Building immunity to cancer with radiation therapy

Cancer Letters

Volumn 368, Issue 2, 2015, Pages 198-208

  Haikerwal, Suresh J ^a   Hagekyriakou, Jim ^a   MacManus, Michael ^a,b   Martin, Olga A ^a,b   Haynes, Nicole M ^a,b  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Anti tumor immunity; Cancer; Immunogenic cell death; Immunotherapy; Ionizing radiation; Radiotherapy

Indexed keywords

CANCER VACCINE; CELL ADHESION MOLECULE; CHEMOKINE; CYTOKINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR;

ADOPTIVE TRANSFER; APOPTOSIS; AUTOPHAGY; CANCER IMMUNOLOGY; CANCER IMMUNOTHERAPY; CANCER RADIOTHERAPY; CELL AGING; CELL DEATH; HUMAN; IMMUNOGENICITY; IMMUNOSTIMULATION; IONIZING RADIATION; MALIGNANT NEOPLASTIC DISEASE; METASTASIS; MITOTIC CATASTROPHE; NONHUMAN; PRIORITY JOURNAL; RADIATION DOSE; RADIATION RESPONSE; RADIOTHERAPY; SHORT SURVEY; STEREOTACTIC ABLATIVE BODY RADIATION THERAPY; STEREOTACTIC BODY RADIATION THERAPY; SYNCHROTRON X RAY MICROBEAM RADIOTHERAPY; IMMUNOLOGY; IMMUNOTHERAPY; NEOPLASMS; PATHOLOGY; PROCEDURES;

CELL DEATH; HUMANS; IMMUNOTHERAPY; NEOPLASMS; RADIOTHERAPY;

EID: 84941880401     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2015.01.009     Document Type: Review

References (178)

1. Old L.J., Boyse E.A. Immunology of experimental tumors. Annu. Rev. Med 1964, 15:167-186.
2. Schreiber R.D., Old L.J., Smyth M.J. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011, 331:1565-1570.
3. Dunn G.P., Old L.J., Schreiber R.D. The three Es of cancer immunoediting. Annu. Rev. Immunol 2004, 22:329-360.
4. Mittal D., Gubin M.M., Schreiber R.D., Smyth M.J. New insights into cancer immunoediting and its three component phases - elimination, equilibrium and escape. Curr. Opin. Immunol 2014, 27:16-25.
5. Vesely M.D., Kershaw M.H., Schreiber R.D., Smyth M.J. Natural innate and adaptive immunity to cancer. Annu. Rev. Immunol 2011, 29:235-271.
6. Matsushita H., Vesely M.D., Koboldt D.C., Rickert C.G., Uppaluri R., Magrini V.J., et al. Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature 2012, 482:400-404.
7. Gajewski T.F., Fuertes M., Spaapen R., Zheng Y., Kline J. Molecular profiling to identify relevant immune resistance mechanisms in the tumor microenvironment. Curr. Opin. Immunol 2011, 23:286-292.
8. Mantovani A., Sica A. Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr. Opin. Immunol 2010, 22:231-237.
9. 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, 313:1960-1964.
10. Galon J., Angell H.K., Bedognetti D., Marincola F.M. The continuum of cancer immunosurveillance: prognostic, predictive, and mechanistic signatures. Immunity 2013, 39:11-26.
11. Loi S., Michiels S., Salgado R., Sirtaine N., Jose V., Fumagalli D., et al. Tumor infiltrating lymphocytes are prognostic in triple negative breast cancer and predictive for trastuzumab benefit in early breast cancer: results from the FinHER trial. Ann. Oncol 2014, 25:1544-1550.
12. Smith E.L., Zamarin D., Lesokhin A.M. Harnessing the immune system for cancer therapy. Curr. Opin. Oncol 2014, 26:600-607.
13. Zitvogel L., Galluzzi L., Smyth M.J., Kroemer G. Mechanism of action of conventional and targeted anticancer therapies: reinstating immunosurveillance. Immunity 2013, 39:74-88.
14. Bernier J., Hall E.J., Giaccia A. Radiation oncology: a century of achievements. Nat. Rev. Cancer 2004, 4:737-747.
15. Eriksson D., Stigbrand T. Radiation-induced cell death mechanisms. Tumour Biol 2010, 31:363-372.
16. Dewey W.C., Ling C.C., Meyn R.E. Radiation-induced apoptosis: relevance to radiotherapy. Int. J. Radiat. Oncol. Biol. Phys 1995, 33:781-796.
17. Palumbo S., Comincini S. Autophagy and ionizing radiation in tumors: the "survive or not survive" dilemma. J. Cell. Physiol 2013, 228:1-8.
18. Castedo M., Perfettini J.L., Roumier T., Valent A., Raslova H., Yakushijin K., et al. Mitotic catastrophe constitutes a special case of apoptosis whose suppression entails aneuploidy. Oncogene 2004, 23:4362-4370.
19. Ianzini F., Bertoldo A., Kosmacek E.A., Phillips S.L., Mackey M.A. Lack of p53 function promotes radiation-induced mitotic catastrophe in mouse embryonic fibroblast cells. Cancer Cell Int 2006, 6:11.
20. Vakifahmetoglu H., Olsson M., Tamm C., Heidari N., Orrenius S., Zhivotovsky B. DNA damage induces two distinct modes of cell death in ovarian carcinomas. Cell Death Differ 2008, 15:555-566.
21. Eriksson D., Joniani H.M., Sheikholvaezin A., Lofroth P.O., Johansson L., Riklund Ahlstrom K., et al. Combined low dose radio- and radioimmunotherapy of experimental HeLa Hep 2 tumours. Eur. J. Nucl. Med. Mol. Imaging 2003, 30:895-906.
22. Sheard M.A., Uldrijan S., Vojtesek B. Role of p53 in regulating constitutive and X-radiation-inducible CD95 expression and function in carcinoma cells. Cancer Res 2003, 63:7176-7184.
23. Kolesnick R., Fuks Z. Radiation and ceramide-induced apoptosis. Oncogene 2003, 22:5897-5906.
24. Corre I., Niaudet C., Paris F. Plasma membrane signaling induced by ionizing radiation. Mutat. Res 2010, 704:61-67.
25. Radford I.R. p53 status, DNA double-strand break repair proficiency, and radiation response of mouse lymphoid and myeloid cell lines. Int. J. Radiat. Biol 1994, 66:557-560.
26. Alvarez S., Drane P., Meiller A., Bras M., Deguin-Chambon V., Bouvard V., et al. A comprehensive study of p53 transcriptional activity in thymus and spleen of gamma irradiated mouse: high sensitivity of genes involved in the two main apoptotic pathways. Int. J. Radiat. Biol 2006, 82:761-770.
27. Golstein P., Kroemer G. Cell death by necrosis: towards a molecular definition. Trends Biochem. Sci 2007, 32:37-43.
28. Hitomi J., Christofferson D.E., Ng A., Yao J., Degterev A., Xavier R.J., et al. Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 2008, 135:1311-1323.
29. Nehs M.A., Lin C.I., Kozono D.E., Whang E.E., Cho N.L., Zhu K., et al. Necroptosis is a novel mechanism of radiation-induced cell death in anaplastic thyroid and adrenocortical cancers. Surgery 2011, 150:1032-1039.
30. Bianchi M.E. DAMPs, PAMPs and alarmins: all we need to know about danger. J. Leukoc. Biol 2007, 81:1-5.
31. Hennel R., Brix N., Seidl K., Ernst A., Scheithauer H., Belka C., et al. Release of monocyte migration signals by breast cancer cell lines after ablative and fractionated gamma-irradiation. Radiat. Oncol 2014, 9:85.
32. Vakkila J., Lotze M.T. Inflammation and necrosis promote tumour growth. Nat. Rev. Immunol 2004, 4:641-648.
33. Kroemer G., Levine B. Autophagic cell death: the story of a misnomer. Nat. Rev. Mol. Cell Biol 2008, 9:1004-1010.
34. Deng Y., Chan S.S., Chang S. Telomere dysfunction and tumour suppression: the senescence connection. Nat. Rev. Cancer 2008, 8:450-458.
35. Sabin R.J., Anderson R.M. Cellular Senescence - its role in cancer and the response to ionizing radiation. Genome Integr 2011, 2:7.
36. Rodier F., Coppe J.P., Patil C.K., Hoeijmakers W.A., Munoz D.P., Raza S.R., et al. Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion. Nat. Cell Biol 2009, 11:973-979.
37. Coppe J.P., Desprez P.Y., Krtolica A., Campisi J. The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu. Rev. Pathol 2010, 5:99-118.
38. Xue W., Zender L., Miething C., Dickins R.A., Hernando E., Krizhanovsky V., et al. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 2007, 445:656-660.
39. Iannello A., Thompson T.W., Ardolino M., Lowe S.W., Raulet D.H. p53-dependent chemokine production by senescent tumor cells supports NKG2D-dependent tumor elimination by natural killer cells. J. Exp. Med 2013, 210:2057-2069.
40. Sokolov M.V., Dickey J.S., Bonner W.M., Sedelnikova O.A. Gamma-H2AX in bystander cells: not just a radiation-triggered event, a cellular response to stress mediated by intercellular communication. Cell Cycle 2007, 6:2210-2212.
41. Prise K.M., O'Sullivan J.M. Radiation-induced bystander signalling in cancer therapy. Nat. Rev. Cancer 2009, 9:351-360.
42. Sprung C.N., Ivashkevich A., Forrester H.B., Redon C.E., Georgakilas A., Martin O.A. Oxidative DNA damage caused by inflammation may link to stress-induced non-targeted effects. Cancer Lett 2015, 356:72-81.
43. Siva S., MacManus M.P., Martin R.F., Martin O.A. Abscopal effects of radiation therapy: a clinical review for the radiobiologist. Cancer Lett 2015, 356:82-90.
44. Dickey J.S., Baird B.J., Redon C.E., Sokolov M.V., Sedelnikova O.A., Bonner W.M. Intercellular communication of cellular stress monitored by gamma-H2AX induction. Carcinogenesis 2009, 30:1686-1695.
45. Redon C.E., Dickey J.S., Nakamura A.J., Kareva I.G., Naf D., Nowsheen S., et al. Tumors induce complex DNA damage in distant proliferative tissues in vivo. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:17992-17997.
46. Martin O.A., Redon C.E., Nakamura A.J., Dickey J.S., Georgakilas A.G., Bonner W.M. Systemic DNA damage related to cancer. Cancer Res 2011, 71:3437-3441.
47. Wasserman J., Blomgren H., Rotstein S., Petrini B., Hammarstrom S. Immunosuppression in irradiated breast cancer patients: in vitro effect of cyclooxygenase inhibitors. Bull. N. Y. Acad. Med 1989, 65:36-44.
48. McBride W.H., Chiang C.S., Olson J.L., Wang C.C., Hong J.H., Pajonk F., et al. A sense of danger from radiation. Radiat. Res 2004, 162:1-19.
49. Reits E.A., Hodge J.W., Herberts C.A., Groothuis T.A., Chakraborty M., Wansley E.K., et al. Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy. J. Exp. Med 2006, 203:1259-1271.
50. Zhang B., Bowerman N.A., Salama J.K., Schmidt H., Spiotto M.T., Schietinger A., et al. Induced sensitization of tumor stroma leads to eradication of established cancer by T cells. J. Exp. Med 2007, 204:49-55.
51. Chakraborty M., Abrams S.I., Camphausen K., Liu K., Scott T., Coleman C.N., et al. Irradiation of tumor cells up-regulates Fas and enhances CTL lytic activity and CTL adoptive immunotherapy. J. Immunol 2003, 170:6338-6347.
52. Gasser S., Orsulic S., Brown E.J., Raulet D.H. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 2005, 436:1186-1190.
53. Gehrmann M., Marienhagen J., Eichholtz-Wirth H., Fritz E., Ellwart J., Jaattela M., et al. Dual function of membrane-bound heat shock protein 70 (Hsp70), Bag-4, and Hsp40: protection against radiation-induced effects and target structure for natural killer cells. Cell Death Differ 2005, 12:38-51.
54. Obeid M., Tesniere A., Ghiringhelli F., Fimia G.M., Apetoh L., Perfettini J.L., et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med 2007, 13:54-61.
55. 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, 13:1050-1059.
56. Ghiringhelli F., Apetoh L., Tesniere A., Aymeric L., Ma Y., Ortiz C., et al. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat. Med 2009, 15:1170-1178.
57. Michaud M., Martins I., Sukkurwala A.Q., Adjemian S., Ma Y., Pellegatti P., et al. Autophagy-dependent anticancer immune responses induced by chemotherapeutic agents in mice. Science 2011, 334:1573-1577.
58. Degenhardt K., Mathew R., Beaudoin B., Bray K., Anderson D., Chen G., et al. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 2006, 10:51-64.
59. Gameiro S.R., Jammeh M.L., Wattenberg M.M., Tsang K.Y., Ferrone S., Hodge J.W. Radiation-induced immunogenic modulation of tumor enhances antigen processing and calreticulin exposure, resulting in enhanced T-cell killing. Oncotarget 2014, 5:403-416.
60. Desai S., Kumar A., Laskar S., Pandey B.N. Cytokine profile of conditioned medium from human tumor cell lines after acute and fractionated doses of gamma radiation and its effect on survival of bystander tumor cells. Cytokine 2013, 61:54-62.
61. Ohba K., Omagari K., Nakamura T., Ikuno N., Saeki S., Matsuo I., et al. Abscopal regression of hepatocellular carcinoma after radiotherapy for bone metastasis. Gut 1998, 43:575-577.
62. Nakanishi M., Chuma M., Hige S., Asaka M. Abscopal effect on hepatocellular carcinoma. Am. J. Gastroenterol 2008, 103:1320-1321.
63. Mothersill C., Seymour C.B. Radiation-induced bystander effects - implications for cancer. Nat. Rev. Cancer 2004, 4:158-164.
64. Siva S., MacManus M., Kron T., Best N., Smith J., Lobachevsky P., et al. A pattern of early radiation-induced inflammatory cytokine expression is associated with lung toxicity in patients with non-small cell lung cancer. PLoS ONE 2014, 9:e109560.
65. Lugade A.A., Sorensen E.W., Gerber S.A., Moran J.P., Frelinger J.G., Lord E.M. Radiation-induced IFN-gamma production within the tumor microenvironment influences antitumor immunity. J. Immunol 2008, 180:3132-3139.
66. Burnette B.C., Liang H., Lee Y., Chlewicki L., Khodarev N.N., Weichselbaum R.R., et al. The efficacy of radiotherapy relies upon induction of type i interferon-dependent innate and adaptive immunity. Cancer Res 2011, 71:2488-2496.
67. Hallahan D.E., Spriggs D.R., Beckett M.A., Kufe D.W., Weichselbaum R.R. Increased tumor necrosis factor alpha mRNA after cellular exposure to ionizing radiation. Proc. Natl. Acad. Sci. U.S.A. 1989, 86:10104-10107.
68. Klug F., Prakash H., Huber P.E., Seibel T., Bender N., Halama N., et al. Low-dose irradiation programs macrophage differentiation to an iNOS(+)/M1 phenotype that orchestrates effective T cell immunotherapy. Cancer Cell 2013, 24:589-602.
69. Matsumura S., Wang B., Kawashima N., Braunstein S., Badura M., Cameron T.O., et al. Radiation-induced CXCL16 release by breast cancer cells attracts effector T cells. J. Immunol 2008, 181:3099-3107.
70. 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, 173:418-425.
71. Hojo S., Koizumi K., Tsuneyama K., Arita Y., Cui Z., Shinohara K., et al. High-level expression of chemokine CXCL16 by tumor cells correlates with a good prognosis and increased tumor-infiltrating lymphocytes in colorectal cancer. Cancer Res 2007, 67:4725-4731.
72. Draghiciu O., Walczak M., Hoogeboom B.N., Franken K.L., Melief K.J., Nijman H.W., et al. Therapeutic immunization and local low-dose tumor irradiation, a reinforcing combination. Int. J. Cancer 2014, 134:859-872.
73. Malik I.A., Moriconi F., Sheikh N., Naz N., Khan S., Dudas J., et al. Single-dose gamma-irradiation induces up-regulation of chemokine gene expression and recruitment of granulocytes into the portal area but not into other regions of rat hepatic tissue. Am. J. Pathol 2010, 176:1801-1815.
74. Hareyama M., Imai K., Oouchi A., Takahashi H., Hinoda Y., Tsujisaki M., et al. The effect of radiation on the expression of intercellular adhesion molecule-1 of human adenocarcinoma cells. Int. J. Radiat. Oncol. Biol. Phys 1998, 40:691-696.
75. Handschel J., Prott F.J., Sunderkotter C., Metze D., Meyer U., Joos U. Irradiation induces increase of adhesion molecules and accumulation of beta2-integrin-expressing cells in humans. Int. J. Radiat. Oncol. Biol. Phys 1999, 45:475-481.
76. Barcellos-Hoff M.H., Derynck R., Tsang M.L., Weatherbee J.A. Transforming growth factor-beta activation in irradiated murine mammary gland. J. Clin. Invest 1994, 93:892-899.
77. Jobling M.F., Mott J.D., Finnegan M.T., Jurukovski V., Erickson A.C., Walian P.J., et al. Isoform-specific activation of latent transforming growth factor beta (LTGF-beta) by reactive oxygen species. Radiat. Res 2006, 166:839-848.
78. Naiki Y., Michelsen K.S., Zhang W., Chen S., Doherty T.M., Arditi M. Transforming growth factor-beta differentially inhibits MyD88-dependent, but not TRAM- and TRIF-dependent, lipopolysaccharide-induced TLR4 signaling. J. Biol. Chem 2005, 280:5491-5495.
79. Chen W., Jin W., Hardegen N., Lei K.J., Li L., Marinos N., et al. Conversion of peripheral CD4+ CD25-naive T cells to CD4+ CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med 2003, 198:1875-1886.
80. Wrzesinski S.H., Wan Y.Y., Flavell R.A. Transforming growth factor-beta and the immune response: implications for anticancer therapy. Clin. Cancer Res 2007, 13:5262-5270.
81. Corradin S.B., Buchmuller-Rouiller Y., Smith J., Suardet L., Mauel J. Transforming growth factor beta 1 regulation of macrophage activation depends on the triggering stimulus. J. Leukoc. Biol 1993, 54:423-429.
82. Boutard V., Havouis R., Fouqueray B., Philippe C., Moulinoux J.P., Baud L. Transforming growth factor-beta stimulates arginase activity in macrophages. Implications for the regulation of macrophage cytotoxicity. J. Immunol 1995, 155:2077-2084.
83. de Waal Malefyt R., Abrams J., Bennett B., Figdor C.G., de Vries J.E. Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med 1991, 174:1209-1220.
84. de Waal Malefyt R., Haanen J., Spits H., Roncarolo M.G., te Velde A., Figdor C., et al. Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J. Exp. Med 1991, 174:915-924.
85. Kuwata H., Watanabe Y., Miyoshi H., Yamamoto M., Kaisho T., Takeda K., et al. IL-10-inducible Bcl-3 negatively regulates LPS-induced TNF-alpha production in macrophages. Blood 2003, 102:4123-4129.
86. Halak B.K., Maguire H.C., Lattime E.C. Tumor-induced interleukin-10 inhibits type 1 immune responses directed at a tumor antigen as well as a non-tumor antigen present at the tumor site. Cancer Res 1999, 59:911-917.
87. Anscher M.S., Murase T., Prescott D.M., Marks L.B., Reisenbichler H., Bentel G.C., et al. Changes in plasma TGF beta levels during pulmonary radiotherapy as a predictor of the risk of developing radiation pneumonitis. Int. J. Radiat. Oncol. Biol. Phys 1994, 30:671-676.
88. Anscher M.S., Samulski T.V., Dodge R., Prosnitz L.R., Dewhirst M.W. Combined external beam irradiation and external regional hyperthermia for locally advanced adenocarcinoma of the prostate. Int. J. Radiat. Oncol. Biol. Phys 1997, 37:1059-1065.
89. Moses A.G., Maingay J., Sangster K., Fearon K.C., Ross J.A. Pro-inflammatory cytokine release by peripheral blood mononuclear cells from patients with advanced pancreatic cancer: relationship to acute phase response and survival. Oncol. Rep 2009, 21:1091-1095.
90. Huynh M.L., Fadok V.A., Henson P.M. Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-beta1 secretion and the resolution of inflammation. J. Clin. Invest 2002, 109:41-50.
91. Kadhim M., Salomaa S., Wright E., Hildebrandt G., Belyakov O.V., Prise K.M., et al. Non-targeted effects of ionising radiation-Implications for low dose risk. Mutat. Res 2013, 752:84-98.
92. Formenti S.C., Demaria S. Systemic effects of local radiotherapy. Lancet Oncol 2009, 10:718-726.
93. Qu Y., Jin S., Zhang A., Zhang B., Shi X., Wang J., et al. Gamma-ray resistance of regulatory CD4+ CD25+ Foxp3+ T cells in mice. Radiat. Res 2010, 173:148-157.
94. Coates P.J., Rundle J.K., Lorimore S.A., Wright E.G. Indirect macrophage responses to ionizing radiation: implications for genotype-dependent bystander signaling. Cancer Res 2008, 68:450-456.
95. Bouquet F., Pal A., Pilones K.A., Demaria S., Hann B., Akhurst R.J., et al. TGFbeta1 inhibition increases the radiosensitivity of breast cancer cells in vitro and promotes tumor control by radiation in vivo. Clin. Cancer Res 2011, 17:6754-6765.
96. Young K.H., Newell P., Cottam B., Friedman D., Savage T., Baird J.R., et al. TGFbeta inhibition prior to hypofractionated radiation enhances efficacy in preclinical models. Cancer Immunol. Res 2014, 2:1011-1022.
97. Maleki Vareki S., Rytelewski M., Figueredo R., Chen D., Ferguson P.J., Vincent M., et al. Indoleamine 2,3-dioxygenase mediates immune-independent human tumor cell resistance to olaparib, gamma radiation, and cisplatin. Oncotarget 2014, 5:2778-2791.
98. Tabatabai G., Frank B., Mohle R., Weller M., Wick W. Irradiation and hypoxia promote homing of haematopoietic progenitor cells towards gliomas by TGF-beta-dependent HIF-1alpha-mediated induction of CXCL12. Brain 2006, 129:2426-2435.
99. Ball H.J., Jusof F.F., Bakmiwewa S.M., Hunt N.H., Yuasa H.J. Tryptophan-catabolizing enzymes - party of three. Front. Immunol 2014, 5:485.
100. Kozin S.V., Kamoun W.S., Huang Y., Dawson M.R., Jain R.K., Duda D.G. Recruitment of myeloid but not endothelial precursor cells facilitates tumor regrowth after local irradiation. Cancer Res 2010, 70:5679-5685.
101. Kioi M., Vogel H., Schultz G., Hoffman R.M., Harsh G.R., Brown J.M. Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. J. Clin. Invest 2010, 120:694-705.
102. Liu S.C., Alomran R., Chernikova S.B., Lartey F., Stafford J., Jang T., et al. Blockade of SDF-1 after irradiation inhibits tumor recurrences of autochthonous brain tumors in rats. Neuro-Oncol 2014, 16:21-28.
103. Rodel F., Frey B., Gaipl U., Keilholz L., Fournier C., Manda K., et al. Modulation of inflammatory immune reactions by low-dose ionizing radiation: molecular mechanisms and clinical application. Curr. Med. Chem 2012, 19:1741-1750.
104. Wunderlich R., Ernst A., Rodel F., Fietkau R., Ott O., Lauber K., et al. Low and moderate doses of ionizing radiation up to 2 Gy modulate transmigration and chemotaxis of activated macrophages, provoke an anti-inflammatory cytokine milieu, but do not impact upon viability and phagocytic function. Clin. Exp. Immunol 2015, 179:50-61.
105. Thanik V.D., Chang C.C., Lerman O.Z., Greives M.R., Le H., Warren S.M., et al. Cutaneous low-dose radiation increases tissue vascularity through upregulation of angiogenic and vasculogenic pathways. J. Vasc. Res 2010, 47:472-480.
106. Kallman R.F. The phenomenon of reoxygenation and its implications for fractionated radiotherapy. Radiology 1972, 105:135-142.
107. Schneider B.F., Eberhard D.A., Steiner L.E. Histopathology of arteriovenous malformations after gamma knife radiosurgery. J. Neurosurg 1997, 87:352-357.
108. Brown J.M. The hypoxic cell: a target for selective cancer therapy - eighteenth Bruce F. Cain Memorial Award lecture. Cancer Res 1999, 59:5863-5870.
109. Demaria S., Formenti S.C. Radiation as an immunological adjuvant: current evidence on dose and fractionation. Front. Oncol 2012, 2:153.
110. Hauser S.H., Calorini L., Wazer D.E., Gattoni-Celli S. Radiation-enhanced expression of major histocompatibility complex class I antigen H-2Db in B16 melanoma cells. Cancer Res 1993, 53:1952-1955.
111. Lee Y., Auh S.L., 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, 114:589-595.
112. Dewan M.Z., Galloway A.E., Kawashima N., Dewyngaert J.K., Babb J.S., Formenti S.C., 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.
113. Brody J.D., Ai W.Z., Czerwinski D.K., Torchia J.A., Levy M., Advani R.H., et al. In situ vaccination with a TLR9 agonist induces systemic lymphoma regression: a phase I/II study. J. Clin. Oncol 2010, 28:4324-4332.
114. Gulley J.L., Arlen P.M., Bastian A., Morin S., Marte J., Beetham P., et al. Combining a recombinant cancer vaccine with standard definitive radiotherapy in patients with localized prostate cancer. Clin. Cancer Res 2005, 11:3353-3362.
115. Postow M.A., Callahan M.K., Barker C.A., Yamada Y., Yuan J., Kitano S., et al. Immunologic correlates of the abscopal effect in a patient with melanoma. N. Engl. J. Med 2012, 366:925-931.
116. Golden E.B., Demaria S., Schiff P.B., Chachoua A., Formenti S.C. An abscopal response to radiation and ipilimumab in a patient with metastatic non-small cell lung cancer. Cancer Immunol. Res 2013, 1:365-372.
117. de la Cruz-Merino L., Illescas-Vacas A., Grueso-Lopez A., Barco-Sanchez A., Miguez-Sanchez C. Radiation for awakening the dormant immune system, a promising challenge to be explored. Front. Immunol 2014, 5:102. Cancer Immunotherapies Spanish Group.
118. Kulzer L., Rubner Y., Deloch L., Allgauer A., Frey B., Fietkau R., et al. Norm- and hypo-fractionated radiotherapy is capable of activating human dendritic cells. J. Immunotoxicol 2014, 11:328-336.
119. Rubner Y., Muth C., Strnad A., Derer A., Sieber R., Buslei R., et al. Fractionated radiotherapy is the main stimulus for the induction of cell death and of Hsp70 release of p53 mutated glioblastoma cell lines. Radiat. Oncol 2014, 9:89.
120. Murphy M.E. The HSP70 family and cancer. Carcinogenesis 2013, 34:1181-1188.
121. Tsai M.H., Cook J.A., Chandramouli G.V., DeGraff W., Yan H., Zhao S., et al. Gene expression profiling of breast, prostate, and glioma cells following single versus fractionated doses of radiation. Cancer Res 2007, 67:3845-3852.
122. John-Aryankalayil M., Palayoor S.T., Cerna D., Simone C.B., Falduto M.T., Magnuson S.R., et al. Fractionated radiation therapy can induce a molecular profile for therapeutic targeting. Radiat. Res 2010, 174:446-458.
123. Schaue D., Ratikan J.A., Iwamoto K.S., McBride W.H. Maximizing tumor immunity with fractionated radiation. Int. J. Radiat. Oncol. Biol. Phys 2012, 83:1306-1310.
124. Glide-Hurst C.K., Chetty I.J. Improving radiotherapy planning, delivery accuracy, and normal tissue sparing using cutting edge technologies. J. Thorac. Dis 2014, 6:303-318.
125. Dhakal S., Corbin K.S., Milano M.T., Philip A., Sahasrabudhe D., Jones C., et al. Stereotactic body radiotherapy for pulmonary metastases from soft-tissue sarcomas: excellent local lesion control and improved patient survival. Int. J. Radiat. Oncol. Biol. Phys 2012, 82:940-945.
126. Heinzerling J.H., Kavanagh B., Timmerman R.D. Stereotactic ablative radiation therapy for primary lung tumors. Cancer J. 2011, 17:28-32.
127. Kothari G., Foroudi F., Gill S., Corcoran N.M., Siva S. Outcomes of stereotactic radiotherapy for cranial and extracranial metastatic renal cell carcinoma: a systematic review. Acta Oncol 2014, 1-10.
128. Comito T., Cozzi L., Clerici E., Campisi M.C., Liardo R.L., Navarria P., et al. Stereotactic Ablative Radiotherapy (SABR) in inoperable oligometastatic disease from colorectal cancer: a safe and effective approach. BMC Cancer 2014, 14:619.
129. Siva S., Pham D., Gill S., Corcoran N.M., Foroudi F. A systematic review of stereotactic radiotherapy ablation for primary renal cell carcinoma. BJU Int 2012, 110:E737-E743.
130. Senan S., Palma D.A., Lagerwaard F.J. Stereotactic ablative radiotherapy for stage I NSCLC: recent advances and controversies. J. Thorac. Dis 2011, 3:189-196.
131. Brown J.M., Carlson D.J., Brenner D.J. The tumor radiobiology of SRS and SBRT: are more than the 5 Rs involved?. Int. J. Radiat. Oncol. Biol. Phys 2014, 88:254-262.
132. Reese A.S., Feigenberg S.J., Husain A., Webb T.J., Hausner P.F., Edelman M.J., et al. Stereotactic ablative radiotherapy (SABR): impact on the immune system and potential for future therapeutic modulation. Mol. Cell Pharmacol 2013, 5:19-25.
133. Zeng J., See A.P., Phallen J., Jackson C.M., Belcaid Z., Ruzevick 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.
134. Sharabi A.B., Nirschl C.J., Kochel C.M., Nirschl T.R., Francica B.J., Velarde E., et al. Stereotactic radiation therapy augments antigen-specific PD-1 mediated anti-tumor immune responses via cross-presentation of tumor antigen. Cancer Immunol. Res 2014, 10.1158/2326-6066.CIR-14-0196.
135. Cho J., Kodym R., Seliounine S., Richardson J.A., Solberg T.D., Story M.D. High dose-per-fraction irradiation of limited lung volumes using an image-guided, highly focused irradiator: simulating stereotactic body radiotherapy regimens in a small-animal model. Int. J. Radiat. Oncol. Biol. Phys 2010, 77:895-902.
136. Serduc R., Brauer-Krisch E., Siegbahn E.A., Bouchet A., Pouyatos B., Carron R., et al. High-precision radiosurgical dose delivery by interlaced microbeam arrays of high-flux low-energy synchrotron X-rays. PLoS ONE 2010, 5:e9028.
137. Rothkamm K., Crosbie J.C., Daley F., Bourne S., Barber P.R., Vojnovic B., et al. In situ biological dose mapping estimates the radiation burden delivered to 'spared' tissue between synchrotron X-ray microbeam radiotherapy tracks. PLoS ONE 2012, 7:e29853.
138. Laissue J.A., Geiser G., Spanne P.O., Dilmanian F.A., Gebbers J.O., Geiser M., et al. Neuropathology of ablation of rat gliosarcomas and contiguous brain tissues using a microplanar beam of synchrotron-wiggler-generated X rays. Int. J. Cancer 1998, 78:654-660.
139. Crosbie J.C., Anderson R.L., Rothkamm K., Restall C.M., Cann L., Ruwanpura S., et al. Tumor cell response to synchrotron microbeam radiation therapy differs markedly from cells in normal tissues. Int. J. Radiat. Oncol. Biol. Phys 2010, 77:886-894.
140. Sprung C.N., Yang Y., Forrester H.B., Li J., Zaitseva M., Cann L., et al. Genome-wide transcription responses to synchrotron microbeam radiotherapy. Radiat. Res 2012, 178:249-259.
141. Kingsley D.P. An interesting case of possible abscopal effect in malignant melanoma. Br. J. Radiol 1975, 48:863-866.
142. Robin H.I., AuBuchon J., Varanasi V.R., Weinstein A.B. The abscopal effect: demonstration in lymphomatous involvement of kidneys. Med. Pediatr. Oncol 1981, 9:473-476.
143. Wersall P.J., Blomgren H., Pisa P., Lax I., Kalkner K.M., Svedman C. Regression of non-irradiated metastases after extracranial stereotactic radiotherapy in metastatic renal cell carcinoma. Acta Oncol 2006, 45:493-497.
144. MacManus M.P., Harte R.J., Stranex S. Spontaneous regression of metastatic renal cell carcinoma following palliative irradiation of the primary tumour. Ir. J. Med. Sci 1994, 163:461-463.
145. Chakravarty P.K., Alfieri A., Thomas E.K., Beri V., Tanaka K.E., Vikram B., et al. Flt3-ligand administration after radiation therapy prolongs survival in a murine model of metastatic lung cancer. Cancer Res 1999, 59:6028-6032.
146. Demaria S., Bhardwaj N., McBride W.H., Formenti S.C. Combining radiotherapy and immunotherapy: a revived partnership. Int. J. Radiat. Oncol. Biol. Phys 2005, 63:655-666.
147. Demaria S., Kawashima N., Yang A.M., Devitt M.L., Babb J.S., Allison J.P., 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.
148. Ruocco M.G., Pilones K.A., Kawashima N., Cammer M., Huang J., Babb J.S., et al. Suppressing T cell motility induced by anti-CTLA-4 monotherapy improves antitumor effects. J. Clin. Invest 2012, 122:3718-3730.
149. Nikitina E.Y., Gabrilovich D.I. Combination of gamma-irradiation and dendritic cell administration induces a potent antitumor response in tumor-bearing mice: approach to treatment of advanced stage cancer. Int. J. Cancer 2001, 94:825-833.
150. Teitz-Tennenbaum S., Li Q., Rynkiewicz S., Ito F., Davis M.A., McGinn C.J., et al. Radiotherapy potentiates the therapeutic efficacy of intratumoral dendritic cell administration. Cancer Res 2003, 63:8466-8475.
151. Kim K.W., Kim S.H., Shin J.G., Kim G.S., Son Y.O., Park S.W., et al. Direct injection of immature dendritic cells into irradiated tumor induces efficient antitumor immunity. Int. J. Cancer 2004, 109:685-690.
152. Newcomb E.W., 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, 12:4730-4737.
153. Grimaldi A.M., Simeone E., Giannarelli D., Muto P., Falivene S., Borzillo V., et al. Abscopal effects of radiotherapy on advanced melanoma patients who progressed after ipilimumab immunotherapy. Oncoimmunology 2014, 3:e28780.
154. Hodi F.S., Day S.J.O., McDermott D.F., Weber R.W., Sosman J.A., Haanen J.B., et al. Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med 2010, 363:711-723.
155. Ascierto P.A., Minor D., Ribas A., Lebbe C., O'Hagan A., Arya N., et al. Phase II trial (BREAK-2) of the BRAF inhibitor dabrafenib (GSK2118436) in patients with metastatic melanoma. J. Clin. Oncol 2013, 31:3205-3211.
156. Henick B.S., Herbst R.S., Goldberg S.B. The PD-1 pathway as a therapeutic target to overcome immune escape mechanisms in cancer. Expert Opin. Ther. Targets 2014, 18:1407-1420.
157. Chambers C.A., Kuhns M.S., Egen J.G., Allison J.P. CTLA-4-mediated inhibition in regulation of T cell responses: mechanisms and manipulation in tumor immunotherapy. Annu. Rev. Immunol 2001, 19:565-594.
158. Mellman I., Coukos G., Dranoff G. Cancer immunotherapy comes of age. Nature 2011, 480:480-489.
159. Dong H., Strome S.E., Salomao D.R., Tamura H., Hirano F., Flies D.B., et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat. Med 2002, 8:793-800.
160. Brahmer J.R., Tykodi S.S., Chow L.Q., Hwu W.J., Topalian S.L., Hwu P., et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N. Engl. J. Med 2012, 366:2455-2465.
161. Topalian S.L., Hodi F.S., Brahmer J.R., Gettinger S.N., Smith D.C., McDermott D.F., et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med 2012, 366:2443-2454.
162. Verbrugge I., Hagekyriakou J., Sharp L.L., Galli M., West A., McLaughlin N.M., et al. Radiotherapy increases the permissiveness of established mammary tumors to rejection by immunomodulatory antibodies. Cancer Res 2012, 72:3163-3174.
163. Dovedi S.J., Adlard A.L., Lipowska-Bhalla G., McKenna C., Jones S., Cheadle E.J., et al. Acquired resistance to fractionated radiotherapy can be overcome by concurrent PD-L1 blockade. Cancer Res 2014, 74:5458-5468.
164. Deng L., Liang H., Burnette B., Beckett M., Darga T., Weichselbaum R.R., et al. Irradiation and anti-PD-L1 treatment synergistically promote antitumor immunity in mice. J. Clin. Invest 2014, 124:687-695.
165. Yokouchi H., Yamazaki K., Chamoto K., Kikuchi E., Shinagawa N., Oizumi S., et al. Anti-OX40 monoclonal antibody therapy in combination with radiotherapy results in therapeutic antitumor immunity to murine lung cancer. Cancer Sci 2008, 99:361-367.
166. Shi W., Siemann D.W. Augmented antitumor effects of radiation therapy by 4-1BB antibody (BMS-469492) treatment. Anticancer Res 2006, 26:3445-3453.
167. Honeychurch J., Glennie M.J., Johnson P.W., Illidge T.M. Anti-CD40 monoclonal antibody therapy in combination with irradiation results in a CD8 T-cell-dependent immunity to B-cell lymphoma. Blood 2003, 102:1449-1457.
168. Newcomb E.W., Lukyanov Y., Kawashima N., Alonso-Basanta M., Wang S.C., Liu M., et al. Radiotherapy enhances antitumor effect of anti-CD137 therapy in a mouse glioma model. Radiat. Res 2010, 173:426-432.
169. Wolchok J.D., Kluger H., Callahan M.K., Postow M.A., Rizvi N.A., Lesokhin A.M., et al. Nivolumab plus ipilimumab in advanced melanoma. N. Engl. J. Med 2013, 369:122-133.
170. Hamilton J.A. Colony-stimulating factors in inflammation and autoimmunity. Nat. Rev. Immunol 2008, 8:533-544.
171. Demaria S., Pilones K.A., Vanpouille-Box C., Golden E.B., Formenti S.C. The optimal partnership of radiation and immunotherapy: from preclinical studies to clinical translation. Radiat. Res 2014, 182:170-181.
172. Kanegasaki S., Matsushima K., Shiraishi K., Nakagawa K., Tsuchiya T. Macrophage inflammatory protein derivative ECI301 enhances the alarmin-associated abscopal benefits of tumor radiotherapy. Cancer Res 2014, 74:5070-5078.
173. Lugade A.A., Moran J.P., Gerber S.A., Rose R.C., Frelinger J.G., Lord E.M. 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.
174. Cao Z.A., Daniel D., Hanahan D. Sub-lethal radiation enhances anti-tumor immunotherapy in a transgenic mouse model of pancreatic cancer. BMC Cancer 2002, 2:11.
175. Filatenkov A., Baker J., Muller A.M., Ahn G.O., Kohrt H., Dutt S., et al. Treatment of 4T1 metastatic breast cancer with combined hypofractionated irradiation and autologous T-cell infusion. Radiat. Res 2014, 182:163-169.
176. Takeshima T., Chamoto K., Wakita D., Ohkuri T., Togashi Y., Shirato H., et al. Local radiation therapy inhibits tumor growth through the generation of tumor-specific CTL: its potentiation by combination with Th1 cell therapy. Cancer Res 2010, 70:2697-2706.
177. Dunn P.L., North R.J. Selective radiation resistance of immunologically induced T cells as the basis for irradiation-induced T-cell-mediated regression of immunogenic tumor. J. Leukoc. Biol 1991, 49:388-396.
178. Yang K.L., Wang Y.S., Chang C.C., Huang S.C., Huang Y.C., Chi M.S., et al. Reciprocal complementation of the tumoricidal effects of radiation and natural killer cells. PLoS ONE 2013, 8:e61797.