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PMID: 16199306 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Review

Combining radiotherapy and immunotherapy: a revived partnership.

International journal of radiation oncology, biology, physics ·Vol. 63 ·No. 3 ·2005-11-01 ·Pages 655-66

Demaria S, Bhardwaj N, McBride WH, Formenti SC

Abstract

Ionizing radiation therapy (RT) is an important local modality for the treatment of cancer. The current rationale for its use is based largely on the ability of RT to kill the cancer cells by a direct cytotoxic effect. Nevertheless, considerable evidence indicates that RT effects extend beyond the mere elimination of the more radiosensitive fraction of cancer cells present within a tumor at the time of radiation exposure. For instance, a large body of evidence is accumulating on the ability of RT to modify the tumor microenvironment and generate inflammation. This might have far-reaching consequences regarding the response of a patient to treatment, especially if radiation-induced tumor cell kill were to translate into the generation of effective antitumor immunity. Although much remains to be learned about how radiation can impact tumor immunogenicity, data from preclinical studies provide the proof of principle that different immunotherapeutic strategies can be combined with RT to enhance antitumor effects. Conversely, RT could be a useful tool to combine with immunotherapy. This article will briefly summarize what is known about the impact of RT on tumor immunity, including tumor-associated antigens, antigen-presenting cells, and effector mechanisms. In addition, the experimental evidence supporting the contention that RT can be used as a tool to induce antitumor immunity is discussed, and a new approach to radioimmunotherapy of cancer is proposed.

MeSH Terms
Animals Antigen Presentation/immunology,radiation effects Antigens, CD Antigens, Differentiation/immunology Antigens, Neoplasm/immunology CTLA-4 Antigen Cancer Vaccines/therapeutic use Clinical Trials, Phase II as Topic Combined Modality Therapy Cytokines/therapeutic use Dendritic Cells/immunology Humans Immune System/radiation effects Immunotherapy/methods Lymphocyte Activation/immunology Mice Neoplasms/immunology,radiotherapy,therapy T-Lymphocytes/immunology
Chemicals
Antigens, CD Antigens, Differentiation Antigens, Neoplasm CTLA-4 Antigen CTLA4 protein, human Cancer Vaccines Ctla4 protein, mouse Cytokines
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Demaria Sandra
Department of Pathology, New York University School of Medicine, New York, NY 10016, USA.
Bhardwaj Nina
McBride William H
Formenti Silvia C
References (127)
127 references, click to expand
  1. Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance.
    Proc Natl Acad Sci U S A. 2002 Jan 8;99(1):351-8 PMID: 11773639
  2. Autologous dendritic cells transfected with prostate-specific antigen RNA stimulate CTL responses against metastatic prostate tumors.
    J Clin Invest. 2002 Feb;109(3):409-17 PMID: 11828001
  3. Tolerance to islet antigens and prevention from diabetes induced by limited apoptosis of pancreatic beta cells.
    Immunity. 2002 Feb;16(2):169-81 PMID: 11869679
  4. Combination of T-cell therapy and trigger of inflammation induces remodeling of the vasculature and tumor eradication.
    Cancer Res. 2002 Mar 1;62(5):1462-70 PMID: 11888921
  5. Local tumor irradiation augments the antitumor effect of cytokine-producing autologous cancer cell vaccines in a murine glioma model.
    Cancer Gene Ther. 2002 Jan;9(1):44-52 PMID: 11916244
  6. Irradiated tumor cell vaccine for treatment of an established glioma. I. Successful treatment with combined radiotherapy and cellular vaccination.
    Cancer Immunol Immunother. 2002 Jun;51(4):179-89 PMID: 12012105
  7. CTL: Caspases Terminate Life, but that's not the whole story.
    Tissue Antigens. 2002 Mar;59(3):175-83 PMID: 12074707
  8. CTLA-4: new insights into its biological function and use in tumor immunotherapy.
    Nat Immunol. 2002 Jul;3(7):611-8 PMID: 12087419
  9. Increased tumor necrosis factor alpha mRNA after cellular exposure to ionizing radiation.
    Proc Natl Acad Sci U S A. 1989 Dec;86(24):10104-7 PMID: 2602359
  10. Synergistic antitumor activity of tumor-infiltrating lymphocytes, interleukin 2, and local tumor irradiation. Studies on the mechanism of action.
    J Exp Med. 1990 Jan 1;171(1):249-63 PMID: 2295878
  11. Tumor eradication by adoptive transfer of cytotoxic T lymphocytes.
    Adv Cancer Res. 1992;58:143-75 PMID: 1532109
  12. Induction of the expression of the interleukin-1 beta gene in mouse spleen by ionizing radiation.
    Radiat Res. 1993 Mar;133(3):321-6 PMID: 8383862
  13. Cytotoxic T cells isolated from ovarian malignant ascites recognize a peptide derived from the HER-2/neu proto-oncogene.
    Cell Immunol. 1993 Oct 1;151(1):225-34 PMID: 7691418
  14. The effect of irradiation on expression of HLA class I antigens in human brain tumors in culture.
    J Neurosurg. 1994 Jun;80(6):1074-7 PMID: 8189262
  15. Tolerance, danger, and the extended family.
    Annu Rev Immunol. 1994;12:991-1045 PMID: 8011301
  16. Induction of acute phase gene expression by brain irradiation.
    Int J Radiat Oncol Biol Phys. 1995 Oct 15;33(3):619-26 PMID: 7558951
  17. MUC-1 epithelial tumor mucin-based immunity and cancer vaccines.
    Immunol Rev. 1995 Jun;145:61-89 PMID: 7590831
  18. Targeting p53 as a general tumor antigen.
    Proc Natl Acad Sci U S A. 1995 Dec 19;92(26):11993-7 PMID: 8618830
  19. Enhancement of antitumor immunity by CTLA-4 blockade.
    Science. 1996 Mar 22;271(5256):1734-6 PMID: 8596936
  20. Effects of irradiation on the expression of surface antigens in human ovarian cancer.
    Gynecol Oncol. 1996 Mar;60(3):468-74 PMID: 8774659
  21. Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells.
    Nat Med. 1996 Oct;2(10):1096-103 PMID: 8837607
  22. Cell adhesion molecules mediate radiation-induced leukocyte adhesion to the vascular endothelium.
    Cancer Res. 1996 Nov 15;56(22):5150-5 PMID: 8912850
  23. Dramatic increase in the numbers of functionally mature dendritic cells in Flt3 ligand-treated mice: multiple dendritic cell subpopulations identified.
    J Exp Med. 1996 Nov 1;184(5):1953-62 PMID: 8920882
  24. Flt3 ligand induces tumor regression and antitumor immune responses in vivo.
    Nat Med. 1997 Jun;3(6):625-31 PMID: 9176488
  25. Effects of IL-3 gene expression on tumor response to irradiation in vitro and in vivo.
    Cancer Res. 1997 Sep 15;57(18):3899-903 PMID: 9307268
  26. Enhanced induction of antitumor T-cell responses by cytotoxic T lymphocyte-associated molecule-4 blockade: the effect is manifested only at the restricted tumor-bearing stages.
    Cancer Res. 1997 Sep 15;57(18):4036-41 PMID: 9307290
  27. IL-3 in the clinic.
    Stem Cells. 1997;15(5):327-33 PMID: 9323793
  28. Prostaglandin E2 and tumor necrosis factor alpha cooperate to activate human dendritic cells: synergistic activation of interleukin 12 production.
    J Exp Med. 1997 Nov 3;186(9):1603-8 PMID: 9348319
  29. Up-regulation of Fas (CD95) in human p53wild-type cancer cells treated with ionizing radiation.
    Int J Cancer. 1997 Nov 27;73(5):757-62 PMID: 9398058
  30. Specific T helper cell requirement for optimal induction of cytotoxic T lymphocytes against major histocompatibility complex class II negative tumors.
    J Exp Med. 1998 Mar 2;187(5):693-702 PMID: 9480979
  31. CTLA-4 blockade synergizes with tumor-derived granulocyte-macrophage colony-stimulating factor for treatment of an experimental mammary carcinoma.
    Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):10067-71 PMID: 9707601
  32. Infusion of cytotoxic T cells for the prevention and treatment of Epstein-Barr virus-induced lymphoma in allogeneic transplant recipients.
    Blood. 1998 Sep 1;92(5):1549-55 PMID: 9716582
  33. Bystander apoptosis triggers dendritic cell maturation and antigen-presenting function.
    J Immunol. 1998 Nov 1;161(9):4467-71 PMID: 9794367
  34. Decreased antigen presentation by dendritic cells in patients with breast cancer.
    Clin Cancer Res. 1997 Mar;3(3):483-90 PMID: 9815709
  35. X-ray-induced P-selectin localization to the lumen of tumor blood vessels.
    Cancer Res. 1998 Nov 15;58(22):5216-20 PMID: 9823335
  36. Degradation of cell proteins and the generation of MHC class I-presented peptides.
    Annu Rev Immunol. 1999;17:739-79 PMID: 10358773
  37. Molecular mechanisms of ionizing radiation-induced apoptosis.
    Immunol Cell Biol. 1999 Jun;77(3):263-71 PMID: 10361259
  38. Accumulation of P-selectin in the lumen of irradiated blood vessels.
    Radiat Res. 1999 Jul;152(1):6-13 PMID: 10381836
  39. Natural adjuvants: endogenous activators of dendritic cells.
    Nat Med. 1999 Nov;5(11):1249-55 PMID: 10545990
  40. Induction of tumor immunity by removing CD25+CD4+ T cells: a common basis between tumor immunity and autoimmunity.
    J Immunol. 1999 Nov 15;163(10):5211-8 PMID: 10553041
  41. Rapid induction of cytokine gene expression in the lung after single and fractionated doses of radiation.
    Int J Radiat Biol. 1999 Nov;75(11):1421-7 PMID: 10597915
  42. Combination immunotherapy of primary prostate cancer in a transgenic mouse model using CTLA-4 blockade.
    Cancer Res. 2000 May 1;60(9):2444-8 PMID: 10811122
  43. Combining radiation therapy with interleukin-3 gene immunotherapy.
    Cancer Gene Ther. 2000 Aug;7(8):1172-8 PMID: 10975678
  44. Radiation induces upregulation of cyclooxygenase-2 (COX-2) protein in PC-3 cells.
    Int J Radiat Oncol Biol Phys. 2000 Sep 1;48(2):325-8 PMID: 10974444
  45. Combination treatment of murine tumors by adenovirus-mediated local B7/IL12 immunotherapy and radiotherapy.
    Mol Ther. 2000 Sep;2(3):195-203 PMID: 10985949
  46. Melanocyte destruction after antigen-specific immunotherapy of melanoma: direct evidence of t cell-mediated vitiligo.
    J Exp Med. 2000 Dec 4;192(11):1637-44 PMID: 11104805
  47. Cell injury releases endogenous adjuvants that stimulate cytotoxic T cell responses.
    Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14590-5 PMID: 11106387
  48. First-line, single-agent Herceptin(trastuzumab) in metastatic breast cancer: a preliminary report.
    Eur J Cancer. 2001 Jan;37 Suppl 1:S25-9 PMID: 11167088
  49. In vivo tracking of tumor-specific T cells.
    Curr Opin Immunol. 2001 Apr;13(2):141-6 PMID: 11228405
  50. Dendritic cells acquire antigens from live cells for cross-presentation to CTL.
    J Immunol. 2001 Mar 15;166(6):3717-23 PMID: 11238612
  51. The extra domain A of fibronectin activates Toll-like receptor 4.
    J Biol Chem. 2001 Mar 30;276(13):10229-33 PMID: 11150311
  52. Dendritic cells resurrect antigens from dead cells.
    Trends Immunol. 2001 Mar;22(3):141-8 PMID: 11286729
  53. Antigen-specific inhibition of effector T cell function in humans after injection of immature dendritic cells.
    J Exp Med. 2001 Jan 15;193(2):233-8 PMID: 11208863
  54. Cell-associated ovalbumin is cross-presented much more efficiently than soluble ovalbumin in vivo.
    J Immunol. 2001 May 15;166(10):6099-103 PMID: 11342628
  55. Immunity to oncogenic human papillomaviruses.
    Adv Cancer Res. 2001;82:205-38 PMID: 11447764
  56. Ionizing radiation as a response-enhancing agent for CD95-mediated apoptosis.
    Int J Cancer. 2001 Aug 20;96(4):213-20 PMID: 11474495
  57. Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4.
    J Immunol. 2001 Sep 1;167(5):2887-94 PMID: 11509636
  58. Tumor-specific responses in lymph nodes draining murine sarcomas are concentrated in cells expressing P-selectin binding sites.
    J Immunol. 2001 Sep 15;167(6):3089-98 PMID: 11544293
  59. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo.
    J Exp Med. 2001 Sep 17;194(6):769-79 PMID: 11560993
  60. Synergism of cytotoxic T lymphocyte-associated antigen 4 blockade and depletion of CD25(+) regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses.
    J Exp Med. 2001 Sep 17;194(6):823-32 PMID: 11560997
  61. Direct evidence that leukemic cells present HLA-associated immunogenic peptides derived from the BCR-ABL b3a2 fusion protein.
    Blood. 2001 Nov 15;98(10):2887-93 PMID: 11698267
  62. Comparative analysis of necrotic and apoptotic tumor cells as a source of antigen(s) in dendritic cell-based immunization.
    Cancer Res. 2001 Nov 15;61(22):8105-9 PMID: 11719436
  63. Efficiency of cross presentation of vaccinia virus-derived antigens by human dendritic cells.
    Eur J Immunol. 2001 Dec;31(12):3432-42 PMID: 11745362
  64. 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 Dec 15;94(6):825-33 PMID: 11745485
  65. Intratumoral administration of low doses of an adenovirus vector encoding tumor necrosis factor alpha together with naive dendritic cells elicits significant suppression of tumor growth without toxicity.
    Hum Gene Ther. 2001 Nov 20;12(17):2035-49 PMID: 11747595
  66. Oligosaccharides of Hyaluronan activate dendritic cells via toll-like receptor 4.
    J Exp Med. 2002 Jan 7;195(1):99-111 PMID: 11781369
  67. Immunogenicity of apoptotic cells in vivo: role of antigen load, antigen-presenting cells, and cytokines.
    J Immunol. 1999 Jul 1;163(1):130-6 PMID: 10384108
  68. Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor alpha) monoclonal antibody.
    Cancer Res. 1999 Jul 1;59(13):3128-33 PMID: 10397255
  69. Mechanisms of exogenous antigen presentation by MHC class I molecules in vitro and in vivo: implications for generating CD8+ T cell responses to infectious agents, tumors, transplants, and vaccines.
    Adv Immunol. 1999;73:1-77 PMID: 10399005
  70. Combination immunotherapy of B16 melanoma using anti-cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) and granulocyte/macrophage colony-stimulating factor (GM-CSF)-producing vaccines induces rejection of subcutaneous and metastatic tumors accompanied by autoimmune depigmentation.
    J Exp Med. 1999 Aug 2;190(3):355-66 PMID: 10430624
  71. Enhanced eradication of local and distant tumors by genetically produced interleukin-12 and radiation.
    Int J Oncol. 1999 Oct;15(4):769-73 PMID: 10493960
  72. Sublethal irradiation of human tumor cells modulates phenotype resulting in enhanced killing by cytotoxic T lymphocytes.
    Cancer Res. 2004 Nov 1;64(21):7985-94 PMID: 15520206
  73. Natural endogenous adjuvants.
    Springer Semin Immunopathol. 2005 Jan;26(3):231-46 PMID: 15609001
  74. A listing of human tumor antigens recognized by T cells: March 2004 update.
    Cancer Immunol Immunother. 2005 Mar;54(3):187-207 PMID: 15309328
  75. Phase I study of a MUC1 vaccine composed of different doses of MUC1 peptide with SB-AS2 adjuvant in resected and locally advanced pancreatic cancer.
    Cancer Immunol Immunother. 2005 Mar;54(3):254-64 PMID: 15372205
  76. Contrasting frequencies of antitumor and anti-vaccine T cells in metastases of a melanoma patient vaccinated with a MAGE tumor antigen.
    J Exp Med. 2005 Jan 17;201(2):249-57 PMID: 15657294
  77. Targeting toll-like receptor 9 with CpG oligodeoxynucleotides enhances tumor response to fractionated radiotherapy.
    Clin Cancer Res. 2005 Jan 1;11(1):361-9 PMID: 15671567
  78. 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 Jan 15;11(2 Pt 1):728-34 PMID: 15701862
  79. Select forms of tumor cell apoptosis induce dendritic cell maturation.
    J Leukoc Biol. 2005 Mar;77(3):361-8 PMID: 15569694
  80. Cross-presentation by intercellular peptide transfer through gap junctions.
    Nature. 2005 Mar 3;434(7029):83-8 PMID: 15744304
  81. Combining a recombinant cancer vaccine with standard definitive radiotherapy in patients with localized prostate cancer.
    Clin Cancer Res. 2005 May 1;11(9):3353-62 PMID: 15867235
  82. Phase I dose-escalation study of tumor necrosis factor-alpha and concomitant radiation therapy.
    Cancer J Sci Am. 1995 Sep-Oct;1(3):204-9 PMID: 9166477
  83. Flt3-ligand administration after radiation therapy prolongs survival in a murine model of metastatic lung cancer.
    Cancer Res. 1999 Dec 15;59(24):6028-32 PMID: 10626784
  84. Consequences of cell death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells.
    J Exp Med. 2000 Feb 7;191(3):423-34 PMID: 10662788
  85. A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes.
    J Exp Med. 2000 Feb 7;191(3):435-44 PMID: 10662789
  86. gamma-ray irradiation induces B7.1 expression in myeloid leukaemic cells.
    Br J Haematol. 2000 Mar;108(4):825-31 PMID: 10792289
  87. Immature myeloid cells and cancer-associated immune suppression.
    Cancer Immunol Immunother. 2002 Aug;51(6):293-8 PMID: 12111117
  88. Cancer vaccines: progress reveals new complexities.
    J Clin Invest. 2002 Aug;110(3):289-94 PMID: 12163445
  89. Immune modulation by ionizing radiation and its implications for cancer immunotherapy.
    Curr Pharm Des. 2002;8(19):1765-80 PMID: 12171547
  90. TNFerade Biologic: preclinical toxicology of a novel adenovector with a radiation-inducible promoter, carrying the human tumor necrosis factor alpha gene.
    Cancer Gene Ther. 2002 Nov;9(11):951-7 PMID: 12386834
  91. Cancer immunoediting: from immunosurveillance to tumor escape.
    Nat Immunol. 2002 Nov;3(11):991-8 PMID: 12407406
  92. Ionizing radiation modulates the exposure of the HUIV26 cryptic epitope within collagen type IV during angiogenesis.
    Int J Radiat Oncol Biol Phys. 2002 Nov 15;54(4):1194-201 PMID: 12419448
  93. Radiation-induced tumour necrosis factor-alpha expression: clinical application of transcriptional and physical targeting of gene therapy.
    Lancet Oncol. 2002 Nov;3(11):665-71 PMID: 12424068
  94. Cancer/testis antigens: an expanding family of targets for cancer immunotherapy.
    Immunol Rev. 2002 Oct;188:22-32 PMID: 12445278
  95. Antigens derived from melanocyte differentiation proteins: self-tolerance, autoimmunity, and use for cancer immunotherapy.
    Immunol Rev. 2002 Oct;188:136-46 PMID: 12445287
  96. Integrin-mediated targeting of drug delivery to irradiated tumor blood vessels.
    Cancer Cell. 2003 Jan;3(1):63-74 PMID: 12559176
  97. Interleukin-12 and the regulation of innate resistance and adaptive immunity.
    Nat Rev Immunol. 2003 Feb;3(2):133-46 PMID: 12563297
  98. Biologic activity of cytotoxic T lymphocyte-associated antigen 4 antibody blockade in previously vaccinated metastatic melanoma and ovarian carcinoma patients.
    Proc Natl Acad Sci U S A. 2003 Apr 15;100(8):4712-7 PMID: 12682289
  99. Radiation-induced leukocyte adhesion to endothelium in normal pancreas and in pancreatic carcinoma of the rat.
    Int J Cancer. 2003 Jul 1;105(4):506-11 PMID: 12712442
  100. Induction of tumor cell apoptosis in vivo increases tumor antigen cross-presentation, cross-priming rather than cross-tolerizing host tumor-specific CD8 T cells.
    J Immunol. 2003 May 15;170(10):4905-13 PMID: 12734333
  101. Irradiation of tumor cells up-regulates Fas and enhances CTL lytic activity and CTL adoptive immunotherapy.
    J Immunol. 2003 Jun 15;170(12):6338-47 PMID: 12794167
  102. Cancer regression and autoimmunity induced by cytotoxic T lymphocyte-associated antigen 4 blockade in patients with metastatic melanoma.
    Proc Natl Acad Sci U S A. 2003 Jul 8;100(14):8372-7 PMID: 12826605
  103. Recognition of microbial infection by Toll-like receptors.
    Curr Opin Immunol. 2003 Aug;15(4):396-401 PMID: 12900270
  104. Molecular identification of a danger signal that alerts the immune system to dying cells.
    Nature. 2003 Oct 2;425(6957):516-21 PMID: 14520412
  105. Tumor immunity meets autoimmunity: antigen levels and dendritic cell maturation.
    Curr Opin Immunol. 2003 Dec;15(6):725-30 PMID: 14630209
  106. Radiotherapy potentiates the therapeutic efficacy of intratumoral dendritic cell administration.
    Cancer Res. 2003 Dec 1;63(23):8466-75 PMID: 14679011
  107. Antitumor applications of stimulating toll-like receptor 9 with CpG oligodeoxynucleotides.
    Curr Oncol Rep. 2004 Mar;6(2):88-95 PMID: 14751085
  108. TNFerade biologic, an adenovector with a radiation-inducible promoter, carrying the human tumor necrosis factor alpha gene: a phase I study in patients with solid tumors.
    J Clin Oncol. 2004 Feb 15;22(4):592-601 PMID: 14726502
  109. Ionizing radiation inhibition of distant untreated tumors (abscopal effect) is immune mediated.
    Int J Radiat Oncol Biol Phys. 2004 Mar 1;58(3):862-70 PMID: 14967443
  110. Cellular protein is the source of cross-priming antigen in vivo.
    Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):3035-40 PMID: 14978273
  111. Direct injection of immature dendritic cells into irradiated tumor induces efficient antitumor immunity.
    Int J Cancer. 2004 May 1;109(5):685-90 PMID: 14999775
  112. Current developments of immunotherapy in the clinic.
    Curr Opin Immunol. 2004 Apr;16(2):130-6 PMID: 15023403
  113. Adenoviral interleukin-3 gene-radiation therapy for prostate cancer in mouse model.
    Int J Radiat Oncol Biol Phys. 2004 Jun 1;59(2):579-83 PMID: 15145179
  114. Danger signals: a time and space continuum.
    Trends Mol Med. 2004 Jun;10(6):251-7 PMID: 15177188
  115. External beam radiation of tumors alters phenotype of tumor cells to render them susceptible to vaccine-mediated T-cell killing.
    Cancer Res. 2004 Jun 15;64(12):4328-37 PMID: 15205348
  116. The exogenous pathway for antigen presentation on major histocompatibility complex class II and CD1 molecules.
    Nat Immunol. 2004 Jul;5(7):685-92 PMID: 15224094
  117. A sense of danger from radiation.
    Radiat Res. 2004 Jul;162(1):1-19 PMID: 15222781
  118. Cancer immunotherapy: a treatment for the masses.
    Science. 2004 Jul 9;305(5681):200-5 PMID: 15247469
  119. CpG oligodeoxynucleotide enhances tumor response to radiation.
    Cancer Res. 2004 Aug 1;64(15):5074-7 PMID: 15289307
  120. Ionizing radiation affects human MART-1 melanoma antigen processing and presentation by dendritic cells.
    J Immunol. 2004 Aug 15;173(4):2462-9 PMID: 15294960
  121. Manipulating dendritic cell biology for the active immunotherapy of cancer.
    Blood. 2004 Oct 15;104(8):2235-46 PMID: 15231572
  122. Antitumor vaccination of patients with glioblastoma multiforme: a pilot study to assess feasibility, safety, and clinical benefit.
    J Clin Oncol. 2004 Nov 1;22(21):4272-81 PMID: 15452186
  123. Recombinant human tumor necrosis factor-alpha: effects on proliferation of normal and transformed cells in vitro.
    Science. 1985 Nov 22;230(4728):943-5 PMID: 3933111
  124. Enhanced responsiveness of endothelium in the growing/motile state to tumor necrosis factor/cachectin.
    J Exp Med. 1989 Sep 1;170(3):913-31 PMID: 2769183
  125. Gene therapy targeted by radiation preferentially radiosensitizes tumor cells.
    Cancer Res. 1994 Aug 15;54(16):4266-9 PMID: 8044769
  126. Generation of human cytotoxic T cells specific for human carcinoembryonic antigen epitopes from patients immunized with recombinant vaccinia-CEA vaccine.
    J Natl Cancer Inst. 1995 Jul 5;87(13):982-90 PMID: 7629885
  127. A p16INK4a-insensitive CDK4 mutant targeted by cytolytic T lymphocytes in a human melanoma.
    Science. 1995 Sep 1;269(5228):1281-4 PMID: 7652577
Article Info
Journal
International journal of radiation oncology, biology, physics
Abbr.
Int J Radiat Oncol Biol Phys
ISSN
0360-3016
Published
2005-11-01
Pages
655-66
Language
English
Region
United States
NLM ID
7603616
PMCID
PMC1489884
Subset
IM
Grants
NCI NIH HHS · R01 CA-101752 · United States
NCI NIH HHS · 5 P30 CA16087-25 · United States
NCI NIH HHS · P30 CA016087 · United States
NCI NIH HHS · K08 CA089336 · United States
NIAID NIH HHS · R01 AI061684 · United States
NCI NIH HHS · R01 CA101752 · United States
PHS HHS · 52731 · United States
NCI NIH HHS · K08 CA89336 · United States
NIAID NIH HHS · AI061684 · United States
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