The optimal partnership of radiation and immunotherapy: From preclinical studies to clinical translation

Radiation Research

Volumn 182, Issue 2, 2014, Pages 170-181

  Demaria, Sandra ^a   Pilones, Karsten A ^a   Vanpouille Box, Claire ^a   Golden, Encouse B ^a   Formenti, Silvia C ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; COMBINED MODALITY THERAPY; HUMANS; IMMUNOTHERAPY; NEOPLASMS; RADIOTHERAPY; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84905730032     PISSN: 00337587     EISSN: 19385404     Source Type: Journal    
DOI: 10.1667/RR13500.1     Document Type: Article

References (80)

1. Kopp E, Medzhitov R. Recognition of microbial infection by Tolllike receptors. Curr Opin Immunol 2003; 15:396-401. (Pubitemid 36930075)
2. Demaria S, Pikarsky E, Karin M, Coussens LM, Chen YC, El-Omar EM, et al. Cancer and inflammation: promise for biologic therapy. J Immunother 2010; 33:335-51.
3. Segal NH, Parsons DW, Peggs KS, Velculescu V, Kinzler KW, Vogelstein B, et al. Epitope landscape in breast and colorectal cancer. Cancer Res 2008; 68:889-92. (Pubitemid 351206767)
4. Diefenbach A, Jamieson AM, Liu SD, Shastri N, Raulet DH. Ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nat Immunol 2000; 1:119-26.
5. Hayakawa Y, Kelly JM, Westwood JA, Darcy PK, Diefenbach A, Raulet D, et al. Cutting edge: tumor rejection mediated by NKG2D receptor-ligand interaction is dependent upon perforin. J Immunol 2002; 169:5377-81. (Pubitemid 35291630)
6. Lotze MT, Zeh HJ, Rubartelli A, Sparvero LJ, Amoscato AA, Washburn NR, et al. The grateful dead: damage-associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol Rev 2007; 220:60-81. (Pubitemid 350045579)
7. Dunn GP, Old LJ, Schreiber RD. The three Es of cancer immunoediting. Annu Rev Immunol 2004; 22:329-60. (Pubitemid 38680426)
8. Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ. Natural innate and adaptive immunity to cancer. Annu Rev Immunol 2011; 29:235-71.
9. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144:646-74.
10. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006; 313:1960-4. (Pubitemid 44498003)
11. Pagès F, Galon F, Dieu-Nosjean MC, Tartour E, Sautès- Fridman C, Fridman WH. Immune infiltration in human tumors: a prognostic factor that should not be ignored. Oncogene 2010; 29:1093-102.
12. 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)
13. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012; 12:252-64.
14. Ribas A, Butterfield LH, Glaspy JA, Economou JS. Current developments in cancer vaccines and cellular immunotherapy. J Clin Oncol 2003; 21:2415-32. (Pubitemid 46621880)
15. Ribas A. Tumor immunotherapy directed at PD-1. N Engl J Med 2012; 366:2517-9.
16. Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 2013; 369:134-44.
17. Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, et al. Nivolumab plus Ipilimumab in Advanced Melanoma. N Engl J Med 2013; 369:122-33.
18. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366:2443-54.
19. Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012; 366:2455-65.
20. Gajewski TF, Meng Y, Blank C, Brown I, Kacha A, Kline J, et al. Immune resistance orchestrated by the tumor microenvironment. Immunol Rev 2006; 213:131-45. (Pubitemid 44401498)
21. Smyth MJ, Godfrey DI, Trapani JA. A fresh look at tumor immunosurveillance and immunotherapy. Nat Immunol 2001; 2:293-9. (Pubitemid 33706339)
22. McBride WH, Chiang C-S, Olson JL, Wang CC, Hong J-H, Pajonk F, et al. A sense of danger from radiation. Radiat Res 2004; 162:1-19. (Pubitemid 39044714)
23. Demaria S, Bhardwaj N, McBride WH, Formenti SC. Combining radiotherapy and immunotherapy: a revived partnership. Int J Radiat Oncol Biol Phys 2005; 63:655-66. (Pubitemid 41400049)
24. Formenti SC, Demaria S, Combining radiotherapy and cancer immunotherapy: a paradigm shift. J Natl Cancer Inst 2013; 105:256-65.
25. Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A, et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007; 13:1050-9. (Pubitemid 47517504)
26. Golden EB, Pellicciotta I, Demaria S, Barcellos-Hoff MH, Formenti SC. The convergence of radiation and immunogenic cell death signaling pathways. Fornt Oncol 2012; 2:88.
27. Matsumura S, Wang B, Kawashima N, Braunstein S, Badura M, Cameron TO, et al. Radiation-induced CXCL16 release by breast cancer cells attracts effector T cells. J Immunol 2008; 181:3099-107.
28. Lugade AA, Sorensen EW, Gerbe SA, Moran JP, Frelinger JG, Lord EM. Radiation-induced IFN-gamma production within the tumor microenvironment influences antitumor immunity. J Immunol 2008; 180:3132-9.
29. Reits EA, Hodge JW, Herberts CA, Groothuis TA, Chakraborty M, Wansley EK, et al. Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy. J Exp Med 2006; 203:1259-71. (Pubitemid 43736595)
30. Ruocco MG, Pilones KA, Kawashima N, Cammer M, Huang J, Babb JS, et al. Suppressing T cell motility induced by anti-CTLA-4 monotherapy improves anti-tumor effects. J Clin Invest 2012; 122:3718-30.
31. Chakraborty M, Abrams SI, Coleman CN, Camphausen K, Schlom J, Hodge JW. External beam radiation of tumors alters phenotype of tumor cells to render them susceptible to vaccine-mediated Tcell killing. Cancer Res 2004; 64:4328-37. (Pubitemid 38802440)
32. Stone HB, Peters LJ, Milas L. Effect of host immune capability on radiocurability and subsequent transplantability of a murine fibrosarcoma. J Natl Cancer Inst 1979; 63:1229-35. (Pubitemid 10159225)
33. Lee Y, Auh SL, Wang Y, Burnette B, Wang Y, Meng Y, et al. Therapeutic effects of ablative radiation on local tumor require CD8\+ T cells: changing strategies for cancer treatment. Blood 2009; 114:589-95.
34. Demaria S, Formenti SC. Role of T lymphocytes in tumor response to radiotherapy. Front Oncol 2012; 2:95.
35. Mole RJ. Whole body irradiation-radiology or medicine? Br J Radiol 1953; 26:234-41.
36. Demaria S, Ng B, Devitt M-L, Babb JS, Kawashima N, Liebes L, Formenti SC. Ionizing radiation inhibition of distant untreated tumors (abscopal effect) is immune mediated. Int J Radiat Oncol Biol Phys 2004; 58:862-70. (Pubitemid 38221143)
37. Postow MA, Callahan MK, Barker CA, Yamada Y, Yuan J, Kitano S, Mu Z, Rasalan T, Adamow M, et al. Immunologic correlates of the abscopal effect in a patient with melanoma. N Engl J Med 2012; 366:925-31.
38. Aslakson CJ, Miller FR. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res 1992; 52:1399-405.
39. Pulaski BA, Ostrand-Rosenberg S. Mouse 4T1 breast tumor model. In J. Coligan, D. Margulies, E. Shevach, W. Strober, A. Kruisbeek, eds. Current Protocols in Immunology, John Wiley & Sons, 2001. pp. 20.22.11-20.22.21.
40. Thurnherr N, Deschner EE, Stonehill EH, Lipkin M. Induction of adenocarcinomas of the colon in mice by weekly injections of 1,2-dimethylhydrazine. Cancer Res 1973; 33:940-5.
41. Rosato A, Santa SD, Zoso A, Giacomelli S, Milan G, Macino B, et al. The cytotoxic T-lymphocyte response against a poorly immunogenic mammary adenocarcinoma is focused on a single immunodominant class I epitope derived from the gp70 Env product of an endogenous retrovirus. Cancer Res 2003; 63:2158-63. (Pubitemid 36538621)
42. Zagzag D, Miller DC, Chiriboga L, Yee H, Newcomb EW. Green fluorescent protein immunohistochemistry as a novel experimental tool for the detection of glioma cell invasion in vivo. Brain Pathol 2003; 13:34-7. (Pubitemid 36133790)
43. Albert ML, Sauter B, Bhardwaj N, Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature 1998; 392:86-9. (Pubitemid 28150594)
44. Lynch DH, Andreasen A, Maraskovsky E, Whitmore J, Miller RE, Schuh JC. Flt3 ligand induces tumor regression and anti-tumor immune responses in vivo. Nat Med 1997; 3:625-31. (Pubitemid 27264971)
45. Chakravarty PK, Alfieri A, Thomas EK, Beri V, Tanaka KE, Vikram B, Guha C. Flt3-Ligand administration after radiation therapy prolongs survival in a murine model of metastatic lung cancer. Cancer Res 1999; 59:6028-32. (Pubitemid 30035614)
46. Kim KW, Kim SH, Shin JG, Kim GS, Son YO, Park SW, et al. Direct injection of immature dendritic cells into irradiated tumor induces efficient antitumor immunity. Int J Cancer 2004; 109:685-90.
47. Finkelstein SE, Iclozan C, Bui MM, Cotter MJ, Ramakrishnan R, Ahmed J, et al. Combination of external beam radiotherapy (EBRT) with intratumoral injection of dendritic cells as neoadjuvant treatment of high-risk soft tissue sarcoma patients. Int J Radiat Oncol Biol Phys 2012; 82:924-32.
48. Adams S. Toll-like receptor agonists in cancer therapy. Immunotherapy 2009; 1:949-64.
49. Cheever MA. Twelve immunotherapy drugs that could cure cancers. Immunol Rev 2008; 222:357-68. (Pubitemid 351430366)
50. Milas L, Mason KA, Ariga H, Hunter N, Neal R, Valdecanas D, et al. CpG oligodeoxynucleotide enhances tumor response to radiation. Cancer Res 2004; 64:5074-7. (Pubitemid 39006521)
51. Adams S, Kozhaya L, Martiniuk F, Meng TC, Chiriboga L, Liebes L, et al. Topical TLR7 agonist imiquimod can induce immunemediated rejection of skin metastases in patients with breast cancer. Clin Cancer Res 2012; 18:6748-57.
52. Dewan Z, Vanpouille-Box C, Kawashima N, Dinapoli S, Babb JS, Formenti SC, et al. Synergy of topical Toll-Like Receptor 7 agonist with radiation and low dose cyclophosphamide in a mouse model of cutaneous breast cancer. Clin Cancer Res 2012; 18:6668-78.
53. Zang X, Allison JP. The B7 family and cancer therapy: costimulation and coinhibition. Clin Cancer Res 2007; 13:5271-9. (Pubitemid 47510350)
54. Peggs KS, Quezada SA, Allison JP. Cell intrinsic mechanisms of T-cell inhibition and application to cancer therapy. Immunol Rev 2008; 224:141-65.
55. Thompson CB, Allison JP. The emerging role of CTLA-4 as an immune attenuator. Immunity 1997; 7:445-50. (Pubitemid 27508696)
56. Qureshi OS, Zheng Y, Nakamura K, Attridge K, Manzotti C, Schmidt EM, et al. Trans-Endocytosis of CD80 and CD86: A Molecular Basis for the Cell-Extrinsic Function of CTLA-4. Science 2011; 332:600-3.
57. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363:711-23.
58. Demaria S, Kawashima N, Yang AM, Devitt M-L, Babb JS, Allison JP, Formenti SC. Immune-mediated inhibition of metastases following treatment with local radiation and CTLA-4 blockade in a mouse model of breast cancer. Clin Cancer Res 2005; 11:728-34. (Pubitemid 40116901)
59. Dewan MZ, Galloway AE, Kawashima N, Dewyngaert JK, Babb JS, Formenti SC, et al. Fractionated but not single dose radiotherapy induces an immune-mediated abscopal effect when combined with anti-CTLA-4 antibody. Clin Cancer Res 2009; 15:5379-88.
60. Matsumura S, Demaria S. Up-regulation of the pro-inflammatory chemokine CXCL16 is a common response of tumor cells to ionizing radiation. Radiat Res 2010; 173:418-25.
61. Somersalo K, Anikeeva N, Sims TN, Thomas VK, Strong RK, Spies T, et al. Cytotoxic T lymphocytes form an antigenindependent ring junction. J Clin Invest 2004; 113:49-57. (Pubitemid 38541631)
62. Demaria S, Dustin ML. Role of the crosstalk between CTLA-4 and NKG2D in the development of anti-CTLA-4 treatment strategies. Immunotherapy 2013; 5: 109-12.
63. Dranoff G, Jaffee E, Lazenby A, Golumbek P, Levitsky H, Brose K, et al. Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity. Proc Natl Acad Sci USA 1993; 90:3539-43. (Pubitemid 23111402)
64. Hege KM, Jooss K, Pardoll D. GM-CSF gene-modifed cancer cell immunotherapies: of mice and men. Int Rev Immunol 2006; 25:321-52. (Pubitemid 44972270)
65. Newcomb EW, Demaria S, Lukyanov Y, Shao Y, Schnee T, Kawashima N, et al. The combination of ionizing radiation and peripheral vaccination produces long-term survival of mice bearing established invasive GL261 gliomas. Clin Cancer Res 2006; 12:4730-7. (Pubitemid 44297827)
66. Prins RM, Odesa SK, Liau LM. Immunotherapeutic targeting of shared melanoma-associated antigens in a murine glioma model. Cancer Res 2003; 63:8487-91. (Pubitemid 37549505)
67. Lynch D. The promise of 4-1BB (CD137)-mediated immunomodulation and the immunotherapy of cancer. Immunol Rev 2008; 222:277-86. (Pubitemid 351430383)
68. Vinay DS, Kwon BS. Immunotherapy of cancer with 4-1BB. Mol Cancer Ther 2012; 11:1062-70.
69. Newcomb EW, Lukyanov Y, Kawashima N, Alonso-Basanta M, Wang S-C, Liu M, Jure-Kunkel M, Zagzag D, Demaria S, Formenti SC. Radiotherapy enhances antitumor effect of anti-CD137 therapy in a mouse Glioma model. Radiat Res 2010; 173:426-32.
70. Wrzesinski SH, Wan YY, Flavell RA. Transforming growth factor-beta and the immune response: implications for anticancer therapy. Clin Cancer Res 2007; 13:5262-70. (Pubitemid 47510349)
71. Barcellos-Hoff MH, Derynck R, Tsang ML, Weatherbee JA. Transforming growth factor-beta activation in irradiated murine mammary gland. J Clin Invest 1994; 93:892-9.
72. Jobling MF, Mott JD, Finnegan MT, Jurukovski V, Erickson AC, Walian PF, et al. Isoform-specific activation of latent transforming growth factor beta (LTGF-beta) by reactive oxygen species. Radiat Res 2006; 166:839-48. (Pubitemid 44888249)
73. Barcellos-Hoff MH, Akhurst RJ. Transforming growth factor-beta in breast cancer: too much, too late. Breast Cancer Res 2009; 11:202.
74. Bouquet F, Pal A, Pilones KA, Demaria S, Hann B, Akhurst RJ, et al. TGFb1 inhibition increases the radiosensitivity of breast cancer cells in vitro and promotes tumor control by radiation in vivo. Clin Cancer Res 2011; 17:6754-65.
75. Postow MA, Callahan MK, Wolchok JD. The antitumor immunity of ipilimumab: (T-cell) memories to last a lifetime? Clin Cancer Res 2012; 18:1821-3.
76. Wolchok JD, Hoos S, O'Day S, Weber JS, Hamid O, Lebbé C, et al. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res 2009; 15:7412-20.
77. Formenti SC, Demaria S. Systemic effects of local radiotherapy. Lancet Oncol 2009; 10:718-26.
78. Formenti S, Adams S, Friedman K, Fenton-Kerimian M, Donach M, Goldberg J, et al. Pilot trial of radiation therapy and GM-CSF in metastatic cancer: abscopal responses. Int J Radiat Oncol Biol Phys 2011; 84:S178.
79. Ledford H. Melanoma drug wins U.S. approval. Nature 2011; 471:561.
80. Stamell EF, Wolchok JD, Gnjatic S, Lee NY, Brownell I. The Abscopal Effect Associated With a Systemic Anti-melanoma Immune Response. Int J Radiat Oncol Biol Phys 2013; 85:293-5.