Radiation-induced cell death and dendritic cells: Potential for cancer immunotherapy?

Clinical Oncology

Volumn 17, Issue 1, 2005, Pages 1-11

  Hatfield , Paul ^a   Merrick, A ^a   Harrington, K ^b   Vile, R ^c   Bateman, A ^d   Selby, A ^a   Melcher, A ^a  

^a ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^c MAYO CLINIC   (United States)

^d SOUTHAMPTON GENERAL HOSPITAL   (United Kingdom)

Author keywords

Apoptosis; Cell death; Dendritic cells; Immunotherapy; Ionising radiation; Necrosis

Indexed keywords

B7 ANTIGEN; CD31 ANTIGEN; DNA; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; FAS ANTIGEN; FAS LIGAND; GAMMA INTERFERON; HEAT SHOCK PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1; INTERLEUKIN 2; LATENCY ASSOCIATED PEPTIDE; LYMPHOTOXIN; PADGEM PROTEIN; PROSTAGLANDIN E2; RITUXIMAB; TRASTUZUMAB; TUMOR ANTIGEN; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1;

ANTIGEN PRESENTATION; APOPTOSIS; CANCER IMMUNOTHERAPY; CANCER RADIOTHERAPY; CELL DEATH; CELL MEDIATED CYTOTOXICITY; DENDRITIC CELL; DNA DAMAGE; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; IN VIVO STUDY; IONIZING RADIATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PRIORITY JOURNAL; REVIEW;

EID: 11844281006     PISSN: 09366555     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.clon.2004.06.014     Document Type: Article

References (127)

1. J.F. Kerr A.H. Wyllie A.R. Currie Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics Br J Cancer 26 1972 239-257
2. K.S. Ravichandran "Recruitment signals"; from apoptotic cells: invitation to a quiet meal Cell 113 2003 817-820
3. I. Tamm F. Schriever B. Dorken Apoptosis: Implications of basic research for clinical oncology Lancet Oncol 2 2001 33-42
4. C.J. Sherr The Pezcoller Lecture: Cancer cell cycles revisited Cancer Res 60 2000 3689-3695
5. J.W. Harbour D.C. Dean Rb function in cell-cycle regulation and apoptosis Nat Cell Biol 2 2000 E65-E67
6. J.T. Opferman S.J. Korsmeyer Apoptosis in the development and maintenance of the immune system Nat Immunol 4 2003 410-415
7. A. Ashkenazi V.M. Dixit Death receptors: Signaling and modulation Science 281 1998 1305-1308
8. A. Gross J.M. McDonnell S.J. Korsmeyer BCL-2 family members and the mitochondria in apoptosis Genes Dev 13 1999 1899-1911
9. M. Leist M. Jaattela Four deaths and a funeral: From caspases to alternative mechanisms Nat Rev Mol Cell Biol 2 2001 589-598
10. T.M. Illidge Radiation-induced apoptosis Clin Oncol (R Coll Radiol) 10 1998 3-13
11. W.C. Dewey C.C. Ling R.E. Meyn Radiation-induced apoptosis: Relevance to radiotherapy Int J Radiat Oncol Biol Phys 33 1995 781-796
12. G.G. Steel The case against apoptosis Acta Oncol 40 2001 968-975
13. E. Finkel Biomedicine: Does cancer therapy trigger cell suicide? Science 286 1999 2256-2258
14. J.M. Brown B.G. Wouters Apoptosis, p53, and tumor cell sensitivity to anticancer agents Cancer Res 59 1999 1391-1399
15. E.C. Jonathan E.J. Bernhard W.G. McKenna How does radiation kill cells? Curr Opin Chem Biol 3 1999 77-83
16. M.A. Sheard S. Uldrijan B. Vojtesek Role of p53 in regulating constitutive and X-radiation-inducible CD95 expression and function in carcinoma cells Cancer Res 63 2003 7176-7184
17. M.A. Sheard P.H. Krammer J. Zaloudik Fractionated gamma-irradiation renders tumour cells more responsive to apoptotic signals through CD95 Br J Cancer 80 1999 1689-1696
18. B. Abdulkarim S. Sabri E. Deutsch et al. Radiation-induced expression of functional Fas ligand in EBV-positive human nasopharyngeal carcinoma cells Int J Cancer 86 2000 229-237
19. J. Albanese N. Dainiak Ionizing radiation alters Fas antigen ligand at the cell surface and on exfoliated plasma membrane-derived vesicles: implications for apoptosis and intercellular signaling Radiat Res 153 2000 49-61
20. C. Belka P. Marini W. Budach et al. Radiation-induced apoptosis in human lymphocytes and lymphoma cells critically relies on the up-regulation of CD95/Fas/APO-1 ligand Radiat Res 149 1998 588-595
21. J.W. Denham M. Hauer-Jensen The radiotherapeutic injury - a complex 'wound' Radiother Oncol 63 2002 129-145
22. G. Klein Tumor antigens Annu Rev Microbiol 20 1966 223-252
23. L.J. Old E.A. Boyse Immunology of experimental tumors Annu Rev Med 15 1964 167-186
24. T. Boon P.G. Coulie B. Van den Eynde Tumor antigens recognized by T cells Immunol Today 18 1997 267-268
25. G.P. Dunn A.T. Bruce H. Ikeda L.J. Old R.D. Schreiber Cancer immunoediting: From immunosurveillance to tumor escape Nat Immunol 3 2002 991-998
26. V. Shankaran H. Ikeda A.T. Bruce et al. FNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity Nature 410 2001 1107-1111
27. A.S. Dighe E. Richards L.J. Old R.D. Schreiber Enhanced in vivo growth and resistance to rejection of tumor cells expressing dominant negative IFN gamma receptors Immunity 1 1994 447-456
28. D.H. Kaplan V. Shankaran A.S. Dighe et al. Demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice Proc Natl Acad Sci U S A 95 1998 7556-7561
29. S.E. Street E. Cretney M.J. Smyth Perforin and interferon-gamma activities independently control tumor initiation, growth, and metastasis Blood 97 2001 192-197
30. M.E. van den Broek D. Kagi F. Ossendorp et al. Decreased tumor surveillance in perforin-deficient mice J Exp Med 184 1996 1781-1790
31. M.J. Smyth K.Y. Thia S.E. et al. Street Differential tumor surveillance by natural killer (NK) and NKT cells J Exp Med 191 2000 661-668
32. H. Jonuleit E. Schmitt The regulatory T cell family: Distinct subsets and their interrelations J Immunol 171 2003 6323-6327
33. T. Sasada M. Kimura Y. Yoshida M. Kanai A. Takabayashi CD4+CD25+ regulatory T cells in patients with gastrointestinal malignancies: possible involvement of regulatory T cells in disease progression Cancer 98 2003 1089-1099
34. U.K. Liyanage T.T. Moore H.G. Joo et al. Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma J Immunol 169 2002 2756-2761
35. E.Y. Woo C.S. Chu T.J. Goletz et al. Regulatory CD4(+)CD25(+) T cells in tumors from patients with early-stage non-small cell lung cancer and late-stage ovarian cancer Cancer Res 61 2001 4766-4772
36. D. Golgher E. Jones F. Powrie T. Elliott A. Gallimore Depletion of CD25+ regulatory cells uncovers immune responses to shared murine tumor rejection antigens Eur J Immunol 32 2002 3267-3275
37. J. Banchereau R.M. Steinman Dendritic cells and the control of immunity Nature 392 1998 245-252
38. J. Banchereau S. Paczesny P. Blanco et al. Dendritic cells: Controllers of the immune system and a new promise for immunotherapy Ann NY Acad Sci 987 2003 180-187
39. R.M. Steinman D. Hawiger K. Liu et al. Dendritic cell function in vivo during the steady state: A role in peripheral tolerance Ann NY Acad Sci 987 2003 15-25
40. R.M. Steinman D. Hawiger M.C. Nussenzweig Tolerogenic dendritic cells Annu Rev Immunol 21 2003 685-711
41. R.M. Steinman M.C. Nussenzweig Avoiding horror autotoxicus: The importance of dendritic cells in peripheral T cell tolerance Proc Natl Acad Sci U S A 99 2002 351-358
42. K.L. Legge R.K. Gregg R. Maldonado-Lopez et al. On the role of dendritic cells in peripheral T cell tolerance and modulation of autoimmunity J Exp Med 196 2002 217-227
43. P. Matzinger Tolerance, danger, and the extended family Annu Rev Immunol 12 1994 991-1045
44. S. Akira Mammalian Toll-like receptors Curr Opin Immunol 15 2003 5-11
45. L.A. O'Neill Z. Brown S.G. Ward Toll-like receptors in the spotlight Nat Immunol 4 2003 299
46. K. Takeda T. Kaisho S. Akira Toll-like receptors Annu Rev Immunol 21 2003 335-376
47. Y. Delneste G. Magistrelli J. Gauchat et al. Involvement of LOX-1 in dendritic cell-mediated antigen cross-presentation Immunity 17 2002 353-362
48. A. Regnault D. Lankar V. Lacabanne et al. Fcgamma receptor-mediated induction of dendritic cell maturation and major histocompatibility complex class I-restricted antigen presentation after immune complex internalization J Exp Med 189 1999 371-380
49. A.D. Santin P.L. Hermonat A. Ravaggi M. Chiriva-Internati S. Pecorelli G.P. Parham Radiation-enhanced expression of E6/E7 transforming oncogenes of human papillomavirus-16 in human cervical carcinoma Cancer 83 1998 2346-2352
50. A.D. Santin P.L. Hermonat A. Ravaggi et al. Effects of retinoic acid combined with irradiation on the expression of major histocompatibility complex molecules and adhesion/costimulation molecules ICAM-1 in human cervical cancer Gynecol Oncol 70 1998 195-201
51. A.D. Santin P.L. Hermonat J.C. Hiserodt et al. Effects of irradiation on the expression of major histocompatibility complex class I antigen and adhesion costimulation molecules ICAM-1 in human cervical cancer Int J Radiat Oncol Biol Phys 39 1997 737-742
52. A.D. Santin J.C. Hiserodt J. Fruehauf P.J. DiSaia S. Pecorelli G.A. Granger Effects of irradiation on the expression of surface antigens in human ovarian cancer Gynecol Oncol 60 1996 468-474
53. B. Klein D. Loven H. Lurie et al. The effect of irradiation on expression of HLA class I antigens in human brain tumors in culture J Neurosurg 80 1994 1074-1077
54. A. Seo F. Ishikawa H. Nakano H. Nakazaki K. Kobayashi T. Kakiuchi Enhancement of B7-1 (CD80) expression on B-lymphoma cells by irradiation Immunology 96 1999 642-648
55. A. Morel N. Fernandez A. de La Coste et al. Gamma-ray irradiation induces B7.1 costimulatory molecule neoexpression in various murine tumor cells Cancer Immunol Immunother 46 1998 277-282
56. R. Vereecque G. Buffenoir R. Gonzalezet al. Gamma-ray irradiation induces B7.1 expression in myeloid leukaemic cells Br J Haematol 108 2000 825-831
57. L. Chen S. Ashe W.A. Brady et al. Costimulation of antitumor immunity by the B7 counterreceptor for the T lymphocyte molecules CD28 and CTLA-4 Cell 71 1992 1093-1102
58. S.E. Townsend J.P. Allison Tumor rejection after direct costimulation of CD8+ T cells by B7-transfected melanoma cells Science 259 1993 368-370
59. X.-F. Bai J. Bender J. Liu et al. Local costimulation reinvigorates tumor-specific cytolytic T lymphocytes for experimental therapy in mice with large tumor burdens J Immunol 167 2001 3936-3943
60. L. Ramarathinam M. Castle Y. Wu Y. Liu T cell costimulation by B7/BB1 induces CD8 T cell-dependent tumor rejection: An important role of B7/BB1 in the induction, recruitment, and effector function of antitumor T cells J Exp Med 179 1994 1205-1214
61. A.F. Ochsenbein S. Sierro B. Odermatt et al. Roles of tumour localization, second signals and cross priming in cytotoxic T-cell induction Nature 411 2001 1058-1064
62. R.M. Zinkernagel On cross-priming of MHC class I-specific CTL: Rule or exception? Eur J Immunol 32 2002 2385-2392
63. A.F. Ochsenbein P. Klenerman U. Karrer et al. Immune surveillance against a solid tumor fails because of immunological ignorance Proc Natl Acad Sci USA 96 1999 2233-2238
64. C.J. Melief Mini-review: Regulation of cytotoxic T lymphocyte responses by dendritic cells: Peaceful coexistence of cross-priming and direct priming? Eur J Immunol 33 2003 2645-2654
65. A.D. Santin J.C. Hiserodt P.J. DiSaia S. Pecorelli G.A. Granger Differential effects of high-dose gamma irradiation on the production of transforming growth factor-beta in fresh and established human ovarian cancer Gynecol Oncol 61 1996 403-408
66. D.E. Hallahan M.J. Staba-Hogan S. Virudachalam A. Kolchinsky X-ray-induced P-selectin localization to the lumen of tumor blood vessels Cancer Res 58 1998 5216-5220
67. D.E. Hallahan S. Virudachalam Ionizing radiation mediates expression of cell adhesion molecules in distinct histological patterns within the lung Cancer Res 57 1997 2096-2099
68. S. Quarmby R.D. Hunter S. Kumar Irradiation induced expression of CD31, ICAM-1 and VCAM-1 in human microvascular endothelial cells Anticancer Res 20 2000 3375-3381
69. S. Quarmby P. Kumar J. Wang et al. Irradiation induces upregulation of CD31 in human endothelial cells Arterioscler Thromb Vasc Biol 19 1999 588-597
70. G. Stammler E.W. Pommerenke U. Masanek J. Mattern M. Volm Messenger RNA expression of resistance factors in human tumor cell lines after single exposure to radiation J Exp Ther Oncol 1 1996 39-48
71. A.D. Santin P.L. Hermonat A. Ravaggi et al. The effects of irradiation on the expression of a tumour rejection antigen (heat shock protein gp96) in human cervical cancer Int J Radiat Biol 73 1998 699-704
72. P.K. Srivastava Hypothesis: Controlled necrosis as a tool for immunotherapy of human cancer Cancer Immun 3 2003 4
73. P. Srivastava Roles of heat-shock proteins in innate and adaptive immunity Nat Rev Immunol 2 2002 185-194
74. M.J. Gething J. Sambrook Protein folding in the cell Nature 355 1992 33-45
75. D.A. Parsell S. Lindquist The function of heat-shock proteins in stress tolerance: Degradation and reactivation of damaged proteins Annu Rev Genet 27 1993 437-496
76. I.G. Haas BiP - a heat shock protein involved in immunoglobulin chain assembly Curr Top Microbiol Immunol 167 1991 71-82
77. S. Lindquist The heat-shock response Annu Rev Biochem 55 1986 1151-1191
78. H. Singh-Jasuja H.U. Scherer N. Hilf et al. The heat shock protein gp96 induces maturation of dendritic cells and down-regulation of its receptor Eur J Immunol 30 2000 2211-2215
79. S. Basu R.J. Binder R. Suto K.M. Anderson P.K. Srivastava Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF-kappa B pathway Int Immunol 12 2000 1539-1546
80. N.E. Blachere Z. Li R.Y. Chandawarkar et al. Heat shock protein-peptide complexes, reconstituted in vitro, elicit peptide-specific cytotoxic T lymphocyte response and tumor immunity J Exp Med 186 1997 1315-1322
81. K.K. Steinauer I. Gibbs S. Ning J.N. French J. Armstrong S.J. Knox Radiation induces upregulation of cyclooxygenase-2 (COX-2) protein in PC-3 cells Int J Radiat Oncol Biol Phys 48 2000 325-328
82. P. Kalinski C.M. Hilkens A. Snijders F.G. Snijdewint M.L. Kapsenberg IL-12-deficient dendritic cells, generated in the presence of prostaglandin E2, promote type 2 cytokine production in maturing human naive T helper cells J Immunol 159 1997 28-35
83. P. Kalinski C.M. Hilkens A. Snijders F.G. Snijdewint M.L. Kapsenberg Dendritic cells, obtained from peripheral blood precursors in the presence of PGE2, promote Th2 responses Adv Exp Med Biol 417 1997 363-367
84. S.G. Harris J. Padilla L. Koumas D. Ray R.P. Phipps Prostaglandins as modulators of immunity Trends Immunol 23 2002 144-150
85. E. Vassiliou H. Jing D. Ganea Prostaglandin E2 inhibits TNF production in murine bone marrow-derived dendritic cells Cell Immunol 223 2003 120-132
86. C.S. Chiang W.H. McBride Radiation enhances tumor necrosis factor alpha production by murine brain cells Brain Res 566 1991 265-269
87. S. Kyrkanides J.A. Olschowka J.P. Williams J.T. Hansen M.K. O'Banion TNF alpha and IL-1beta mediate intercellular adhesion molecule-1 induction via microglia-astrocyte interaction in CNS radiation injury J Neuroimmunol 95 1999 95-106
88. J.H. Hong C.S. Chiang I.L. Campbell J.R. Sun H.R. Withers W.H. McBride Induction of acute phase gene expression by brain irradiation Int J Radiat Oncol Biol Phys 33 1995 619-626
89. M. Chakraborty S.I. Abrams K. Camphausen et al. Irradiation of tumor cells up-regulates Fas and enhances CTL lytic activity and CTL adoptive immunotherapy J Immunol 170 2003 6338-6347
90. N.P. Restifo Not so Fas: Re-evaluating the mechanisms of immune privilege and tumor escape Nat Med 6 2000 493-495
91. Y. Tada J. Ow A. Wada et al. Fas ligand-expressing tumors induce tumor-specific protective immunity in the inoculated hosts but vaccination with the apoptotic tumors suppresses antitumor immunity Cancer Gene Ther 10 2003 134-140
92. N.P. Restifo Building better vaccines: How apoptotic cell death can induce inflammation and activate innate and adaptive immunity Curr Opin Immunol 12 2000 597-603
93. R.M. Steinman S. Turley I. Mellman K. Inaba The induction of tolerance by dendritic cells that have captured apoptotic cells J Exp Med 191 2000 411-416
94. R.E. Voll M. Herrmann E.A. Roth C. Stach J.R. Kalden I. Girkontaite Immunosuppressive effects of apoptotic cells Nature 390 1997 350-351
95. S. Gallucci M. Lolkema P. Matzinger Natural adjuvants: Endogenous activators of dendritic cells Nat Med 5 1999 1249-1255
96. B. Sauter M.L. Albert L. Francisco M. Larsson S. Somersan N. Bhardwaj 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 191 2000 423-434
97. P. Rovere C. Vallinoto A. Bondanza et al. Cutting edge: Bystander apoptosis triggers dendritic cell maturation and antigen-presenting function J Immunol 161 1998 4467-4471
98. T.K. Hoffmann N. Meidenbauer G. Dworacki H. Kanaya T.L. Whiteside Generation of tumor-specific T lymphocytes by cross-priming with human dendritic cells ingesting apoptotic tumor Cells Cancer Res 60 2000 3542-3549
99. M.L. Albert B. Sauter N. Bhardwaj Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs Nature 392 1998 86-89
100. M. Shaif-Muthana C. McIntyre K. Sisley I. Rennie A. Murray Dead or alive: Immunogenicity of human melanoma cells when presented by dendritic cells Cancer Res 60 2000 6441-6447
101. S.R. Scheffer H. Nave F. Korangy et al. Apoptotic, but not necrotic, tumor cell vaccines induce a potent immune response in vivo Int J Cancer 103 2003 205-211
102. S.E. Strome S. Voss R. Wilcox et al. Strategies for antigen loading of dendritic cells to enhance the antitumor immune response Cancer Res 62 2002 1884-1889
103. Y. Kotera K. Shimizu J.J. Mule Comparative analysis of necrotic and apoptotic tumor cells as a source of antigen(s) in dendritic cell-based immunization Cancer Res 61 2001 8105-8109
104. A. Ronchetti P. Rovere G. Iezzi et al. Immunogenicity of apoptotic cells in vivo: Role of antigen load, antigen-presenting cells, and cytokines J Immunol 163 1999 130-136
105. S. Paczesny S. Beranger J.-L. Salzmann D. Klatzmann B.M. Colombo Protection of mice against leukemia after vaccination with bone marrow-derived dendritic cells loaded with apoptotic leukemia cells Cancer Res 61 2001 2386-2389
106. R.S. Goldszmid J. Idoyaga A.I. Bravo R. Steinman J. Mordoh R. Wainstok Dendritic cells charged with apoptotic tumor cells induce long-lived protective CD4+ and CD8+ T cell immunity against B16 melanoma J Immunol 171 2003 5940-5947
107. H. Feng Y. Zeng M.W. Graner E. Katsanis Stressed apoptotic tumor cells stimulate dendritic cells and induce specific cytotoxic T cells Blood 100 2002 4108-4115
108. H. Feng Y. Zeng M.W. Graner A. Likhacheva E. Katsanis Exogenous stress proteins enhance the immunogenicity of apoptotic tumor cells and stimulate antitumor immunity Blood 101 2003 245-252
109. H. Feng Y. Zeng L. Whitesell E. Katsanis Stressed apoptotic tumor cells express heat shock proteins and elicit tumor-specific immunity Blood 97 2001 3505-3512
110. S. Buttiglieri A. Galetto S. Forno M. De Andrea L. Matera Influence of drug-induced apoptotic death on processing and presentation of tumor antigens by dendritic cells Int J Cancer 106 2003 516-520
111. S. Somersan M. Larsson J.F. Fonteneau S. Basu P. Srivastava N. Bhardwaj Primary tumor tissue lysates are enriched in heat shock proteins and induce the maturation of human dendritic cells J Immunol 167 2001 4844-4852
112. M. Barcellos-Hoff T. Dix Redox-mediated activation of latent transforming growth factor-beta 1 Mol Endocrinol 10 1996 1077-1083
113. M.H. Barcellos-Hoff R. Derynck M.L. Tsang J.A. Weatherbee Transforming growth factor-beta activation in irradiated murine mammary gland J Clin Invest 93 1994 892-899
114. L.M. Wakefield A.B. Roberts TGF-[beta] signaling: Positive and negative effects on tumorigenesis Curr Opin Genet Dev 12 2002 22-29
115. R. Derynck R.J. Akhurst A. Balmain TGF-beta signaling in tumor suppression and cancer progression Nat Genet 29 2001 117-129
116. J.J. Letterio A.B. Roberts Regulation of immune responses by TGF-beta Annu Rev Immunol 16 1998 137-161
117. J.Y. Kao Y. Gong C.-M. Chen Q.-D. Zheng J.-J. Chen Tumor-derived TGF-{beta} reduces the efficacy of dendritic cell/tumor fusion vaccine J Immunol 170 2003 3806-3811
118. J.J. Kobie R.S. Wu R.A. Kurt et al. Transforming growth factor {beta} inhibits the antigen-presenting functions and antitumor activity of dendritic cell vaccines Cancer Res 63 2003 1860-1864
119. C.M. Lin F.H. Wang P.K. Lee Activated human CD4+ T cells induced by dendritic cell stimulation are most sensitive to transforming growth factor-beta: Implications for dendritic cell immunization against cancer Clin Immunol 102 2002 96-105
120. J.H. Kehrl A.B. Roberts L.M. Wakefield S. Jakowlew M.B. Sporn A.S. Fauci Transforming growth factor beta is an important immunomodulatory protein for human B lymphocytes J Immunol 137 1986 3855-3860
121. G. Caron Y. Delneste E. Roelandts et al. Histamine polarizes human dendritic cells into Th2 cell-promoting effector dendritic cells J Immunol 167 2001 3682-3686
122. J.C. Acker L.B. Marks D.P. Spencer et al. Serial in vivo observations of cerebral vasculature after treatment with a large single fraction of radiation Radiat Res 149 1998 350-359
123. E.Y. Nikitina D.I. Gabrilovich 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 94 2001 825-833
124. K.A. Candido K. Shimizu J.C. McLaughlin et al. Local administration of dendritic cells inhibits established breast tumor growth: Implications for apoptosis-inducing agents Cancer Res 61 2001 228-236
125. S. Teitz-Tennenbaum Q. Li S. Rynkiewicz et al. Radiotherapy potentiates the therapeutic efficacy of intratumoral dendritic cell administration Cancer Res 63 2003 8466-8475
126. K.W. Kim S.H. Kim J.G. Shin et al. Direct injection of immature dendritic cells into irradiated tumor induces efficient antitumor immunity Int J Cancer 109 2004 685-690
127. N.P. Restifo Building better vaccines: How apoptotic cell death can induce inflammation and activate innate and adaptive immunity Curr Opin Immunol 12 2000 597-603