Abscopal effects of radiation therapy: A clinical review for the radiobiologist

Cancer Letters

Volumn 356, Issue 1, 2015, Pages 82-90

  Siva, Shankar ^a,b   MacManus, Michael P ^a,b   Martin, Roger F ^b   Martin, Olga A ^a,b  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Abscopal effects; Cytokines; Immune system; Normal tissue effects; Radiotherapy; Tumors

Indexed keywords

C REACTIVE PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; IPILIMUMAB; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE;

ABSCOPAL EFFECT; ADRENAL METASTASIS; BREAST CANCER; CANCER IMMUNOTHERAPY; CANCER RADIOTHERAPY; CELL DEATH; CHEMORADIOTHERAPY; CHRONIC INFLAMMATION; CYTOKINE RELEASE; DISTANT METASTASIS; FATIGUE; GENOMIC INSTABILITY; HEMATOLOGIC MALIGNANCY; HUMAN; KIDNEY CARCINOMA; LUNG ADENOCARCINOMA; LUNG METASTASIS; LYMPH NODE METASTASIS; MALIGNANT TRANSFORMATION; MELANOMA; OXIDATIVE STRESS; PROSTATE CANCER; RADIATION CARCINOGENESIS; RADIATION DOSE FRACTIONATION; RADIATION EXPOSURE; RADIATION RESPONSE; RADIOBIOLOGY; SECOND CANCER; SHORT SURVEY; STEREOTACTIC ABLATIVE BODY RADIATION THERAPY; STEREOTACTIC BODY RADIATION THERAPY; T LYMPHOCYTE ACTIVATION; TUMOR REGRESSION; ADULT; AGED; APOPTOSIS; BYSTANDER EFFECT; CELL TRANSFORMATION; FEMALE; IMMUNOLOGY; INFLAMMATION; MALE; METASTASIS; MIDDLE AGED; NEOPLASMS;

ADULT; AGED; APOPTOSIS; BYSTANDER EFFECT; CELL TRANSFORMATION, NEOPLASTIC; CYTOKINES; FEMALE; GENOMIC INSTABILITY; HUMANS; INFLAMMATION; MALE; MIDDLE AGED; NEOPLASM METASTASIS; NEOPLASMS;

EID: 84912558665     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.09.018     Document Type: Review

References (124)

1. Mole R. Whole body irradiation - radiobiology or medicine?. Br. J. Radiol. 1953, 26:234-241.
2. J.R. Andrews, Radiobiol. Human Cancer Radiotherapy. (1968).
3. W. Boyd, The Spontaneous Regression of Cancer, CC Thomas, 1966.
4. T.C. Everson, W.H. Cole, Spontaneous Regression of Cancer: a Study and Abstract of Reports in the World Medical Literature and of Personal Communications Concerning Spontaneous Regression of Malignant Disease, Saunders (WB) Co Ltd., 1966.
5. B. O'Regan, C. Hirshberg, Spontaneous Remission: An Annotated Bibliography, Institute of Noetic Sciences Sausalito, 1993.
6. Papac R.J. Spontaneous regression of cancer. Cancer Treat. Rev. 1996, 22:395-424.
7. Fowler J.F. The linear-quadratic formula and progress in fractionated radiotherapy. Br. J. Radiol. 1989, 62:679-694.
8. MacManus M., Harte R., Stranex S. Spontaneous regression of metastatic renal cell carcinoma following palliative irradiation of the primary tumour. Ir. J. Med. Sci. 1994, 163:461-463.
9. Ehlers G., Fridman M. Abscopal effect of radiation in papillary adenocarcinoma. Br. J. Radiol. 1973, 46:220-222.
10. Kingsley D. An interesting case of possible abscopal effect in malignant melanoma. Br. J. Radiol. 1975, 48:863-866.
11. Fairlamb D. Spontaneous regression of metastases of renal cancer: a report of two cases including the first recorded regression following irradiation of a dominant metastasis and review of the world literature. Cancer 1981, 47:2102-2106.
12. Rees G., Ross C. Abscopal regression following radiotherapy for adenocarcinoma. Br. J. Radiol. 1983, 56:63-66.
13. Ohba K., Omagari K., Nakamura T., Ikuno N., Saeki S., Matsuo I., Kinoshita H., Masuda J., Hazama H., Sakamoto I. Abscopal regression of hepatocellular carcinoma after radiotherapy for bone metastasis. Gut 1998, 43:575-577.
14. Takaya M., Niibe Y., Tsunoda S., Jobo T., Imai M., Kotani S., Unno N., Hayakawa K. Abscopal effect of radiation on toruliform para-aortic lymph node metastases of advanced uterine cervical carcinoma - a case report. Anticancer Res. 2007, 27:499-503.
15. Okuma K., Yamashita H., Niibe Y., Hayakawa K., Nakagawa K. Abscopal effect of radiation on lung metastases of hepatocellular carcinoma: a case report. J. Med. Case Reports 2011, 5:1-4.
16. Cotter S.E., Dunn G.P., Collins K.M., Sahni D., Zukotynski K.A., Hansen J.L., O'Farrell D.A., Ng A.K., Devlin P.M., Wang L.C. Abscopal effect in a patient with metastatic Merkel cell carcinoma following radiation therapy: potential role of induced antitumor immunity. Arch. Dermatol. 2011, 147:870.
17. Brock J., Ashley S., Bedford J., Nioutsikou E., Partridge M., Brada M. Review of hypofractionated small volume radiotherapy for early-stage non-small cell lung cancer. Clin. Oncol. 2008, 20:666-676.
18. Fuss M., Thomas C.R. Stereotactic body radiation therapy: an ablative treatment option for primary and secondary liver tumors. Ann. Surg. Oncol. 2004, 11:130-138.
19. Siva S., MacManus M., Ball D. Stereotactic radiotherapy for pulmonary oligometastases: a systematic review. J. Thoracic Oncol. 2010, 5:1091-1099.
20. 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.
21. P.J. Wersäll, H. Blomgren, P. Pisa, I. Lax, K.-M. Kälkner, C. Svedman, Regression of non-irradiated metastases after extracranial stereotactic radiotherapy in metastatic renal cell carcinoma. Acta Oncol. (Stockholm, Sweden) 45 (2006) 493.
22. H. Ishiyama, B.S. Teh, H. Ren, S. Chiang, A. Tann, A.I. Blanco, A.C. Paulino, R. Amato, Spontaneous regression of thoracic metastases while progression of brain metastases after stereotactic radiosurgery and stereotactic body radiotherapy for metastatic renal cell carcinoma: abscopal effect prevented by the blood-brain barrier? Clin. Genitourinary Cancer (2012).
23. Siva S., Callahan J., Macmanus M.P., Martin O., Hicks R.J., Ball D.L. Abscopal effects after conventional and stereotactic lung irradiation of non-small-cell lung cancer. J. Thorac. Oncol. 2013, 8:e71-72.
24. Stone H.B., Coleman C.N., Anscher M.S., McBride W.H. Effects of radiation on normal tissue: consequences and mechanisms. Lancet Oncol. 2003, 4:529-536.
25. Brush J., Lipnick S.L., Phillips T., Sitko J., McDonald J.T., McBride W.H. Molecular mechanisms of late normal tissue injury. Seminars Radiat. Oncol. 2007, 17:121-130.
26. Szatrowski T.P., Nathan C.F. Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res. 1991, 51:794-798.
27. Hiscox S., Barrett-Lee P., Nicholson R.I. Therapeutic targeting of tumor-stroma interactions. Expert Opin. Ther. Targets 2011, 15:609-621.
28. Lisanti M.P., Martinez-Outschoorn U.E., Lin Z., Pavlides S., Whitaker-Menezes D., Pestell R.G., Howell A., Sotgia F. Hydrogen peroxide fuels aging, inflammation, cancer metabolism and metastasis: the seed and soil also needs "fertilizer". Cell Cycle 2011, 10:2440-2449.
29. Coghlin C., Murray G.I. Current and emerging concepts in tumour metastasis. J. Pathol. 2010, 222:1-15.
30. Paget S. The distribution of secondary growths in cancer of the breast. Cancer Metast. Rev. 1889, 8(1989):98-101.
31. Solinas G., Marchesi F., Garlanda C., Mantovani A., Allavena P. Inflammation-mediated promotion of invasion and metastasis. Cancer Metastasis Rev. 2010, 29:243-248.
32. Redon C.E., Dickey J.S., Nakamura A.J., Kareva I.G., Naf D., Nowsheen S., Kryston T.B., Bonner W.M., Georgakilas A.G., Sedelnikova O.A. Tumors induce complex DNA damage in distant proliferative tissues in vivo. Proc. Nat. Acad. Sci. USA 2010, 107:17992-17997.
33. Burdak-Rothkamm S., Rothkamm K., Prise K.M. ATM acts downstream of ATR in the DNA damage response signaling of bystander cells. Cancer Res. 2008, 68:7059-7065.
34. Dickey J.S., Baird B.J., Redon C.E., Avdoshina V., Palchik G., Wu J., Kondratyev A., Bonner W.M., Martin O.A. Susceptibility to bystander DNA damage is influenced by replication and transcriptional activity. Nucleic Acids Res. 2012, 40:10274-10286.
35. E.J. Hall, A.J. Giaccia, Radiobiol. Radiol., LWW, 2012.
36. Nobler M.P. The abscopal effect in malignant lymphoma and its relationship to lymphocyte circulation. Radiology 1969, 93:410-412.
37. Morgan G., Breit S. Radiation and the lung: a re-evaluation of the mechanisms mediating pulmonary injury. Int. J. Radiat. Oncol. Biol. Phys. 1994, 30(Suppl. 1):161.
38. J.G. Hollowell, L.G. Littlefield, Chromosome damage induced by plasma of X-rayed patients an indirect effect of X-ray, in: Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine (New York, NY), Royal Society of Medicine, 1968, pp. 240-244.
39. Emerit I. Reactive oxygen species, chromosome mutation, and cancer: possible role of clastogenic factors in carcinogenesis. Free Radical Biol. Med. 1994, 16:99-109.
40. V. Moiseenko, J. Van Dyk, J. Battista, E. Travis, Limitations in using dose-volume histograms for radiotherapy dose optimization, in: The Use of Computers in Radiation Therapy, Springer, 2000, pp. 239-241.
41. Bower J.E., Ganz P.A., Tao M.L., Hu W., Belin T.R., Sepah S., Cole S., Aziz N. Inflammatory biomarkers and fatigue during radiation therapy for breast and prostate cancer. Clin. Cancer Res. 2009, 15:5534-5540.
42. Schubert C., Hong S., Natarajan L., Mills P.J., Dimsdale J.E. The association between fatigue and inflammatory marker levels in cancer patients: a quantitative review. Brain Behav. Immun. 2007, 21:413.
43. Kaminski J.M., Shinohara E., Summers J.B., Niermann K.J., Morimoto A., Brousal J. The controversial abscopal effect. Cancer Treat. Rev. 2005, 31:159-172.
44. Doweck I., Robbins K.T., Vieira F. Analysis of risk factors predictive of distant failure after targeted chemoradiation for advanced head and neck cancer. Arch. Otolaryngol. - Head Neck Surg. 2001, 127:1315-1318.
45. MacManus M.R., Hicks R., Fisher R., Rischin D., Michael M., Wirth A., Ball D.L. FDG-PET-detected extracranial metastasis in patients with non-small cell lung cancer undergoing staging for surgery or radical radiotherapy-survival correlates with metastatic disease burden. Acta Oncol. 2003, 42:48-54.
46. Mac Manus M.P., Hicks R.J., Matthews J.P., Wirth A., Rischin D., Ball D.L. Metabolic (FDG-PET) response after radical radiotherapy/chemoradiotherapy for non-small cell lung cancer correlates with patterns of failure. Lung Cancer 2005, 49:95-108.
47. Hall E.J. Intensity-modulated radiation therapy, protons, and the risk of second cancers. Int. J. Radiat. Oncol. Biol. Phys. 2006, 65:1-7.
48. Prise K.M., O'Sullivan J.M. Radiation-induced bystander signalling in cancer therapy. Nat. Rev. Cancer 2009, 9:351-360.
49. Hei T.K., Zhou H., Chai Y., Ponnaiya B., Ivanov V.N. Radiation induced non-targeted response: mechanism and potential clinical implications. Curr. Mol. Pharmacol. 2011, 4:96-105.
50. Bostrom P.J., Soloway M.S. Secondary cancer after radiotherapy for prostate cancer: should we be more aware of the risk?. Eur. Urol. 2007, 52:973-982.
51. Hussain S.P., Hofseth L.J., Harris C.C. Radical causes of cancer. Nat. Rev. Cancer 2003, 3:276-285.
52. Hamada N., Maeda M., Otsuka K., Tomita M. Signaling pathways underpinning the manifestations of ionizing radiation-induced bystander effects. Curr. Mol. Pharmacol. 2011, 4:79-95.
53. Schaue D., Ratikan J.A., Iwamoto K.S., McBride W.H. Maximizing tumor immunity with fractionated radiation. Int. J. Radiat. Oncol. Biol. Phys. 2011.
54. Verbrugge I., Hagekyriakou J., Sharp L.L., Galli M., West A., McLaughlin N.M., Duret H., Yagita H., Johnstone R.W., Smyth M.J., Haynes N.M. Radiotherapy increases the permissiveness of established mammary tumors to rejection by immunomodulatory antibodies. Cancer Res. 2012, 72:3163-3174.
55. Finkelstein S.E., Timmerman R., McBride W.H., Schaue D., Hoffe S.E., Mantz C.A., Wilson G.D. The confluence of stereotactic ablative radiotherapy and tumor immunology. Clin. Dev. Immunol. 2011.
56. Park H.J., Griffin R.J., Hui S., Levitt S.H., Song C.W. Radiation-induced vascular damage in tumors: implications of vascular damage in ablative hypofractionated radiotherapy (SBRT and SRS). Radiat. Res. 2012, 177:311-327.
57. Fuks Z., Kolesnick R. Engaging the vascular component of the tumor response. Cancer Cell 2005, 8:89-91.
58. Lee Y., Auh S.L., Wang Y., Burnette B., Wang Y., Meng Y., Beckett M., Sharma R., Chin R., Tu T. Therapeutic effects of ablative radiation on local tumor require CD8+ T cells: changing strategies for cancer treatment. Blood 2009, 114:589-595.
59. 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.
60. Dewan M.Z., Galloway A.E., Kawashima N., Dewyngaert J.K., Babb J.S., Formenti S.C., Demaria S. Fractionated but not single-dose radiotherapy induces an immune-mediated abscopal effect when combined with anti-CTLA-4 antibody. Clin. Cancer Res.: Official J. Am. Assoc. Cancer Res. 2009, 15:5379-5388.
61. Diallo I., Haddy N., Adjadj E., Samand A., Quiniou E., Chavaudra J., Alziar I., Perret N., Guerin S., Lefkopoulos D., de Vathaire F. Frequency distribution of second solid cancer locations in relation to the irradiated volume among 115 patients treated for childhood cancer. Int. J. Radiat. Oncol. Biol. Phys. 2009, 74:876-883.
62. Formenti S.C., Demaria S. Systemic effects of local radiotherapy. Lancet Oncol. 2009, 10:718-726.
63. Sokolov M.V., Smilenov L.B., Hall E.J., Panyutin I.G., Bonner W.M., Sedelnikova O.A. Ionizing radiation induces DNA double-strand breaks in bystander primary human fibroblasts. Oncogene 2005, 24:7257-7265.
64. Smilenov L.B., Hall E.J., Bonner W.M., Sedelnikova O.A. A microbeam study of DNA double-strand breaks in bystander primary human fibroblasts. Radiat. Prot. Dosimetry. 2006, 122:256-259.
65. 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.
66. K. Shiraishi, abscopal effect of radiation therapy: current concepts and future applications, modern practices in radiation therapy, in: Gopishankar Natanasabapathi (Ed.), Modern Practices in Radiation Therapy, InTech ISBN: 978-953-51-0427-8, 2012, pp. 275-288.
67. Shiraishi K., Nakagawa K., Niibe Y., Ishiwata Y., Yokochi S., Ohtomo K., Matsushima K. Abscopal effect of radiation therapy and signal transduction. Curr. Signal Transduct. Ther. 2010, 5:212-222.
68. Ilnytskyy Y., Kovalchuk O. Non-targeted radiation effects-an epigenetic connection. Mutat. Res. 2011, 714:113-125.
69. Chai Y., Hei T.K. Radiation induced bystander effect in vivo. Acta Med. Nagasakiensia 2008, 53:S65-S69.
70. Kovalchuk O., Baulch J.E. Epigenetic changes and nontargeted radiation effects - is there a link?. Environ. Mol. Mutagen. 2008, 49:16-25.
71. Shiraishi K., Ishiwata Y., Nakagawa K., Yokochi S., Taruki C., Akuta T., Ohtomo K., Matsushima K., Tamatani T., Kanegasaki S. Enhancement of antitumor radiation efficacy and consistent induction of the abscopal effect in mice by ECI301, an active variant of macrophage inflammatory protein-1alpha. Clin. Cancer Res.: Official J. Am. Assoc. Cancer Res. 2008, 14:1159-1166.
72. Camphausen K., Moses M.A., Beecken W.D., Khan M.K., Folkman J., O'Reilly M.S. Radiation therapy to a primary tumor accelerates metastatic growth in mice. Cancer Res. 2001, 61:2207-2211.
73. Yasuda K., Nirei T., Tsuno N.H., Nagawa H., Kitayama J. Intratumoral injection of interleukin-2 augments the local and abscopal effects of radiotherapy in murine rectal cancer. Cancer Sci. 2011, 102:1257-1263.
74. Ludgate C.M. Optimizing cancer treatments to induce an acute immune response: radiation Abscopal effects, PAMPs, and DAMPs. Clin. Cancer Res.: Official J. Am. Assoc. Cancer Res. 2012, 18:4522-4525.
75. Mothersill C., Seymour C.B. Radiation-induced bystander effects - implications for cancer. Nat. Rev. Cancer 2004, 4:158-164.
76. Matsumoto H., Tomita M., Otsuka K., Hatashita M., Hamada N. Nitric oxide is a key molecule serving as a bridge between radiation-induced bystander and adaptive responses. Curr. Mol. Pharmacol. 2011, 4:126-134.
77. Morgan W.F. Communicating non-targeted effects of ionizing radiation to achieve adaptive homeostasis in tissues. Curr. Mol. Pharmacol. 2011, 4:135-140.
78. Mothersill C., Seymour C. Radiation-induced bystander and other non-targeted effects: novel intervention points in cancer therapy?. Curr. Cancer Drug Targets 2006, 6:447-454.
79. Koturbash I., Zemp F.J., Pogribny I., Kovalchuk O. Small molecules with big effects: the role of the microRNAome in cancer and carcinogenesis. Mutat. Res. 2011, 722:94-105.
80. Okunieff P., Cornelison T., Mester M., Liu W., Ding I., Chen Y., Zhang H., Williams J.P., Finkelstein J. Mechanism and modification of gastrointestinal soft tissue response to radiation: role of growth factors. Int. J. Radiat. Oncol. Biol. Phys. 2005, 62:273-278.
81. Polistena A., Johnson L.B., Ohiami-Masseron S., Wittgren L., Back S., Thornberg C., Gadaleanu V., Adawi D., Jeppsson B. Local radiotherapy of exposed murine small bowel: apoptosis and inflammation. BMC Surg. 2008, 8:1.
82. Xanthinaki A., Nicolatou-Galitis O., Athanassiadou P., Gonidi M., Kouloulias V., Sotiropoulou-Lontou A., Pissakas G., Kyprianou K., Kouvaris J., Patsouris E. Apoptotic and inflammation markers in oral mucositis in head and neck cancer patients receiving radiotherapy: preliminary report. Support. Care Cancer 2008, 16:1025-1033.
83. Khan M.A., Van Dyk J., Yeung I.W., Hill R.P. Partial volume rat lung irradiation; assessment of early DNA damage in different lung regions and effect of radical scavengers. Radiother. Oncol. 2003, 66:95-102.
84. Calveley V.L., Khan M.A., Yeung I.W., Vandyk J., Hill R.P. Partial volume rat lung irradiation: temporal fluctuations of in-field and out-of-field DNA damage and inflammatory cytokines following irradiation. Int. J. Radiat. Biol. 2005, 81:887-899.
85. Kryston T.B., Georgiev A.B., Pissis P., Georgakilas A.G. Role of oxidative stress and DNA damage in human carcinogenesis. Mutat. Res. 2011, 711:193-201.
86. Nowsheen S., Aziz K., Kryston T.B., Ferguson N.F., Georgakilas A. The interplay between inflammation and oxidative stress in carcinogenesis. Curr. Mol. Med. 2012, 12:672-680.
87. Sedelnikova O.A., Redon C.E., Dickey J.S., Nakamura A.J., Georgakilas A.G., Bonner W.M. Role of oxidatively induced DNA lesions in human pathogenesis. Mutat. Res. 2010, 704:152-159.
88. Frenkel K. Carcinogen-mediated oxidant formation and oxidative DNA damage. Pharmacol. Ther. 1992, 53:127-166.
89. 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.
90. Schmid T.E., Multhoff G. Non-targeted effects of photon and particle irradiation and the interaction with the immune system. Front. Oncol. 2012, 2:80.
91. Wratten C., Kilmurray J., Nash S., Seldon M., Hamilton C.S., O'Brien P.C., Denham J. Fatigue during breast radiotherapy and its relationship to biological factors. Int. J. Radiat. Oncol. Biol. Phys. 2004, 59:160-167.
92. Greenberg D.B., Gray J.L., Mannix C.M., Eisenthal S., Carey M. Treatment-related fatigue and serum interleukin-1 levels in patients during external beam irradiation for prostate cancer. J. Pain Symptom Manage. 1993, 8:196-200.
93. Geinitz H., Zimmermann F.B., Stoll P., Thamm R., Kaffenberger W., Ansorg K., Keller M., Busch R., van Beuningen D., Molls M. Fatigue, serum cytokine levels, and blood cell counts during radiotherapy of patients with breast cancer. Int. J. Radiat. Oncol. Biol. Phys. 2001, 51:691.
94. Ahlberg K., Ekman T., Gaston-Johansson F. Levels of fatigue compared to levels of cytokines and hemoglobin during pelvic radiotherapy: a pilot study. Biol. Res. Nurs. 2004, 5:203-210.
95. Melief C.J. Cancer immunotherapy by dendritic cells. Immunity 2008, 29:372-383.
96. Trikha M., Corringham R., Klein B., Rossi J.-F. Targeted anti-interleukin-6 monoclonal antibody therapy for cancer a review of the rationale and clinical evidence. Clin. Cancer Res. 2003, 9:4653-4665.
97. Matzinger P. Tolerance, danger, and the extended family. Annu. Rev. Immunol. 1994, 12:991-1045.
98. Matzinger P. The danger model: a renewed sense of self. Sci. Signall. 2002, 296:301.
99. Obeid M., Tesniere A., Ghiringhelli F., Fimia G.M., Apetoh L., Perfettini J.L., Castedo M., Mignot G., Panaretakis T., Casares N. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med. 2006, 13:54-61.
100. Apetoh L., Ghiringhelli F., Tesniere A., Obeid M., Ortiz C., Criollo A., Mignot G., Maiuri M.C., Ullrich E., Saulnier P. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat. Med. 2007, 13:1050-1059.
101. Ghiringhelli F., Apetoh L., Tesniere A., Aymeric L., Ma Y., Ortiz C., Vermaelen K., Panaretakis T., Mignot G., Ullrich E., Perfettini J.L., Schlemmer F., Tasdemir E., Uhl M., Genin P., Civas A., Ryffel B., Kanellopoulos J., Tschopp J., Andre F., Lidereau R., McLaughlin N.M., Haynes N.M., Smyth M.J., Kroemer G., Zitvogel L. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat. Med. 2009, 15:1170-1178.
102. Chakraborty M., Abrams S.I., Coleman C.N., Camphausen K., Schlom J., Hodge J.W. External beam radiation of tumors alters phenotype of tumor cells to render them susceptible to vaccine-mediated T-cell killing. Cancer Res. 2004, 64:4328-4337.
103. Lugade A.A., Sorensen E.W., Gerber S.A., Moran J.P., Frelinger J.G., Lord E.M. Radiation-induced IFN-γ production within the tumor microenvironment influences antitumor immunity. J. Immunol. 2008, 180:3132-3139.
104. Wynn T.A., Chawla A., Pollard J.W. Macrophage biology in development, homeostasis and disease. Nature 2013, 496:445-455.
105. Mukherjee D., Coates P.J., Rastogi S., Lorimore S.A., Wright E.G. Radiation-induced bone marrow apoptosis, inflammatory bystander-type signaling and tissue cytotoxicity. Int. J. Radiat. Biol. 2013, 89:139-146.
106. Lorimore S.A., Chrystal J.A., Robinson J.I., Coates P.J., Wright E.G. Chromosomal instability in unirradiated hemaopoietic cells induced by macrophages exposed in vivo to ionizing radiation. Cancer Res. 2008, 68:8122-8126.
107. Lorimore S.A., Mukherjee D., Robinson J.I., Chrystal J.A., Wright E.G. Long-lived inflammatory signaling in irradiated bone marrow is genome dependent. Cancer Res. 2011, 71:6485-6491.
108. Fehsel K., Kolb-Bachofen V., Kolb H. Analysis of TNF alpha-induced DNA strand breaks at the single cell level. Am. J. Pathol. 1991, 139:251-254.
109. Vassalli P. The pathophysiology of tumor necrosis factors. Annu. Rev. Immunol. 1992, 10:411-452.
110. Lorimore S.A., Coates P.J., Scobie G.E., Milne G., Wright E.G. Inflammatory-type responses after exposure to ionizing radiation in vivo: a mechanism for radiation-induced bystander effects?. Oncogene 2001, 20:7085-7095.
111. Byhardt R.W., Brace K.C., Wiernik P.H. The role of splenic irradiation in chronic lymphocytic leukemia. Cancer 1975, 35:1621-1625.
112. Li J.G. The leukocytopenic effect of focal splenic X-irradiation in leukemic patients. Radiology 1963, 80:471-476.
113. Rees G. Abscopal regression in lymphoma: a mechanism in common with total body irradiation?. Clin. Radiol. 1981, 32:475-480.
114. Mothersill C., Seymour C. Radiation-induced bystander effects: are they good, bad or both?. Medicine Conflict Survival 2005, 21:101-110.
115. Sedelnikova O.A., Bonner W.M. GammaH2AX in cancer cells: a potential biomarker for cancer diagnostics, prediction and recurrence. Cell Cycle 2006, 5:2909-2913.
116. Nakamura A.J., Redon C.E., Bonner W.M., Sedelnikova O.A. Telomere-dependent and telomere-independent origins of endogenous DNA damage in tumor cells. Aging 2009, 1:212-218.
117. Nakamura A.J., Redon C.E., Bonner W.M. GammaH2AX: applications for the evaluation of telomerase-based cancer therapy. Cell Cycle 2010, 9:3385-3386.
118. L.A. Pollack, J. Li, Z. Berkowitz, H.K. Weir, X.-C. Wu, U.A. Ajani, D.U. Ekwueme, C. Li, B.P. Pollack, Melanoma survival in the United States, 1992 to 2005, Journal of the American Academy of Dermatology 65 (2011) S78. e71-S78. e10.
119. Chapman P.B., Hauschild A., Robert C., Haanen J.B., Ascierto P., Larkin J., Dummer R., Garbe C., Testori A., Maio M. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N. Engl. J. Med. 2011, 364:2507-2516.
120. Garbe C., Eigentler T.K., Keilholz U., Hauschild A., Kirkwood J.M. Systematic review of medical treatment in melanoma: current status and future prospects. Oncologist 2011, 16:5-24.
121. Khan M.K., Khan N., Almasan A., Macklis R. Future of radiation therapy for malignant melanoma in an era of newer, more effective biological agents. Onco Targets Therapy 2011, 4:137.
122. Postow M.A., Callahan M.K., Barker C.A., Yamada Y., Yuan J., Kitano S., Mu Z., Rasalan T., Adamow M., Ritter E. Immunologic correlates of the abscopal effect in a patient with melanoma. N. Engl. J. Med. 2012, 366:925-931.
123. Stamell E.F., Wolchok J.D., Gnjatic S., Lee N.Y., Brownell I. The abscopal effect associated with a systemic anti-melanoma immune response. Int. J. Radiat. Oncol. Biol. Phys. 2012.
124. Okwan-Duodu D., Pollack B.P., Lawson D., Khan M.K. Role of radiation therapy as immune activator in the era of modern immunotherapy for metastatic malignant melanoma. Am. J. Clin. Oncol. 2013.