Local tumour hyperthermia as immunotherapy for metastatic cancer

International Journal of Hyperthermia

Volumn 30, Issue 8, 2014, Pages 531-539

  Toraya Brown, Seiko ^a   Fiering, Steven ^a,b  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b NORRIS COTTON CANCER CENTER   (United States)

Author keywords

Biology; Immunotherapy; Local hyperthermia; Tumor immunology; Tumor immunotherapy

Indexed keywords

HEAT SHOCK PROTEIN;

CANCER IMMUNOTHERAPY; CANCER THERAPY; EXOSOME; HYPERTHERMIC THERAPY; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; METASTASIS; REVIEW; TEMPERATURE; TUMOR CELL; TUMOR HYPERTHERMIA; TUMOR VASCULARIZATION; ANIMAL; HISTORY; HUMAN; IMMUNOTHERAPY; NEOPLASMS; PROCEDURES;

ANIMALS; HISTORY, 19TH CENTURY; HISTORY, 20TH CENTURY; HISTORY, ANCIENT; HUMANS; HYPERTHERMIA, INDUCED; IMMUNOTHERAPY; NEOPLASMS;

EID: 84914125557     PISSN: 02656736     EISSN: 14645157     Source Type: Journal    
DOI: 10.3109/02656736.2014.968640     Document Type: Review

References (88)

1. den Brok MH, Sutmuller RP, van der Voort R, Bennink EJ, Figdor CG, Ruers TJ, et al. In situ tumor ablation creates an antigen source for the generation of antitumor immunity. Cancer Res 2004; 64:4024-9.
2. van der Zee J. Heating the patient: A promising approach? Ann Oncol 2002;13:1173-84.
3. Wust P, Hildebrandt B, Sreenivasa G, Rau B, Gellermann J, Riess H, et al. Hyperthermia in combined treatment of cancer. Lancet Oncol 2002;3:487-97.
4. Obeid M, Tesniere A, Panaretakis T, Tufi R, Joza N, van Endert P, et al. Ecto-calreticulin in immunogenic chemotherapy. Immunol Rev 2007;220:22-34.
5. Cao C, Han Y, Ren Y, Wang Y. Mitoxantrone-mediated apoptotic B16-F1 cells induce specific anti-tumor immune response. Cell Mol Immunol 2009;6:469-75.
6. Schiavoni G, Sistigu A, Valentini M, Mattei F, Sestili P, Spadaro F, et al. Cyclophosphamide synergizes with type I interferons through systemic dendritic cell reactivation and induction of immunogenic tumor apoptosis. Cancer Res 2011;71:768-78.
7. Fucikova J, Kralikova P, Fialova A, Brtnicky T, Rob L, Bartunkova J, et al. Human tumor cells killed by anthracyclines induce a tumor-specific immune response. Cancer Res 2011;71: 4821-33.
8. Hornback NB. Historical aspects of hyperthermia in cancer therapy. Radiol Clin North Am 1989;27:481-8.
9. Wiemann B, Starnes CO. Coley's toxins, tumor necrosis factor and cancer research: A historical perspective. Pharmacol Ther 1994;64: 529-64.
10. Miller TR, Nicholson JT. End results in reticulum cell sarcoma of bone treated by bacterial toxin therapy alone or combined with surgery and-or radiotherapy (47 cases) or with concurrent infection (5 cases). Cancer 1971;27:524-48.
11. Nauts HC. Bacterial vaccine therapy of cancer. Dev Biol Stand 1977;38:487-94.
12. Frey B, Weiss EM, Rubner Y, Wunderlich R, Ott OJ, Sauer R, et al. Old and new facts about hyperthermia-induced modulations of the immune system. Int J Hyperthermia 2012;28:528-42.
13. Mayo WJ. Grafting and traumatic dissemination of carcinoma in the course of operations for malignant disease. JAMA 1913;60: 512-13.
14. Curley SA. Radiofrequency ablation of malignant liver tumors. Oncologist 2001;6:14-23.
15. Takada T, Yamashita T, Sato M, Sato A, Ono I, Tamura Y, et al. Growth inhibition of re-challenge B16 melanoma transplant by conjugates of melanogenesis substrate and magnetite nanoparticles as the basis for developing melanoma-targeted chemo-thermo-immunotherapy. J Biomed Biotechnol 2009;2009:457936.
16. Toraya-Brown S, Sheen MR, Zhang P, Chen L, Baird JR, Demidenko E, et al. Local hyperthermia treatment of tumors induces CD8(+) T cell-mediated resistance against distal and secondary tumors. Nanomed Nanotechnol Biol Med 2014;10: 1273-85.
17. Xiaoping L, Leizhen Z. Advances of high intensity focused ultrasound (HIFU) for pancreatic cancer. Int J Hyperthermia 2013;29:678-82.
18. Partanen A, Tillander M, Yarmolenko PS, Wood BJ, Dreher MR, Kohler MO. Reduction of peak acoustic pressure and shaping of heated region by use of multifoci sonications in MR-guided high-intensity focused ultrasound mediated mild hyperthermia. Med Phys 2013;40:013301.
19. Krishnan S, Diagaradjane P, Cho SH. Nanoparticle-mediated thermal therapy: Evolving strategies for prostate cancer therapy. Int J Hyperthermia 2010;26:775-89.
20. Wust P, Gneveckow U, Johannsen M, Bohmer D, Henkel T, Kahmann F, et al. Magnetic nanoparticles for interstitial thermo-therapy-Feasibility, tolerance and achieved temperatures. Int J Hyperthermia 2006;22:673-85.
21. Hildebrandt B, Wust P, Ahlers O, Dieing A, Sreenivasa G, Kerner T, et al. The cellular and molecular basis of hyperthermia. Crit Rev Oncol Hematol 2002;43:33-56.
22. Vidair CA, Dewey WC. Evaluation of a role for intracellular Na+, K+, Ca2+, and Mg2+ in hyperthermic cell killing. Radiat Res 1986;105:187-200.
23. Stevenson MA, Calderwood SK, Hahn GM. Effect of hyperthermia (45 °C) on calcium flux in Chinese hamster ovary HA-1 fibroblasts and its potential role in cytotoxicity and heat resistance. Cancer Res 1987;47:3712-17.
24. Malhotra A, Heynen ML, Lepock JR. Role of extracellular calcium in the hyperthermic killing of CHL V79 cells. Radiat Res 1987;112: 478-89.
25. Nishida T, Akagi K, Tanaka Y Correlation between cell killing effect and cell membrane potential after heat treatment: Analysis using fluorescent dye and flow cytometry. Int J Hyperthermia 1997; 13:227-34.
26. Henle KJ, Leeper DB. Effects of hyperthermia (45°) on macro-molecular synthesis in Chinese hamster ovary cells. Cancer Res 1979;39:2665-74.
27. Spiro IJ, Denman DL, Dewey WC. Effect of hyperthermia on CHO DNA polymerases alpha and beta. Radiat Res 1982;89: 134-49.
28. Kampinga HH, Jorritsma JB, Konings AW. Heat-induced alterations in DNA polymerase activity of HeLa cells and of isolated nuclei. Relation to cell survival. Int J Radiat Biol Relat Stud Phys Chem Med 1985;47:29-40.
29. Jorritsma JB, Kampinga HH, Scaf AH, Konings AW. Strand break repair, DNA polymerase activity and heat radiosensitization in thermotolerant cells. Int J Hyperthermia 1985;1:131-45.
30. Green DR, Ferguson T, Zitvogel L, Kroemer G Immunogenic and tolerogenic cell death. Nat Rev Immunol 2009;9:353-63.
31. Sapareto SA, Dewey WC. Thermal dose determination in cancer therapy. Int J Radiat Oncol Biol Phys 1984;10:787-800.
32. Lepock JR. Cellular effects of hyperthermia: Relevance to the minimum dose for thermal damage. Int J Hyperthermia 2003;19: 252-66.
33. Ostberg JR, Dayanc BE, Yuan M, Oflazoglu E, Repasky EA. Enhancement of natural killer (NK) cell cytotoxicity by fever-range 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;82:1322-31.
34. Ito A, Tanaka K, Kondo K, Shinkai M, Honda H, Matsumoto K, et al. Tumor regression by combined immunotherapy and hyperthermia using magnetic nanoparticles in an experimental subcutaneous murine melanoma. Cancer Sci 2003;94:308-13.
35. Jaattela M. Heat shock proteins as cellular lifeguards. Ann Med 1999;31:261-71.
36. 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;158:4341-50.
37. Botzler C, Li G, Issels RD, Multhoff G. Definition of extracellular localized epitopes of Hsp70 involved in an NK immune response. Cell Stress Chaperon 1998;3:6-11.
38. Roigas J, Wallen ES, Loening SA, Moseley PL. Heat shock protein (Hsp72) surface expression enhances the lysis of a human renal cell carcinoma by IL-2 stimulated NK cells. Adv Exp Med Biol 1998; 451:225-9.
39. Multhoff G, Mizzen L, Winchester CC, Milner CM, Wenk S, Eissner G, et al. Heat shock protein 70 (Hsp70) stimulates proliferation and cytolytic activity of natural killer cells. Exp Hematol 1999;27:1627-36.
40. Vabulas RM, Ahmad-Nejad P, Ghose S, Kirschning CJ, Issels RD, Wagner H. Hsp70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. J Biol Chem 2002;277:15107-12.
41. Asea A, Rehli M, Kabingu E, Boch JA, Bare O, Auron PE, et al. Novel signal transduction pathway utilized by extracellular Hsp70: Role of Toll-like receptor (TLR) 2 and TLR4. J Biol Chem 2002; 277:15028-34.
42. Todryk S, Melcher AA, Hardwick N, Linardakis E, Bateman A, Colombo MP, et al. Heat shock protein 70 induced during tumor cell killing induces Th1 cytokines and targets immature dendritic cell precursors to enhance antigen uptake. J Immunol 1999;163: 1398-408.
43. Noessner E, Gastpar R, Milani V, Brandl A, Hutzler PJ, Kuppner MC, et al. Tumor-derived heat shock protein 70 peptide complexes are cross-presented by human dendritic cells. J Immunol 2002;169:5424-32.
44. Suzue K, Zhou X, Eisen HN, Young RA. Heat shock fusion proteins as vehicles for antigen delivery into the major histocom-patibility complex class I presentation pathway. Proc Natl Acad Sci USA 1997;94:13146-51.
45. Suto R, Srivastava PK. A mechanism for the specific immunogen-icity of heat shock protein-chaperoned peptides. Science 1995;269: 1585-8.
46. Binder RJ, Srivastava PK. Peptides chaperoned by heat-shock proteins are a necessary and sufficient source of antigen in the cross-priming of CD8+ T cells. Nat Immunol 2005;6: 593-9.
47. Udono H, Levey DL, Srivastava PK. Cellular requirements for tumor-specific immunity elicited by heat shock proteins: Tumor rejection antigen gp96 primes CD8+ T cells in vivo. Proc Natl Acad Sci USA 1994;91:3077-81.
48. Bethke K, Staib F, Distler M, Schmitt U, Jonuleit H, Enk AH, et al. Different efficiency of heat shock proteins (HSP) to activate human monocytes and dendritic cells: superiority of Hsp60. J Immunol 2002;169:6141-8.
49. Breloer M, Dorner B, More SH, Roderian T, Fleischer B, von Bonin A. Heat shock proteins as 'danger signals': eukaryotic Hsp60 enhances and accelerates antigen-specific IFN-gamma production in T cells. Eur J Immunol 2001;31:2051-9.
50. Neckers L. Hsp90 inhibitors as novel cancer chemotherapeutic agents. Trends Mol Med 2002;8:S55-61.
51. Lin K, Rockliffe N, Johnson GG, Sherrington PD, Pettitt AR. Hsp90 inhibition has opposing effects on wild-type and mutant p53 and induces p21 expression and cytotoxicity irrespective of p53/ATM status in chronic lymphocytic leukaemia cells. Oncogene 2008;27:2445-55.
52. Huntoon CJ, Nye MD, Geng L, Peterson KL, Flatten KS, Haluska P, et al. Heat shock protein 90 inhibition depletes LATS1 and LATS2, two regulators of the mammalian hippo tumor suppressor pathway. Cancer Res 2010;70:8642-50.
53. Qian J, Yi H, Guo C, Yu X, Zuo D, Chen X, et al. CD204 suppresses large heat shock protein-facilitated priming of tumor antigen gp100-specific T cells and chaperone vaccine activity against mouse melanoma. J Immunol 2011;187:2905-14.
54. Ito A, Fujioka M, Tanaka K, Kobayashi T, Honda H. Screening of cytokines to enhance vaccine effects of heat shock protein 70-rich tumor cell lysate. J Biosci Bioeng 2005;100:36-42.
55. DeNardo DG, Brennan DJ, Rexhepaj E, Ruffell B, Shiao SL, Madden SF, et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov 2011;1:54-67.
56. Mitchem JB, Brennan DJ, Knolhoff BL, Belt BA, Zhu Y, Sanford DE, et al. Targeting tumor-infiltrating macrophages decreases tumor-initiating cells, relieves immunosuppression, and improves chemotherapeutic responses. Cancer Res 2013;73: 1128-41.
57. Drake CG. Combination immunotherapy approaches. Ann Oncol 2012;23:Sviii41-6.
58. Thery C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol 2002;2:569-79.
59. Wolfers J, Lozier A, Raposo G, Regnault A, Thery C, Masurier C, et al. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med 2001;7: 297-303.
60. Andre F, Schartz NE, Movassagh M, Flament C, Pautier P, Morice P, et al. Malignant effusions and immunogenic tumour-derived exosomes. Lancet 2002;360(9329):295-305.
61. Bu N, Wu H, Sun B, Zhang G, Zhan S, Zhang R, et al. Exosome-loaded dendritic cells elicit tumor-specific CD8+ cytotoxic T cells in patients with glioma. J Neurooncol 2011;104:659-67.
62. Clayton A, Mitchell JP, Court J, Mason MD, Tabi Z. Human tumor-derived exosomes selectively impair lymphocyte responses to interleukin-2. Cancer Res 2007;67:7458-66.
63. King HW, Michael MZ, Gleadle JM. Hypoxic enhancement of exosome release by breast cancer cells. BMC Cancer 2012;12:421.
64. de Jong OG, Verhaar MC, Chen Y, Vader P, Gremmels H, Posthuma G, et al. Cellular stress conditions are reflected in the protein and RNA content of endothelial cell-derived exosomes. J Extracell Vesicles 2012;1:18396. DOI: 10.3402/jev.v1i0.18396.
65. Dai S, Wan T, Wang B, Zhou X, Xiu F, Chen T, et al. More efficient induction of HLA-A∗0201-restricted and carcinoembryonic antigen (CEA)-specific CTL response by immunization with exosomes prepared from heat-stressed CEA-positive tumor cells. Clin Cancer Res 2005;11:7554-63.
66. Chen T, Guo J, Yang M, Zhu X, Cao X. Chemokine-containing exosomes are released from heat-stressed tumor cells via lipid raft-dependent pathway and act as efficient tumor vaccine. J Immunol 2011;186:2219-28.
67. Andreola G, Rivoltini L, Castelli C, Huber V, Perego P, Deho P, et al. Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. J Exp Med 2002;195:1303-16.
68. Huber V, Fais S, Iero M, Lugini L, Canese P, Squarcina P, et al. Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: Role in immune escape. Gastroenterology 2005;128:1796-804.
69. Clayton A, Tabi Z. Exosomes and the MICA-NKG2D system in cancer. Blood Cells Mol Dis 2005;34:206-13.
70. Valenti R, Huber V, Filipazzi P, Pilla L, Sovena G, Villa A, et al. Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-beta-mediated suppressive activity on T lymphocytes. Cancer Res 2006;66:9290-8.
71. Mace TA, Zhong L, Kokolus KM, Repasky EA. Effector CD8+ T cell IFN-gamma production and cytotoxicity are enhanced by mild hyperthermia. Int J Hyperthermia 2012;28:9-18.
72. Zheng H, Benjamin IJ, Basu S, Li Z. Heat shock factor 1-independent activation of dendritic cells by heat shock: Implication for the uncoupling of heat-mediated immunoregulation from the heat shock response. Eur J Immunol 2003;33:1754-62.
73. Basu S, Srivastava PK. Fever-like temperature induces maturation of dendritic cells through induction of hsp90. Int Immunol 2003;15: 1053-61.
74. Pritchard MT, Li Z, Repasky EA. Nitric oxide production is regulated by fever-range thermal stimulation of murine macrophages. J Leukoc Biol 2005;78:630-8.
75. Yoshioka H, Koga S, Maeta M, Shimizu N, Hamazoe R, Murakami A. The influence of hyperthermia in vitro on the functions of peritoneal macrophages in mice. Jpn J Surg 1990;20: 119-22.
76. van Bruggen I, Robertson TA, Papadimitriou JM. The effect of mild hyperthermia on the morphology and function of murine resident peritoneal macrophages. Exp Mol Pathol 1991;55:119-34.
77. Ostberg JR, Repasky EA. Emerging evidence indicates that physiologically relevant thermal stress regulates dendritic cell function. Cancer Immunol Immunother 2006;55:292-8.
78. Meyer RE, Braun RD, Rosner GL, Dewhirst MW. Local 42°C hyperthermia improves vascular conductance of the R3230Ac rat mammary adenocarcinoma during sodium nitroprusside infusion. Radiat Res 2000;154:196-201.
79. Song CW, Shakil A, Griffin RJ, Okajima K. Improvement of tumor oxygenation status by mild temperature hyperthermia alone or in combination with carbogen. Semin Oncol 1997;24: 626-32.
80. Kong G, Braun RD, Dewhirst MW. Characterization of the effect of hyperthermia on nanoparticle extravasation from tumor vascula-ture. Cancer Res 2001;61:3027-32.
81. Fisher DT, Chen Q, Skitzki JJ, Muhitch JB, Zhou L, Appenheimer MM, et al. IL-6 trans-signaling licenses mouse and human tumor microvascular gateways for trafficking of cytotoxic T cells. J Clin Invest 2011;121:3846-59.
82. Yanase M, Shinkai M, Honda H, Wakabayashi T, Yoshida J, Kobayashi T. Antitumor immunity induction by intracellular hyperthermia using magnetite cationic liposomes. Jpn J Cancer Res 1998;89:775-82.
83. Suzuki M, Shinkai M, Honda H, Kobayashi T. Anticancer effect and immune induction by hyperthermia of malignant melanoma using magnetite cationic liposomes. Melanoma Res 2003;13: 129-35.
84. Tanaka K, Ito A, Kobayashi T, Kawamura T, Shimada S, Matsumoto K, et al. Intratumoral injection of immature dendritic cells enhances antitumor effect of hyperthermia using magnetic nanoparticles. Int J Cancer 2005;116:624-33.
85. Petryk AA, Giustini AJ, Gottesman RE, Trembly BS, Hoopes PJ. Comparison of magnetic nanoparticle and microwave hyperthermia cancer treatment methodology and treatment effect in a rodent breast cancer model. Int J Hyperthermia 2013;29:819-27.
86. Kubes J, Svoboda J, Rosina J, Starec M, Fiserova A. Immunological response in the mouse melanoma model after local hyperthermia. Physiol Res 2008;57:459-65.
87. Chen T, Guo J, Han C, Yang M, Cao X. Heat shock protein 70, released from heat-stressed tumor cells, initiates antitumor immunity by inducing tumor cell chemokine production and activating dendritic cells via TLR4 pathway. J Immunol 2009; 182:1449-59.
88. Bear AS, Kennedy LC, Young JK, Perna SK, Mattos Almeida JP, Lin AY, et al. Elimination of metastatic melanoma using gold nanoshell-enabled photothermal therapy and adoptive T cell transfer. PLoS One 2013;8:e69073.