Tumour infiltrating host cells and their significance for hyperthermia

International Journal of Hyperthermia

Volumn 26, Issue 3, 2010, Pages 247-255

  Muthana, Munitta ^a   Multhoff, Gabriele ^b,c   Pockley, A Graham ^d  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Adaptive immunity; Antigen presentation; Cytotoxicity; Hyperthermia; Innate immunity; NK cells; T cells

Indexed keywords

ALPHA INTERFERON; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LECTIN RECEPTOR; LIPOPOLYSACCHARIDE; MONOCYTE CHEMOTACTIC PROTEIN 1; PHOSPHATIDYLSERINE; PLACENTAL GROWTH FACTOR; PROSTAGLANDIN E2; RANTES; TRANSCRIPTION FACTOR FOXP3; TUMOR ANTIGEN; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTING CELL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CD4+ CD25+ T LYMPHOCYTE; CELL ACTIVATION; CELL DEATH; CELL INFILTRATION; COLON ADENOCARCINOMA; HEAD AND NECK CARCINOMA; HUMAN; HYPERTHERMIA; IMMUNOGENICITY; LUNG CANCER; MACROPHAGE ACTIVATION; MELANOMA; MICROENVIRONMENT; NATURAL KILLER CELL; NONHUMAN; PANCREAS ADENOCARCINOMA; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVIEW; TH1 CELL; TH2 CELL; THERMOREGULATION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR IMMUNITY;

ANTIGEN-PRESENTING CELLS; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; HYPERTHERMIA, INDUCED; IMMUNOSUPPRESSION; MICROCIRCULATION; NEOPLASMS; T-LYMPHOCYTES;

EID: 77951125440     PISSN: 02656736     EISSN: 14645157     Source Type: Journal    
DOI: 10.3109/02656730903413375     Document Type: Review

References (122)

1. Garrido F, Algarra I. MHC antigens and tumor escape from immune surveillance. Adv Cancer Res 2001;83:117-158.
2. Bubenik J. Tumour MHC class I down regulation and immunotherapy. Oncol Rep 2003;10:2005-2008.
3. Marincola FM, Jaffee EM, Hicklin DJ, Ferrone S. Escape of human solid tumors from T-cell recognition: Molecular mechanisms and functional significance. Adv Immunol 2000;74:181-273.
4. Ljunggren HG, Käre K. In search of the 'missing self': MHC molecules and NK cell recognition. Immunol Today 1990;11:237-244.
5. Madjd Z, Spendlove I, Pinder SE, Ellis IO, Durrant LG. Total loss of MHC class I is an independent indicator of good prognosis in breast cancer. Int J Cancer 2005;117:248-255.
6. Ramnath N, Tan D, Li Q, Hylander BL, Bogner P, Ryes L, Ferrone S. Is down regulation of MHC class I antigen expression in human non-small cell lung cancer associated with prolonged survival? Cancer Immunol Immunother 2006;55:891-899.
7. Jager MJ, Hurks HM, Levitskaya J, Kiessling R. HLA expression in uveal melanoma: There is no rule without some exception. Hum Immunol 2002;63:444-451.
8. Menon AG, Morreau H, Tollenaar RA, Alphenaar E, Van Puijenbroek M, Putter H, Janssen-Van Rhijn CM, Van De Velde CJ, Fleuren GJ, Kuppen PJ. Down-regulation of HLA-A expression correlates with a better prognosis in colorectal cancer patients. Lab Invest 2002;82:1725-1733.
9. Roti Roti JL. Cellular responses to hyperthermia (40-46°C): Cell killing and molecular events. Int J Hyperthermia 2008;24:3-15.
10. Milani V, Noessner E. Effects of thermal stress on tumor antigenicity and recognition by immune effector cells. Cancer Immunol Immunother 2006;55:312-319.
11. Baronzio G, Gramaglia A, Fiorentini G. Hyperthermia and immunity. A brief overview. In Vivo 2006;20:689-695.
12. Dieing A, Ahlers O, Hildebrandt B, Kerner T, Tamm I, Possinger K, Wust P. The effect of induced hyperthermia on the immune system. Prog Brain Res 2007;162:137-152.
13. Zhang HG, Mehta K, Cohen P, Guha C. Hyperthermia on immune regulation: A temperature's story. Cancer Lett 2008;271:191-204.
14. Gravante G, Sconocchia G, Ong SL, Dennison AR, Lloyd DM. Immunoregulatory effects of liver ablation therapies for the treatment of primary and metastatic liver malignancies. Liver Int 2009;29:18-24.
15. Skitzki JJ, Repasky EA, Evans SS. Hyperthermia as an immunotherapy strategy for cancer. Curr Opin Investig Drugs 2009;10:550-558.
16. Wong JY, Mivechi NF, Paxton RJ, Williams LE, Beatty BG, Beatty JD, Shively JE. The effects of hyperthermia on tumor carcinoembryonic antigen expression. Int J Radiat Oncol Biol Phys 1989;17:803-808.
17. Takahashi T, Mitsuhashi N, Sakurai H, Niibe H. Modifications of tumor-associated antigen expression on human lung cancer cells by hyperthermia and cytokine. Anticancer Res 1995;15:2601-2606.
18. Shi H, Cao T, Connolly JE, Monnet L, Bennett L, Chapel S, Bagnis C, Mannoni P, Davoust J, Palucka AK, et al. Hyperthermia enhances CTL cross-priming. J Immunol 2006;176:2134-2141.
19. Davies CD, Western A, Lindmo T, Moan J. Changes in antigen expression on human FME melanoma cells after exposure to photoactivated hematoporphyrin derivative. Cancer Res 1986;46:6068-6072.
20. Davies CD, Lindmo T. Hyperthermia-induced shedding and masking of melanoma-associated antigen. Int J Hyperthermia 1990;6:1053-1064.
21. Blom DJ, De Waard-Siebinga I, Apte RS, Luyten GP, Niederkorn JY, Jager MJ. Effect of hyperthermia on expression of histocompatibility antigens and heat-shock protein molecules on three human ocular melanoma cell lines. Melanoma Res 1997;7:103-109.
22. Dressel R, Elsner L, Quentin T, Walter L, Günther E. Heat shock protein 70 is able to prevent heat shock-induced resistance of target cells to CTL. J Immunol 2000;164: 2362-2371.
23. Wells AD, Rai SK, Salvato MS, Band H, Malkovsky M. Hsp72-mediated augmentation of MHC class I surface expression and endogenous antigen presentation. Int Immunol 1998;10:609-617.
24. Ito A, Shinkai M, Honda H, Wakabayashi T, Yoshida J, Kobayashi T. Augmentation of MHC class I antigen presentation via heat shock protein expression by hyperthermia. Cancer Immunol Immunother 2001;50:515-522.
25. Cippitelli M, Fionda C, Di Bona D, Piccoli M, Frati L, Santoni A. Hyperthermia enhances CD95-ligand gene expression in T lymphocytes. J Immunol 2005;174:223-232.
26. Kagi D, Vignaux F, Ledermann B, Burki K, Depraetere V, Nagata S, Hengartner H, Golstein P. Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity. Science 1994;265:528-530.
27. Jackson KM, DeLeon M, Sistonen L, Verret CR. Heatshocked A20 lymphoma cells fail to induce degranulation of cytotoxic T lymphocytes: Possible mechanism of resistance. Cell Immunol 2000;203:12-18.
28. Mise K, Kan N, Okino T, Nakanishi M, Satoh K, Teramura Y, Yamasaki S, Ohgaki K, Tobe T. Effect of heat treatment on tumor cells and antitumor effector cells. Cancer Res 1990;50:6199-6202.
29. Wells AD, Malkovsky M. Heat shock proteins, tumor immunogenicity and antigen presentation: An integrated view. Immunol Today 2000;21:129-132.
30. Mëoret A, Patry Y, Burg C, Le Pendu J. Co-segregation of tumor immunogenicity with expression of inducible but not constitutive hsp70 in rat colon carcinomas. J Immunol 1995;155:740-747.
31. + suppressor T cells: More questions than answers. Nat Rev Immunol 2002;2:389-400.
32. + T cells. Curr Opin Immunol 2003;15:690-696.
33. Waldmann H, Graca L, Cobbold S, Adams E, Tone M, Tone Y. Regulatory T cells and organ transplantation. Semin Immunol 2004;16:119-126.
34. + regulatory T cells: Evidence for in vivo inhibition of effector cell proliferation. J Immunol 2004;172:6539-6544.
35. Wood KJ, Sakaguchi S. Regulatory T cells in transplantation tolerance. Nat Rev Immunol 2003;3:199-210.
36. + regulatory T cells for immunologic self-tolerance and negative control of immune responses. Ann Rev Immunol 2004;22:531-562.
37. Nelson BH. IL-2, regulatory T cells, and tolerance. J Immunol 2004;172:3983-3988.
38. + regulatory cells uncovers immune responses to shared murine tumor rejection antigens. Eur J Immunol 2002;32:3267-3275.
39. + regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses. J Exp Med 2001;194:823-832.
40. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor α-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995;155:1151-1164.
41. + T cells: A common basis between tumor immunity and autoimmunity. J Immunol 1999;163:5211-5218.
42. Onizuka S, Tawara I, Shimizu J, Sakaguchi S, Fujita T, Nakayama E. Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor alpha) monoclonal antibody. Cancer Res 1999;59:3128-3133.
43. + T-cell-dependent immune defense of B16 melanoma. Cancer Res 2001;61:8643-8646.
44. + regulatory cells results in suppression of melanoma growth and induction of autoreactivity in mice. Cancer Immun 2002;2:1.
45. Wolf AM, Wolf D, Steurer M, Gastl G, Gunsilius E, Grubeck-Loebenstein B. Increase of regulatory T cells in the peripheral blood of cancer patients. Clin Cancer Res 2003;9:606-612.
46. + T cells with IFN-γ dependent antiangiogenic activity, as well as long-lasting tumor immunity elicited by peptide vaccination. J Immunol 2003;171:5931-5939.
47. + T helper cells and hindered by naturally occurring T regulatory cells. J Immunol 2005;174:2591-2601.
48. + regulatory T cells promotes a tumor-specific immune response in pancreas cancer-bearing mice. Ann Surg Oncol 2006;13:1252-1258.
49. + regulatory T cells. Lab Invest 2007;87:582-590.
50. Rudge G, Barrett SP, Scott B, van Driel IR. Infiltration of a mesothelioma by IFN-γ-producing cells and tumor rejection after depletion of regulatory T cells. J Immunol 2007;178:4089-4096.
51. Bluestone JA, Abbas AK. Natural versus adaptive regulatory T cells. Nat Rev Immunol 2003;3:253-257.
52. Vigouroux S, Yvon E, Biagi E, Brenner MK. Antigen-induced regulatory T cells. Blood 2004;104:26-33.
53. Zhou G, Levitsky HI. Natural regulatory T cells and de novoinduced regulatory T cells contribute independently to tumorspecific tolerance. J Immunol 2007;178:2155-2162.
54. Liyanage UK, Goedegebuure PS, Moore TT, Viehl CT, Moo-Young TA, Larson JW, Frey DM, Ehlers JP, Eberlein TJ, Linehan DC. Increased prevalence of regulatory T cells (Treg) is induced by pancreas adenocarcinoma. J Immunother 2006;29:416-424.
55. + regulatory T cell is increased in the patients with ovarian carcinoma. Cancer Invest 2005;23:399-403.
56. Schmidtner J, Distel LV, Ott OJ, Nkenke E, Sprung CN, Fietkau R, Lubgan D. Hyperthermia and irradiation of head and neck squamous cancer cells causes migratory profile changes of tumour infiltrating lymphocytes. Int J Hyperthermia 2009;25:347-354.
57. + regulatory T cells inhibit natural killer cell functions in a transforming growth factor-β-dependent manner. J Exp Med 2005;202:1075-1085.
58. JääteläM. Effects of heat shock on cytolysis mediated by NK cells, LAK cells, activated monocytes and TNFs alpha and beta. Scand J Immunol 1990;31:175-182.
59. Ostberg JR, Dayanc BE, Yuan M, Oflazoglu E, Repasky EA. Enhancement of natural killer (NK) cell cytotoxicity by feverrange thermal stress is dependent on NKG2D function and is associated with plasma membrane NKG2D clustering and increased expression of MICA on target cells. J Leukoc Biol 2007;82:1322-1331.
60. Dayanc BE, Beachy SH, Ostberg JR, Repasky EA. Dissecting the role of hyperthermia in natural killer cell mediated antitumor responses. Int J Hyperthermia 2008;24:41-56.
61. Multhoff G, Botzler C, Jennen L, Schmidt J, Ellwart J, Issels R. Heat shock protein 72 on tumor cells: A recognition structure for natural killer cells. J Immunol 1997;158:4341-4350.
62. Elsner L, Muppala V, Gehrmann M, Lozano J, Malzahn D, Bickeböller H, Brunner E, Zientkowska M, Herrmann T, Walter L, et al. The heat shock protein HSP70 promotes mouse NK cell activity against tumors that express inducible NKG2D ligands. J Immunol 2007;179:5523-5533.
63. Elsner L, Flugge PF, Lozano J, Muppala V, Eiz-Vesper B, Demiroglu SY, Malzahn D, Herrmann T, Brunner E, Bickeböller H, Multhoff G, Walter L, Dressel R. The endogenous danger signals HSP70 and MICA cooperate in the activation of cytotoxic effector functions of NK cells. J Cell Mol Med 2009, in press.
64. Gehrmann M, Schmetzer H, Eissner G, Haferlach T, Hiddemann W, Multhoff G. Membrane-bound heat shock protein 70 (Hsp70) in acute myeloid leukemia: A tumor specific recognition structure for the cytolytic activity of autologous NK cells. Haematologica 2003;88:474-476.
65. Multhoff G. Heat shock protein 70 (Hsp70): Membrane location, export and immunological relevance. Methods 2007;43:229-237.
66. Schilling D, Gehrmann M, Steinem C, De Maio A, Pockley AG, Abend M, Molls M, Multhoff G. Binding of heat shock protein 70 to extracellular phosphatidylserine promotes killing of normoxic and hypoxic tumor cells. FASEB J 2009;23:2467-2477.
67. Elliott JI, Surprenant A, Marelli-Berg FM, Cooper JC, Cassady-Cain RL, Wooding C, Linton K, Alexander DR, Higgins CF. Membrane phosphatidylserine distribution as a non-apoptotic signalling mechanism in lymphocytes. Nat Cell Biol 2005;7:808-816.
68. Robbins JR, Lee SM, Filipovich AH, Szigligeti P, Neumeier L, Petrovic M, Conforti L. Hypoxia modulates early events in T cell receptor-mediated activation in human T lymphocytes via Kv1.3 channels. J Physiol 2005;564:131-143.
69. Roman J, Rangasamy T, Guo J, Sugunan S, Meednu N, Packirisamy G, Shimoda L, Golding A, Semenza G, Georas SN. T cell activation under hypoxic conditions enhances interferon-γ secretion. Am J Respir Cell Mol Biol 2009, in press.
70. Gehrmann M, Radons J, Molls M, Multhoff G. The therapeutic implications of clinically applied modifiers of heat shock protein 70 (Hsp70) expression by tumor cells. Cell Stress Chaperones 2008;13:1-10.
71. Pockley AG, Georgiades A, Thulin T, de Faire U, Frostegärd J. Serum heat shock protein 70 levels predict the development of atherosclerosis in subjects with established hypertension. Hypertension 2003;42:235-238.
72. Pockley AG, Shepherd J, Corton J. Detection of heat shock protein 70 (Hsp70) and anti-Hsp70 antibodies in the serum of normal individuals. Immunol Invest 1998;27:367-377.
73. Wang MH, Grossmann ME, Young CY. Forced expression of heat-shock protein 70 increases the secretion of Hsp70 and provides protection against tumour growth. Brit J Cancer 2004;90:926-931.
74. Kocsis J, Madaras B, Toth EK, Fust G, Prohäzka Z. Serum level of soluble 70-kD heat shock protein is associated with high mortality in patients with colorectal cancer without distant metastasis. Cell Stress Chaperones 2009, in press.
75. Gastpar R, Gehrmann M, Bausero MA, Asea A, Gross C, Schroeder JA, Multhoff G. Heat shock protein 70 surfacepositive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells. Cancer Res 2005;65:5238-5247.
76. Zitvogel L, Apetoh L, Ghiringhelli F, Kroemer G. Immunological aspects of cancer chemotherapy. Nat Rev Immunol 2008;8:59-73.
77. Viaud S, Ullrich E, Zitvogel L, Chaput N. Exosomes for the treatment of human malignancies. Horm Metab Res 2008;40:82-88.
78. Pepin E, Villiers CL, Gabert FM, Serra VA, Marche PN, Colomb MG. Heat shock increases antigenic peptide generation but decreases antigen presentation. Eur J Immunol 1996;26:2939-2943.
79. Kuperberg G, Ellis J, Marcinkiewicz J, Chain BM. Temperature-induced stress abrogates co-stimulatory function in antigen-presenting cells. Eur J Immunol 1991;21: 2791-2795.
80. Ostberg JR, Kabingu E, Repasky EA. Thermal regulation of dendritic cell activation and migration from skin explants. Int J Hyperthermia 2003;19:520-533.
81. Ostberg JR, Repasky EA. Emerging evidence indicates that physiologically relevant thermal stress regulates dendritic cell function. Cancer Immunol Immunother 2006;55: 292-298.
82. Chen Q, Fisher DT, Clancy KA, Gauguet JM, Wang WC, Unger E, Rose-John S, von Andrian UH, Baumann H, Evans SS. Fever-range thermal stress promotes lymphocyte trafficking across high endothelial venules via an interleukin 6 trans-signaling mechanism. Nat Immunol 2006;7: 1299-1308.
83. Chen Q, Fisher DT, Kucinska SA, Wang WC, Evans SS. Dynamic control of lymphocyte trafficking by fever-range thermal stress. Cancer Immunol Immunother 2006;55: 299-311.
84. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: Tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 2002;23:549-555.
85. Bingle L, Brown NJ, Lewis CE. The role of tumour-associated macrophages in tumour progression: Implications for new anticancer therapies. J Pathol 2002;196:254-265.
86. Yamashiro S, Takeya M, Nishi T, Kuratsu J, Yoshimura T, Ushio Y, Takahashi K. Tumor-derived monocyte chemoattractant protein-1 induces intratumoral infiltration of monocyte- derived macrophage subpopulation in transplanted rat tumors. Am J Pathol 1994;145:856-867.
87. Fischer C, Jonckx B, Mazzone M, Zacchigna S, Loges S, Pattarini L, Chorianopoulos E, Liesenborghs L, Koch M, De Mol M, et al. Anti-PlGF inhibits growth of VEGF(R)- inhibitor-resistant tumors without affecting healthy vessels. Cell 2007;131:463-475.
88. Scotton C, Milliken D, Wilson J, Raju S, Balkwill F. Analysis of CC chemokine and chemokine receptor expression in solid ovarian tumours. Brit J Cancer 2001;85:891-897.
89. Leek RD, Lewis CE, Whitehouse R, Greenall M, Clarke J, Harris AL. Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res 1996;56:4625-4629.
90. Onita T, Ji PG, Xuan JW, Sakai H, Kanetake H, Maxwell PH, Fong GH, Gabril MY, Moussa M, Chin JL. Hypoxiainduced, perinecrotic expression of endothelial Per-ARNTSim domain protein-1/hypoxia-inducible factor-2α correlates with tumor progression, vascularization, and focal macrophage infiltration in bladder cancer. Clin Cancer Res 2002;8:471-480.
91. Valkovic T, Dobrila F, Melato M, Sasso F, Rizzardi C, Jonjic N. Correlation between vascular endothelial growth factor, angiogenesis, and tumor-associated macrophages in invasive ductal breast carcinoma. Virchows Arch 2002;440:583-588.
92. Li C, Shintani S, Terakado N, Nakashiro K, Hamakawa H. Infiltration of tumor-associated macrophages in human oral squamous cell carcinoma. Oncol Rep 2002;9:1219-1223.
93. Biswas SK, Gangi L, Paul S, Schioppa T, Saccani A, Sironi M, Bottazzi B, Doni A, Vincenzo B, Pasqualini F, et al. A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF-κB and enhanced IRF-3/STAT1 activation). Blood 2006;107: 2112-2122.
94. Saccani A, Schioppa T, Porta C, Biswas SK, Nebuloni M, Vago L, Bottazzi B, Colombo MP, Mantovani A, Sica A. p50 Nuclear factor-κB overexpression in tumor-associated macrophages inhibits M1 inflammatory responses and antitumor resistance. Cancer Res 2006;66:11432-11440.
95. Dirkx AE, Oude Egbrink MG, Wagstaff J, Griffioen AW. Monocyte/macrophage infiltration in tumors: Modulators of angiogenesis. J Leukoc Biol 2006;80:1183-1196.
96. Biswas SK, Sica A, Lewis CE. Plasticity of macrophage function during tumor progression: Regulation by distinct molecular mechanisms. J Immunol 2008;180:2011-2017.
97. Muckle DS, Dickson JA, Johnston ID. The adjuvant effect of hyperthermia on the response of the VX2 carcinoma in rabbits to methotrexate or radiotherapy. Brit J Surg 1971;58:869.
98. Overgaard K, Overgaard J. Investigation on the possibility of a thermic tumour therapy. II. Action of combined heatroentgen treatment on a transplanted mouse mammary carcinoma. Eur J Cancer 1972;8:573-575.
99. Shah SA. Participation of the immune system in regression of a rat Mc7 sarcoma by hyperthermia. Cancer Res 1981;41:1742-1747.
100. Ito A, Tanaka K, Kondo K, Shinkai M, Honda H, Matsumoto K, Saida T, Kobayashi T. Tumor regression by combined immunotherapy and hyperthermia using magnetic nanoparticles in an experimental subcutaneous murine melanoma. Cancer Sci 2003;94:308-313.
101. Ivarsson K, Myllymaki L, Jansner K, Stenram U, Tranberg KG. Resistance to tumour challenge after tumour laser thermotherapy is associated with a cellular immune response. Brit J Cancer 2005;93:435-440.
102. Kubes J, Svoboda J, Rosina J, Starec M, Fiserova A. Immunological response in the mouse melanoma model after local hyperthermia. Physiol Res 2008;57: 459-465.
103. van Note S, Kisailus A, Hylander B, Ostberg J, Evans S, Repasky E. The effects of fever-range whole body hyperthermia on macrophage infiltration in tumors. In: World Conference on Interventional Oncology. Los Angeles, CA; 2007; Poster no. 31.
104. Szmigielski S, Janiak M, Hryniewicz W, Jeljaszewicz J, Pulverer G. Local microwave hyperthermia (43°C) and stimulation of the macrophage and T-lymphocyte systems in treatment of Guerin epithelioma in rats. Z Krebsforsch Klin Onkol Cancer Res Clin Oncol 1978;91:35-48.
105. Klostergaard J, Barta M, Tomasovic SP. Hyperthermic modulation of tumor necrosis factor-dependent monocyte/ macrophage tumor cytotoxicity in vitro. J Biol Response Mod 1989;8:262-277. (Pubitemid 19146192)
106. Tomasovic SP, Barta M, Klostergaard J. Temporal dependence of hyperthermic augmentation of macrophage-TNF production and tumor cell-TNF sensitization. Int J Hyperthermia 1989;5:625-639.
107. Tomasovic SP, Klostergaard J. Hyperthermic modulation of macrophage-tumor cell interactions. Cancer Metastasis Rev 1989;8:215-229.
108. Jedinak A, Dudhgaonkar S, Sliva D. Activated macrophages induce metastatic behavior of colon cancer cells. Immunobiology 2009, in press.
109. Vukanovic J, Isaacs JT. Linomide inhibits angiogenesis, growth, metastasis, and macrophage infiltration within rat prostatic cancers. Cancer Res 1995;55:1499-1504.
110. Leek RD, Harris AL. Tumor-associated macrophages in breast cancer. J Mammary Gland Biol Neoplasia 2002;7:177-189.
111. Murdoch C, Muthana M, Coffelt SB, Lewis CE. The role of myeloid cells in the promotion of tumour angiogenesis. Nat Rev Cancer 2008;8:618-631.
112. Chen BD, Sapareto SA, Chou TH. Induction of prostaglandin production by hyperthermia in murine peritoneal exudate macrophages. Cancer Res 1987;47:11-15.
113. Cameron DJ, Stromberg BV. The ability of macrophages from head and neck cancer patients to kill tumor cells. Effect of prostaglandin inhibitors on cytotoxicity. Cancer 1984;54:2403-2408.
114. Wang D, Wang H, Brown J, Daikoku T, Ning W, Shi Q, Richmond A, Strieter R, Dey SK, DuBois RN. CXCL1 induced by prostaglandin E2 promotes angiogenesis in colorectal cancer. J Exp Med 2006;203:941-951.
115. Bonney RJ, Humes JL. Physiological and pharmacological regulation of prostaglandin and leukotriene production by macrophages. J Leukoc Biol 1984;35:1-10.
116. Leek RD, Landers RJ, Harris AL, Lewis CE. Necrosis correlates with high vascular density and focal macrophage infiltration in invasive carcinoma of the breast. Brit J Cancer 1999;79:991-995.
117. Ohno S, Ohno Y, Suzuki N, Kamei T, Koike K, Inagawa H, Kohchi C, Soma G, Inoue M. Correlation of histological localization of tumor-associated macrophages with clinicopathological features in endometrial cancer. Anticancer Res 2004;24:3335-3342.
118. Negus RP, Stamp GW, Hadley J, Balkwill FR. Quantitative assessment of the leukocyte infiltrate in ovarian cancer and its relationship to the expression of C-C chemokines. Am J Pathol 1997;150:1723-1734.
119. Bailey C, Negus R, Morris A, Ziprin P, Goldin R, Allavena P, Peck D, Darzi A. Chemokine expression is associated with the accumulation of tumour associated macrophages (TAMs) and progression in human colorectal cancer. Clin Exp Metastasis 2007;24:121-130.
120. Kim JH, Kim SH, Hahn EW, Song CW. 5-Thio-D-glucose selectively potentiates hyperthermic killing of hypoxic tumor cells. Science 1978;200:206-207.
121. Herman TS, Teicher BA, Chan V, Collins LS, Abrams MJ. Effect of heat on the cytotoxicity and interaction with DNA of a series of platinum complexes. Int J Radiat Oncol Biol Phys 1989;16:443-449.
122. Jackson IL, Batinic-Haberle I, Sonveaux P, Dewhirst MW, Vujaskovic Z. ROS production and angiogenic regulation by macrophages in response to heat therapy. Int J Hyperthermia 2006;22:263-273.