Immune effects of targeted radiation therapy for cancer

Discovery Medicine

Volumn 19, Issue 104, 2015, Pages 219-228

  Sridharan, Vishwajith ^a   Schoenfeld, Jonathan D ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CHEMOKINE RECEPTOR CXCR3; CHEMOKINE RECEPTOR CXCR6; CXCL16 CHEMOKINE; FAS LIGAND; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HIGH MOBILITY GROUP B1 PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1; INTERLEUKIN 6; IPILIMUMAB; LYMPHOTOXIN; PROGRAMMED DEATH 1 LIGAND 1; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; ANTINEOPLASTIC AGENT; CHEMOKINE; CYTOKINE; INTERFERON;

ADAPTIVE IMMUNITY; ARTICLE; CANCER IMMUNOTHERAPY; CANCER RADIOTHERAPY; CD3+ T LYMPHOCYTE; HISTONE ACETYLATION; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; METASTATIC MELANOMA; MOLECULARLY TARGETED THERAPY; NATURAL KILLER CELL; OVERALL SURVIVAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; TH1 CELL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT; ANIMAL; CHEMISTRY; IMMUNE SYSTEM; IMMUNOLOGY; IMMUNOTHERAPY; INFLAMMATION; MELANOMA; METABOLISM; METASTASIS; MOUSE; NEOPLASMS; PATHOLOGY; PROCEDURES;

ANIMALS; ANTINEOPLASTIC AGENTS; CHEMOKINES; CYTOKINES; HUMANS; IMMUNE SYSTEM; IMMUNOTHERAPY; INFLAMMATION; INTERFERONS; MELANOMA; MICE; NEOPLASM METASTASIS; NEOPLASMS; RADIOTHERAPY; T-LYMPHOCYTES; TUMOR MICROENVIRONMENT;

EID: 84940537227     PISSN: 15396509     EISSN: 19447930     Source Type: Journal    
DOI: None     Document Type: Article

References (73)

1. Ahmad SS, Duke S, Jena R, Williams MV, Burnet NG. Advances in radiotherapy. BMJ 345:e7765, 2012.
2. Akmansu M, Unsal D, Bora H, Elbeg S. Influence of locoregional radiation treatment on tumor necrosis factor-alpha and interleukin-6 in the serum of patients with head and neck cancer. Cytokine 31(1):41-45, 2005.
3. Ansell SM, Lesokhin AM, Borrello I, Halwani A, Scott EC, Gutierrez M, Schuster SJ, Millenson MM, Cattry D, Freeman GJ, Rodig SJ, Chapuy B, Ligon AH, Zhu L, Grosso JF, Kim SY, Timmerman JM, Shipp MA, Armand P. PD-1 blockade with nivolumab in relapsed or refractory Hodgkin's lymphoma. N Engl J Med 372(4):311-319, 2015.
4. Ao X, Zhao L, Davis MA, Lubman DM, Lawrence TS, Kong FM. Radiation produces differential changes in cytokine profiles in radiation lung fibrosis sensitive and resistant mice. J Hematol Oncol 2:6, 2009.
5. Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A, Mignot G, Maiuri MC, Ullrich E, Saulnier P, Yang H, Amigorena S, Ryffel B, Barrat FJ, Saftig P, Levi F, Lidereau R, Nogues C, Mira JP, Chompret A, et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 13(9):1050-1059, 2007.
6. Balermpas P, Michel Y, Wagenblast J, Seitz O, Weiss C, Rodel F, Rodel C, Fokas E. Tumour-infiltrating lymphocytes predict response to definitive chemoradiotherapy in head and neck cancer. Br J Cancer 110(2):501-509, 2014.
7. Baskar R, Lee KA, Yeo R, Yeoh KW. Cancer and radiation therapy: current advances and future directions. Int J Med Sci 9(3):193-199, 2012.
8. Bouquet F, Pal A, Pilones KA, Demaria S, Hann B, Akhurst RJ, Babb JS, Lonning SM, Dewyngaert JK, Formenti SC, Barcellos-Hoff MH. TGFbeta1 inhibition increases the radiosensitivity of breast cancer cells in vitro and promotes tumor control by radiation in vivo. Clin Cancer Res 17(21):6754-6765, 2011.
9. Burnette BC, Liang H, Lee Y, Chlewicki L, Khodarev NN, Weichselbaum RR, Fu YX, Auh SL. The efficacy of radiotherapy relies upon induction of type i interferon-dependent innate and adaptive immunity. Cancer Res 71(7):2488-2496, 2011.
10. Chakraborty M, Abrams SI, Camphausen K, Liu K, Scott T, Coleman CN, Hodge JW. Irradiation of tumor cells up-regulates Fas and enhances CTL lytic activity and CTL adoptive immunotherapy. J Immunol 170(12):6338-6347, 2003.
11. Chen MF, Kuan FC, Yen TC, Lu MS, Lin PY, Chung YH, Chen WC, Lee KD. IL-6-stimulated CD11b+ CD14+ HLA-DR-myeloid-derived suppressor cells, are associated with progression and poor prognosis in squamous cell carcinoma of the esophagus. Oncotarget 5(18):8716-8728, 2014.
12. Colotta F, Allavena P, Sica A, Garlanda C, Mantovani A. Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 30(7):1073-1081, 2009.
13. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, Evdemon-Hogan M, Conejo-Garcia JR, Zhang L, Burow M, Zhu Y, Wei S, Kryczek I, Daniel B, Gordon A, Myers L, Lackner A, Disis ML, Knutson KL, Chen L, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 10(9):942-949, 2004.
14. De Jaeger K, Seppenwoolde Y, Kampinga HH, Boersma LJ, Belderbos JS, Lebesque JV. Significance of plasma transforming growth factor-beta levels in radiotherapy for non-small-cell lung cancer. Int J Radiat Oncol Biol Phys 58(5):1378-1387, 2004.
15. Demaria S, Kawashima N, Yang AM, Devitt ML, Babb JS, Allison JP, Formenti SC. Immune-mediated inhibition of metastases after treatment with local radiation and CTLA-4 blockade in a mouse model of breast cancer. Clin Cancer Res 11(2 Pt 1):728-734, 2005.
16. Deng L, Liang H, Burnette B, Beckett M, Darga T, Weichselbaum RR, Fu YX. Irradiation and anti-PD-L1 treatment synergistically promote antitumor immunity in mice. J Clin Invest 124(2):687-695, 2014a.
17. Deng L, Liang H, Xu M, Yang X, Burnette B, Arina A, Li XD, Mauceri H, Beckett M, Darga T, Huang X, Gajewski TF, Chen ZJ, Fu YX, Weichselbaum RR. STING-Dependent Cytosolic DNA Sensing Promotes Radiation-Induced Type I Interferon-Dependent Antitumor Immunity in Immunogenic Tumors. Immunity 41(5):843-852, 2014b.
18. Dewan MZ, Galloway AE, Kawashima N, Dewyngaert JK, Babb JS, Formenti SC, Demaria S. Fractionated but not single-dose radiotherapy induces an immune-mediated abscopal effect when combined with anti-CTLA-4 antibody. Clin Cancer Res 15(17):5379-5388, 2009.
19. Ding NH, Li JJ, Sun LQ. Molecular mechanisms and treatment of radiation-induced lung fibrosis. Curr Drug Targets 14(11):1347-1356, 2013.
20. Dovedi SJ, Adlard AL, Lipowska-Bhalla G, Mckenna C, Jones S, Cheadle EJ, Stratford IJ, Poon E, Morrow M, Stewart R, Jones H, Wilkinson RW, Honeychurch J, Illidge TM. Acquired resistance to fractionated radiotherapy can be overcome by concurrent PD-L1 blockade. Cancer Res 74(19):5458-5468, 2014.
21. Dranoff G. Cytokines in cancer pathogenesis and cancer therapy. Nat Rev Cancer 4(1):11-22, 2004.
22. Dunn GP, Koebel CM, Schreiber RD. Interferons, immunity and cancer immunoediting. Nat Rev Immunol 6(11):836-848, 2006.
23. Faget J, Biota C, Bachelot T, Gobert M, Treilleux I, Goutagny N, Durand I, Leon-Goddard S, Blay JY, Caux C, Menetrier-Caux C. Early detection of tumor cells by innate immune cells leads to T(reg) recruitment through CCL22 production by tumor cells. Cancer Res 71(19):6143-6152, 2011.
24. Formenti SC, Demaria S. Combining radiotherapy and cancer immunotherapy: a paradigm shift. J Natl Cancer Inst 105(4):256-265, 2013.
25. Gameiro SR, Jammeh ML, Wattenberg MM, Tsang KY, Ferrone S, Hodge JW. Radiation-induced immunogenic modulation of tumor enhances antigen processing and calreticulin exposure, resulting in enhanced T-cell killing. Oncotarget 5(2):403-416, 2014.
26. Garnett CT, Palena C, Chakraborty M, Tsang KY, Schlom J, Hodge JW. Sublethal irradiation of human tumor cells modulates phenotype resulting in enhanced killing by cytotoxic T lymphocytes. Cancer Res 64(21):7985-7994, 2004.
27. Gehrmann M, Specht HM, Bayer C, Brandstetter M, Chizzali B, Duma M, Breuninger S, Hube K, Lehnerer S, Van Phi V, Sage E, Schmid TE, Sedelmayr M, Schilling D, Sievert W, Stangl S, Multhoff G. Hsp70-a biomarker for tumor detection and monitoring of outcome of radiation therapy in patients with squamous cell carcinoma of the head and neck. Radiat Oncol 9:131, 2014.
28. 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 1(6):365-372, 2013.
29. Gooden MJ, De Bock GH, Leffers N, Daemen T, Nijman HW. The prognostic influence of tumour-infiltrating lymphocytes in cancer: a systematic review with meta-analysis. Br J Cancer 105(1):93-103, 2011.
30. Gyorki DE, Callahan M, Wolchok JD, Ariyan CE. The delicate balance of melanoma immunotherapy. Clin Transl Immunology 2(8):e5, 2013.
31. Hodi FS, O'day SJ, Mcdermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, Akerley W, Van Den Eertwegh AJ, Lutzky J, Lorigan P, Vaubel JM, Linette GP, Hogg D, Ottensmeier CH, Lebbe C, Peschel C, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 363(8):711-723, 2010.
32. Kachikwu EL, Iwamoto KS, Liao YP, Demarco JJ, Agazaryan N, Economou JS, Mcbride WH, Schaue D. Radiation enhances regulatory T cell representation. Int J Radiat Oncol Biol Phys 81(4):1128-1135, 2011.
33. Kaplan DH, Shankaran V, Dighe AS, Stockert E, Aguet M, Old LJ, Schreiber RD. Demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice. Proc Natl Acad Sci U S A 95(13):7556-7561, 1998.
34. Kim JY, Son YO, Park SW, Bae JH, Chung JS, Kim HH, Chung BS, Kim SH, Kang CD. Increase of NKG2D ligands and sensitivity to NK cell-mediated cytotoxicity of tumor cells by heat shock and ionizing radiation. Exp Mol Med 38(5):474-484, 2006.
35. Klug F, Prakash H, Huber PE, Seibel T, Bender N, Halama N, Pfirschke C, Voss RH, Timke C, Umansky L, Klapproth K, Schakel K, Garbi N, Jager D, Weitz J, Schmitz-Winnenthal H, Hammerling GJ, Beckhove P. Low-dose irradiation programs macrophage differentiation to an iNOS(+)/M1 phenotype that orchestrates effective T cell immunotherapy. Cancer Cell 24(5):589-602, 2013.
36. Kobayashi K, Tanaka Y, Horiguchi S, Yamamoto S, Toshinori N, Sugimoto A, Okamoto Y. The effect of radiotherapy on NKT cells in patients with advanced head and neck cancer. Cancer Immunol Immunother 59(10):1503-1509, 2010.
37. Kondo T, Kobayashi J, Saitoh T, Maruyama K, Ishii KJ, Barber GN, Komatsu K, Akira S, Kawai T. DNA damage sensor MRE11 recognizes cytosolic double-stranded DNA and induces type I interferon by regulating STING trafficking. Proc Natl Acad Sci U S A 110(8):2969-2974, 2013.
38. Kovacs C. Cytokine profiles in patients receiving wide-field + prostate boost radiotherapy (xRT) for adenocarcinoma of the prostate. Cytokine 23(6):151-163, 2003.
39. Kumari A, Cacan E, Greer SF, Garnett-Benson C. Turning T cells on: epigenetically enhanced expression of effector T-cell costimulatory molecules on irradiated human tumor cells. J Immunother Cancer 1:17, 2013.
40. Leone P, Shin EC, Perosa F, Vacca A, Dammacco F, Racanelli V. MHC class I antigen processing and presenting machinery: organization, function, and defects in tumor cells. J Natl Cancer Inst 105(16):1172-1187, 2013.
41. Lim JY, Gerber SA, Murphy SP, Lord EM. Type I interferons induced by radiation therapy mediate recruitment and effector function of CD8(+) T cells. Cancer Immunol Immunother 63(3):259-271, 2014.
42. Ma JL, Jin L, Li YD, He CC, Guo XJ, Liu R, Yang YY, Han SX. The intensity of radiotherapy-elicited immune response is associated with esophageal cancer clearance. J Immunol Res 2014:794249, 2014.
43. Matsumura S, Demaria S. Up-regulation of the pro-inflammatory chemokine CXCL16 is a common response of tumor cells to ionizing radiation. Radiat Res 173(4):418-425, 2010.
44. Matsumura S, Wang B, Kawashima N, Braunstein S, Badura M, Cameron TO, Babb JS, Schneider RJ, Formenti SC, Dustin ML, Demaria S. Radiation-induced CXCL16 release by breast cancer cells attracts effector T cells. J Immunol 181(5):3099-3107, 2008.
45. Mellman I, Coukos G, Dranoff G. Cancer immunotherapy comes of age. Nature 480(7378):480-489, 2011.
46. Meyer C, Cagnon L, Costa-Nunes CM, Baumgaertner P, Montandon N, Leyvraz L, Michielin O, Romano E, Speiser DE. Frequencies of circulating MDSC correlate with clinical outcome of melanoma patients treated with ipilimumab. Cancer Immunol Immunother 63(3):247-257, 2014.
47. Miyamoto Y, Hosotani R, Doi R, Wada M, Ida J, Tsuji S, Kawaguchi M, Nakajima S, Kobayashi H, Masui T, Imamura M. Interleukin-6 inhibits radiation induced apoptosis in pancreatic cancer cells. Anticancer Res 21(4a):2449-2456, 2001.
48. Nishikawa H, Sakaguchi S. Regulatory T cells in cancer immunotherapy. Curr Opin Immunol 27:1-7, 2014.
49. Ostrand-Rosenberg S. Myeloid-derived suppressor cells: more mechanisms for inhibiting antitumor immunity. Cancer Immunol Immunother 59(10):1593-1600, 2010.
50. Ott PA, Hodi FS, Robert C. CTLA-4 and PD-1/PD-L1 blockade: new immunotherapeutic modalities with durable clinical benefit in melanoma patients. Clin Cancer Res 19(19):5300-5309, 2013.
51. Parikh F, Duluc D, Imai N, Clark A, Misiukiewicz K, Bonomi M, Gupta V, Patsias A, Parides M, Demicco EG, Zhang DY, Kim-Schulze S, Kao J, Gnjatic S, Oh S, Posner MR, Sikora AG. Chemoradiotherapy-induced upregulation of PD-1 antagonizes immunity to HPV-related oropharyngeal cancer. Cancer Res 74(24):7205-7216, 2014.
52. Postow MA, Callahan MK, Barker CA, Yamada Y, Yuan J, Kitano S, Mu Z, Rasalan T, Adamow M, Ritter E, Sedrak C, Jungbluth AA, Chua R, Yang AS, Roman RA, Rosner S, Benson B, Allison JP, Lesokhin AM, Gnjatic S, et al. Immunologic correlates of the abscopal effect in a patient with melanoma. N Engl J Med 366(10):925-931, 2012.
53. Prestwich RJ, Errington F, Hatfield P, Merrick AE, Ilett EJ, Selby PJ, Melcher AA. The immune system-is it relevant to cancer development, progression and treatment? Clin Oncol (R Coll Radiol) 20(2):101-112, 2008.
54. Qu Y, Zhang B, Liu S, Zhang A, Wu T, Zhao Y. 2-Gy whole-body irradiation significantly alters the balance of CD4+ CD25-T effector cells and CD4+ CD25+ Foxp3+ T regulatory cells in mice. Cell Mol Immunol 7(6):419-427, 2010.
55. Reits EA, Hodge JW, Herberts CA, Groothuis TA, Chakraborty M, Wansley EK, Camphausen K, Luiten RM, De Ru AH, Neijssen J, Griekspoor A, Mesman E, Verreck FA, Spits H, Schlom J, Van Veelen P, Neefjes JJ. Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy. J Exp Med 203(5):1259-1271, 2006.
56. Rizvi NA, Mazieres J, Planchard D, Stinchcombe TE, Dy GK, Antonia SJ, Horn L, Lena H, Minenza E, Mennecier B, Otterson GA, Campos LT, Gandara DR, Levy BP, Nair SG, Zalcman G, Wolf J, Souquet PJ, Baldini E, Cappuzzo F, et al. Activity and safety of nivolumab, an anti-PD-1 immune checkpoint inhibitor, for patients with advanced, refractory squamous non-small-cell lung cancer (CheckMate 063): a phase 2, single-arm trial. Lancet Oncol 16(3):257-265, 2015.
57. Robertson FC, Berzofsky JA, Terabe M. NKT cell networks in the regulation of tumor immunity. Front Immunol 5:543, 2014.
58. Sakaguchi S. Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 22:531-562, 2004.
59. Sato H, Suzuki Y, Ide M, Katoh T, Noda SE, Ando K, Oike T, Yoshimoto Y, Okonogi N, Mimura K, Asao T, Kuwano H, Nakano T. HLA class I expression and its alteration by preoperative hyperthermo-chemoradiotherapy in patients with rectal cancer. PLoS One 9(9):e108122, 2014.
60. Schaue D, Kachikwu EL, Mcbride WH. Cytokines in radiobiological responses: a review. Radiat Res 178(6):505-523, 2012a.
61. Schaue D, Xie MW, Ratikan JA, Mcbride WH. Regulatory T cells in radiotherapeutic responses. Front Oncol 2:90, 2012b.
62. Schmidt MA, Fortsch C, Schmidt M, Rau TT, Fietkau R, Distel LV. Circulating regulatory T cells of cancer patients receiving radiochemotherapy may be useful to individualize cancer treatment. Radiother Oncol 104(1):131-138, 2012.
63. Schroder K, Hertzog PJ, Ravasi T, Hume DA. Interferon-gamma: an overview of signals, mechanisms and functions. J Leukoc Biol 75(2):163-189, 2004.
64. Siva S, Macmanus M, Kron T, Best N, Smith J, Lobachevsky P, Ball D, Martin O. A pattern of early radiation-induced inflammatory cytokine expression is associated with lung toxicity in patients with non-small cell lung cancer. PLoS One 9(10):e109560, 2014.
65. Sliwkowski MX, Mellman I. Antibody therapeutics in cancer. Science 341(6151):1192-1198, 2013.
66. Stone HB, Coleman CN, Anscher MS, Mcbride WH. Effects of radiation on normal tissue: consequences and mechanisms. Lancet Oncol 4(9):529-536, 2003.
67. Sznol M, Chen L. Antagonist antibodies to PD-1 and B7-H1 (PD-L1) in the treatment of advanced human cancer-response. Clin Cancer Res 19(19):5542, 2013.
68. Tang Y, Xu X, Guo S, Zhang C, Tang Y, Tian Y, Ni B, Lu B, Wang H. An increased abundance of tumor-infiltrating regulatory T cells is correlated with the progression and prognosis of pancreatic ductal adenocarcinoma. PLoS One 9(3):e91551, 2014.
69. Van Der Meeren A, Monti P, Vandamme M, Squiban C, Wysocki J, Griffiths N. Abdominal radiation exposure elicits inflammatory responses and abscopal effects in the lungs of mice. Radiation Res 163(2):144-152, 2005.
70. Wan S, Pestka S, Jubin RG, Lyu YL, Tsai YC, Liu LF. Chemotherapeutics and radiation stimulate MHC class I expression through elevated interferon-beta signaling in breast cancer cells. PLoS One 7(3):e32542, 2012.
71. Wang B, Li B, Dai Z, Ren S, Bai M, Wang Z, Li Z, Lin S, Wang Z, Huang N, Yang P, Liu M, Min W, Ma H. Low-dose splenic radiation inhibits liver tumor development of rats through functional changes in CD4+CD25+Treg cells. Int J Biochem Cell Biol 55:98-108, 2014.
72. Yasuda K, Nirei T, Sunami E, Nagawa H, Kitayama J. Density of CD4(+) and CD8(+) T lymphocytes in biopsy samples can be a predictor of pathological response to chemoradiotherapy (CRT) for rectal cancer. Radiat Oncol 6:49, 2011.
73. Zhao L, Wang L, Ji W, Wang X, Zhu X, Hayman JA, Kalemkerian GP, Yang W, Brenner D, Lawrence TS, Kong FM. Elevation of plasma TGF-beta1 during radiation therapy predicts radiation-induced lung toxicity in patients with non-small-cell lung cancer: a combined analysis from Beijing and Michigan. Int J Radiat Oncol Biol Phys 74(5):1385-1390, 2009.