Cancer immunotherapy using a bispecific NK receptor fusion protein that engages both T cells and tumor cells

Cancer Research

Volumn 71, Issue 6, 2011, Pages 2066-2076

  Zhang, Tong ^a   Sentman, Charles L ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIBODY; CD3 EPSILON ANTIBODY; CD3 EPSILON SINGLE CHAIN FRAGMENT VARIABLE NATURAL KILLER CELL RECEPTOR NKG2D FUSION PROTEIN; GAMMA INTERFERON; HYBRID PROTEIN; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE FREE SURVIVAL; DRUG BINDING; DRUG CYTOTOXICITY; DRUG DESIGN; DRUG EFFICACY; DRUG SELECTIVITY; DRUG SPECIFICITY; GAMMA DELTA T LYMPHOCYTE; HOST RANGE; IMMUNOLOGICAL MEMORY; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE COUNT; LYMPHOCYTIC INFILTRATION; LYMPHOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SUPPRESSOR CELL; T LYMPHOCYTE ACTIVATION; TUMOR VOLUME;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGENS, CD3; CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; FLOW CYTOMETRY; HEK293 CELLS; HUMANS; IMMUNOTHERAPY; INTERFERON-GAMMA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOPLASMS; NEOPLASMS, EXPERIMENTAL; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; SINGLE-CHAIN ANTIBODIES; T-LYMPHOCYTES; TUMOR MICROENVIRONMENT;

EID: 79952755728     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-3200     Document Type: Article

References (46)

1. Ho WY, Blattman JN, Dossett ML, Yee C, Greenberg PD. Adoptive immunotherapy: engineering T cell responses as biologic weapons for tumor mass destruction. Cancer Cell 2003;3:431-7. (Pubitemid 38340289)
2. Leen AM, Rooney CM, Foster AE. Improving T cell therapy for cancer. Annu Rev Immunol 2007;25:243-65. (Pubitemid 46697909)
3. Blattman JN, Greenberg PD. Cancer immunotherapy: a treatment for the masses. Science 2004;305:200-5. (Pubitemid 38886725)
4. Rabinovich GA, Gabrilovich D, Sotomayor EM. Immunosuppressive strategies that are mediated by tumor cells. Annu Rev Immunol 2007;25:267-96. (Pubitemid 46697910)
5. Bargou R, Leo E, Zugmaier G, Klinger M, Goebeler M, Knop S, et al. Tumor regression in cancer patients by very low doses of a T cell-engaging antibody. Science 2008;321:974-7.
6. Baeuerle PA, Kufer P, Bargou R. BiTE: teaching antibodies to engage T-cells for cancer therapy. Curr Opin Mol Ther 2009;11:22-30.
7. Lanier LL. NK cell recognition. Annu Rev Immunol 2005;23:225-74. (Pubitemid 40563170)
8. Raulet DH. Roles of the NKG2D immunoreceptor and its ligands. Nat Rev Immunol 2003;3:781-90. (Pubitemid 37328656)
9. Gonzalez S, Lopez-Soto A, Suarez-Alvarez B, Lopez-Vazquez A, Lopez-Larrea C. NKG2D ligands: key targets of the immune response. Trends Immunol 2008;29:397-403.
10. Nausch N, Galani IE, Schlecker E, Cerwenka A. Mononuclear myeloidderived "suppressor" cells express RAE-1 and activate natural killer cells. Blood 2008;112:4080-9.
11. Barber A, Rynda A, Sentman CL. Chimeric NKG2D expressing T cells eliminate immunosuppression and activate immunity within the ovarian tumor microenvironment. J Immunol 2009;183:6939-47.
12. Shastri N, Gonzalez F. Endogenous generation and presentation of the ovalbumin peptide/Kb complex to T cells. J Immunol 1993;150:2724-36. (Pubitemid 23127522)
13. Zhang T, Barber A, Sentman CL. Chimeric NKG2D modified T cells inhibit systemic T-cell lymphoma growth in a manner involving multiple cytokines and cytotoxic pathways. Cancer Res 2007;67:11029-36. (Pubitemid 350145933)
14. Barber A, Zhang T, Sentman CL. Immunotherapy with chimeric NKG2D receptors leads to long-term tumor-free survival and development of host antitumor immunity in murine ovarian cancer. J Immunol 2008;180:72-8.
15. Grundy MA, Zhang T, Sentman CL. NK cells rapidly remove B16F10 tumor cells in a perforin and interferon-gamma independent manner in vivo. Cancer Immunol Immunother 2007;56:1153-61. (Pubitemid 46763930)
16. Zhang T, Lemoi BA, Sentman CL. Chimeric NK-receptor-bearing T cells mediate antitumor immunotherapy. Blood 2005;106:1544-51. (Pubitemid 41208564)
17. Zhang T, Barber A, Sentman CL. Generation of antitumor responses by genetic modification of primary human T cells with a chimeric NKG2D receptor. Cancer Res 2006;66:5927-33. (Pubitemid 43927148)
18. Eriksson M, Meadows SK, Basu S, Mselle TF, Wira CR, Sentman CL. TLRs mediate IFN-gamma production by human uterine NK cells in endometrium. J Immunol 2006;176:6219-24.
19. Kabelitz D, Wesch D, He W. Perspectives of gammadelta T cells in tumor immunology. Cancer Res 2007;67:5-8. (Pubitemid 46142752)
20. Philpott KL, Viney JL, Kay G, Rastan S, Gardiner EM, Chae S, et al. Lymphoid development in mice congenitally lacking T cell receptor alpha beta-expressing cells. Science 1992;256:1448-52.
21. Banchereau J, Palucka AK. Dendritic cells as therapeutic vaccines against cancer. Nat Rev Immunol 2005;5:296-306. (Pubitemid 40516155)
22. Janikashvili N, Larmonier N, Katsanis E. Personalized dendritic cell-based tumor immunotherapy. Immunotherapy 2010;2:57-68.
23. Carnevale-Schianca F, Cignetti A, Capaldi A, Vitaggio K, Vallario A, Ricchiardi A, et al. Allogeneic nonmyeloablative hematopoietic cell transplantation in metastatic colon cancer: tumor-specific T cells directed to a tumor-associated antigen are generated in vivo during GVHD. Blood 2006;107:3795-803.
24. Grakoui A, Bromley SK, Sumen C, Davis MM, Shaw AS, Allen PM, et al. The immunological synapse: a molecular machine controlling T cell activation. Science 1999;285:221-7. (Pubitemid 29329988)
25. Shiao SL, McNiff JM, Pober JS. Memory T cells and their costimulators in human allograft injury. J Immunol 2005;175:4886-96. (Pubitemid 41456370)
26. Weiner GJ, Kostelny SA, Hillstrom JR, Cole MS, Link BK, Wang SL, et al. The role of T cell activation in anti-CD3 x antitumor bispecific antibody therapy. J Immunol 1994;152:2385-92.
27. Tibben JG, Boerman OC, Claessens RA, Corstens FH, van Deuren M, de Mulder PH, et al. Cytokine release in an ovarian carcinoma patient following intravenous administration of bispecific antibody OC/TR F (ab′)2. J Natl Cancer Inst 1993;85:1003-4.
28. Davis ID, Desai J. Clinical use of therapies targeting tumor vasculature and stroma. Curr Cancer Drug Targets 2008;8:498-508.
29. Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer 2009;9:239-52.
30. Roy S, Barnes PF, Garg A, WuS, Cosman D, Vankayalapati R. NK cells lyse T regulatory cells that expand in response to an intracellular pathogen. J Immunol 2008;180:1729-36.
31. Beetz S, Wesch D, Marischen L, Welte S, Oberg HH, Kabelitz D. Innate immune functions of human gammadelta T cells. Immunobiology 2008;213:173-82. (Pubitemid 351484782)
32. Todaro M, D'Asaro M, Caccamo N, Iovino F, Francipane MG, Meraviglia S, et al. Efficient killing of human colon cancer stem cells by gammadelta T lymphocytes. J Immunol 2009;182:7287-96.
33. Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, et al. Activation of NK cells and T cells by NKG2D, a receptor for stressinducible MICA. Science 1999;285:727-9.
34. Fujii S, Shimizu K, Kronenberg M, Steinman RM. Prolonged IFNgamma-producing NKT response induced with alpha-galactosylceramide-loaded DCs. Nat Immunol 2002;3:867-74.
35. Stirnemann K, Romero JF, Baldi L, Robert B, Cesson V, Besra GS, et al. Sustained activation and tumor targeting of NKT cells using a CD1d-anti-HER2-scFv fusion protein induce antitumor effects in mice. J Clin Invest 2008;118:994-1005. (Pubitemid 351364607)
36. Galili U, Clark MR, Shohet SB, Buehler J, Macher BA. Evolutionary relationship between the natural anti-Gal antibody and the Gal alpha 1-3Gal epitope in primates. Proc Natl Acad Sci U S A 1987;84:1369-73. (Pubitemid 17027355)
37. Terabe M, Berzofsky JA. The role of NKT cells in tumor immunity. Adv Cancer Res 2008;101:277-348.
38. Cullen R, Germanov E, Shimaoka T, Johnston B. Enhanced tumor metastasis in response to blockade of the chemokine receptor CXCR6 is overcome by NKT cell activation. J Immunol 2009;183:5807-15.
39. Lee CH, Chiang YH, Chang SE, Chong CL, Cheng BM, Roffler SR. Tumor-localized ligation of CD3 and CD28 with systemic regulatory Tcell depletion induces potent innate and adaptive antitumor responses. Clin Cancer Res 2009;15:2756-66.
40. Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M, Regnani G, et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 2003;348:203-13. (Pubitemid 36077915)
41. Sato E, Olson SH, Ahn J, Bundy B, Nishikawa H, Qian F, et al. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci U S A 2005;102:18538-43. (Pubitemid 43011261)
42. Badoual C, Hans S, Rodriguez J, Peyrard S, Klein C, Agueznay Nel H, et al. Prognostic value of tumor-infiltrating CD4+ T-cell subpopulations in head and neck cancers. Clin Cancer Res 2006;12:465-72. (Pubitemid 43166137)
43. Quezada SA, Simpson TR, Peggs KS, Merghoub T, Vider J, Fan X, et al. Tumor-reactive CD4(+) T cells develop cytotoxic activity and eradicate large established melanoma after transfer into lymphopenic hosts. J Exp Med 2010;207:637-50.
44. Xie Y, Akpinarli A, Maris C, Hipkiss EL, Lane M, Kwon EK, et al. Naive tumor-specific CD4(+) T cells differentiated in vivo eradicate established melanoma. J Exp Med 2010;207:651-67.
45. Gasser S, Orsulic S, Brown EJ, Raulet DH. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 2005;436:1186-90. (Pubitemid 41232299)
46. Diermayr S, Himmelreich H, Durovic B, Mathys-Schneeberger A, Siegler U, Langenkamp U, et al. NKG2D ligand expression in AML increases in response to HDAC inhibitor valproic acid and contributes to allorecognition by NK-cell lines with single KIR-HLA class I specificities. Blood 2008;111:1428-36. (Pubitemid 351213430)