Opportunities and challenges for TCR mimic antibodies in cancer therapy

References

• Bassani-Sternberg M, Pletscher-Frankild S, Jensen LJ, et al. Mass spectrometry of human leukocyte antigen class I peptidomes reveals strong effects of protein abundance and turnover on antigen presentation. Mol Cell Proteomics. 2015;14(3):658–673. doi:10.1074/mcp.M114.042812.
   PubMed Web of Science ®Google Scholar
• Draper LM, Kwong MLM, Gros A, et al. Targeting of HPV-16+ epithelial cancer cells by TCR gene engineered T cells directed against E6. Clin Cancer Res. 2015;21(19):4431–4439. doi:10.1158/1078-0432.CCR-14-3341.
   PubMed Web of Science ®Google Scholar
• Mizukoshi E, Nakamoto Y, Tsuji H, et al. Identification of alpha-fetoprotein-derived peptides recognized by cytotoxic T lymphocytes in HLA-A24+ patients with hepatocellular carcinoma. Int J Cancer. 2006;118(5):1194–1204. doi:10.1002/ijc.21468.
   PubMed Web of Science ®Google Scholar
• Wittman VP, Woodburn D, Nguyen T, et al. Antibody targeting to a class I MHC-peptide epitope promotes tumor cell death. J Immunol. 2006;177(6):4187–4195. doi:10.4049/jimmunol.177.6.4187.
   PubMed Web of Science ®Google Scholar
• Polakova K, Plaksin D, Chung DH, et al. Antibodies directed against the MHC-I molecule H-2Dd complexed with an antigenic peptide: similarities to a T cell receptor with the same specificity. J Immunol. 2000;165(10):5703–5712. doi:10.4049/jimmunol.165.10.5703.
   PubMed Web of Science ®Google Scholar
• Lev A, Denkberg G, Cohen CJ, et al. Isolation and characterization of human recombinant antibodies endowed with the antigen-specific, major histocompatibility complex-restricted specificity of T cells directed toward the widely expressed tumor T-cell epitopes of the telomerase catalytic sub. Cancer Res. 2002;62(11):3184–3194.
   PubMed Web of Science ®Google Scholar
• Denkberg G, Cohen CJ, Lev A, et al. Direct visualization of distinct T cell epitopes derived from a melanoma tumor-associated antigen by using human recombinant antibodies with MHC-restricted T cell receptor-like specificity. Proc Natl Acad Sci U S A. 2002;99(14):9421–9426. doi:10.1073/pnas.132285699.
   PubMed Web of Science ®Google Scholar
• Dahan R, Reiter Y. T-cell-receptor-like antibodies - generation, function and applications. Expert Rev Mol Med. 2012;14:e6. doi:10.1017/erm.2012.2.
   Google Scholar
• Luckey CJ, King GM, Marto JA, et al. Proteasomes can either generate or destroy MHC Class I epitopes: evidence for nonproteasomal epitope generation in the cytosol. J Immunol. 1998;161:112–121.
   PubMed Web of Science ®Google Scholar
• Ataie N, Xiang J, Cheng N, et al. Structure of a TCR mimic antibody with target predicts pharmacogenetics. J Mol Biol. 2015. doi:10.1016/j.jmb.2015.12.002.
   PubMed Web of Science ®Google Scholar
• Stewart-jones G, Hombach A, Shenderov E, et al. Rational development of high-affinity T-cell receptor-like antibodies. Proc Natl Acad Sci. 2009;106(26):10872–10872. doi:10.1073/pnas.0905399106.
   Web of Science ®Google Scholar
• Gill S, June CH. Going viral: chimeric antigen receptor T-cell therapy for hematological malignancies. Immunol Rev. 2015;263(1):68–89. doi:10.1111/imr.12243.
   PubMed Web of Science ®Google Scholar
• Curran KJ, Brentjens RJ. Chimeric antigen receptor T cells for cancer immunotherapy. J Clin Oncol. 2015;33(15):1703–1706. doi:10.1200/JCO.2014.60.3449.
   PubMed Web of Science ®Google Scholar
• Brentjens RJ, Davila ML, Riviere I, et al. CD19-targeted T cells rapidly induce molecular remissions in adults with chemotherapy-refractory acute lymphoblastic leukemia. Sci Transl Med. 2013;5(177):177ra38. doi:10.1126/scitranslmed.3005930.
   PubMed Web of Science ®Google Scholar
• Starck L, Popp K, Pircher H, et al. Immunotherapy with TCR-redirected T cells: comparison of TCR-transduced and TCR-engineered hematopoietic stem cell-derived T cells. J Immunol. 2014;192(1):206–213. doi:10.4049/jimmunol.1202591.
   PubMed Web of Science ®Google Scholar
• Dao T, Yan S, Veomett N, et al. Targeting the intracellular WT1 oncogene product with a therapeutic human antibody. Sci Transl Med. 2013;5(176). doi:10.1126/scitranslmed.3005661.
   Web of Science ®Google Scholar
• Sergeeva A, Alatrash G, He H, et al. An anti-PR1/HLA-A2 T-cell receptor-like antibody mediates complement-dependent cytotoxicity against acute myeloid leukemia progenitor cells. Blood. 2011;117(16):4262–4272. doi:10.1182/blood-2010-07-299248.
   PubMed Web of Science ®Google Scholar
• Sastry KSR, Too CT, Kaur K, et al. Targeting hepatitis B virus-infected cells with a T-cell receptor-like antibody. J Virol. 2011;85(5):1935–1942. doi:10.1128/JVI.01990-10.
   PubMed Web of Science ®Google Scholar
• Kim S, Pinto AK, Myers NB, et al. A novel T-cell receptor mimic defines dendritic cells that present an immunodominant West Nile virus epitope in mice. Eur J Immunol. 2014;44(7):1936–1946. doi:10.1002/eji.201444450.
   PubMed Web of Science ®Google Scholar
• Correale P, Walmsley K, Nieroda C, et al. In vitro generation of human cytotoxic T lymphocytes specific for peptides derived from prostate-specific antigen. J Natl Cancer Inst. 1997;89(4):293–300.
   PubMedGoogle Scholar
• Almstedt M, Blagitko-Dorfs N, Duque-Afonso J, et al. The DNA demethylating agent 5-aza-2ʹ-deoxycytidine induces expression of NY-ESO-1 and other cancer/testis antigens in myeloid leukemia cells. Leuk Res. 2010;34(7):899–905. doi:10.1016/j.leukres.2010.02.004.
   PubMed Web of Science ®Google Scholar
• Valmori BD, Gileadi U, Servis C, et al. Modulation of proteasomal activity required for the generation of a cytotoxic T lymphocyte – defined peptide derived from the tumor antigen MAGE-3. J Exp Med. 1999;189:6.
   Web of Science ®Google Scholar
• Michaeli Y, Denkberg G, Sinik K, et al. Expression hierarchy of T cell epitopes from melanoma differentiation antigens: unexpected high level presentation of tyrosinase-HLA-A2 Complexes revealed by peptide-specific, MHC-restricted, TCR-like antibodies. J Immunol. 2009;182(10):6328–6341. doi:10.4049/jimmunol.0801898.
   PubMed Web of Science ®Google Scholar
• Tran E, Ahmadzadeh M, Lu Y, et al. Immunogenicity of somatic mutations in human gastrointestinal cancers. Sci (80-). 2015;350(6266):1387–1390. doi:10.1126/science.aad1253.
   PubMed Web of Science ®Google Scholar
• Karasaki T, Nagayama K, Kawashima M, et al. Identification of individual cancer-specific somatic mutations for neoantigen-based immunotherapy of lung cancer. J Thorac Oncol. 2015; doi:10.1016/j.jtho.2015.11.006.
   PubMed Web of Science ®Google Scholar
• Ito D, Visus C, Hoffmann TK, et al. Immunological characterization of missense mutations occurring within cytotoxic T cell-defined p53 epitopes in HLA-A*0201+ squamous cell carcinomas of the head and neck. Int J Cancer. 2007;120(12):2618–2624. doi:10.1002/ijc.22584.
   PubMed Web of Science ®Google Scholar
• Cai A, Keskin DB, DeLuca DS, et al. Mutated BCR-ABL generates immunogenic T-cell epitopes in CML patients. Clin Cancer Res. 2012;18(20):5761–5772. doi:10.1158/1078-0432.CCR-12-1182.
   PubMed Web of Science ®Google Scholar
• Bocchia M, Korontsvit T, Xu Q, et al. Specific human cellular immunity to bcr-abl oncogene-derived peptides. Blood. 1996;87(9):3587–3592.
   PubMed Web of Science ®Google Scholar
• Chang K, Creighton CJ, Davis C, et al. The Cancer Genome Atlas Pan-Cancer analysis project. Nat Genet. 2013;45(10):1113–1120. doi:10.1038/ng.2764.
   PubMed Web of Science ®Google Scholar
• Dahan R, Gebe JA, Preisinger A, et al. Antigen-specific immunomodulation for type 1 diabetes by novel recombinant antibodies directed against diabetes-associates auto-reactive T cell epitope. J Autoimmun. 2013;47:83–93. doi:10.1016/j.jaut.2013.08.009.
   PubMed Web of Science ®Google Scholar
• Chang AY, Dao T, Scott A, et al. A therapeutic TCR mimic monoclonal antibody for intracellular PRAME protein in leukemias. Poster Presentation: 57th American Society of Hematologists Annual Meeting. Dec 2015. Orlando, FL
   Google Scholar
• Schrump DS, Fischette MR, Nguyen DM, et al. Phase I study of decitabine-mediated gene expression in patients with cancers involving the lungs, esophagus, or pleura. Clin Cancer Res. 2006;12(19):5777–5785. doi:10.1158/1078-0432.CCR-06-0669.
   PubMed Web of Science ®Google Scholar
• Gang AO, Frøsig TM, Brimnes MK, et al. 5-Azacytidine treatment sensitizes tumor cells to T-cell mediated cytotoxicity and modulates NK cells in patients with myeloid malignancies. Blood Cancer J. 2014;4:e197. doi:10.1038/bcj.2014.14.
   PubMed Web of Science ®Google Scholar
• Ma W, Vigneron N, Chapiro J, et al. A MAGE-C2 antigenic peptide processed by the immunoproteasome is recognized by cytolytic T cells isolated from a melanoma patient after successful immunotherapy. Int J Cancer. 2011;129(10):2427–2434. doi:10.1002/ijc.25911.
   PubMed Web of Science ®Google Scholar
• Cabrera T, Angustias Fernandez M, Sierra A, et al. High frequency of altered HLA class I phenotypes in invasive breast carcinomas. Hum Immunol. 1996;50(2):127–134. doi:10.1016/0198-8859(96)00145-0.
   PubMed Web of Science ®Google Scholar
• Campoli M, Ferrone S. HLA antigen changes in malignant cells: epigenetic mechanisms and biologic significance. Oncogene. 2008;27(45):5869–5885. doi:10.1038/onc.2008.273.
   PubMed Web of Science ®Google Scholar
• Mimura K, Shiraishi K, Mueller A, et al. The MAPK pathway is a predominant regulator of HLA-A expression in esophageal and gastric cancer. J Immunol. 2013;191(12):6261–6272. doi:10.4049/jimmunol.1301597.
   PubMed Web of Science ®Google Scholar
• Pollack BP, Sapkota B, Cartee TV. Epidermal growth factor receptor inhibition augments the expression of MHC class I and II genes. Clin Cancer Res. 2011;17(13):4400–4413. doi:10.1158/1078-0432.CCR-10-3283.
   PubMed Web of Science ®Google Scholar
• Srivastava RM, Trivedi S, Concha-Benavente F, et al. STAT1-induced HLA class I upregulation enhances immunogenicity and clinical response to anti-EGFR mAb cetuximab therapy in HNC patients. Cancer Immunol Res. 2015;1–11. doi:10.1158/2326-6066.CIR-15-0053.
   PubMed Web of Science ®Google Scholar
• Palmisano GL, Pistillo MP, Capanni P, et al. Investigation of HLA class I downregulation in breast cancer by RT-PCR. Hum Immunol. 2001;62(2):133–139. doi:10.1016/S0198-8859(00)00241-X.
   PubMed Web of Science ®Google Scholar
• Diebolder CA, Beurskens FJ, de Jong RN, et al. Complement is activated by IgG hexamers assembled at the cell surface. Science. 2014;343:1260–1263. doi:10.1126/science.1248943.
   PubMed Web of Science ®Google Scholar
• Verma B, Neethling FA, Caseltine S, et al. TCR mimic monoclonal antibody targets a specific peptide/HLA class I complex and significantly impedes tumor growth in vivo using breast cancer models. J Immunol. 2010;184(4):2156–2165. doi:10.4049/jimmunol.0902414.
   PubMed Web of Science ®Google Scholar
• Hayes JM, Cosgrave EF, Struwe WB, et al. Glycosylation and Fc receptors. Curr Top Microbial Immunol. 2014;382:165–199. doi:10.1007/978-3-319-07911-0_8.
   PubMed Web of Science ®Google Scholar
• Dubrovsky L, Pankov D, Brea EJ, et al. A TCR-mimic antibody to WT1 bypasses tyrosine kinase inhibitor resistance in human BCR-ABL+ leukemias. Blood. 2014;123(21):3296–3304. doi:10.1182/blood-2014-01-549022.
   PubMed Web of Science ®Google Scholar
• Veomett N, Dao T, Liu H, et al. Therapeutic efficacy of an Fc-enhanced TCR-like antibody to the intracellular WT1 oncoprotein. Clin Cancer Res. 2014;20(15):4036–4046. doi:10.1158/1078-0432.CCR-13-2756.
   PubMed Web of Science ®Google Scholar
• Dao T, Pankov D, Scott A, et al. Therapeutic bispecific T-cell engager antibody targeting the intracellular oncoprotein WT1. Nat Biotechnol. 2015;33:1–10. doi:10.1038/nbt.3349.
   PubMed Web of Science ®Google Scholar
• Jung ST, Kelton W, Kang TH, et al. Effective phagocytosis of low Her2 tumor cell lines with engineered, aglycosylated IgG displaying high FcγRIIa affinity and selectivity. ACS Chem Biol. 2013;8(2):368–375.
   PubMed Web of Science ®Google Scholar
• McCracken MN, Cha AC, Weissman IL. Molecular pathways: activating T cells after cancer cell phagocytosis from blockade of CD47 “Don’t eat Me” signals. Clin Cancer Res. 2015;21(16):3597–3601. doi:10.1158/1078-0432.CCR-14-2520.
   PubMed Web of Science ®Google Scholar
• Chao MP, Alizadeh AA, Tang C, et al. Anti-CD47 antibody synergizes with rituximab to promote phagocytosis and eradicate non-Hodgkin lymphoma. Cell. 2010;142(5):699–713. doi:10.1016/j.cell.2010.07.044.
   PubMed Web of Science ®Google Scholar
• Nagorsen D, Baeuerle PA. Immunomodulatory therapy of cancer with T cell-engaging BiTE antibody blinatumomab. Exp Cell Res. 2011;317(9):1255–1260. doi:10.1016/j.yexcr.2011.03.010.
   PubMed Web of Science ®Google Scholar
• Curran KJ, Pegram HJ, Brentjens RJ. Chimeric antigen receptors for T cell immunotherapy: current understanding and future directions. J Gene Med. 2012;14(6):405–415. doi:10.1002/jgm.2604.
   PubMed Web of Science ®Google Scholar
• Rafiq S, Dao T, Liu C, et al. Engineered T cell receptor-mimic antibody, (TCRm) chimeric antigen receptor (CAR) T cells against the intracellular protein Wilms tumor-1 (WT1) for treatment of hematologic and solid cancers. Poster Presentation: 56th American Society of Hematologists Annual Meeting. Dec 2014. San Francisco, CA
   Google Scholar
• Zhang G, Wang L, Cui H, et al. Anti-melanoma activity of T cells redirected with a TCR-like chimeric antigen receptor. Sci Rep. 2014;4:3571. doi:10.1038/srep03571.
   PubMed Web of Science ®Google Scholar
• Oren R, Hod-Marco M, Haus-Cohen M, et al. Functional comparison of engineered T cells carrying a native TCR versus TCR-like antibody-based chimeric antigen receptors indicates affinity/avidity thresholds. J Immunol. 2014;193(11):5733–5743. doi:10.4049/jimmunol.1301769.
   PubMed Web of Science ®Google Scholar
• Klechevsky E, Gallegos M, Denkberg G, et al. Antitumor activity of immunotoxins with T-cell receptor-like specificity against human melanoma xenografts. Cancer Res. 2008;68(15):6360–6367. doi:10.1158/0008-5472.CAN-08-0928.
   PubMed Web of Science ®Google Scholar
• McDevitt MR, Ma D, Lai LTL, et al. Tumor therapy with targeted atomic nanogenerators. Sci (80-). 2001;294(5546):1537–1540. doi:10.1126/science.1064126.
   PubMed Web of Science ®Google Scholar
• Tang K-W, Alaei-Mahabadi B, Samuelsson T, et al. The landscape of viral expression and host gene fusion and adaptation in human cancer. Nat Commun. 2013;4:2513. doi:10.1038/ncomms3513.
   PubMed Web of Science ®Google Scholar
• Makler O, Oved K, Netzer N, et al. Direct visualization of the dynamics of antigen presentation in human cells infected with cytomegalovirus revealed by antibodies mimicking TCR specificity. Eur J Immunol. 2010;40(6):1552–1565. doi:10.1002/eji.200939875.
   PubMed Web of Science ®Google Scholar
• Worley BS, van den Broeke LT, Goletz TJ, et al. Antigenicity of fusion proteins from sarcoma-associated chromosomal translocations. Cancer Res. 2001;61(18):6868–6875.
   PubMed Web of Science ®Google Scholar