Irradiation and immunotherapy: From concept to the clinic

Cancer

Volumn 122, Issue 11, 2016, Pages 1659-1671

  Salama, April K S ^a   Postow, Michael A ^b,c   Salama, Joseph K ^d  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Cytotoxic T lymphocyte associated protein 4 (CTLA 4); Immunotherapy; Ipilimumab; Programmed cell death 1 programmed death ligand 1 (PD 1 PD L1); Radiotherapy

Indexed keywords

ALPHA2B INTERFERON; BETA INTERFERON; CARRIER PROTEINS AND BINDING PROTEINS; CYTOTOXIC T LYMPHOCYTE ASSOCIATED PROTEIN 4; DOUBLE STRANDED DNA; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERFERON; INTERLEUKIN 2; IPILIMUMAB; NATURAL KILLER CELL RECEPTOR NKG2D; PLACEBO; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; MONOCLONAL ANTIBODY;

ADVERSE OUTCOME; CANCER RADIOTHERAPY; CASTRATION RESISTANT PROSTATE CANCER; CD8+ T LYMPHOCYTE; HUMAN; IMMUNE RESPONSE; IMMUNITY; IMMUNOSTIMULATION; LYMPHOCYTIC INFILTRATION; MELANOMA; METASTASIS; METASTATIC MELANOMA; MULTIMODALITY CANCER THERAPY; NON SMALL CELL LUNG CANCER; PALLIATIVE THERAPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RADIATION DOSE; RADIATION DOSE FRACTIONATION; RADIOIMMUNOTHERAPY; RADIOSURGERY; REVIEW; THERAPY EFFECT; ANTAGONISTS AND INHIBITORS; CELL CYCLE CHECKPOINT; IMMUNOLOGY; IMMUNOSUPPRESSIVE TREATMENT; IMMUNOTHERAPY; NEOPLASMS; PHYSIOLOGY; PROCEDURES; RADIATION RESPONSE; RADIATION TOLERANCE; RADIOTHERAPY; SKULL IRRADIATION; T LYMPHOCYTE; TUMOR MICROENVIRONMENT;

ANTIBODIES, MONOCLONAL; ANTIGENS, CD274; CELL CYCLE CHECKPOINTS; COMBINED MODALITY THERAPY; CRANIAL IRRADIATION; CTLA-4 ANTIGEN; HUMANS; IMMUNOSUPPRESSION; IMMUNOTHERAPY; NEOPLASMS; RADIATION TOLERANCE; RADIOSURGERY; RADIOTHERAPY; T-LYMPHOCYTES; TUMOR MICROENVIRONMENT;

EID: 84959419787     PISSN: 0008543X     EISSN: 10970142     Source Type: Journal    
DOI: 10.1002/cncr.29889     Document Type: Review

References (88)

1. Contamin M,. Immunisation contre le cancer de la souris inoculé avec les tumeurs modifiees par les rayons X. C R Acad Sci Paris. 1910; 128.
2. Wedd BH, Morson AC, Russ S,. On the immunity conferred upon mice by radium-irradiated mouse carcinoma. J Pathol Bacteriol. 1913; 18: 566-571.
3. Connell PP, Hellman S,. Advances in radiotherapy and implications for the next century: a historical perspective. Cancer Res. 2009; 69: 383-392.
4. Boyer MJ, Salama JK, Lee WR,. Palliative radiotherapy for prostate cancer. Oncology (Williston Park). 2014; 28: 306-312.
5. Kirkpatrick JP, Kelsey CR, Palta M, et al., Stereotactic body radiotherapy: a critical review for nonradiation oncologists. Cancer. 2014; 120: 942-954.
6. Fuks Z, Kolesnick R,. Engaging the vascular component of the tumor response. Cancer Cell. 2005; 8: 89-91.
7. Lee Y, Auh SL, Wang Y, et al., Therapeutic effects of ablative radiation on local tumor require CD8 + T cells: changing strategies for cancer treatment. Blood. 2009; 114: 589-595.
8. Moding EJ, Castle KD, Perez BA, et al., Tumor cells, but not endothelial cells, mediate eradication of primary sarcomas by stereotactic body radiation therapy [serial online]. Sci Transl Med. 2015; 7: 278ra234.
9. Formenti SC, Demaria S,. Combining radiotherapy and cancer immunotherapy: a paradigm shift. J Natl Cancer Inst. 2013; 105: 256-265.
10. Gangadhar TC, Salama AK,. Clinical applications of PD-1-based therapy: a focus on pembrolizumab (MK-3475) in the management of melanoma and other tumor types [serial online]. Onco Targets Ther. 2015; 8: 929-937.
11. Salama AK, Hodi FS,. Cytotoxic T-lymphocyte-associated antigen-4. Clin Cancer Res. 2011; 17: 4622-4628.
12. Eriksson D, Stigbrand T,. Radiation-induced cell death mechanisms. Tumour Biol. 2010; 31: 363-372.
13. Hoskin PJ, Kirkwood AA, Popova B, et al., 4 Gy versus 24 Gy radiotherapy for patients with indolent lymphoma (FORT): a randomised phase 3 non-inferiority trial. Lancet Oncol. 2014; 15: 457-463.
14. Reits EA, Hodge JW, Herberts CA, et al., Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy. J Exp Med. 2006; 203: 1259-1271.
15. Casares N, Pequignot MO, Tesniere A, et al., Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med. 2005; 202: 1691-1701.
16. Lugade AA, Moran JP, Gerber SA, Rose RC, Frelinger JG, Lord EM,. Local radiation therapy of B16 melanoma tumors increases the generation of tumor antigen-specific effector cells that traffic to the tumor. J Immunol. 2005; 174: 7516-7523.
17. Lugade AA, Sorensen EW, Gerber SA, Moran JP, Frelinger JG, Lord EM,. Radiation-induced IFN-gamma production within the tumor microenvironment influences antitumor immunity. J Immunol. 2008; 180: 3132-3139.
18. Blankenstein T,. The role of tumor stroma in the interaction between tumor and immune system. Curr Opin Immunol. 2005; 17: 180-186.
19. Formenti SC, Demaria S,. Systemic effects of local radiotherapy. Lancet Oncol. 2009; 10: 718-726.
20. Drake CG,. Combination immunotherapy approaches. Ann Oncol. 2012; 23 (suppl 8): viii41-viii46.
21. Spiotto MT, Rowley DA, Schreiber H,. Bystander elimination of antigen loss variants in established tumors. Nat Med. 2004; 10: 294-298.
22. Zhang B, Bowerman NA, Salama JK, et al., Induced sensitization of tumor stroma leads to eradication of established cancer by T cells. J Exp Med. 2007; 204: 49-55.
23. Eigentler TK, Weide B, de Braud F, et al., A dose-escalation and signal-generating study of the immunocytokine L19-IL2 in combination with dacarbazine for the therapy of patients with metastatic melanoma. Clin Cancer Res. 2011; 17: 7732-7742.
24. Johannsen M, Spitaleri G, Curigliano G, et al., The tumour-targeting human L19-IL2 immunocytokine: preclinical safety studies, phase I clinical trial in patients with solid tumours and expansion into patients with advanced renal cell carcinoma. Eur J Cancer. 2010; 46: 2926-2935.
25. Zegers CM, Rekers NH, Quaden DH, et al., Radiotherapy combined with the immunocytokine L19-IL2 provides long-lasting antitumor effects. Clin Cancer Res. 2015; 21: 1151-1160.
26. Hodi FS, O'Day SJ, McDermott DF, et al., Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010; 363: 711-723.
27. Demaria S, Kawashima N, Yang AM, et al., Immune-mediated inhibition of metastases after treatment with local radiation and CTLA-4 blockade in a mouse model of breast cancer. Clin Cancer Res. 2005; 11: 728-734.
28. Dewan MZ, Galloway AE, Kawashima N, 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: 5379-5388.
29. Ruocco MG, Pilones KA, Kawashima N, et al., Suppressing T cell motility induced by anti-CTLA-4 monotherapy improves antitumor effects. J Clin Invest. 2012; 122: 3718-3730.
30. Belcaid Z, Phallen JA, Zeng J, et al., Focal radiation therapy combined with 4-1BB activation and CTLA-4 blockade yields long-term survival and a protective antigen-specific memory response in a murine glioma model [serial online]. PLoS One. 2014; 9: e101764.
31. Verbrugge I, Hagekyriakou J, Sharp LL, et al., Radiotherapy increases the permissiveness of established mammary tumors to rejection by immunomodulatory antibodies. Cancer Res. 2012; 72: 3163-3174.
32. Zeng J, See AP, Phallen J, et al., Anti-PD-1 blockade and stereotactic radiation produce long-term survival in mice with intracranial gliomas. Int J Radiat Oncol Biol Phys. 2013; 86: 343-349.
33. Deng L, Liang H, Burnette B, et al., Irradiation and anti-PD-L1 treatment synergistically promote antitumor immunity in mice. J Clin Invest. 2014; 124: 687-695.
34. Sharabi AB, Nirschl CJ, Kochel CM, et al., Stereotactic radiation therapy augments antigen-specific PD-1-mediated antitumor immune responses via cross-presentation of tumor antigen. Cancer Immunol Res. 2015; 3: 345-355.
35. Vanpouille-Box C, Diamond JM, Pilones KA, et al., TGFbeta is a master regulator of radiation therapy-induced antitumor immunity. Cancer Res. 2015; 75: 2232-2242.
36. Finkelstein SE, Trotti A, Rao N, et al., The Florida Melanoma Trial I: A prospective multicenter phase I/II trial of postoperative hypofractionated adjuvant radiotherapy with concurrent interferon-alfa-2b in the treatment of advanced stage III melanoma with long-term toxicity follow-up [serial online]. ISRN Immunol. 2012; 2012: 324235.
37. Bradley JD, Scott CB, Paris KJ, et al., A phase III comparison of radiation therapy with or without recombinant beta-interferon for poor-risk patients with locally advanced non-small-cell lung cancer (RTOG 93-04). Int J Radiat Oncol Biol Phys. 2002; 52: 1173-1179.
38. Seung SK, Curti BD, Crittenden M, et al., Phase 1 study of stereotactic body radiotherapy and interleukin-2-tumor and immunological responses [serial online]. Sci Transl Med. 2012; 4: 137ra174.
39. Raj S, Indelicato D, Chiappori A, et al., Neoadjuvant administration of radiation therapy and intratumoral autologous dendritic cells in patients with localized high-risk soft tissue sarcomas [abstract]. J Clin Oncol. 2014; 32S. Abstract 10519.
40. Formenti SC, Adams S, Friedman K, et al., Pilot trial of radiation therapy and GM-CSF in metastatic cancer: abscopal responses [abstract]. Int J Radiat Oncol Biol Phys. 2012; 84: S178.
41. Golden EB, Chhabra A, Chachoua A, et al., Local radiotherapy and granulocyte-macrophage colony-stimulating factor to generate abscopal responses in patients with metastatic solid tumours: a proof-of-principle trial. Lancet Oncol. 2015; 16: 795-803.
42. Hazard LJ, Sause WT, Noyes RD,. Combined adjuvant radiation and interferon-alpha 2B therapy in high-risk melanoma patients: the potential for increased radiation toxicity. Int J Radiat Oncol Biol Phys. 2002; 52: 796-800.
43. Conill C, Jorcano S, Domingo-Domenech J, et al., Toxicity of combined treatment of adjuvant irradiation and interferon alpha2b in high-risk melanoma patients. Melanoma Res. 2007; 17: 304-309.
44. Gyorki DE, Ainslie J, Joon ML, Henderson MA, Millward M, McArthur GA,. Concurrent adjuvant radiotherapy and interferon-alpha2b for resected high risk stage III melanoma-a retrospective single centre study. Melanoma Res. 2004; 14: 223-230.
45. Maasilta P, Holsti LR, Halme M, Kivisaari L, Cantell K, Mattson K,. Natural alpha-interferon in combination with hyperfractionated radiotherapy in the treatment of non-small cell lung cancer. Int J Radiat Oncol Biol Phys. 1992; 23: 863-868.
46. Lange JR, Raubitschek AA, Pockaj BA, et al., A pilot study of the combination of interleukin-2-based immunotherapy and radiation therapy. J Immunother (1991). 1992; 12: 265-271.
47. Kirkwood JM, Ibrahim JG, Sondak VK, et al., High- and low-dose interferon alfa-2b in high-risk melanoma: first analysis of intergroup trial E1690/S9111/C9190. J Clin Oncol. 2000; 18: 2444-2458.
48. Kirkwood JM, Ibrahim JG, Sosman JA, et al., High-dose interferon alfa-2b significantly prolongs relapse-free and overall survival compared with the GM2-KLH/QS-21 vaccine in patients with resected stage IIB-III melanoma: results of intergroup trial E1694/S9512/C509801. J Clin Oncol. 2001; 19: 2370-2380.
49. Kirkwood JM, Strawderman MH, Ernstoff MS Smith TJ, Borden EC, Blum RH,. Interferon alfa-2b adjuvant therapy of high-risk resected cutaneous melanoma: the Eastern Cooperative Oncology Group Trial EST 1684. J Clin Oncol. 1996; 14: 7-17.
50. Ang KK, Byers RM, Peters LJ, et al., Regional radiotherapy as adjuvant treatment for head and neck malignant melanoma. Preliminary results. Arch Otolaryngol Head Neck Surg. 1990; 116: 169-172.
51. Henderson MA, Burmeister BH, Ainslie J, et al., Adjuvant lymph-node field radiotherapy versus observation only in patients with melanoma at high risk of further lymph-node field relapse after lymphadenectomy (ANZMTG 01.02/TROG 02.01): 6-year follow-up of a phase 3, randomised controlled trial. Lancet Oncol. 2015; 16: 1049-1060.
52. McDonald S, Chang AY, Rubin P, et al., Combined Betaseron R (recombinant human interferon beta) and radiation for inoperable non-small cell lung cancer. Int J Radiat Oncol Biol Phys. 1993; 27: 613-619.
53. Atkins MB, Lotze MT, Dutcher JP, et al., High-dose recombinant interleukin 2 therapy for patients with metastatic melanoma: analysis of 270 patients treated between 1985 and 1993. J Clin Oncol. 1999; 17: 2105-2116.
54. Demaria S, Pilones KA, Vanpouille-Box C, Golden EB, Formenti SC,. The optimal partnership of radiation and immunotherapy: from preclinical studies to clinical translation. Radiat Res. 2014; 182: 170-181.
55. Zeng J, Harris TJ, Lim M, Drake CG, Tran PT,. Immune modulation and stereotactic radiation: improving local and abscopal responses [serial online]. Biomed Res Int. 2013; 2013: 658126.
56. Barker CA, Postow MA, Khan SA, et al., Concurrent radiotherapy and ipilimumab immunotherapy for patients with melanoma. Cancer Immunol Res. 2013; 1: 92-98.
57. Qin R, Singh B, Olson AC, et al., Safety and efficacy of radiation in advanced melanoma patients treated with ipilimumab. Pigment Cell Melanoma Res. 2015; 28: 753-826.
58. Slovin SF, Higano CS, Hamid O, et al., Ipilimumab alone or in combination with radiotherapy in metastatic castration-resistant prostate cancer: results from an open-label, multicenter phase I/II study. Ann Oncol. 2013; 24: 1813-1821.
59. Kwon ED, Drake CG, Scher HI, et al., Ipilimumab versus placebo after radiotherapy in patients with metastatic castration-resistant prostate cancer that had progressed after docetaxel chemotherapy (CA184-043): a multicentre, randomised, double-blind, phase 3 trial. Lancet Oncol. 2014; 15: 700-712.
60. Twyman-Saint Victor C, Rech AJ, Maity A, et al., Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature. 2015; 520: 373-377.
61. Bapodra A, Esteves I, Pires Da Silva D, et al., Clinical outcome and CD4 + differentiation in andti-CTLA-4/radiation and anti-CTLA-4/steroid therapy [abstract]. J Clin Oncol. 2014; 32 (suppl). Abstract 3019.
62. Hiniker SM, Reddy SA, Maecker HT, Swetter SM, Shura L, Knox SJ,. A prospective clinical trial combining radiation therapy with systemic immunotherapy in metastatic melanoma [abstract]. Int J Radiat Oncol Biol Phys. 2015; 93: S95.
63. Kiess AP, Wolchok JD, Barker CA, et al., Stereotactic radiosurgery for melanoma brain metastases in patients receiving ipilimumab: safety profile and efficacy of combined treatment. Int J Radiat Oncol Biol Phys. 2015; 92: 368-375.
64. Knisely JP, Yu JB, Flanigan J, Sznol M, Kluger HM, Chiang VL,. Radiosurgery for melanoma brain metastases in the ipilimumab era and the possibility of longer survival. J Neurosurg. 2012; 117: 227-233.
65. Mathew M, Tam M, Ott PA, et al., Ipilimumab in melanoma with limited brain metastases treated with stereotactic radiosurgery. Melanoma Res. 2013; 23: 191-195.
66. Olson AC, Quin R, Singh B, Salama JK, Kirkpatrick J, Salama AK,. Radiosurgery for brain metastases in melanoma patients receiving ipilimumab [abstract]. Int J Radiat Oncol Biol Phys. 2015; 93: E88.
67. Silk AW, Bassetti MF, West BT, Tsien CI, Lao CD,. Ipilimumab and radiation therapy for melanoma brain metastases. Cancer Med. 2013; 2: 899-906.
68. Telera S, Fabi A, Pace A, et al., Radionecrosis induced by stereotactic radiosurgery of brain metastases: results of surgery and outcome of disease. J Neurooncol. 2013; 113: 313-325.
69. Minniti G, Clarke E, Lanzetta G, et al., Stereotactic radiosurgery for brain metastases: analysis of outcome and risk of brain radionecrosis [serial online]. Radiat Oncol. 2011; 6: 48.
70. Hodi FS, Oble DA, Drappatz J, et al., CTLA-4 blockade with ipilimumab induces significant clinical benefit in a female with melanoma metastases to the CNS. Nat Clin Pract Oncol. 2008; 5: 557-561.
71. Patel KR, Shoukat S, Oliver DE, et al., Ipilimumab and stereotactic radiosurgery versus stereotactic radiosurgery alone for newly diagnosed melanoma brain metastases [published online ahead of print May 16, 2015]. Am J Clin Oncol. doi: 10.1097/COC.00199.
72. Du Four S, Hong A, Chan M, et al., Symptomatic histologically proven necrosis of brain following stereotactic radiation and ipilimumab in six lesions in four melanoma patients [serial online]. Case Rep Oncol Med. 2014; 2014: 417913.
73. Du Four S, Wilgenhof S, Duerinck J, et al., Radiation necrosis of the brain in melanoma patients successfully treated with ipilimumab, three case studies. Eur J Cancer. 2012; 48: 3045-3051.
74. Lin NU, Lee EQ, Aoyama H, et al., Challenges relating to solid tumour brain metastases in clinical trials, part 1: patient population, response, and progression. A report from the RANO Group. Lancet Oncol. 2013; 14: e396-e406.
75. Lin NU, Lee EQ, Aoyama H, et al., Response assessment criteria for brain metastases: proposal from the RANO group. Lancet Oncol. 2015; 16: e270-e278.
76. Mole R,. Whole body irradiation therapy-radiobiology or medicine? Br J Radiol. 1953; 26: 234-241.
77. Konski A, Meyer JE, Joiner M, et al., Multi-institutional phase I study of low-dose ultra-fractionated radiotherapy as a chemosensitizer for gemcitabine and erlotinib in patients with locally advanced or limited metastatic pancreatic cancer. Radiother Oncol. 2014; 113: 35-40.
78. Hiniker SM, Chen DS, Reddy S, et al., A systemic complete response of metastatic melanoma to local radiation and immunotherapy. Transl Oncol. 2012; 5: 404-407.
79. Kingsley DP,. An interesting case of possible abscopal effect in malignant melanoma. Br J Radiol. 1975; 48: 863-866.
80. Reynders K, Illidge T, Siva S, Chang JY, De Ruysscher D,. The abscopal effect of local radiotherapy: using immunotherapy to make a rare event clinically relevant. Cancer Treat Rev. 2015; 41: 503-510.
81. Grimaldi AM, Simeone E, Giannarelli D, et al., Abscopal effects of radiotherapy on advanced melanoma patients who progressed after ipilimumab immunotherapy [serial online]. Oncoimmunology. 2014; 3: e28780.
82. 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: 293-295.
83. Postow MA, Callahan MK, Barker CA, et al., Immunologic correlates of the abscopal effect in a patient with melanoma. N Engl J Med. 2012; 366: 925-931.
84. Golden EB, Demaria S, Schiff PB, Chachoua A, Formenti SC,. An abscopal response to radiation and ipilimumab in a patient with metastatic non-small cell lung cancer. Cancer Immunol Res. 2013; 1: 365-372.
85. Postow MA, Chesney J, Pavlick AC, et al., Nivolumab and ipilimumab versus ipilimumab in untreated melanoma. N Engl J Med. 2015; 372: 2006-2017.
86. Borghaei H, Paz-Ares L, Horn L, et al., Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med. 2015; 373: 1627-1639.
87. Brahmer J, Reckamp KL, Baas P, et al., Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med. 2015; 373: 123-135.
88. Gandhi SJ, Minn AJ, Vonderheide RH, Wherry EJ, Hahn SM, Maity A,. Awakening the immune system with radiation: optimal dose and fractionation. Cancer Lett. 2015; 368: 185-190.