Selective antibody-mediated targeting of class I MHC to EGFR-expressing tumor cells induces potent antitumor CTL activity in vitro and in vivo

International Journal of Cancer

Volumn 120, Issue 2, 2007, Pages 329-336

  Novak, Hila ^a   Noy, Roy ^a   Oved, Kfir ^a   Segal, Dina ^a   Wels, Winfried S ^b   Reiter, Yoram ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b INSTITUTE FOR TUMOR BIOLOGY AND EXPERIMENTAL THERAPY   (Germany)

Author keywords

Antibody targeting; MHC; T cell; Tumor immunotherapy

Indexed keywords

CETUXIMAB; CHIMERIC PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; HLA A2 ANTIGEN; HYBRID PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEIN SCFV; RECOMBINANT PROTEIN; SCFV MHC PROTEIN;

ANTIBODY AFFINITY; ANTIGEN BINDING; ANTIGEN EXPRESSION; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CARCINOMA; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DRUG EFFICACY; DRUG SPECIFICITY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VIVO STUDY; MAJOR HISTOCOMPATIBILITY COMPLEX; MELANOMA; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; PROTEIN INDUCTION; SOLID TUMOR; SQUAMOUS CELL CARCINOMA; TARGET CELL; TUMOR XENOGRAFT;

ANIMALS; ANTIBODIES, MONOCLONAL; CYTOTOXICITY, IMMUNOLOGIC; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNOTHERAPY; MICE; MICE, INBRED BALB C; NEOPLASMS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES, CYTOTOXIC; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 33845625695     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.22168     Document Type: Article

References (55)

1. Harris M. Monoclonal antibodies as therapeutic agents for cancer. Lancet Oncol 2004;5:292-302.
2. Levene AP, Singh G, Palmieri C. Therapeutic monoclonal antibodies in oncology. J R Soc Med 2005;98:146-52.
3. Pastan I. Targeted therapy of cancer with recombinant immunotoxins. Biochim Biophys Acta 1997;1333:C1-C6.
4. Lode HN, Reisfeld RA. Targeted cytokines for cancer immunotherapy. Immunol Res 2000;21:279-88.
5. Offringa R, van der Burg SH, Ossendorp F, Toes RE, Melief CJ. Design and evaluation of antigen-specific vaccination strategies against cancer. Curr Opin Immunol 2000;12:576-82.
6. Esche C, Shurin MR, Lotze MT. The use of dendritic cells for cancer vaccination. Curr Opin Mol Ther 1999;1:72-81.
7. Wang E, Phan GQ, Marincola FM. T-cell-directed cancer vaccines: the melanoma model. Expert Opin Biol Ther 2001;1:277-90.
8. Boon T, van der Bruggen P. Human tumor antigens recognized by T lymphocytes. J Exp Med 1996;183:725-9.
9. Renkvist N, Castelli C, Robbins PF, Parmiani G. A listing of human tumor antigens recognized by T cells. Cancer Immunol Immunother 2001;50:3-15.
10. Dudley M, Rosenberg SA. Adoptive-cell-transfer therapy for the treatment of patients with cancer. Nat Rev Cancer 2003;3:666-75.
11. Rosenberg SA. The emergence of modern cancer immunotherapy. Ann Surg Oncol 2005;12:344-6.
12. Dudley ME, Wunderlich JR, Robbins PF, Yang JC, Hwu P, Schwartzentruber DJ, Topalian SL, Sherry R, Restifo NP, Hubicki AM, Robinson MR, Raffeld M, et al. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 2002;298:850-4.
13. Gilboa E. How tumors escape immune destruction and what we can do about it. Cancer Immunol Immunother 1999;48:343-5.
14. Seliger B, Maeurer MJ, Ferrone S. Antigen-processing machinery breakdown and tumor growth. Immunol Today 2000;21:455-64.
15. Garrido F, Algarra I. MHC antigens and tumor escape from immune surveillance. Adv Cancer Res 2001;83:117-58.
16. Ferrone S, Finerty JF, Jaffee EM, Nabel GJ. How much longer will tumour cells fool the immune system? Immunol Today 2000;21:70-2.
17. Marincola FM, Jaffee EM, Hicklin DJ, Ferrone S. Escape of human solid tumors from T-cell recognition: molecular mechanisms and functional significance. Adv Immunol 2000;74:181-273.
18. Mendez R, et al. Analysis of HLA class I expression in different metastases from two melanoma patients undergoing peptide immunotherapy. Tissue Antigens 2001;57:508-19.
19. Real LM, et al. Multiple mechanisms of immune evasion can coexist in melanoma tumor cell lines derived from the same patient. Cancer Immunol Immunother 2001;49:621-8.
20. Restifo NP, Marincola FM, Kawakami Y, Taubenberger J, Yannelli JR, Rosenberg SA. Loss of functional β2-microglobulin in metastatic melanomas from five patients receiving immunotherapy. J Natl Cancer Inst 1996;88:100-8.
21. Lev A, Noy R, Oved K, Novak H, Segal D, Walden P, Zehn D, Reiter Y. Tumor-specific Ab-mediated targeting of MHC-peptide complexes induces regression of human tumor xenografts in vivo. Proc Natl Acad Sci USA 2004;101:9051-6.
22. Higa GM. Signaling multiplex of the epidermal growth factor receptor. Expert Rev Anticancer Ther 2004;4:1145-56.
23. Singh AB, Harris RC. Autocrine, paracrine and juxtacrine signaling by EGFR ligands. Cell Signal 2005;17:1183-93.
24. Richter M, Zhang H. Receptor-targeted cancer therapy. DNA Cell Biol 2005;24:271-82.
25. Ganti AK, Potti A. Epidermal growth factor inhibition in solid tumours. Expert Opin Biol Ther 2005;5:1165-74.
26. Masui H, Kawamoto T, Sato JD, Wolf B, Sato G, Mendelsohn J. Growth inhibition of human tumor cells in athymic mice by anti-epidermal growth factor receptor monoclonal antibodies. Cancer Res 1984; 44:1002-7.
27. Mendelsohn J, Baselga J. Status of epidermal growth factor receptor antagonists in the biology and treatment of cancer. J Clin Oncol 2003; 21:2787-99.
28. Bianco R, Daniele G, Ciardiello F, Tortora G. Monoclonal antibodies targeting the epidermal growth factor receptor. Curr Drug Targets 2005;6:275-87.
29. Goldberg RM. Cetuximab. Nat Rev Drug Discov 2005; (Suppl) S10, S11.
30. Weis W, Beerli R, Hellmann P, Schmidt M, Marte BM, Kornilova ES, Hekele A, Mendelsohn J, Groner B, Hynes NE. EGF receptor and p185erbB-2-specific single-chain antibody toxins differ in their cell-killing activity on tumor cells expressing both receptor proteins. Int J Cancer 1995;60:137-44.
31. Denkberg G, Cohen CJ, Segal D, Kirkin AF, Reiter Y. Recombinant human single-chain MHC-peptide complexes made from E. coli by in vitro refolding: functional single-chain MHC-peptide complexes and tetramers with tumor associated antigens. Eur J Immunol 2000;30: 3522-32.
32. Denkberg G, Cohen CJ, Reiter Y. Critical role for cd8 in binding of mhc tetramers to tcr: cd8 antibodies block specific binding of human tumor-specific mhc-peptide tetramers to TCR. J Immunol 2001;167: 270-6.
33. Parkhurst MR, Salgaller ML, Southwood S, Robbins PF, Sette A, Rosenberg SA, Kawakami Y. Improved induction of melanoma-reactive CTL with peptides from the melanoma antigen gp100 modified at HLA-A*0201-binding residues. J Immunol 2001;157:2539-48.
34. Tussey L, Speller S, Gallimore A, Vessey R. Functionally distinct CD8+ memory T cell subsets in persistent EBV infection are differentiated by migratory receptor expression. Eur J Immunol 2000;30: 1823-9.
35. Oved K, Lev A, Noy R, Segal D, Reiter Y. Antibody-mediated targeting of human single-chain class I MHC with covalently linked peptides induces efficient killing of tumor cells by tumor or viral-specific cytotoxic T lymphocytes. Cancer Immunol Immunother 2005;54:867-79.
36. Laskin JJ, Sandler AB. Epidermal growth factor receptor: a promising target in solid tumours. Cancer Treat Rev 2004;30:1-17.
37. Castillo M, Etienne-Grimaldi MC, Fischel JL, Formento P, Magne N, Milano G. Pharmacological background of EGFR targeting. Ann Oncol 2004;15:1007-12.
38. Wells A. EGF receptor. Int J Biochem Cell Biol 1999;31:637-43.
39. Govindan R. Cetuximab in advanced non-small cell lung cancer. Clin Cancer Res 2004;10:4241-44.
40. Curnow RT. Clinical experience with CD64-directed immunotherapy. An overview. Cancer Immunol Immunother 1997;45:210-15.
41. Goldstein J, Graziano RF, Sundarapandiyan K, Somasundaram C, Deo YM. Cytolytic and cytostatic properties of an anti-human Fc γR1 (CD64) X epidermal growth factor bispecific fusion protein. J Immunol 1997;158:872-9.
42. Lee PP, Yee C, Savage PA, Fong L, Brockstedt D, Weber JS, Johnson D, Swetter S, Thompson J, Greenberg PD, Roederer M, Davis MM. Characterization of circulating T cells specific for tumor-associated antigens in melanoma patients. Nat Med 1999;5:677-85.
43. Porgador A, Yewdell JW, Deng Y, Bennink JR, Germain RN. Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody. Immunity 1997;6:715-26.
44. Christinck ER, Luscher MA, Barber BH, Williams DB. Peptide binding to class I MHC on living cells and quantitation of complexes required for CTL lysis. Nature 1991;352:67-70.
45. Cohen CJ, Hoffmann N, Farago M, Hoogenboom HR, Eisenbach L, Reiter Y. Direct detection and quantitation of a distinct T-cell epitope derived from tumor-specific epithelial cell-associated mucin using human recombinant antibodies endowed with the antigen-specific, major histocompatibility complex-restricted specificity of T cells. Cancer Res 2002;62:5835-44.
46. Ogg GS, Dunbar PR, Cerundolo V, McMichael AJ, Lemoine NR, Savage P. Sensitization of tumor cells to lysis by virus-specific CTL using antibody-targeted MHC class 1/peptide complexes. Br J Cancer 2000;82:1058-62.
47. Robert B, Guillaume P, Luescher I, Romero P, Mach JP. Antibody-conjugated MHC class I tetramers can target tumor cells for specific lysis by T lymphocytes. Eur J Immunol 2000;30:3165-70.
48. Robert B, Guillaume P, Luescher I, Doucey MA, Cerottini JC, Romero P, Mach JP. Redirecting anti-viral CTL against cancer cells by surface targeting of monomeric MHC class I-viral peptide conjugated to antibody fragments. Cancer Immun 2001;1:2-9.
49. Savage P, Cowburn P, Clayton A, Man S, Lawson T, Ogg G, Lemoine N, McMichael A, Epenetos A. Anti-viral cytotoxic T cells inhibit the growth of cancer cells with antibody targeted HLA class I/peptide complexes in SCID mice. Int J Cancer 2002;98:561-66.
50. Lanzavecchia A, Lezzi G, Viola A. From TCR engagement to T cell activation: a kinetic view of T cell behavior. Cell 1999;96:1-4.
51. Bromely SK, Burack WR, Johnson KG, Somersalo K, Sims TN, Sumen C, Davis MM, Shaw AS, Allen PM, Dustin ML. The immunological synapse. Annu Rev Immunol 2001;19:375-96.
52. Donda A, Cesson V, Mach JP, Corradin G, Primus FJ, Robert B. In vivo targeting of an anti-tumor antibody coupled to antigenic MHC class I complexes induces specific growth inhibition and regression of established syngeneic tumor grafts. Cancer Immun 2003;3:11-28.
53. Jain RK. Transport of molecules, particles and cells in solid tumors. Annu Rev Biomed 1999;1:241-63.
54. Lechner F, Cuero AL, Kantzanou M, Klenerman P. Studies of human antiviral CD8+ lymphocytes using class I peptide tetramers. Rev Med Virol 2001;11:11-22.
55. Wang BR, Malie R, Greenwood EJ, Collins, Frelinger JA. Naive CD8+ T cells do not require costimulation for proliferation and differentiation into cytotoxic effector cells. J Immunol 2000;164:1216-22.