Targeting CD137 enhances the efficacy of cetuximab

Journal of Clinical Investigation

Volumn 124, Issue 6, 2014, Pages 2668-2682

  Kohrt, Holbrook E ^a   Colevas, A Dimitrios ^a   Houot, Roch ^a,b,c   Weiskopf, Kipp ^a   Goldstein, Matthew J ^a   Lund, Peder ^a   Mueller, Antonia ^a   Sagiv Barfi, Idit ^a   Marabelle, Aurelien ^a,d   Lira, Ruth ^a   Troutner, Emily ^a   Richards, Lori ^a   Rajapaska, Amanda ^a   Hebb, Jonathan ^a   Chester, Cariad ^a   Waller, Erin ^a   Ostashko, Anton ^a   Weng, Wen Kai ^a   Chen, Lieping ^e   Czerwinski, Debra ^a   Fu, Yang Xin ^f   Sunwoo, John ^a   Levy, Ronald ^a   more..

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b RENNES UNIVERSITY HOSPITAL   (France)

^c INSERM   (France)

^d UNIVERSITÉ DE LYON   (France)

^e YALE CANCER CENTER   (United States)

^f UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD137 LIGAND; CD16 ANTIGEN; CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR; K RAS PROTEIN; URELUMAB;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL LINE; CANCER COMBINATION CHEMOTHERAPY; CANCER REGRESSION; CANCER SURVIVAL; CD8+ T LYMPHOCYTE; CIRCULATING TUMOR CELL; CONTROLLED STUDY; DEGRANULATION; DOSE TIME EFFECT RELATION; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG POTENTIATION; DRUG RECEPTOR BINDING; DRUG TARGETING; FEMALE; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; MONOTHERAPY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN POLYMORPHISM; REPEATED DRUG DOSE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR XENOGRAFT;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTIGENS, CD137; ANTINEOPLASTIC AGENTS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; FEMALE; HEAD AND NECK NEOPLASMS; HUMANS; IMMUNOTHERAPY, ADOPTIVE; KILLER CELLS, NATURAL; MICE; MICE, INBRED BALB C; MICE, NUDE; MUTATION; PROTO-ONCOGENE PROTEINS; RAS PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 84902137525     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI73014     Document Type: Article

References (62)

1. American Cancer Society. Cancer Facts and Figures 2013. Atlanta, Georgia, USA: American Cancer Society; 2013.
2. Lee CM, Tannock IF. The distribution of the therapeutic monoclonal antibodies cetuximab and trastuzumab within solid tumors. BMC Cancer. 2010;10:255.
3. De Roock W, De Vriendt V, Normanno N, Ciardiello F, Tejpar S. KRAS, BRAF, PIK3CA, and PTEN mutations: implications for targeted therapies in metastatic colorectal cancer. Lancet Oncol. 2011;12(6):594-603.
4. Baselga J, et al. Phase II multicenter study of the antiepidermal growth factor receptor monoclonal antibody cetuximab in combination with platinum-based chemotherapy in patients with platinum-refractory metastatic and/or recurrent squamous cell carcinoma of the head and neck. J Clin Oncol. 2005;23(24):5568- 5577.
5. Vermorken JB, et al. Open-label, uncontrolled, multicenter phase II study to evaluate the efficacy and toxicity of cetuximab as a single agent in patients with recurrent and/or metastatic squamous cell carcinoma of the head and neck who failed to respond to platinum-based therapy. J Clin Oncol. 2007;25(16):2171-2177.
6. Liu L, Cao Y, Tan A, Liao C, Gao F. Cetuximabbased therapy versus non-cetuximab therapy for advanced cancer: a meta-analysis of 17 randomized controlled trials. Cancer Chemother Pharmacol. 2010;65(5):849-861.
7. Li X, Lu Y, Liang K, Pan T, Mendelsohn J, Fan Z. Requirement of hypoxia-inducible factor-1alpha down-regulation in mediating the antitumor activity of the anti-epidermal growth factor receptor monoclonal antibody cetuximab. Mol Cancer Ther. 2008;7(5):1207-1217.
8. Huang SM, Li J, Harari PM. Molecular inhibition of angiogenesis and metastatic potential in human squamous cell carcinomas after epidermal growth factor receptor blockade. Mol Cancer Ther. 2002;1(7):507-514.
9. Clynes RA, Towers TL, Presta LG, Ravetch JV. Inhibitory Fc receptors modulate in vivo cytoxicity against tumor targets. Nat Med. 2000;6(4):443-446.
10. Kurai J, et al. Antibody-dependent cellular cytotoxicity mediated by cetuximab against lung cancer cell lines. Clin Cancer Res. 2007;13(5):1552-1561.
11. Steiner P, et al. Tumor growth inhibition with cetuximab and chemotherapy in non-small cell lung cancer xenografts expressing wild-type and mutated epidermal growth factor receptor. Clin Cancer Res. 2007;13(5):1540-1551.
12. Raben D, et al. The effects of cetuximab alone and in combination with radiation and/or chemotherapy in lung cancer. Clin Cancer Res. 2005;11(2 pt 1):795-805.
13. Wilson NS, et al. An Fcγ receptor-dependent mechanism drives antibody-mediated targetreceptor signaling in cancer cells. Cancer Cell. 2011;19(1):101-113.
14. Marechal R, et al. Putative contribution of CD56 positive cells in cetuximab treatment efficacy in first-line metastatic colorectal cancer patients. BMC Cancer. 2010;10:340.
15. Lopez-Albaitero A, et al. Role of polymorphic Fc γ receptor IIIa and EGFR expression level in cetuximab mediated, NK cell dependent in vitro cytotoxicity of head and neck squamous cell carcinoma cells. Cancer Immunol Immunother. 2009;58(11):1853-1864.
16. Bibeau F, et al. Impact of Fc{gamma}RIIa-Fc{gamma}RIIIa polymorphisms and KRAS mutations on the clinical outcome of patients with metastatic colorectal cancer treated with cetuximab plus irinotecan. J Clin Oncol. 2009;27(7):1122-1129.
17. Ferris RL, Jaffee EM, Ferrone S. Tumor antigen-targeted, monoclonal antibody-based immunotherapy: clinical response, cellular immunity, and immunoescape. J Clin Oncol. 2010;28(28):4390-4399.
18. Qiu LX, et al. Predictive and prognostic value of KRAS mutations in metastatic colorectal cancer patients treated with cetuximab: a meta-analysis of 22 studies. Eur J Cancer. 2010;46(15):2781-2787.
19. Rodriguez J, et al. Fc γ receptor polymorphisms as predictive markers of Cetuximab efficacy in epidermal growth factor receptor downstream-mutated metastatic colorectal cancer. Eur J Cancer. 2012;48(12):1774-1780.
20. Lee SC, Srivastava RM, Lopez-Albaitero A, Ferrone S, Ferris RL. Natural killer (NK): dendritic cell (DC) cross talk induced by therapeutic monoclonal antibody triggers tumor antigen-specific T cell immunity. Immunol Res. 2011;50(2-3):248-254.
21. Lin W, et al. Fc-dependent expression of CD137 on human NK cells: insights into "agonistic" effects of anti-CD137 monoclonal antibodies. Blood. 2008;112(3):699-707.
22. Yang X, Zhang X, Mortenson ED, Radkevich-Brown O, Wang Y, Fu YX. Cetuximab-mediated tumor regression depends on innate and adaptive immune responses. Mol Ther. 2013;21(1):91-100.
23. Schuler PJ, et al. EGFR-specific T cell frequencies correlate with EGFR expression in head and neck squamous cell carcinoma. J Transl Med. 2011;9:168.
24. Srivastava RM, et al. Cetuximab-activated natural killer and dendritic cells collaborate to trigger tumor antigen-specific T-cell immunity in head and neck cancer patients. Clin Cancer Res. 2013;19(7):1858-1872.
25. Mendelsohn J, Baselga J. Status of epidermal growth factor receptor antagonists in the biology and treatment of cancer. J Clin Oncol. 2003;21(14):2787-2799.
26. Dassonville O, et al. Expression of epidermal growth factor receptor and survival in upper aerodigestive tract cancer. J Clin Oncol. 1993;11(10):1873- 1878.
27. Kohrt HE, et al. CD137 stimulation enhances the antilymphoma activity of anti-CD20 antibodies. Blood. 2011;117(8):2423-2432.
28. Kohrt HE, et al. Stimulation of natural killer cells with a CD137-specific antibody enhances trastuzumab efficacy in xenotransplant models of breast cancer. J Clin Invest. 2012;122(3):1066-1075.
29. Melero I, Hervas-Stubbs S, Glennie M, Pardoll DM, Chen L. Immunostimulatory monoclonal antibodies for cancer therapy. Nat Rev Cancer. 2007;7(2):95-106.
30. Wilcox RA, et al. Cutting edge: Expression of functional CD137 receptor by dendritic cells. J Immunol. 2002;168(9):4262-4267.
31. Narazaki H, Zhu Y, Luo L, Zhu G, Chen L. CD137 agonist antibody prevents cancer recurrence: contribution of CD137 on both hematopoietic and nonhematopoietic cells. Blood. 2010;115(10):1941-1948.
32. Baessler T, et al. CD137 ligand mediates opposite effects in human and mouse NK cells and impairs NK cell reactivity against human acute myeloid leukemia cells. Blood. 2010;115(15):3058-3069.
33. Melero I, Johnston JV, Shufford WW, Mittler RS, Chen L. NK1.1 cells express 4-1BB (CDw137) costimulatory molecule and are required for tumor immunity elicited by anti-4-1BB monoclonal antibodies. Cell Immunol. 1998;190(2):167-172.
34. + cytolytic T cells and responsiveness to IL-2 but not cytolytic activity. J Immunol. 2002;169(8):4230-4236.
35. Maniar A, et al. Human {gamma}{delta} T lymphocytes induce robust NK cell mediated antitumor cytotoxicity through CD137 engagement. Blood. 2010;116(10):1726-1733.
36. Gong W, et al. Immobilized MHC class I chainrelated protein A synergizes with IL-15 and soluble 4-1BB ligand to expand NK cells with high cytotoxicity ex vivo. Cell Mol Immunol. 2010;7(6):477-484.
37. Kohrt HE, et al. CD137 stimulation enhances the anti-lymphoma activity of anti-CD20 antibodies. Blood. 2010;117(8):2423-2432.
38. Cooper MA, Fehniger TA, Caligiuri MA. The biology of human natural killer-cell subsets. Trends Immunol. 2001;22(11):633-640.
39. Bowles JA, Weiner GJ. CD16 polymorphisms and NK activation induced by monoclonal antibody-coated target cells. J Immunol Methods. 2005;304(1-2):88-99.
40. Juelke K, et al. CD62L expression identifies a unique subset of polyfunctional CD56dim NK cells. Blood. 2010;116(8):1299-1307.
41. Mani A, et al. A phase II trial of trastuzumab in combination with low-dose interleukin-2 (IL-2) in patients (PTS) with metastatic breast cancer (MBC) who have previously failed trastuzumab. Breast Cancer Res Treat. 2009;117(1):83-89.
42. Acquavella N, et al. Toxicity and activity of a twice daily high-dose bolus interleukin 2 regimen in patients with metastatic melanoma and metastatic renal cell cancer. J Immunother. 2008;31(6):569-576.
43. Gluck WL, et al. Phase I studies of interleukin (IL)-2 and rituximab in B-cell non-hodgkin's lymphoma: IL-2 mediated natural killer cell expansion correlations with clinical response. Clin Cancer Res. 2004;10(7):2253-2264.
44. Ansell SM, et al. Phase 1 study of interleukin-12 in combination with rituximab in patients with B-cell non-Hodgkin lymphoma. Blood. 2002;99(1):67-74.
45. Houot R, et al. Therapeutic effect of CD137 immunomodulation in lymphoma and its enhancement by Treg depletion. Blood. 2009;114(16):3431-3438.
46. Kohrt HE, et al. CD137 stimulation enhances the anti-lymphoma activity of anti-CD20 antibodies. Blood. 2011;117(8):2423-2432.
47. Genovesi EV, Pettey CL, Collins JJ. Use of adoptive transfer and Winn assay procedures in the further analysis of antiviral acquired immunity in mice protected against Friend leukemia virus-induced disease by passive serum therapy. Cancer Res. 1984;44(4):1489-1498.
48. Jiang D, Schwarz H. Regulation of granulocyte and macrophage populations of murine bone marrow cells by G-CSF and CD137 protein. PLoS One. 2010;5(12):e15565.
49. Zhang X, et al. CD137 promotes proliferation and survival of human B cells. J Immunol. 2010;184(2):787-795.
50. Murillo O, et al. In vivo depletion of DC impairs the anti-tumor effect of agonistic anti-CD137 mAb. Eur J Immunol. 2009;39(9):2424-2436.
51. Sharma RK, et al. 4-1BB ligand as an effective multifunctional immunomodulator and antigen delivery vehicle for the development of therapeutic cancer vaccines. Cancer Res. 2010;70(10):3945-3954.
52. Piccioli D, Sbrana S, Melandri E, Valiante NM. Contact-dependent stimulation and inhibition of dendritic cells by natural killer cells. J Exp Med. 2002;195(3):335-341.
53. Wehner R, Dietze K, Bachmann M, Schmitz M. The bidirectional crosstalk between human dendritic cells and natural killer cells. J Innate Immun. 2011;3(3):258-263.
54. + DC subset. Presented at: 15th International Congress of Immunology; August 22-27, 2013; Milan, Italy. Abstract P1.08.18.
55. Gerosa F, Baldani-Guerra B, Nisii C, Marchesini V, Carra G, Trinchieri G. Reciprocal activating interaction between natural killer cells and dendritic cells. J Exp Med. 2002;195(3):327-333.
56. Mailliard RB, et al. Dendritic cells mediate NK cell help for Th1 and CTL responses: two-signal requirement for the induction of NK cell helper function. J Immunol. 2003;171(5):2366-2373.
57. Agaugue S, Marcenaro E, Ferranti B, Moretta L, Moretta A. Human natural killer cells exposed to IL-2, IL-12, IL-18, or IL-4 differently modulate priming of naive T cells by monocyte-derived dendritic cells. Blood. 2008;112(5):1776-1783.
58. Matsuo T, Nishizuka SS, Ishida K, Iwaya T, Ikeda M, Wakabayashi G. Analysis of the anti-tumor effect of cetuximab using protein kinetics and mouse xenograft models. BMC Res Notes. 2011;4:140.
59. Wilcox RA, et al. Provision of antigen and CD137 signaling breaks immunological ignorance, promoting regression of poorly immunogenic tumors. J Clin Invest. 2002;109(5):651-659.
60. Kim GG, Donnenberg VS, Donnenberg AD, Gooding W, Whiteside TL. A novel multiparametric flow cytometry-based cytotoxicity assay simultaneously immunophenotypes effector cells: comparisons to a 4 h 51Cr-release assay. J Immunol Methods. 2007;325(1-2):51-66.
61. Kotecha N, et al. Single-cell profiling identifies aberrant STAT5 activation in myeloid malignancies with specific clinical and biologic correlates. Cancer Cell. 2008;14(4):335-343.
62. Koene HR, Kleijer M, Algra J, Roos D, von dem Borne AE, de Haas M. FcγRIIIa-158V/F polymorphism influences the binding of IgG by natural killer cell FcγRIIIa, independently of the FcγRIIIa-48L/R/H phenotype. Blood. 1997;90(3):1109-1114.