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http://dx.doi.org/10.5352/JLS.2016.26.9.1088

Effects of Regional Hyperthermia with Moderate Temperature on Cancer Treatment  

Kang, Chi-Dug (Department of Biochemistry, Pusan National University School of Medicine)
Kim, Sun-Hee (Department of Biochemistry, Pusan National University School of Medicine)
Publication Information
Journal of Life Science / v.26, no.9, 2016 , pp. 1088-1096 More about this Journal
Abstract
Despite that moderate hyperthermia can exert various antitumor activities such as direct cytotoxic effects on tumor cells, effects on tumor vasculatures and immunological effects, hyperthermia has been usually combined with radiotherapy or chemotherapy due to its limited efficacy in cancer treatment, showing some positive clinical benefits with generally well-tolerated side effects. Since heat shock responses itself can interfere with the anti-tumor effects of hyperthermia, not all of these studies might have demonstrated positive clinical outcomes in cancer patients. Therefore, the negative anti-tumor effect of hyperthermia should be reduced to enhance the effectiveness of hyperthermia. Although the responses to heat stress of tumor tissues containing vessels, immune cells, connective tissues as well as cancer cells, are very complicated, it is needed to study in the near future if some clinically available drugs, which can modulate heat stress responses, can improve the efficacy of hyperthermia in patients with cancer. In this review, the effect of clinical hyperthermia centered on non-invasive external hyperthermia using radiofrequency at moderate temperature will be discussed, since it is the state-of-the-art technology in the current clinical practice of hyperthermia, and a moderate operational temperature is used to increase the therapeutic effectiveness of conventional therapy without additional toxicity to normal tissues.
Keywords
Cancer; Hyperthermia; Heat stress; Heat shock response;
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1 Richter, K., Haslbeck, M. and Buchner, J. 2010. The heat shock response: life on the verge of death. Mol. Cell 40, 253-266.   DOI
2 Roussakow, S. 2013. The History of Hyperthermia Rise and Decline. Conference Papers in Medicine 2013, http://dx.doi.org/10.1155/2013/428027.
3 Sanchez-Ortiz, R. F., Tannir, N., Ahrar, K. and Wood, C. G. 2003. Spontaneous regression of pulmonary metastases from renal cell carcinoma after radio frequency ablation of primary tumor: an in situ tumor vaccine? J. Urol. 170, 178-179.   DOI
4 Sapareto, S. A. and Dewey, W. C. 1984. Thermal dose determination in cancer therapy. Int. J. Radiat. Oncol. Biol. Phys. 10, 787-800.   DOI
5 Shamovsky, I. and Nudler, E. 2008. New insights into the mechanism of heat shock response activation. Cell Mol. Life Sci. 65, 855-861.   DOI
6 Savina, A., Furlan, M., Vidal, M. and Colombo, M. I. 2003. Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J. Biol. Chem. 278, 20083-20090.   DOI
7 Schlom, J. 2012. Therapeutic cancer vaccines: current status and moving forward. J. Natl. Cancer Inst. 104, 599-613.   DOI
8 Schmitt, E., Maingret, L., Puig, P. E., Rerole, A. L., Ghiringhelli, F., Hammann, A., Solary, E., Kroemer, G. and Garrido, C. 2006. Heat shock protein 70 neutralization exerts potent antitumor effects in animal models of colon cancer and melanoma. Cancer Res. 66, 4191-4197.   DOI
9 Shen, R. N., Lu, L., Young, P., Shidnia, H., Hornback, N. B. and Broxmeyer, H. E. 1994. Influence of elevated temperature on natural killer cell activity, lymphokine-activated killer cell activity and lectin-dependent cytotoxicity of human umbilical cord blood and adult blood cells. Int. J. Radiat. Oncol. Biol. Phys. 29, 821-826.   DOI
10 Shevtsov, M. and Multhoff, G. 2016. Heat shock proteinpeptide and HSP-based immunotherapies for the treatment of cancer. Front. Immunol. 7, 171.
11 Siemann, D. W. and Horsman, M. R. 2015. Modulation of the tumor vasculature and oxygenation to improve therapy. Pharmacol. Ther. 153, 107-124.   DOI
12 Srivastava, P. K. and Amato, R. J. 2001. Heat shock proteins: the ′Swiss Army Knife′ vaccines against cancers and infectious agents. Vaccine 19, 2590-2597.   DOI
13 Srivastava, P. K. and Udono, H. 1994. Heat shock protein-peptide complexes in cancer immunotherapy. Curr. Opin. Immunol. 6, 728-732.   DOI
14 Starnes, C. O. 1992. Coley's toxins in perspective. Nature 357, 11-12.   DOI
15 Valenti, R., Huber, V., Filipazzi, P., Pilla, L., Sovena, G., Villa, A., Corbelli, A., Fais, S., Parmiani, G. and Rivoltini, L. 2006. Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-beta-mediated suppressive activity on T lymphocytes. Cancer Res. 66, 9290-9298.   DOI
16 Tonkiss, J. and Calderwood, S. K. 2005. Regulation of heat shock gene transcription in neuronal cells. Int J Hyperthermia 21, 433-444.   DOI
17 Toraya-Brown, S. and Fiering, S. 2014. Local tumour hyperthermia as immunotherapy for metastatic cancer. Int. J. Hyperthermia 30, 531-539.   DOI
18 Udono, H. and Srivastava, P. K. 1994. Comparison of tumor-specific immunogenicities of stress-induced proteins gp96, hsp90, and hsp70. J. Immunol. 152, 5398-5403.
19 van der Zee, J. 2002. Heating the patient: a promising approach? Ann. Oncol. 13, 1173-1184.   DOI
20 Voellmy, R. 1994. Transduction of the stress signal and mechanisms of transcriptional regulation of heat shock/stress protein gene expression in higher eukaryotes. Crit. Rev. Eukaryot. Gene Expr. 4, 357-401.
21 Whitesell, L. and Lin, N. U. 2012. HSP90 as a platform for the assembly of more effective cancer chemotherapy. Biochim. Biophys. Acta 1823, 756-766.   DOI
22 Whitesell, L. and Lindquist, S. 2009. Inhibiting the transcription factor HSF1 as an anticancer strategy. Expert Opin. Ther. Targets 13, 469-478.   DOI
23 Wolfers, J., Lozier, A., Raposo, G., Regnault, A., Thery, C., Masurier, C., Flament, C., Pouzieux, S., Faure, F., Tursz, T., Angevin, E., Amigorena, S. and Zitvogel, L. 2001. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat. Med. 7, 297-303.   DOI
24 Zhang, Y., Huang, L., Zhang, J., Moskophidis, D. and Mivechi, N. F. 2002. Targeted disruption of hsf1 leads to lack of thermotolerance and defines tissue-specific regulation for stress-inducible Hsp molecular chaperones. J. Cell Biochem. 86, 376-393.   DOI
25 Wust, P., Hildebrandt, B., Sreenivasa, G., Rau, B., Gellermann, J., Riess, H., Felix, R. and Schlag, P. M. 2002. Hyperthermia in combined treatment of cancer. Lancet Oncol. 3, 487-497.   DOI
26 Yang, H. X. and Mitchel, R. E. 1991. Hyperthermic inactivation, recovery and induced thermotolerance of human natural killer cell lytic function. Int. J. Hyperthermia 7, 35-49.   DOI
27 Yao, Y., Wang, C., Wei, W., Shen, C., Deng, X., Chen, L., Ma, L. and Hao, S. 2014. Dendritic cells pulsed with leukemia cell-derived exosomes more efficiently induce antileukemic immunities. PLoS One 9, e91463.   DOI
28 Amaya, C., Kurisetty, V., Stiles, J., Nyakeriga, A. M., Arumugam, A., Lakshmanaswamy, R., Botez, C. E., Mitchell, D. C. and Bryan, B. A. 2014. A genomics approach to identify susceptibilities of breast cancer cells to "fever-range" hyperthermia. BMC Cancer 14, 81.   DOI
29 Ahmed, K. and Zaidi, S. F. 2013. Treating cancer with heat: hyperthermia as promising strategy to enhance apoptosis. J. Pak. Med. Assoc. 63, 504-508.
30 Banerji, U. 2009. Heat shock protein 90 as a drug target: some like it hot. Clin. Cancer Res. 15, 9-14.   DOI
31 Andre, F., Schartz, N. E., Movassagh, M., Flament, C., Pautier, P., Morice, P., Pomel, C., Lhomme, C., Escudier, B., Le Chevalier, T., Tursz, T., Amigorena, S., Raposo, G., Angevin, E. and Zitvogel, L. 2002. Malignant effusions and immunogenic tumour-derived exosomes. Lancet 360, 295-305.   DOI
32 Andreola, G., Rivoltini, L., Castelli, C., Huber, V., Perego, P., Deho, P., Squarcina, P., Accornero, P., Lozupone, F., Lugini, L., Stringaro, A., Molinari, A., Arancia, G., Gentile, M., Parmiani, G. and Fais, S. 2002. Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. J. Exp. Med. 195, 1303-1316.   DOI
33 Chu, K. F. and Dupuy, D. E. 2014. Thermal ablation of tumours: biological mechanisms and advances in therapy. Nat. Rev. Cancer 14, 199-208.   DOI
34 Binder, R. J. and Srivastava, P. K. 2005. Peptides chaperoned by heat-shock proteins are a necessary and sufficient source of antigen in the cross-priming of CD8+ T cells. Nat. Immunol. 6, 593-599.
35 Calderwood, S. K., Khaleque, M. A., Sawyer, D. B. and Ciocca, D. R. 2006. Heat shock proteins in cancer: chaperones of tumorigenesis. Trends Biochem. Sci. 31, 164-172.   DOI
36 Calderwood, S. K., Theriault, J. R. and Gong, J. 2005. How is the immune response affected by hyperthermia and heat shock proteins? Int. J. Hyperthermia 21, 713-716.   DOI
37 Chalmin, F., Ladoire, S., Mignot, G., Vincent, J., Bruchard, M., Remy-Martin, J. P., Boireau, W., Rouleau, A., Simon, B., Lanneau, D., De Thonel, A., Multhoff, G., Hamman, A., Martin, F., Chauffert, B., Solary, E., Zitvogel, L., Garrido, C., Ryffel, B., Borg, C., Apetoh, L., Rebe, C. and Ghiringhelli, F. 2010. Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J. Clin. Invest. 120, 457-471.
38 Chen, T., Guo, J., Yang, M., Zhu, X. and Cao, X. 2011. Chemokine-containing exosomes are released from heatstressed tumor cells via lipid raft-dependent pathway and act as efficient tumor vaccine. J Immunol. 186, 2219-2228.   DOI
39 Chicheł, A., Skowronek, J., Kubaszewska, M. and Kanikowski, M. 2007. Hyperthermia – description of a method and a review of clinical applications. Rep. Pract. Oncol. Radiother. 12, 267-275.   DOI
40 Cihoric, N., Tsikkinis, A., van Rhoon, G., Crezee, H., Aebersold, D. M., Bodis, S., Beck, M., Nadobny, J., Budach, V., Wust, P. and Ghadjar, P. 2015. Hyperthermia-related clinical trials on cancer treatment within the ClinicalTrials. gov registry. Int. J. Hyperthermia 31, 609-614.   DOI
41 Clayton, A., Mitchell, J. P., Court, J., Mason, M. D. and Tabi, Z. 2007. Human tumor-derived exosomes selectively impair lymphocyte responses to interleukin-2. Cancer Res. 67, 7458-7466.   DOI
42 Dai, S., Wan, T., Wang, B., Zhou, X., Xiu, F., Chen, T., Wu, Y. and Cao, X. 2005. 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. 11, 7554-7563.   DOI
43 Endo, H., Yano, M., Okumura, Y. and Kido, H. 2014. Ibuprofen enhances the anticancer activity of cisplatin in lung cancer cells by inhibiting the heat shock protein 70. Cell Death Dis. 5, e1027.   DOI
44 Datta, N. R., Ordonez, S. G., Gaipl, U. S., Paulides, M. M., Crezee, H., Gellermann, J., Marder, D., Puric, E. and Bodis, S. 2015. Local hyperthermia combined with radiotherapy and-/or chemotherapy: recent advances and promises for the future. Cancer Treat. Rev. 41, 742-753.   DOI
45 Dewhirst, M. W., Viglianti, B. L., Lora-Michiels, M., Hanson, M. and Hoopes, P. J. 2003. Basic principles of thermal dosimetry and thermal thresholds for tissue damage from hyperthermia. Int. J. Hyperthermia 19, 267-294.   DOI
46 Dickson, J. A. and Calderwood, S. K. 1980. Temperature range and selective sensitivity of tumors to hyperthermia: a critical review. Ann. N. Y. Acad. Sci. 335, 180-205.   DOI
47 Habash, R. W., Bansal, R., Krewski, D. and Alhafid, H. T. 2006. Thermal therapy, part 2: hyperthermia techniques. Crit. Rev. Biomed. Eng. 34, 491-542.   DOI
48 Frey, B., Weiss, E. M., Rubner, Y., Wunderlich, R., Ott, O. J., Sauer, R., Fietkau, R. and Gaipl, U. S. 2012. Old and new facts about hyperthermia-induced modulations of the immune system. Int. J. Hyperthermia 28, 528-542.   DOI
49 Fuggetta, M. P., Alvino, E., Tricarico, M., D′Atri, S., Pepponi, R., Prete, S. P. and Bonmassar, E. 2000. In vitro effect of hyperthermia on natural cell-mediated cytotoxicity. Anticancer Res. 20, 1667-1672.
50 Groh, V., Bahram, S., Bauer, S., Herman, A., Beauchamp, M. and Spies, T. 1996. Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc. Natl. Acad. Sci. USA 93, 12445-12450.   DOI
51 Hildebrandt, B., Wust, P., Ahlers, O., Dieing, A., Sreenivasa, G., Kerner, T., Felix, R. and Riess, H. 2002. The cellular and molecular basis of hyperthermia. Crit. Rev. Oncol. Hematol. 43, 33-56.   DOI
52 Harada, H., Murakami, T., Tea, S. S., Takeuchi, A., Koga, T., Okada, S., Suico, M. A., Shuto, T. and Kai, H. 2007. Heat shock suppresses human NK cell cytotoxicity via regulation of perforin. Int. J. Hyperthermia 23, 657-665.   DOI
53 Hedlund, M., Nagaeva, O., Kargl, D., Baranov, V. and Mincheva-Nilsson, L. 2011. Thermal- and oxidative stress causes enhanced release of NKG2D ligand-bearing immunosuppressive exosomes in leukemia/lymphoma T and B cells. PLoS One 6, e16899.   DOI
54 Heike, M., Noll, B. and Meyer zum Buschenfelde, K. H. 1996. Heat shock protein-peptide complexes for use in vaccines. J. Leukoc. Biol. 60, 153-158.
55 Hobohm, U. 2001. Fever and cancer in perspective. Cancer Immunol. Immunother. 50, 391-396.
56 Kennedy, D., Jager, R., Mosser, D. D. and Samali, A. 2014. Regulation of apoptosis by heat shock proteins. IUBMB Life 66, 327-338.   DOI
57 Horsman, M. R. and Overgaard, J. 2007. Hyperthermia: a potent enhancer of radiotherapy. Clin. Oncol. (R. Coll. Radiol.) 19, 418-426.   DOI
58 Huber, V., Fais, S., Iero, M., Lugini, L., Canese, P., Squarcina, P., Zaccheddu, A., Colone, M., Arancia, G., Gentile, M., Seregni, E., Valenti, R., Ballabio, G., Belli, F., Leo, E., Parmiani, G. and Rivoltini, L. 2005. Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: role in immune escape. Gastroenterology 128, 1796-1804.   DOI
59 Ischia, J. and So, A. I. 2013. The role of heat shock proteins in bladder cancer. Nat. Rev. Urol. 10, 386-395.   DOI
60 Ishii, T., Udono, H., Yamano, T., Ohta, H., Uenaka, A., Ono, T., Hizuta, A., Tanaka, N., Srivastava, P. K. and Nakayama, E. 1999. Isolation of MHC class I-restricted tumor antigen peptide and its precursors associated with heat shock proteins hsp70, hsp90, and gp96. J. Immunol. 162, 1303-1309.
61 Iwata, K., Shakil, A., Hur, W. J., Makepeace, C. M., Griffin, R. J. and Song, C. W. 1996. Tumour pO2 can be increased markedly by mild hyperthermia. Br. J. Cancer Suppl. 27, S217- 221.
62 Jego, G., Hazoume, A., Seigneuric, R. and Garrido, C. 2013. Targeting heat shock proteins in cancer. Cancer Lett. 332, 275-285.   DOI
63 Kim, H., Park, B. K. and Kim, C. K. 2008. Spontaneous regression of pulmonary and adrenal metastases following percutaneous radiofrequency ablation of a recurrent renal cell carcinoma. Kor. J. Radiol. 9, 470-472.   DOI
64 Mallory, M., Gogineni, E., Jones, G. C., Greer, L. and Simone, C. B. 2nd. 2016. Therapeutic hyperthermia: The old, the new, and the upcoming. Crit. Rev. Oncol. Hematol. 97, 56-64.   DOI
65 Kim, J. Y., Son, Y. O., Park, S. W., Bae, J. H., Chung, J. S., Kim, H. H., Chung, B. S., Kim, S. H. and Kang, C. D. 2006. Increase of NKG2D ligands and sensitivity to NK cell-mediated cytotoxicity of tumor cells by heat shock and ionizing radiation. Exp. Mol. Med. 38, 474-484.   DOI
66 Kim, S. J., Ha, G. H., Kim, S. H. and Kang, C. D. 2014. Combination of cancer immunotherapy with clinically available drugs that can block immunosuppressive cells. Immunol. Invest. 43, 517-534.   DOI
67 Labani-Motlagh, A., Israelsson, P., Ottander, U., Lundin, E., Nagaev, I., Nagaeva, O., Dehlin, E., Baranov, V. and Mincheva-Nilsson, L. 2016. Differential expression of ligands for NKG2D and DNAM-1 receptors by epithelial ovarian cancer-derived exosomes and its influence on NK cell cytotoxicity. Tumour Biol. 37, 5455-5466.   DOI
68 Lanneau, D., Brunet, M., Frisan, E., Solary, E., Fontenay, M. and Garrido, C. 2008. Heat shock proteins: essential proteins for apoptosis regulation. J. Cell Mol. Med. 12, 743-761.   DOI
69 Lepock, J. R. 2003. Cellular effects of hyperthermia: relevance to the minimum dose for thermal damage. Int. J. Hyperthermia 19, 252-266.   DOI
70 Lopez-Soto, A., Huergo-Zapico, L., Acebes-Huerta, A., Villa-Alvarez, M. and Gonzalez, S. 2015. NKG2D signaling in cancer immunosurveillance. Int. J. Cancer 136, 1741-1750.   DOI
71 Marleau, A. M., Chen, C. S., Joyce, J. A. and Tullis, R. H. 2012. Exosome removal as a therapeutic adjuvant in cancer. J. Transl. Med. 10, 134.   DOI
72 Multhoff, G. 1997. Heat shock protein 72 (HSP72), a hyperthermia-inducible immunogenic determinant on leukemic K562 and Ewing's sarcoma cells. Int. J. Hyperthermia 13, 39-48.   DOI
73 Melero, I., Berman, D. M., Aznar, M. A., Korman, A. J., Perez Gracia, J. L. and Haanen, J. 2015. Evolving synergistic combinations of targeted immunotherapies to combat cancer. Nat. Rev. Cancer 15, 457-472.   DOI
74 Mincheva-Nilsson, L. and Baranov, V. 2014. Cancer exosomes and NKG2D receptor-ligand interactions: impairing NKG2D-mediated cytotoxicity and anti-tumour immune surveillance. Semin. Cancer Biol. 28, 24-30.   DOI
75 Morimoto, R. I. 1998. Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 12, 3788-3796.   DOI
76 Rampersaud, E. N., Vujaskovic, Z. and Inman, B. A. 2010. Hyperthermia as a treatment for bladder cancer. Oncology (Williston Park) 24, 1149-1155.
77 Multhoff, G., Botzler, C., Wiesnet, M., Eissner, G. and Issels, R. 1995. CD3- large granular lymphocytes recognize a heat-inducible immunogenic determinant associated with the 72-kD heat shock protein on human sarcoma cells. Blood 86, 1374-1382.
78 Multhoff, G., Botzler, C., Wiesnet, M., Muller, E., Meier, T., Wilmanns, W. and Issels, R. D. 1995. A stress-inducible 72-kDa heat-shock protein (HSP72) is expressed on the surface of human tumor cells, but not on normal cells. Int. J. Cancer 61, 272-279.   DOI
79 Piper, P. W. and Millson, S. H. 2011. Mechanisms of resistance to Hsp90 inhibitor drugs: a complex mosaic emerges. Pharmaceuticals 1400-1422.
80 Raulet, D. H., Gasser, S., Gowen, B. G., Deng, W. and Jung, H. 2013. Regulation of ligands for the NKG2D activating receptor. Annu. Rev. Immunol. 31, 413-441.   DOI