Concomitant targeting of programmed death-1 (PD-1) and CD137 improves the efficacy of radiotherapy in a mouse model of human BRAFV600-mutant melanoma

Cancer Immunology, Immunotherapy

Volumn 65, Issue 6, 2016, Pages 753-763

  Kroon, Paula ^a   Gadiot, Jules ^a   Peeters, Marlies ^a   Gasparini, Alessia ^a   Deken, Marcel A ^a   Yagita, Hideo ^b   Verheij, Marcel ^a   Borst, Jannie ^a   Blank, Christian U ^a   Verbrugge, Inge ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

BRAFV600; CD137; Melanoma; PD 1; Radiotherapy; Stereotactic

Indexed keywords

B RAF KINASE; CD137 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CELL SURFACE RECEPTOR; CYTOKINE RECEPTOR AGONIST; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 LIGAND 1 ALPHA; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; BIOLOGICAL MARKER; CODON; MONOCLONAL ANTIBODY; PROGRAMMED DEATH 1 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER RADIOTHERAPY; CELL STIMULATION; CONE BEAM COMPUTED TOMOGRAPHY; CONTROLLED STUDY; DRUG EFFICACY; DRUG MEGADOSE; GENE MUTATION; GENETICALLY ENGINEERED MOUSE STRAIN; IMMUNOHISTOCHEMISTRY; MELANOMA; MOUSE; MOUSE MODEL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STEREOTACTIC BODY RADIATION THERAPY; T CELL DEPLETION; T LYMPHOCYTE; THERAPY EFFECT; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; TUMOR VOLUME; ANIMAL; ANTAGONISTS AND INHIBITORS; CODON; DISEASE MODEL; DRUG EFFECTS; GENETICS; HUMAN; IMMUNOLOGY; IMMUNOMODULATION; LYMPHOCYTE SUBPOPULATION; METABOLISM; MULTIMODALITY CANCER THERAPY; MUTATION; PATHOLOGY; RADIATION RESPONSE; TRANSGENIC MOUSE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD137; ANTINEOPLASTIC AGENTS; BIOMARKERS; CODON; COMBINED MODALITY THERAPY; DISEASE MODELS, ANIMAL; HUMANS; IMMUNOMODULATION; LYMPHOCYTE SUBSETS; LYMPHOCYTES, TUMOR-INFILTRATING; MELANOMA; MICE; MICE, TRANSGENIC; MUTATION; PROGRAMMED CELL DEATH 1 RECEPTOR; PROTO-ONCOGENE PROTEINS B-RAF;

EID: 84966588491     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-016-1843-4     Document Type: Article

References (39)

1. Alexandrov LB, Nik-Zainal S, Wedge DC et al (2013) Signatures of mutational processes in human cancer. Nature 500:415–421. doi:10.1038/nature12477
2. Rosenberg SA, Lotze MT, Muul LM et al (1985) Observations on the systemic administration of autologous lymphokine-activated killer cells and recombinant interleukin-2 to patients with metastatic cancer. N Engl J Med 313:1485–1492. doi:10.1056/NEJM198512053132327
3. Atkins MB, Lotze MT, Dutcher JP et al (1999) High-dose recombinant interleukin 2 therapy for patients with metastatic melanoma: analysis of 270 patients treated between 1985 and 1993. J Clin Oncol 17:2105–2116
4. Hodi FS, O’Day SJ, McDermott DF et al (2010) Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 363:711–723. doi:10.1056/NEJMoa1003466
5. Robert C, Schachter J, Long GV et al (2015) Pembrolizumab versus Ipilimumab in Advanced Melanoma. N Engl J Med 372:2521–2532. doi:10.1056/NEJMoa1503093
6. Robert C, Long GV, Brady B et al (2015) Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med 372:320–330. doi:10.1056/NEJMoa1412082
7. Postow MA, Chesney J, Pavlick AC et al (2015) Nivolumab and ipilimumab versus ipilimumab in untreated melanoma. N Engl J Med 372:2006–2017. doi:10.1056/NEJMoa1414428
8. Larkin J, Chiarion-Sileni V, Gonzalez R et al (2015) Combined Nivolumab and Ipilimumab or Monotherapy in Untreated Melanoma. N Engl J Med 373:23–34. doi:10.1056/NEJMoa1504030
9. Schadendorf D, Hodi FS, Robert C et al (2015) Pooled Analysis of Long-Term Survival Data From Phase II and Phase III Trials of Ipilimumab in Unresectable or Metastatic Melanoma. J Clin Oncol 33:1889–1894. doi:10.1200/JCO.2014.56.2736
10. Hodi FS, Sznol M, Kluger HM et al (2014) Long-term survival of ipilimumab-naïve patients with advanced melaona (MEL) treated with nivolumab (anti-PD-1; BMS-936558, ONO-4538) in a phase 1 trial. J Clin Oncol 32:2014 suppl; abstr 9002
11. Tumeh PC, Harview CL, Yearley JH et al (2014) PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 515:568–571. doi:10.1038/nature13954
12. Schaer DA, Hirschhorn-Cymerman D, Wolchok JD (2014) Targeting tumor-necrosis factor receptor pathways for tumor immunotherapy. J Immunother Cancer 2:7. doi:10.1186/2051-1426-2-7
13. Kocak E, Lute K, Chang X et al (2006) Combination therapy with anti-CTL antigen-4 and anti-4-1BB antibodies enhances cancer immunity and reduces autoimmunity. Cancer Res 66:7276–7284. doi:10.1158/0008-5472.CAN-05-2128
14. Verbrugge I, Hagekyriakou J, Sharp LL et al (2012) Radiotherapy increases the permissiveness of established mammary tumors to rejection by immunomodulatory antibodies. Cancer Res 72:3163–3174. doi:10.1158/0008-5472.CAN-12-0210
15. Formenti SC, Demaria S (2012) Radiation therapy to convert the tumor into an in situ vaccine. Int J Radiat Oncol Biol Phys 84:879–880. doi:10.1016/j.ijrobp.2012.06.020
16. Twyman-Saint Victor C, Rech AJ, Maity A et al (2015) Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature 520:373–377. doi:10.1038/nature14292
17. Reits EA, Hodge JW, Herberts CA et al (2006) Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy. J Exp Med 203:1259–1271. doi:10.1084/jem.20052494
18. Vereecque R, Buffenoir G, Gonzalez R, Cambier N, Hetuin D, Bauters F, Fenaux P, Quesnel B (2000) gamma-ray irradiation induces B7.1 expression in myeloid leukaemic cells. Br J Haematol 108:825–831
19. Reap EA, Roof K, Maynor K, Borrero M, Booker J, Cohen PL (1997) Radiation and stress-induced apoptosis: a role for Fas/Fas ligand interactions. Proc Natl Acad Sci USA 94:5750–5755
20. Chakraborty M, Abrams SI, Camphausen K, Liu K, Scott T, Coleman CN, Hodge JW (2003) Irradiation of tumor cells up-regulates Fas and enhances CTL lytic activity and CTL adoptive immunotherapy. J Immunol 170:6338–6347
21. Lugade AA, Moran JP, Gerber SA, Rose RC, Frelinger JG, Lord EM (2005) Local radiation therapy of B16 melanoma tumors increases the generation of tumor antigen-specific effector cells that traffic to the tumor. J Immunol 174:7516–7523
22. Verbrugge I, Gasparini A, Haynes NM et al (2014) The curative outcome of radioimmunotherapy in a mouse breast cancer model relies on mTOR signaling. Radiat Res 182:219–229. doi:10.1667/RR13511.1
23. Dewan MZ, Galloway AE, Kawashima N, Dewyngaert JK, Babb JS, Formenti SC, Demaria S (2009) Fractionated but not single-dose radiotherapy induces an immune-mediated abscopal effect when combined with anti-CTLA-4 antibody. Clin Cancer Res 15:5379–5388. doi:10.1158/1078-0432.CCR-09-0265
24. Huang J, Wang Y, Guo J, Lu H, Lin X, Ma L, Teitz-Tennenbaum S, Chang AE, Li Q (2007) Radiation-induced apoptosis along with local and systemic cytokine elaboration is associated with DC plus radiotherapy-mediated renal cell tumor regression. Clin Immunol 123:298–310. doi:10.1016/j.clim.2007.02.005
25. Hooijkaas AI, Gadiot J, van der Valk M, Mooi WJ, Blank CU (2012) Targeting BRAFV600E in an inducible murine model of melanoma. Am J Pathol 181:785–794. doi:10.1016/j.ajpath.2012.06.002
26. Hooijkaas A, Gadiot J, Morrow M, Stewart R, Schumacher T, Blank CU (2012) Selective BRAF inhibition decreases tumor-resident lymphocyte frequencies in a mouse model of human melanoma. Oncoimmunology 1:609–617. doi:10.4161/onci.20226
27. Seung SK, Curti BD, Crittenden M et al (2012) Phase 1 study of stereotactic body radiotherapy and interleukin-2–tumor and immunological responses. Sci Transl Med 4:137ra74. doi:10.1126/scitranslmed.3003649
28. Dankort D, Curley DP, Cartlidge RA et al (2009) Braf(V600E) cooperates with Pten loss to induce metastatic melanoma. Nat Genet 41:544–552. doi:10.1038/ng.356
29. Takeda K, Yamaguchi N, Akiba H et al (2004) Induction of tumor-specific T cell immunity by anti-DR5 antibody therapy. J Exp Med 199:437–448. doi:10.1084/jem.20031457
30. Yamazaki T, Akiba H, Koyanagi A, Azuma M, Yagita H, Okumura K (2005) Blockade of B7-H1 on macrophages suppresses CD4+ T cell proliferation by augmenting IFN-gamma-induced nitric oxide production. J Immunol 175:1586–1592
31. Derksen PW, Liu X, Saridin F et al (2006) Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 10:437–449. doi:10.1016/j.ccr.2006.09.013
32. Wolchok JD, Kluger H, Callahan MK et al (2013) Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 369:122–133. doi:10.1056/NEJMoa1302369
33. Blank CU (2014) The perspective of immunotherapy: new molecules and new mechanisms of action in immune modulation. Curr Opin Oncol 26:204–214. doi:10.1097/CCO.0000000000000054
34. Wei H, Zhao L, Li W et al (2013) Combinatorial PD-1 blockade and CD137 activation has therapeutic efficacy in murine cancer models and synergizes with cisplatin. PLoS One 8:e84927. doi:10.1371/journal.pone.0084927
35. Vinay DS, Kwon BS (2011) 4-1BB signaling beyond T cells. Cell Mol Immunol 8:281–284. doi:10.1038/cmi.2010.82
36. Palazon A, Teijeira A, Martinez-Forero I et al (2011) Agonist anti-CD137 mAb act on tumor endothelial cells to enhance recruitment of activated T lymphocytes. Cancer Res 71:801–811. doi:10.1158/0008-5472.CAN-10-1733
37. Futagawa T, Akiba H, Kodama T, Takeda K, Hosoda Y, Yagita H, Okumura K (2002) Expression and function of 4-1BB and 4-1BB ligand on murine dendritic cells. Int Immunol 14:275–286
38. Deng L, Liang H, Burnette B, Beckett M, Darga T, Weichselbaum RR, Fu YX (2014) Irradiation and anti-PD-L1 treatment synergistically promote antitumor immunity in mice. J Clin Invest 124:687–695. doi:10.1172/JCI67313
39. Rizvi NA, Hellmann MD, Snyder A et al (2015) Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 348:124–128. doi:10.1126/science.aaa1348