The Role of Adaptive Immunity in the Efficacy of Targeted Cancer Therapies

Trends in Immunology

Volumn 37, Issue 2, 2016, Pages 141-153

  Xu, Meng Michelle ^a   Pu, Yang ^a   Zhang, Yuan ^a   Fu, Yang Xin ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; CELL MATURATION; CLINICAL STUDY; CLINICAL TRIAL; CYTOTOXIC T LYMPHOCYTE; DENDRITE; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOSUPPRESSIVE TREATMENT; MOLECULARLY TARGETED THERAPY; NATURAL KILLER CELL; ONCOLOGY; PREVENTION; TUMOR CELL; TUMOR MICROENVIRONMENT; TUMOR RESISTANCE; ANIMAL; CLINICAL TRIAL (TOPIC); IMMUNOLOGY; IMMUNOTHERAPY; MULTIMODALITY CANCER THERAPY; NEOPLASMS; PROCEDURES; TRANSPLANTATION;

ADAPTIVE IMMUNITY; ANIMALS; CLINICAL TRIALS AS TOPIC; COMBINED MODALITY THERAPY; HUMANS; IMMUNOTHERAPY; MOLECULAR TARGETED THERAPY; NEOPLASMS; T-LYMPHOCYTES, CYTOTOXIC; TUMOR MICROENVIRONMENT;

EID: 84983196456     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2015.12.007     Document Type: Review

References (79)

1. 1 Alexandrov, L.B., et al. Signatures of mutational processes in human cancer. Nature 500 (2013), 415–421.
2. 2 Lawrence, M.S., et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 499 (2013), 214–218.
3. 3 Hyman, D.M., et al. Vemurafenib in multiple nonmelanoma cancers with BRAF V600 mutations. N. Engl. J. Med. 373 (2015), 726–736.
4. 4 Druker, B.J., et al. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N. Engl. J. Med. 355 (2006), 2408–2417.
5. 5 Blanke, C.D., et al. Long-term results from a randomized phase II trial of standard- versus higher-dose imatinib mesylate for patients with unresectable or metastatic gastrointestinal stromal tumors expressing KIT. J. Clin. Oncol. 26 (2008), 620–625.
6. 6 Misale, S., et al. Emergence of KRAS mutations and acquired resistance to anti-EGFR therapy in colorectal cancer. Nature 486 (2012), 532–536.
7. 7 Balak, M.N., et al. Novel D761Y and common secondary T790M mutations in epidermal growth factor receptor-mutant lung adenocarcinomas with acquired resistance to kinase inhibitors. Clin. Cancer Res. 12 (2006), 6494–6501.
8. 8 Diaz, L.A. Jr, et al. The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature 486 (2012), 537–540.
9. 9 Loibl, S., et al. PIK3CA mutations are associated with lower rates of pathologic complete response to anti-human epidermal growth factor receptor 2 (her2) therapy in primary HER2-overexpressing breast cancer. J. Clin. Oncol. 32 (2014), 3212–3220.
10. 10 Misale, S., et al. Blockade of EGFR and MEK intercepts heterogeneous mechanisms of acquired resistance to anti–EGFR therapies in colorectal cancer. Sci. Transl. Med., 6, 2014, 224ra226.
11. 11 Heinrich, M.C., et al. Molecular correlates of imatinib resistance in gastrointestinal stromal tumors. J. Clin. Oncol. 24 (2006), 4764–4774.
12. 12 Boussen, H., et al. Phase II study to evaluate the efficacy and safety of neoadjuvant lapatinib plus paclitaxel in patients with inflammatory breast cancer. J. Clin. Oncol. 28 (2010), 3248–3255.
13. 13 Robert, C., et al. Improved overall survival in melanoma with combined dabrafenib and trametinib. N. Engl. J. Med. 372 (2015), 30–39.
14. 14 Corcoran, R.B., et al. Combined BRAF and MEK inhibition with dabrafenib and trametinib in BRAF V600-mutant colorectal cancer. J. Clin. Oncol. 33 (2015), 4023–4031.
15. 15 Park, S., et al. The therapeutic effect of anti-HER2/neu antibody depends on both innate and adaptive immunity. Cancer Cell 18 (2010), 160–170.
16. 16 Stagg, J., et al. Anti-ErbB-2 mAb therapy requires type I and II interferons and synergizes with anti-PD-1 or anti-CD137 mAb therapy. Proc. Natl. Acad. Sci. U.S.A. 108 (2011), 7142–7147.
17. 17 Yang, X., et al. Cetuximab-mediated tumor regression depends on innate and adaptive immune responses. Mol. Ther. 21 (2013), 91–100.
18. 18 Knight, D.A., et al. Corrigendum: Host immunity contributes to the anti-melanoma activity of BRAF inhibitors. J. Clin. Invest., 2015, 10.1172/JCI84828 Published online November 23, 2015.
19. 19 Balachandran, V.P., et al. Imatinib potentiates antitumor T cell responses in gastrointestinal stromal tumor through the inhibition of Ido. Nat. Med. 17 (2011), 1094–1100.
20. 20 Sagiv-Barfi, I., et al. Ibrutinib enhances the antitumor immune response induced by intratumoral injection of a TLR9 ligand in mouse lymphoma. Blood 125 (2015), 2079–2086.
21. 21 Frederick, D.T., et al. BRAF inhibition is associated with enhanced melanoma antigen expression and a more favorable tumor microenvironment in patients with metastatic melanoma. Clin. Cancer Res. 19 (2013), 1225–1231.
22. 22 Albiges, L., et al. Efficacy of targeted therapies after PD-1/PD-L1 blockade in metastatic renal cell carcinoma. Eur. J. Cancer 51 (2015), 2580–2586.
23. 23 Hu-Lieskovan, S., et al. Improved antitumor activity of immunotherapy with BRAF and MEK inhibitors in BRAF(V600E) melanoma. Sci. Transl. Med., 7, 2015, 279ra241.
24. 24 Baselga, J., Albanell, J., Mechanism of action of anti-HER2 monoclonal antibodies. Ann. Oncol. 12:Suppl. 1 (2001), S35–S41.
25. 25 Baselga, J., The EGFR as a target for anticancer therapy: focus on cetuximab. Eur. J. Cancer 37:Suppl. 4 (2001), S16–S22.
26. 26 Arnould, L., et al. Trastuzumab-based treatment of HER2-positive breast cancer: an antibody-dependent cellular cytotoxicity mechanism?. Br. J. Cancer 94 (2006), 259–267.
27. 27 Benavides, L.C., et al. The impact of HER2/neu expression level on response to the E75 vaccine: from U.S. Military Cancer Institute Clinical Trials Group Study I-01 and I-02. Clin. Cancer Res. 15 (2009), 2895–2904.
28. 28 Rafiq, K., et al. Immune complex-mediated antigen presentation induces tumor immunity. J. Clin. Invest. 110 (2002), 71–79.
29. 29 Kurts, C., et al. Cross-priming in health and disease. Nat. Rev. Immunol. 10 (2010), 403–414.
30. 30 Correale, P., et al. Cetuximab +/− chemotherapy enhances dendritic cell-mediated phagocytosis of colon cancer cells and ignites a highly efficient colon cancer antigen-specific cytotoxic T-cell response in vitro. Int. J. Cancer 130 (2012), 1577–1589.
31. 31 Moretta, L., et al. Effector and regulatory events during natural killer-dendritic cell interactions. Immunol. Rev. 214 (2006), 219–228.
32. 32 Liu, C., et al. Plasmacytoid dendritic cells induce NK cell-dependent, tumor antigen-specific T cell cross-priming and tumor regression in mice. J. Clin. Invest. 118 (2008), 1165–1175.
33. 33 Srivastava, R.M., 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. 19 (2013), 1858–1872.
34. 34 Alfaro, C., et al. Influence of bevacizumab, sunitinib and sorafenib as single agents or in combination on the inhibitory effects of VEGF on human dendritic cell differentiation from monocytes. Br. J. Cancer 100 (2009), 1111–1119.
35. + T cells in tumors. J. Exp. Med. 212 (2015), 139–148.
36. 36 Osada, T., et al. The effect of anti-VEGF therapy on immature myeloid cell and dendritic cells in cancer patients. Cancer Immunol. Immunother. 57 (2008), 1115–1124.
37. 37 Roland, C.L., et al. Cytokine levels correlate with immune cell infiltration after anti-VEGF therapy in preclinical mouse models of breast cancer. PLoS ONE, 4, 2009, e7669.
38. 38 Huang, Y., et al. Vascular normalizing doses of antiangiogenic treatment reprogram the immunosuppressive tumor microenvironment and enhance immunotherapy. Proc. Natl. Acad. Sci. U.S.A. 109 (2012), 17561–17566.
39. 39 Wu, P., et al. Small-molecule kinase inhibitors: an analysis of FDA-approved drugs. Drug Discov. Today, 2015, 10.1016/j.drudis.2015.07.008 Published online July 23, 2015.
40. 40 Koretzky, G.A., The legacy of the Philadelphia chromosome. J. Clin. Invest. 117 (2007), 2030–2032.
41. 41 Carroll, M., et al. CGP 57148, a tyrosine kinase inhibitor, inhibits the growth of cells expressing BCR-ABL, TEL-ABL, and TEL-PDGFR fusion proteins. Blood 90 (1997), 4947–4952.
42. 42 Dewar, A.L., et al. Macrophage colony-stimulating factor receptor c-fms is a novel target of imatinib. Blood 105 (2005), 3127–3132.
43. 43 Melnick, J.S., et al. An efficient rapid system for profiling the cellular activities of molecular libraries. Proc. Natl. Acad. Sci. U.S.A. 103 (2006), 3153–3158.
44. 44 Marin, D., et al. The next questions in chronic myeloid leukaemia and their answers. Curr. Opin. Hematol. 20 (2013), 163–168.
45. 45 Byrd, J.C., et al. Targeting BTK with ibrutinib in relapsed chronic lymphocytic leukemia. N. Engl. J. Med. 369 (2013), 32–42.
46. 46 Wang, M.L., et al. Targeting BTK with ibrutinib in relapsed or refractory mantle-cell lymphoma. N. Engl. J. Med. 369 (2013), 507–516.
47. 47 Dubovsky, J.A., et al. Ibrutinib is an irreversible molecular inhibitor of ITK driving a Th1-selective pressure in T lymphocytes. Blood 122 (2013), 2539–2549.
48. 48 Sagiv-Barfi, I., et al. Therapeutic antitumor immunity by checkpoint blockade is enhanced by ibrutinib, an inhibitor of both BTK and ITK. Proc. Natl. Acad. Sci. U.S.A. 112 (2015), E966–E972.
49. 49 Hannesdottir, L., et al. Lapatinib and doxorubicin enhance the Stat1-dependent antitumor immune response. Eur. J. Immunol. 43 (2013), 2718–2729.
50. 50 Pao, W., Miller, V.A., Epidermal growth factor receptor mutations, small-molecule kinase inhibitors, and non-small-cell lung cancer: current knowledge and future directions. J. Clin. Oncol. 23 (2005), 2556–2568.
51. 51 Lynch, T.J., et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N. Engl. J. Med. 350 (2004), 2129–2139.
52. 52 Paez, J.G., et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 304 (2004), 1497–1500.
53. 53 He, S., et al. Enhanced interaction between natural killer cells and lung cancer cells: involvement in gefitinib-mediated immunoregulation. J. Transl. Med., 11, 2013, 186.
54. 54 Kim, H., et al. EGFR inhibitors enhanced the susceptibility to NK cell-mediated lysis of lung cancer cells. J. Immunother. 34 (2011), 372–381.
55. 55 Seliger, B., et al. Antitumour and immune-adjuvant activities of protein-tyrosine kinase inhibitors. Trends Mol. Med. 16 (2010), 184–192.
56. 56 Porta, C., et al. Immunological effects of multikinase inhibitors for kidney cancer: a clue for integration with cellular therapies?. J. Cancer 2 (2011), 333–338.
57. 57 Xin, H., et al. Sunitinib inhibition of Stat3 induces renal cell carcinoma tumor cell apoptosis and reduces immunosuppressive cells. Cancer Res. 69 (2009), 2506–2513.
58. 58 Finke, J.H., et al. Sunitinib reverses type-1 immune suppression and decreases T-regulatory cells in renal cell carcinoma patients. Clin. Cancer Res. 14 (2008), 6674–6682.
59. 59 Zhao, W., et al. Sorafenib inhibits activation of human peripheral blood T cells by targeting LCK phosphorylation. Leukemia 22 (2008), 1226–1233.
60. 60 Zakharia, Y., et al. Axitinib: from preclinical development to future clinical perspectives in renal cell carcinoma. Expert Opin. Drug Discov. 10 (2015), 925–935.
61. 61 Stehle, F., et al. Reduced immunosuppressive properties of axitinib in comparison with other tyrosine kinase inhibitors. J. Biol. Chem. 288 (2013), 16334–16347.
62. 62 Davies, H., et al. Mutations of the BRAF gene in human cancer. Nature 417 (2002), 949–954.
63. 63 Rahman, M.A., et al. Multiple proliferation-survival signalling pathways are simultaneously active in BRAF V600E mutated thyroid carcinomas. Exp. Mol. Pathol. 99 (2015), 492–497.
64. 64 Wilmott, J.S., et al. Selective BRAF inhibitors induce marked T-cell infiltration into human metastatic melanoma. Clin. Cancer Res. 18 (2012), 1386–1394.
65. 65 Khalili, J.S., et al. Oncogenic BRAF(V600E) promotes stromal cell-mediated immunosuppression via induction of interleukin-1 in melanoma. Clin. Cancer Res. 18 (2012), 5329–5340.
66. 66 Steinberg, S.M., et al. BRAF inhibition alleviates immune suppression in murine autochthonous melanoma. Cancer Immunol. Res. 2 (2014), 1044–1050.
67. 67 Ferrari de Andrade, L., et al. Natural killer cells are essential for the ability of BRAF inhibitors to control BRAFV600E-mutant metastatic melanoma. Cancer Res. 74 (2014), 7298–7308.
68. 68 Jiang, X., et al. The activation of MAPK in melanoma cells resistant to BRAF inhibition promotes PD-L1 expression that is reversible by MEK and PI3K inhibition. Clin. Cancer Res. 19 (2013), 598–609.
69. 69 Yang, J.C., et al. Ipilimumab (anti-CTLA4 antibody) causes regression of metastatic renal cell cancer associated with enteritis and hypophysitis. J. Immunother. 30 (2007), 825–830.
70. 70 Hamid, O., et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N. Engl. J. Med. 369 (2013), 134–144.
71. 71 Robert, C., et al. Nivolumab in previously untreated melanoma without BRAF mutation. N. Engl. J. Med. 372 (2015), 320–330.
72. 72 Postow, M.A., et al. Nivolumab and ipilimumab versus ipilimumab in untreated melanoma. N. Engl. J. Med. 372 (2015), 2006–2017.
73. 73 Porter, D.L., et al. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N. Engl. J. Med. 365 (2011), 725–733.
74. 74 Kim, P.S., et al. Antibody association with HER-2/neu-targeted vaccine enhances CD8 T cell responses in mice through Fc-mediated activation of DCs. J. Clin. Invest. 118 (2008), 1700–1711.
75. 75 Kohrt, H.E., et al. Stimulation of natural killer cells with a CD137-specific antibody enhances trastuzumab efficacy in xenotransplant models of breast cancer. J. Clin. Invest. 122 (2012), 1066–1075.
76. 76 Yang, X., et al. Targeting the tumor microenvironment with interferon-beta bridges innate and adaptive immune responses. Cancer Cell 25 (2014), 37–48.
77. 77 Zhu, E.F., et al. Synergistic innate and adaptive immune response to combination immunotherapy with anti-tumor antigen antibodies and extended serum half-life IL-2. Cancer Cell 27 (2015), 489–501.
78. 78 Penichet, M.L., et al. A recombinant IgG3-(IL-2) fusion protein for the treatment of human HER2/neu expressing tumors. Hum. Antibodies 10 (2001), 43–49.
79. 79 Payne, M.J., et al. Phase II pilot study of intravenous high-dose interferon with or without maintenance treatment in melanoma at high risk of recurrence. J. Clin. Oncol. 32 (2014), 185–190.