1,586
Views
1
CrossRef citations to date
0
Altmetric
Original Research

Novel Fab-peptide-HLA-I fusion proteins for redirecting pre-existing anti-CMV T cell immunity to selectively eliminate carcinoma cells

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon show all
Article: 2207868 | Received 22 Feb 2023, Accepted 24 Apr 2023, Published online: 10 May 2023

References

  • Jenkins RW, Barbie DA, Flaherty KT. Mechanisms of resistance to immune checkpoint inhibitors. Br J Cancer. 2018;118:9–15. doi:10.1038/bjc.2017.434.
  • Syn NL, Teng MWL, Mok TSK, Soo RA. De-novo and acquired resistance to immune checkpoint targeting. Lancet Oncol. 2017;18:e731–741. doi:10.1016/S1470-2045(17)30607-1.
  • O’Donnell JS, L Teng MW, Smyth MJ. Cancer immunoediting and resistance to T cell-based immunotherapy. Nat Rev Clin Oncol. 2019;16:151–167. doi:10.1038/s41571-018-0142-8.
  • O’Hara GA, Welten SPM, Klenerman P, Arens R. Memory T cell inflation: understanding cause and effect. Trends Immunol. 2012;33:84–90. doi:10.1016/j.it.2011.11.005.
  • Khan N, Shariff N, Cobbold M, Bruton R, Ainsworth JA, Sinclair AJ, Nayak L, Moss PA, et al. Cytomegalovirus seropositivity drives the CD8 T Cell repertoire toward greater clonality in healthy elderly individuals. J Immunol. 2002;169:1984–1992. doi:10.4049/jimmunol.169.4.1984.
  • Ouyang Q, Wagner WM, Wikby A, Walter S, Aubert G, Dodi AI, Travers P, Pawelec G. Large numbers of dysfunctional CD8 + T lymphocytes bearing receptors for a single dominant CMV epitope in the very old. J Clin Immunol. 2003;23:247–257. doi:10.1023/A:1024580531705.
  • Wills MR, Carmichael AJ, Mynard K, Jin X, Weekes MP, Plachter B, Sissons JG. The human cytotoxic T-lymphocyte (CTL) response to cytomegalovirus is dominated by structural protein pp65: frequency, specificity, and T-cell receptor usage of pp65-specific CTL. J Virol. 1996;70:7569–7579. doi:10.1128/jvi.70.11.7569-7579.1996.
  • Snyder CM, Cho KS, Bonnett EL, van Dommelen S, Shellam GR, Hill AB. Memory inflation during chronic viral infection is maintained by continuous production of short-lived, functional T cells. Immunity. 2008;29:650–659. doi:10.1016/j.immuni.2008.07.017.
  • Derhovanessian E, Maier AB, Hähnel K, Beck R, de Craen AJM, Slagboom EP, Westendorp RGJ, Pawelec G. Infection with cytomegalovirus but not herpes simplex virus induces the accumulation of late-differentiated CD4 + and CD8 + T-cells in humans. J Gen Virol. 2011;92:2746–2756. doi:10.1099/vir.0.036004-0.
  • Wills MR, Okecha G, Weekes MP, Gandhi MK, Sissons PJG, Carmichael AJ. Identification of naive or antigen-experienced human CD8(+) T cells by expression of costimulation and chemokine receptors: analysis of the human cytomegalovirus-specific CD8(+) T cell response. J Immunol. 2002;168:5455–5464. doi:10.4049/jimmunol.168.11.5455.
  • Rosato PC, Wijeyesinghe S, Stolley JM, Nelson CE, Davis RL, Manlove LS, Pennell CA, Blazar BR, Chen CC, Geller MA, et al. Virus-specific memory T cells populate tumors and can be repurposed for tumor immunotherapy. Nat Commun. 2019;10. doi:10.1038/s41467-019-08534-1.
  • Simoni Y, Becht E, Fehlings M, Loh CY, Koo S-L, Teng KWW, Yeong JPS, Nahar R, Zhang T, Kared H, et al. Bystander CD8 + T cells are abundant and phenotypically distinct in human tumour infiltrates. Nature. 2018;557:575–579. doi:10.1038/s41586-018-0130-2.
  • Schmittnaegel M, Levitsky V, Hoffmann E, Georges G, Mundigl O, Klein C, Knoetgen H. Committing cytomegalovirus-specific cd8 t cells to eliminate tumor cells by bifunctional major histocompatibility class i antibody fusion molecules. Cancer Immunol Res. 2015;3:764–776. doi:10.1158/2326-6066.CIR-15-0037.
  • Schmittnaegel M, Hoffmann E, Imhof-Jung S, Fischer C, Drabner G, Georges G, Klein C, Knoetgen H. A new class of bifunctional major histocompatibility class I antibody fusion molecules to redirect CD8 T cells. Mol Cancer Ther. 2016;15:2130–2142. doi:10.1158/1535-7163.MCT-16-0207.
  • Lacey SF, Villacres MC, La Rosa C, Wang Z, Longmate J, Martinez J, Brewer JC, Mekhoubad S, Maas R, Leedom JM, et al. Relative dominance of HLA-B*07 restricted CD8+ T-lymphocyte immune responses to human cytomegalovirus pp65 in persons sharing HLA-A*02 and HLA-B*07 Alleles. Hum Immunol. 2003;64:440–452. doi:10.1016/S0198-8859(03)00028-4.
  • Gillespie GMA, Wills MR, Appay V, O’Callaghan C, Murphy M, Smith N, Sissons P, Rowland-Jones S, Bell JI, Moss PAH. Functional heterogeneity and high frequencies of cytomegalovirus-specific CD8+ T lymphocytes in healthy seropositive donors. J Virol. 2000;74:8140–8150. doi:10.1128/JVI.74.17.8140-8150.2000.
  • Went PT, Lugli A, Meier S, Bundi M, Mirlacher M, Sauter G, Dirnhofer S. Frequent EpCam protein expression in human carcinomas. Hum Pathol. 2004;35:122–128. doi:10.1016/j.humpath.2003.08.026.
  • Hosie L, Pachnio A, Zuo J, Pearce H, Riddell S, Moss P. Cytomegalovirus-specific t cells restricted by HLA-Cw*0702 increase markedly with age and dominate the CD8+ T-Cell repertoire in older people. Front Immunol. 2017;8. doi:10.3389/fimmu.2017.01776.
  • Yang J, Isaji T, Zhang G, Qi F, Duan C, Fukuda T, Gu J. EpCAM associates with integrin and regulates cell adhesion in cancer cells. Biochem Biophys Res Commun. 2020;522:903–909. doi:10.1016/j.bbrc.2019.11.152.
  • Willuda J, Honegger A, Waibel R, Schubiger PA, Stahel R, Zangemeister-Wittke U, Plückthun A. High thermal stability is essential for tumor targeting of antibody fragments: engineering of a humanized anti-epithelial glycoprotein-2 (epithelial cell adhesion molecule) single-chain Fv fragment. Cancer Res. 1999;59:5758–5767.
  • Kettleborough CA, Saldanha J, Heath VJ, Morrison CJ, Bendig MM. Humanization of a mouse monoclonal antibody by CDR-grafting: the importance of framework residues on loop conformation. Protein Eng. 1991;4:773–783. doi:10.1093/protein/4.7.773.
  • Purbhoo MA, Irvine DJ, Huppa JB, Davis MM. T cell killing does not require the formation of a stable mature immunological synapse. Nat Immunol. 2004;5:524–530. doi:10.1038/ni1058.
  • Goldman JL, Miller JO, Miller N, Eveleigh R, Gibson A, Phillips EJ, Pastinen T. HLA-B*07: 02 and HLA-C*07: 02 are associated with trimethoprim-sulfamethoxazole respiratory failure. Pharmacogenomics J. 2022;22:124–129. doi:10.1038/s41397-022-00266-8.
  • Shimabukuro-Vornhagen A, Gödel P, Subklewe M, Stemmler HJ, Schlößer HA, Schlaak M, Kochanek M, Böll B, von Bergwelt-Baildon MS. Cytokine release syndrome. J ImmunoTher Cancer. 2018;6. doi:10.1186/s40425-018-0343-9.
  • Millar DG, Ramjiawan RR, Kawaguchi K, Gupta N, Chen J, Zhang S, Nojiri T, Ho WW, Aoki S, Jung K, et al. Antibody-mediated delivery of viral epitopes to tumors harnesses CMV-specific T cells for cancer therapy. Nat Biotechnol. 2020;38:420–425. doi:10.1038/s41587-019-0404-8.
  • Jung K, Son M-J, Lee S-Y, Kim J-A, Ko D-H, Yoo S, Kim C-H, Kim Y-S. Antibody-mediated delivery of a viral MHC-I epitope into the cytosol of target tumor cells repurposes virus-specific CD8+ T cells for cancer immunotherapy. Mol Cancer. 2022;21:102. doi:10.1186/s12943-022-01574-0.
  • Aptsiauri N, Carretero R, Garcia-Lora A, Real LM, Cabrera T, Garrido F. Regressing and progressing metastatic lesions: resistance to immunotherapy is predetermined by irreversible HLA class I antigen alterations. Cancer Immunol, Immunother. 2008;57:1727–1733. doi:10.1007/s00262-008-0532-3.
  • Söderberg-Nauclér C. New mechanistic insights of the pathogenicity of high-risk cytomegalovirus (CMV) strains derived from breast cancer: hope for new cancer therapy options. EBioMedicine. 2022;81:104103. doi:10.1016/j.ebiom.2022.104103.
  • Zuhair M, Smit GSA, Wallis G, Jabbar F, Smith C, Devleesschauwer B, Griffiths P. Estimation of the worldwide seroprevalence of cytomegalovirus: a systematic review and meta-analysis. Rev Med Virol. 2019;29:e2034. doi:10.1002/rmv.2034.
  • Gonzalez-Galarza FF, McCabe A, Melo dos Santos EJ, Jones AR, Middleton D. A snapshot of human leukocyte antigen (hla) diversity using data from the Allele Frequency Net Database. Hum Immunol. 2021;82:496–504. doi:10.1016/j.humimm.2020.10.004.
  • Barnes S, Schilizzi O, Audsley KM, Newnes HV, Foley B. Deciphering the immunological phenomenon of adaptive natural killer (NK) cells and cytomegalovirus (CMV). Int J Mol Sci. 2020;21:1–17. doi:10.3390/ijms21228864.