The tumor-immune microenvironment and response to radiation therapy

Journal of Mammary Gland Biology and Neoplasia

Volumn 15, Issue 4, 2010, Pages 411-421

  Shiao, Stephen L ^a   Coussens, Lisa M ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cancer; Immune cell; Inflammation; Leukocytes; Radiation therapy

Indexed keywords

ANTHRACYCLINE; CANCER ANTIBODY; CELL ADHESION MOLECULE; CYTOKINE; IMATINIB; TAXANE DERIVATIVE;

CANCER CELL; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER RADIOTHERAPY; CELL DEATH; CELLULAR STRESS RESPONSE; CYTOTOXICITY; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; NONHUMAN; REVIEW; TREATMENT RESPONSE; TUMOR; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT;

ANIMALS; BREAST NEOPLASMS; FEMALE; HUMANS; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 79952537676     PISSN: 10833021     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10911-010-9194-9     Document Type: Review

References (132)

1. Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? Lancet. 2001;357(9255):539-45.
2. de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer. 2006;6:24-37. (Pubitemid 43053650)
3. Bui JD, Schreiber RD. Cancer immunosurveillance, immunoediting and inflammation: independent or interdependent processes? Curr Opin Immunol. 2007;19(2):203-8.
4. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature. 2008;454(7203):436-44.
5. Zitvogel L, Apetoh L, Ghiringhelli F, Kroemer G. Immunological aspects of cancer chemotherapy. Nat Rev Immunol. 2008;8 (1):59-73.
6. Formenti SC, Demaria S. Systemic effects of local radiotherapy. Lancet Oncol. 2009;10(7):718-26.
7. Harris J, Part G. Breast cancer. Overview. In: Gunderson L, Tepper J, editors. Clinical radiation oncology. 2nd ed. Philadelphia: Elsevier Churchill Livingstone; 2007.
8. Locher C, Conforti R, Aymeric L, et al. Desirable cell death during anticancer chemotherapy. Ann NYAcad Sci. 2010;1209(1):99-108.
9. Tesniere A, Apetoh L, Ghiringhelli F, et al. Immunogenic cancer cell death: a key-lock paradigm. Curr Opin Immunol. 2008;20 (5):504-11.
10. Haynes NM, van der Most RG, Lake RA, Smyth MJ. Immunogenic anti-cancer chemotherapy as an emerging concept. Curr Opin Immunol. 2008;20(5):545-57.
11. Apetoh L, Ghiringhelli F, Tesniere A, et al. Toll-like receptor 4- dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med. 2007;13(9):1050-9. (Pubitemid 47517504)
12. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100(1):57-70. (Pubitemid 30046295)
13. Laconi E, Doratiotto S, Vineis P. The microenvironments of multistage carcinogenesis. Semin Cancer Biol. 2008;18(5):322-9.
14. Coronella JA, Telleman P, Kingsbury GA, Truong TD, Hays S, Junghans RP. Evidence for an antigen-driven humoral immune response in medullary ductal breast cancer. Cancer Res. 2001;61 (21):7889-99. (Pubitemid 33050986)
15. Punt CJ, Barbuto JA, Zhang H, Grimes WJ, Hatch KD, Hersh EM. Anti-tumor antibody produced by human tumor-infiltrating and peripheral blood B lymphocytes. Cancer Immunol Immunother. 1994;38(4):225-32. (Pubitemid 24108733)
16. Coronella-Wood JA, Hersh EM. Naturally occurring B-cell responses to breast cancer. Cancer Immunol Immunother. 2003;52(12):715-38. (Pubitemid 37491701)
17. Shimokawara I, Imamura M, Yamanaka N, Ishii Y, Kikuchi K. Identification of lymphocyte subpopulations in human breast cancer tissue and its significance: an immunoperoxidase study with anti-human T- and B-cell sera. Cancer. 1982;49 (7):1456-64. (Pubitemid 12143070)
18. Fernandez Madrid F. Autoantibodies in breast cancer sera: candidate biomarkers and reporters of tumorigenesis. Cancer Lett. 2005;230(2):187-98. (Pubitemid 41612462)
19. Lee YT, Sheikh KM, Quismorio Jr FP, Friou GJ. Circulating antitumor and autoantibodies in breast carcinoma: relationship to stage and prognosis. Breast Cancer Res Treat. 1985;6(1):57-65. (Pubitemid 15241230)
20. Chin Y, Janseens J, Vandepitte J, Vandenbrande J, Opdebeek L, Raus J. Phenotypic analysis of tumor-infiltrating lymphocytes from human breast cancer. Anticancer Res. 1992;12 (5):1463-6.
21. Kohrt HE, Nouri N, Nowels K, Johnson D, Holmes S, Lee PP. Profile of immune cells in axillary lymph nodes predicts diseasefree survival in breast cancer. PLoS Med. 2005;2(9):e284.
22. Bates GJ, Fox SB, Han C, et al. Quantification of regulatory T cells enables the identification of high-risk breast cancer patients and those at risk of late relapse. J Clin Oncol. 2006;24(34):5373-80. (Pubitemid 46623168)
23. Denkert C, Loibl S, Noske A, et al. Tumor-associated lymphocytes as an independent predictor of response to neoadjuvant chemotherapy in breast cancer. J Clin Oncol. 2010;28(1):105-13.
24. Tsutsui S, Yasuda K, Suzuki K, Tahara K, Higashi H, Era S. Macrophage infiltration and its prognostic implications in breast cancer: the relationship with VEGF expression and microvessel density. Oncol Rep. 2005;14(2):425-31.
25. Steidl C, Lee T, Shah SP, et al. Tumor-associated macrophages and survival in classic Hodgkin's lymphoma. N Engl J Med. 2010;362(10):875-85.
26. Bolat F, Kayaselcuk F, Nursal TZ, Yagmurdur MC, Bal N, Demirhan B. Microvessel density, VEGF expression, and tumor-associated macrophages in breast tumors: correlations with prognostic parameters. J Exp Clin Cancer Res. 2006;25 (3):365-72. (Pubitemid 44763728)
27. Chen JJ, Lin YC, Yao PL, et al. Tumor-associated macrophages: the double-edged sword in cancer progression. J Clin Oncol. 2005;23(5):953-64. (Pubitemid 46202315)
28. Zhang J, Patel L, Pienta KJ. CC chemokine ligand 2 (CCL2) promotes prostate cancer tumorigenesis and metastasis. Cytokine Growth Factor Rev. 2010;21(1):41-8.
29. Campbell MJ, Tonlaar NY, Garwood ER, et al. Proliferating macrophages associated with high grade, hormone receptor negative breast cancer and poor clinical outcome. Breast Cancer Res Treat. Sep 15 2010.
30. Kawai O, Ishii G, Kubota K, et al. Predominant infiltration of macrophages and CD8(+) T Cells in cancer nests is a significant predictor of survival in stage IV nonsmall cell lung cancer. Cancer. 2008;113(6):1387-95.
31. Mantovani A, Sica A, Locati M. New vistas on macrophage differentiation and activation. Eur J Immunol. 2007;37(1):14-6. (Pubitemid 46128780)
32. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol. 2008;8(12):958-69.
33. Mantovani A, Allavena P, Sica A. Tumour-associated macrophages as a prototypic type II polarised phagocyte population: role in tumour progression. Eur J Cancer. 2004;40(11):1660-7. (Pubitemid 38902900)
34. Ruffell B, Denardo DG, Affara NI, Coussens LM. Lymphocytes in cancer development: Polarization towards pro-tumor immunity. Cytokine Growth Factor Rev. 2010;21:3-10.
35. Appelbaum FR. The influence of total dose, fractionation, dose rate, and distribution of total body irradiation on bone marrow transplantation. Semin Oncol. 1993;20(4 Suppl 4):3-10. quiz 11.
36. Strasser A, Jost PJ, Nagata S. The many roles of FAS receptor signaling in the immune system. Immunity. 2009;30(2):180-92.
37. Lavin MF. Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer. Nat Rev Mol Cell Biol. 2008;9(10):759-69.
38. Wu ZH, Miyamoto S. Many faces of NF-kappaB signaling induced by genotoxic stress. J Mol Med. 2007;85(11):1187-202. (Pubitemid 47622222)
39. Rashi-Elkeles S, Elkon R, Weizman N, et al. Parallel induction of ATM-dependent pro- and antiapoptotic signals in response to ionizing radiation in murine lymphoid tissue. Oncogene. 2006;25 (10):1584-92. (Pubitemid 43361943)
40. Li N, Karin M. Ionizing radiation and short wavelength UV activate NF-kappaB through two distinct mechanisms. Proc Natl Acad Sci USA. 1998;95(22):13012-7. (Pubitemid 28509515)
41. Shakhov AN, Collart MA, Vassalli P, Nedospasov SA, Jongeneel CV. Kappa B-type enhancers are involved in lipopolysaccharide-mediated transcriptional activation of the tumor necrosis factor alpha gene in primary macrophages. J Exp Med. 1990;171 (1):35-47. (Pubitemid 20040597)
42. Mori N, Prager D. Transactivation of the interleukin-1alpha promoter by human T-cell leukemia virus type I and type II Tax proteins. Blood. 1996;87(8):3410-7. (Pubitemid 26115373)
43. Wickremasinghe MI, Thomas LH, O'Kane CM, Uddin J, Friedland JS. Transcriptional mechanisms regulating alveolar epithelial cell-specific CCL5 secretion in pulmonary tuberculosis. J Biol Chem. 2004;279(26):27199-210. (Pubitemid 38812557)
44. Caldenhoven E, Coffer P, Yuan J, et al. Stimulation of the human intercellular adhesion molecule-1 promoter by interleukin-6 and interferon-gamma involves binding of distinct factors to a palindromic response element. J Biol Chem. 1994;269 (33):21146-54. (Pubitemid 24266488)
45. van de Stolpe A, Caldenhoven E, Stade BG, et al. 12-O- tetradecanoylphorbol- 13-acetate- and tumor necrosis factor alpha-mediated induction of intercellular adhesion molecule-1 is inhibited by dexamethasone. Functional analysis of the human intercellular adhesion molecular-1 promoter. J Biol Chem. 1994;269(8):6185-92.
46. Schindler U, Baichwal VR. Three NF-kappa B binding sites in the human E-selectin gene required for maximal tumor necrosis factor alpha-induced expression. Mol Cell Biol. 1994;14(9):5820-31.
47. Iademarco MF, McQuillan JJ, Rosen GD, Dean DC. Characterization of the promoter for vascular cell adhesion molecule-1 (VCAM-1). J Biol Chem. 1992;267(23):16323-9.
48. Johnson DR, Pober JS. HLA class I heavy-chain gene promoter elements mediating synergy between tumor necrosis factor and interferons. Mol Cell Biol. 1994;14(2):1322-32. (Pubitemid 24036582)
49. Lawrence T. The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb Perspect Biol. 2009;1(6): a001651.
50. Brach MA, Hass R, Sherman ML, Gunji H, Weichselbaum R, Kufe D. Ionizing radiation induces expression and binding activity of the nuclear factor kappa B. J Clin Invest. 1991;88 (2):691-5.
51. Criswell T, Leskov K, Miyamoto S, Luo G, Boothman DA. Transcription factors activated in mammalian cells after clinically relevant doses of ionizing radiation. Oncogene. 2003;22(37):5813-27. (Pubitemid 37176702)
52. Lee SJ, Dimtchev A, Lavin MF, Dritschilo A, Jung M. A novel ionizing radiation-induced signaling pathway that activates the transcription factor NF-kappaB. Oncogene. 1998;17(14):1821-6. (Pubitemid 28482785)
53. Germano G, Allavena P, Mantovani A. Cytokines as a key component of cancer-related inflammation. Cytokine. 2008;43 (3):374-9.
54. Balkwill F. Tumour necrosis factor and cancer. Nat Rev Cancer. 2009;9(5):361-71.
55. Hallahan DE, Spriggs DR, Beckett MA, Kufe DW, Weichselbaum RR. Increased tumor necrosis factor alpha mRNA after cellular exposure to ionizing radiation. Proc Natl Acad Sci USA. 1989;86(24):10104-7. (Pubitemid 20030785)
56. Baker WH, Limanni A, Chang CM, Jackson WE, Seemann R, Patchen ML. Comparison of interleukin-1 alpha gene expression and protein levels in the murine spleen after lethal and sublethal total-body irradiation. Radiat Res. 1995;143(3):320-6.
57. O'Brien-Ladner A, Nelson ME, Kimler BF, Wesselius LJ. Release of interleukin-1 by human alveolar macrophages after in vitro irradiation. Radiat Res. 1993;136(1):37-41. (Pubitemid 23342597)
58. Hong JH, Chiang CS, Tsao CY, Lin PY, McBride WH, Wu CJ. Rapid induction of cytokine gene expression in the lung after single and fractionated doses of radiation. Int J Radiat Biol. 1999;75(11):1421-7.
59. Okunieff P, Chen Y, Maguire DJ, Huser AK. Molecular markers of radiation-related normal tissue toxicity. Cancer Metastasis Rev. 2008;27(3):363-74.
60. Calveley VL, Khan MA, Yeung IW, Vandyk J, Hill RP. 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(12):887-99. (Pubitemid 43361946)
61. Pober JS, Sessa WC. Evolving functions of endothelial cells in inflammation. Nat Rev Immunol. 2007;7(10):803-15. (Pubitemid 47480307)
62. Hallahan D, Kuchibhotla J, Wyble C. Cell adhesion molecules mediate radiation-induced leukocyte adhesion to the vascular endothelium. Cancer Res. 1996;56(22):5150-5. (Pubitemid 26383029)
63. Ahn GO, Tseng D, Liao CH, Dorie MJ, Czechowicz A, Brown JM. Inhibition of Mac-1 (CD11b/CD18) enhances tumor response to radiation by reducing myeloid cell recruitment. Proc Natl Acad Sci USA. 2010;107(18):8363-8.
64. Handschel J, Prott FJ, 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(2):475-81. (Pubitemid 29408567)
65. 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(5):3132-9.
66. Matsumura S, Wang B, Kawashima N, et al. Radiation-induced CXCL16 release by breast cancer cells attracts effector T cells. J Immunol. 2008;181(5):3099-107.
67. 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(4):418-25.
68. Zong ZW, Cheng TM, Su YP, et al. Recruitment of transplanted dermal multipotent stem cells to sites of injury in rats with combined radiation and wound injury by interaction of SDF-1 and CXCR4. Radiat Res. 2008;170(4):444-50.
69. 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 (Pt 9):2426-35. (Pubitemid 44522127)
70. Kozin SV, Kamoun WS, Huang Y, Dawson MR, Jain RK, Duda DG. Recruitment of myeloid but not endothelial precursor cells facilitates tumor regrowth after local irradiation. Cancer Res. 2010;70(14):5679-85.
71. 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(12):7516-23. (Pubitemid 40806254)
72. Newcomb EW, Demaria S, Lukyanov Y, et al. The combination of ionizing radiation and peripheral vaccination produces longterm survival of mice bearing established invasive GL261 gliomas. Clin Cancer Res. 2006;12(15):4730-7. (Pubitemid 44297827)
73. Liao YP, Wang CC, Butterfield LH, et al. Ionizing radiation affects human MART-1 melanoma antigen processing and presentation by dendritic cells. J Immunol. 2004;173(4):2462-9. (Pubitemid 39063103)
74. Cao ZA, Daniel D, Hanahan D. Sub-lethal radiation enhances anti-tumor immunotherapy in a transgenic mouse model of pancreatic cancer. BMC Cancer. 2002;2:11.
75. 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(5):1259-71. (Pubitemid 43736595)
76. Galluzzi L, Maiuri MC, Vitale I, et al. Cell death modalities: classification and pathophysiological implications. Cell Death Differ. 2007;14(7):1237-43. (Pubitemid 46969863)
77. Kroemer G, Galluzzi L, Vandenabeele P, et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 2009;16(1):3-11.
78. Savill J, Dransfield I, Gregory C, Haslett C. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat Rev Immunol. 2002;2(12):965-75. (Pubitemid 37323217)
79. Obeid M, Tesniere A, Ghiringhelli F, et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med. 2007;13(1):54-61. (Pubitemid 46067386)
80. Perez CA, Fu A, Onishko H, Hallahan DE, Geng L. Radiation induces an antitumour immune response to mouse melanoma. Int J Radiat Biol. 2009;85(12):1126-36.
81. Obeid M, Panaretakis T, Joza N, et al. Calreticulin exposure is required for the immunogenicity of gamma-irradiation and UVC light-induced apoptosis. Cell Death Differ. 2007;14(10):1848-50. (Pubitemid 47423653)
82. Ghiringhelli F, Apetoh L, Tesniere A, et al. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat Med. 2009;15(10):1170-8.
83. Iwasaki A, Medzhitov R. Regulation of adaptive immunity by the innate immune system. Science. 2010;327(5963):291-5.
84. Merrick A, Errington F, Milward K, et al. Immunosuppressive effects of radiation on human dendritic cells: reduced IL-12 production on activation and impairment of naive T-cell priming. Br J Cancer. 2005;92(8):1450-8. (Pubitemid 40705012)
85. Moyer JS, Li J,Wei S, Teitz-Tennenbaum S, Chang AE. Intratumoral dendritic cells and chemoradiation for the treatment of murine squamous cell carcinoma. J Immunother. 2008;31(9):885-95.
86. Mantovani A, Sica A. Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr Opin Immunol. 2010;22(2):231-7.
87. Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420(6917):860-7. (Pubitemid 36019639)
88. Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell. 2010;141(1):39-51.
89. Lambert LE, Paulnock DM. Modulation of macrophage function by gamma-irradiation. Acquisition of the primed cell intermediate stage of the macrophage tumoricidal activation pathway. J Immunol. 1987;139(8):2834-41. (Pubitemid 17153968)
90. Shan YX, Jin SZ, Liu XD, Liu Y, Liu SZ. Ionizing radiation stimulates secretion of pro-inflammatory cytokines: dose-response relationship, mechanisms and implications. Radiat Environ Biophys. 2007;46(1):21-9. (Pubitemid 46354798)
91. Milas L, Wike J, Hunter N, Volpe J, Basic I. Macrophage content of murine sarcomas and carcinomas: associations with tumor growth parameters and tumor radiocurability. Cancer Res. 1987;47(4):1069-75. (Pubitemid 17027931)
92. Ahn GO, Brown JM. Matrix metalloproteinase-9 is required for tumor vasculogenesis but not for angiogenesis: role of bone marrow-derived myelomonocytic cells. Cancer Cell. 2008;13(3):193-205. (Pubitemid 351318369)
93. Meng Y, Beckett MA, Liang H, et al. Blockade of tumor necrosis factor alpha signaling in tumor-associated macrophages as a radiosensitizing strategy. Cancer Res. 2010;70(4):1534-43.
94. Tsai CS, Chen FH, Wang CC, et al. Macrophages from irradiated tumors express higher levels of iNOS, arginase-I and COX-2, and promote tumor growth. Int J Radiat Oncol Biol Phys. 2007;68(2):499-507.
95. Doedens AL, Stockmann C, Rubinstein MP, et al. Macrophage expression of HIF-1α suppresses T cell function and promotes tumor progression. Cancer Res. 2010;70:7465-75.
96. Orr MT, Lanier LL. Natural killer cell education and tolerance. Cell. 2010;142(6):847-56.
97. Kim JY, Son YO, Park SW, et al. Increase of NKG2D ligands and sensitivity to NK cell-mediated cytotoxicity of tumor cells by heat shock and ionizing radiation. Exp Mol Med. 2006;38 (5):474-84.
98. Gasser S, Orsulic S, Brown EJ, Raulet DH. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature. 2005;436(7054):1186-90. (Pubitemid 41232299)
99. Sherman M, Multhoff G. Heat shock proteins in cancer. Ann NY Acad Sci. 2007;1113:192-201. (Pubitemid 350015025)
100. Gehrmann M, Marienhagen J, Eichholtz-Wirth H, 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(1):38-51. (Pubitemid 40090027)
101. Porta C, Larghi P, Rimoldi M, et al. Cellular and molecular pathways linking inflammation and cancer. Immunobiology. 2009;214(9-10):761-77.
102. Heissig B, Rafii S, Akiyama H, et al. Low-dose irradiation promotes tissue revascularization through VEGF release from mast cells and MMP-9-mediated progenitor cell mobilization. J Exp Med. 2005;202(6):739-50. (Pubitemid 41345963)
103. Majori M, Poletti V, Curti A, Corradi M, Falcone F, Pesci A. Bronchoalveolar lavage in bronchiolitis obliterans organizing pneumonia primed by radiation therapy to the breast. J Allergy Clin Immunol. 2000;105(2 Pt 1):239-44. (Pubitemid 30109035)
104. Thomas DM, Fox J, Haston CK. Imatinib therapy reduces radiation-induced pulmonary mast cell influx and delays lung disease in the mouse. Int J Radiat Biol. 2010;86(6):436-44.
105. Sherbenou DW, Druker BJ. Applying the discovery of the Philadelphia chromosome. J Clin Invest. 2007;117(8):2067-74. (Pubitemid 47219546)
106. Gleixner KV, Rebuzzi L, Mayerhofer M, et al. Synergistic antiproliferative effects of KIT tyrosine kinase inhibitors on neoplastic canine mast cells. Exp Hematol. 2007;35(10):1510-21. (Pubitemid 47419130)
107. Oertel S, Krempien R, Lindel K, et al. Human glioblastoma and carcinoma xenograft tumors treated by combined radiation and imatinib (Gleevec). Strahlenther Onkol. 2006;182(7):400-7. (Pubitemid 44025008)
108. Demaria S, Ng B, Devitt ML, et al. Ionizing radiation inhibition of distant untreated tumors (abscopal effect) is immune mediated. Int J Radiat Oncol Biol Phys. 2004;58(3):862-70. (Pubitemid 38221143)
109. Gough MJ, Crittenden MR, Sarff M, et al. Adjuvant therapy with agonistic antibodies to CD134 (OX40) increases local control after surgical or radiation therapy of cancer in mice. J Immunother. 2010;33(8):798-809.
110. 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(3):589-95.
111. Takeshima T, Chamoto K, Wakita D, 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(7):2697-706.
112. Tabi Z, Spary LK, Coleman S, Clayton A, Mason MD, Staffurth J. Resistance of CD45RA- T cells to apoptosis and functional impairment, and activation of tumor-antigen specific T cells during radiation therapy of prostate cancer. J Immunol. 2010;185 (2):1330-9.
113. Rochman Y, Spolski R, Leonard WJ. New insights into the regulation of T cells by gamma(c) family cytokines. Nat Rev Immunol. 2009;9(7):480-90.
114. Lee J, Moran JP, Fenton BM, et al. Alteration of tumour response to radiation by interleukin-2 gene transfer. Br J Cancer. 2000;82 (4):937-44. (Pubitemid 30085249)
115. Yamini B, Yu X, Pytel P, et al. Adenovirally delivered tumor necrosis factor-alpha improves the antiglioma efficacy of concomitant radiation and temozolomide therapy. Clin Cancer Res. 2007;13(20):6217-23. (Pubitemid 350075083)
116. Lohr F, Hu K, Haroon Z, et al. Combination treatment of murine tumors by adenovirus-mediated local B7/IL12 immunotherapy and radiotherapy. Mol Ther. 2000;2(3):195-203.
117. Seetharam S, Staba MJ, Schumm LP, et al. Enhanced eradication of local and distant tumors by genetically produced interleukin- 12 and radiation. Int J Oncol. 1999;15(4):769-73.
118. AldinucciD,Olivo K, Lorenzon D, et al. The role of interleukin-3 in classical Hodgkin's disease. Leuk Lymphoma. 2005;46(3):303-11. (Pubitemid 40220389)
119. Oh YT, Chen DW, Dougherty GJ, McBride WH. Adenoviral interleukin-3 gene-radiation therapy for prostate cancer in mouse model. Int J Radiat Oncol Biol Phys. 2004;59(2):579-83. (Pubitemid 38622617)
120. Mason KA, Ariga H, Neal R, et al. Targeting toll-like receptor 9 with CpG oligodeoxynucleotides enhances tumor response to fractionated radiotherapy. Clin Cancer Res. 2005;11(1):361-9. (Pubitemid 40075816)
121. Driessens G, Kline J, Gajewski TF. Costimulatory and coinhibitory receptors in anti-tumor immunity. Immunol Rev. 2009;229(1):126-44.
122. Redmond WL, Ruby CE, Weinberg AD. The role of OX40- mediated co-stimulation in T-cell activation and survival. Crit Rev Immunol. 2009;29(3):187-201.
123. Chakraborty M, Abrams SI, Coleman CN, Camphausen K, Schlom J, Hodge JW. External beam radiation of tumors alters phenotype of tumor cells to render them susceptible to vaccine-mediated T-cell killing. Cancer Res. 2004;64(12):4328-37.
124. 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(2 Pt 1):728-34. (Pubitemid 40116901)
125. Pilones KA, Kawashima N, Yang AM, Babb JS, Formenti SC, Demaria S. Invariant natural killer T cells regulate breast cancer response to radiation and CTLA-4 blockade. Clin Cancer Res. 2009;15(2):597-606.
126. 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(17):5379-88.
127. Nesslinger NJ, Sahota RA, Stone B, et al. Standard treatments induce antigen-specific immune responses in prostate cancer. Clin Cancer Res. 2007;13(5):1493-502. (Pubitemid 46450440)
128. Roden AC, Moser MT, Tri SD, et al. Augmentation of T cell levels and responses induced by androgen deprivation. J Immunol. 2004;173(10):6098-108. (Pubitemid 39487766)
129. Johnke RM, Edwards JM, Kovacs CJ, et al. Response of T lymphocyte populations in prostate cancer patients undergoing radiotherapy: influence of neoajuvant total androgen suppression. Anticancer Res. 2005;25(4):3159-66. (Pubitemid 41044714)
130. Gulley JL, Arlen PM, Bastian A, et al. Combining a recombinant cancer vaccine with standard definitive radiotherapy in patients with localized prostate cancer. Clin Cancer Res. 2005;11 (9):3353-62. (Pubitemid 40627887)
131. Soiffer R, Lynch T, Mihm M, et al. Vaccination with irradiated autologous melanoma cells engineered to secrete human granulocyte-macrophage colony-stimulating factor generates potent antitumor immunity in patients with metastatic melanoma. Proc Natl Acad Sci USA. 1998;95(22):13141-6.
132. Chi KH, Liu SJ, Li CP, et al. Combination of conformal radiotherapy and intratumoral injection of adoptive dendritic cell immunotherapy in refractory hepatoma. J Immunother. 2005;28 (2):129-35.