human colorectal cancer. Cancer Immunol Immunother. 2007;56:839–847. doi:10.1007/s00262-006-0228-5.
   PubMed Web of Science ®Google Scholar
• Barrow C, Browning J, MacGregor D, Davis ID, Sturrock S, Jungbluth AA, Cebon J. Tumor antigen expression in melanoma varies according to antigen and stage. Clin Cancer Res. 2006;12:764–771. doi:10.1158/1078-0432.CCR-05-1544.
   PubMed Web of Science ®Google Scholar
• Otte M, Zafrakas M, Riethdorf L, Pichlmeier U, Löning T, Jänicke F, Pantel K. MAGE-A gene expression pattern in primary breast cancer. Cancer Res. 2001;61:6682–6687.
   PubMed Web of Science ®Google Scholar
• Tajima K, Obata Y, Tamaki H, Yoshida M, Chen Y-T, Scanlan MJ, Old LJ, Kuwano H, Takahashi T, Takahashi T, et al. Expression of cancer/testis (CT) antigens in lung cancer. Lung Cancer. 2003;42:23–33. doi:10.1016/S0169-5002(03)00244-7.
   PubMed Web of Science ®Google Scholar
• Grossman RL, Heath AP, Ferretti V, Varmus HE, Lowy DR, Kibbe WA, Staudt LM. Toward a Shared Vision for Cancer Genomic Data. N Engl J Med. 2016;375:1109–1112. doi:10.1056/NEJMp1607591.
   PubMed Web of Science ®Google Scholar
• Peters B, Sette A. Generating quantitative models describing the sequence specificity of biological processes with the stabilized matrix method. BMC Bioinformatics. 2005;6:132. doi:10.1186/1471-2105-6-132.
   PubMed Web of Science ®Google Scholar
• 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. 2017;23:6012–6020. doi:10.1158/1078-0432.CCR-17-1012.
   PubMed Web of Science ®Google Scholar
• Harper J, Adams KJ, Bossi G, Wright DE, Stacey AR, Bedke N, Martinez-Hague R, Blat D, Humbert L, Buchanan H, et al. An approved in vitro approach to preclinical safety and efficacy evaluation of engineered T cell receptor anti-CD3 bispecific (ImmTAC) molecules. PLoS One. 2018;13:e0205491. doi:10.1371/journal.pone.0205491.
   PubMed Web of Science ®Google Scholar
• Pampaloni F, Reynaud EG, Stelzer EH. The third dimension bridges the gap between cell culture and live tissue. Nat Rev Mol Cell Biol. 2007;8:839–845. doi:10.1038/nrm2236.
   PubMed Web of Science ®Google Scholar
• Mason D. A very high level of crossreactivity is an essential feature of the T-cell receptor. Immunol Today. 1998;19:395–404. doi:10.1016/S0167-5699(98)01299-7.
   PubMedGoogle Scholar
• Sewell AK. Why must T cells be cross-reactive?. Nat Rev Immunol. 2012;12:669–677. doi:10.1038/nri3279.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Bendle GM, Linnemann C, Hooijkaas AI, Bies L, de Witte MA, Jorritsma A, Kaiser AD, Pouw N, Debets R, Kieback E, et al. Lethal graft-versus-host disease in mouse models of T cell receptor gene therapy. Nat Med. 2010;16:565–570. 561p following 570. doi:10.1038/nm.2128.
   PubMed Web of Science ®Google Scholar
• van Loenen MM, de Boer R, Amir AL, Hagedoorn RS, Volbeda GL, Willemze R, van Rood JJ, Falkenburg JF, Heemskerk MH. Mixed T cell receptor dimers harbor potentially harmful neoreactivity. Proc Natl Acad Sci U S A. 2010;107:10972–10977. doi:10.1073/pnas.1005802107.
   PubMed Web of Science ®Google Scholar
• Birnbaum ME, Mendoza JL, Sethi DK, Dong S, Glanville J, Dobbins J, Özkan E, Davis MM, Wucherpfennig KW, and Garcia KC. Deconstructing the peptide-MHC specificity of T cell recognition. Cell. 2014;157:1073–1087. doi:10.1016/j.cell.2014.03.047.
   PubMed Web of Science ®Google Scholar
• Kula T, Dezfulian MH, Wang CI, Abdelfattah NS, Hartman ZC, Wucherpfennig KW, Lyerly HK, Elledge SJ, et al. T-scan: a genome-wide method for the systematic discovery of T cell epitopes. Cell. 2019;178:1016–1028 e1013. doi:10.1016/j.cell.2019.07.009.
   PubMed Web of Science ®Google Scholar
• Li Pira G, Ivaldi F, Bottone L, Manca F. High throughput functional microdissection of pathogen-specific T-cell immunity using antigen and lymphocyte arrays. J Immunol Methods. 2007;326:22–32. doi:10.1016/j.jim.2007.06.012.
   PubMed Web of Science ®Google Scholar
• UniProt Consortium T. UniProt: the universal protein knowledgebase. Nucleic Acids Res. 2018;46:2699. doi:10.1093/nar/gky092.
   PubMed Web of Science ®Google Scholar
• Sherry ST, Ward MH, Kholodov M, Baker J, Phan L, Smigielski EM, and Sirotkin K. dbSNP: the NCBI database of genetic variation. Nucleic Acids Res. 2001;29:308–311. doi:10.1093/nar/29.1.308.
   PubMed Web of Science ®Google Scholar