Increasing the rate of heating: A potential therapeutic approach for achieving synergistic tumour killing in combined hyperthermia and chemotherapy

References

• Mostafa EM, Ganguli S, Faintuch S, Mertyna P, Goldberg SN. Optimal strategies for combining transcatheter arterial chemoembolization and radiofrequency ablation in rabbit VX2 hepatic tumors. J Vasc Intervent Radiol 2008; 19: 1740–1748
   PubMed Web of Science ®Google Scholar
• Taeger G, Grabellus F, Podleska LE, Mèuller S, Ruchholtz S. Effectiveness of regional chemotherapy with TNF-alpha/melphalan in advanced soft tissue sarcoma of the extremities. Int J Hyperthermia 2008; 24: 193–203
   PubMed Web of Science ®Google Scholar
• Ko SH, Ueno T, Yoshimoto Y, Yoo JS, Abdel-Wahab OI, Abdel-Wahab Z, et al. Optimizing a novel regional chemotherapeutic agent against melanoma: Hyperthermia-induced enhancement of temozolomide cytotoxicity. Clin Cancer Res 2006; 12: 289–297
   PubMed Web of Science ®Google Scholar
• Kampinga HH. Cell biological effects of hyperthermia alone or combined with radiation or drugs: A short introduction to newcomers in the field. Int J Hyperthermia 2006; 22: 191–196
   PubMed Web of Science ®Google Scholar
• Gottesman MM. How cancer cells evade chemotherapy: Sixteenth Richard and Hinda Rosenthal Foundation Award Lecture. Cancer Res 1993; 53: 747–754
   PubMed Web of Science ®Google Scholar
• Riordan JR, Deuchars K, Kartner N, Alon N, Trent J, Ling V. Amplification of P-glycoprotein genes in multidrug-resistant mammalian cell lines. Nature 1985; 316: 817–819
   PubMed Web of Science ®Google Scholar
• Liu Y, Cho CW, Yan X, Henthorn TK, Lillehei KO, Cobb WN, et al. Ultrasound-induced hyperthermia increases cellular uptake and cytotoxicity of P-glycoprotein substrates in multi-drug resistant cells. Pharm Res 2001; 18: 1255–1261
   PubMed Web of Science ®Google Scholar
• Huang CH, Li YP, Cao PG, Xie ZX, Qin ZQ. Synergistic effect of hyperthermia and neferine on reverse multidrug resistance in adriamycin-resistant SGC7901/ADM gastric cancer cells. J Huazhong Univ Sci Tech Med Sci 2011; 31: 488–496
   PubMed Web of Science ®Google Scholar
• Bidwell GL, Davis AN, Fokt I, Priebe W, Raucher D. A thermally targeted elastin-like polypeptide-doxorubicin conjugate overcomes drug resistance. Investig New Drug 2007; 25: 313–326
   PubMed Web of Science ®Google Scholar
• Moriyama-Gonda N, Igawa M, Shiina H, Wada Y. Heat-induced membrane damage combined with adriamycin on prostate carcinoma PC-3 cells: Correlation of cytotoxicity, permeability and P-glycoprotein or metallothionein expression. Br J Urology 1998; 82: 552–559
   PubMedGoogle Scholar
• Pietzner K, Schmuck RB, Fotopoulou C, Gellermann J, Ismaeel F, Cho CH, et al. Long term combination treatment with bevacizumab, pegylated liposomal doxorubicin and regional abdominal hyperthermia in platinum refractory ovarian cancer: A case report and review of the literature. Anticancer Res 2011; 31: 2675–2677
   PubMed Web of Science ®Google Scholar
• Feyerabend S, Stevanovic S, Gouttefangeas C, Wernet D, Hennenlotter J, Bedke J, et al. Novel multi-peptide vaccination in HLA-A2+ hormone sensitive patients with biochemical relapse of prostate cancer. Prostate 2009; 69: 917–927
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Christophi C, Winkworth A, Muralihdaran V, Evans P. The treatment of malignancy by hyperthermia. Surg Oncol 1998; 7: 83–90
   PubMed Web of Science ®Google Scholar
• Tang Y, McGoron AJ. Combined effects of laser-ICG photothermotherapy and doxorubicin chemotherapy on ovarian cancer cells. J Photochem Photobiol B Biol 2009; 97: 138–144
   PubMed Web of Science ®Google Scholar
• Li GC, Mivechi NF, Weitzel G. Heat shock proteins, thermotolerance, and their relevance to clinical hyperthermia. Int J Hyperthermia 1995; 11: 459–488
   PubMed Web of Science ®Google Scholar
• Anderson RL, Herman TS, van Kersen I, Hahn GM. Thermotolerance and heat shock protein induction by slow rates of heating. Int J Radiat Oncol Biol Phys 1988; 15: 717–725
   PubMed Web of Science ®Google Scholar
• Herman TS, Sweets CC, White DM, Gerner EW. Effect of heating on lethality due to hyperthermia and selected chemotherapeutic drugs. J Natl Cancer Inst 1982; 68: 487–491
   PubMedGoogle Scholar
• Hahn GM, Strande DP. Cytotoxic effects of hyperthermia and adriamycin on Chinese hamster cells. J Natl Cancer Inst 1976; 57: 1063–1067
   PubMed Web of Science ®Google Scholar
• Ponce AM, Vujaskovic Z, Yuan F, Needham D, Dewhirst MW. Hyperthermia mediated liposomal drug delivery. Int J Hyperthermia 2006; 22: 205–213
   PubMed Web of Science ®Google Scholar
• Mackay JA, Chilkoti A. Temperature sensitive peptides: Engineering hyperthermia-directed therapeutics. Int J Hyperthermia 2008; 24: 483–495
   PubMed Web of Science ®Google Scholar
• Yarmolenko PS, Zhao Y, Landon C, Spasojevic I, Yuan F, Needham D, et al. Comparative effects of thermosensitive doxorubicin-containing liposomes and hyperthermia in human and murine tumours. Int J Hyperthermia 2010; 26: 485–498
   PubMed Web of Science ®Google Scholar
• Kampinga HH. Hyperthermia, thermotolerance and topoisomerase II inhibitors. Br J Cancer 1995; 72: 333–338
   PubMed Web of Science ®Google Scholar
• Ciocca DR, Oesterreich S, Chamness GC, McGuire WL, Fuqua SA. Biological and clinical implications of heat shock protein 27 000 (Hsp27): A review. J Natl Cancer Institute 1993; 85: 1558–1570
   PubMed Web of Science ®Google Scholar
• Oh HJ, Chen X, Subjeck JR. Hsp110 protects heat-denatured proteins and confers cellular thermoresistance. J Biol Chem 1997; 272: 31636–31640
   PubMed Web of Science ®Google Scholar
• Fisher B, Kraft P, Hahn GM, Anderson RL. Thermotolerance in the absence of induced heat shock proteins in a murine lymphoma. Cancer Res 1992; 52: 2854–2861
   PubMed Web of Science ®Google Scholar
• Sapareto SA, Dewey WC. Thermal dose determination in cancer therapy. Int J Radiat Oncol Biol Phys 1984; 10: 787–800
   PubMed Web of Science ®Google Scholar
• Rezai KA, Farrokh-Siar L, Ernest JT, van Seventer GA. Indocyanine green induces apoptosis in human retinal pigment epithelial cells. Am J Ophthalmol 2004; 137: 931–933
   PubMed Web of Science ®Google Scholar
• Wolfe JD, Csaky KG. Indocyanine green enhanced retinal vessel laser closure in rats: Histologic and immunohistochemical observations. Exp Eye Res 2004; 79: 631–638
   PubMed Web of Science ®Google Scholar
• Flanagan SW, Ryan AJ, Gisolfi CV, Moseley PL. Tissue-specific Hsp70 response in animals undergoing heat-stress. Am J Physiol-Regulat Integr Compar Physiol 1995; 268: R28–R32
   PubMed Web of Science ®Google Scholar
• Burns CP, Lambert BJ, Haugstad BN, Guffy MM. Influence of rate of heating on thermosensitivity of L1210 leukemia – membrane-lipids and Mr 70 000 heat-shock protein. Cancer Res 1986; 46: 1882–1887
   PubMed Web of Science ®Google Scholar
• Herman TS, Gerner EW, Magun BE, Stickney D, Sweets CC, White DM. Rate of heating as a determinant of hyperthermic cyto-toxicity. Cancer Res 1981; 41: 3519–3523
   PubMed Web of Science ®Google Scholar
• Amorim FT, Yamada PM, Robergs RA, Schneider SM, Moseley PL. The effect of the rate of heat storage on serum heat shock protein 72 in humans. Eur J Appl Physiol 2008; 104: 965–972
   PubMed Web of Science ®Google Scholar
• De Maio A. Heat shock proteins: Facts, thoughts, and dreams. Shock 1999; 11: 1–12
   PubMed Web of Science ®Google Scholar
• Donaldson SS, Gordon LF, Hahn GM. Protective effect of hyperthermia against the cytotoxicity of actinomycin D on Chinese hamster cells. Cancer Treat Rep 1978; 62: 1489–1495
   PubMedGoogle Scholar
• Wallner K, Li GC. Adriamycin resistance, heat resistance and radiation response in Chinese hamster fibroblasts. Int J Radiat Oncol Biol Phys 1986; 12: 829–833
   PubMed Web of Science ®Google Scholar
• Pirity M, Hever-Szabo A, Venetianer A. Overexpression of P-glycoprotein in heat- and/or drug-resistant hepatoma variants. Cytotechnol 1996; 19: 207–214
   PubMed Web of Science ®Google Scholar
• Tchénio T, Havard M, Martinez LA, Dautry F. Heat shock-independent induction of multidrug resistance by heat shock factor 1. Mol Cell Biol 2006; 26: 580–591
   PubMed Web of Science ®Google Scholar
• Thorburn A, Frankel AE. Apoptosis and anthracycline cardiotoxicity. Mol Cancer Therapeut 2006; 5: 197–199
   PubMed Web of Science ®Google Scholar
• Ling YH, Priebe W, Perez-Soler R. Apoptosis induced by anthracycline antibiotics in P388 parent and multidrug-resistant cells. Cancer Res 1993; 53: 1845–1852
   PubMed Web of Science ®Google Scholar
• Skladanowski A, Konopa J. Adriamycin and daunomycin induce programmed cell death (apoptosis) in tumour cells. Biochem Pharmacol 1993; 46: 375–382
   PubMed Web of Science ®Google Scholar
• Zaleskis G, Berleth E, Verstovsek S, Ehrke MJ, Mihich E. Doxorubicin-induced DNA degradation in murine thymocytes. Mol Pharmacol 1994; 46: 901–908
   PubMed Web of Science ®Google Scholar
• Bose R, Verheij M, Haimovitz-Friedman A, Scotto K, Fuks Z, Kolesnick R. Ceramide synthase mediates daunorubicin-induced apoptosis: An alternative mechanism for generating death signals. Cell 1995; 82: 405–414
   PubMed Web of Science ®Google Scholar
• Jaffrâezou JP, Levade T, Bettaèieb A, Andrieu N, Bezombes C, Maestre N, et al. Daunorubicin-induced apoptosis: Triggering of ceramide generation through sphingomyelin hydrolysis. EMBO J 1996; 15: 2417–2424
   PubMed Web of Science ®Google Scholar
• Angelini A, Iezzi M, Di Febbo C, Di Ilio C, Cuccurullo F, Porreca E. Reversal of P-glycoprotein-mediated multidrug resistance in human sarcoma MES-SA/Dx-5 cells by nonsteroidal anti-inflammatory drugs. Oncol Rep 2008; 20: 731–735
   PubMed Web of Science ®Google Scholar
• Samali A, Holmberg CI, Sistonen L, Orrenius S. Thermotolerance and cell death are distinct cellular responses to stress: Dependence on heat shock proteins. FEBS Lett 1999; 461: 306–310
   PubMed Web of Science ®Google Scholar
• Milleron RS, Bratton SB. 'Heated' debates in apoptosis. Cell Mol Life Sci 2007; 64: 2329–2333
   PubMed Web of Science ®Google Scholar
• Bettaieb A, Averill-Bates DA. Thermotolerance induced at a mild temperature of 40°C protects cells against heat shock-induced apoptosis. J Cell Physiol 2005; 205: 47–57
   PubMed Web of Science ®Google Scholar
• Weiss RB. The anthracyclines: Will we ever find a better doxorubicin?. Semin Oncol 1992; 19: 670–686
   PubMed Web of Science ®Google Scholar
• Singal PK, Li T, Kumar D, Danelisen I, Iliskovic N. Adriamycin-induced heart failure: Mechanism and modulation. Mol Cell Biochem 2000; 207: 77–86
   PubMed Web of Science ®Google Scholar
• Minotti G, Menna P, Salvatorelli E, Cairo G, Gianni L. Anthracyclines: Molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol Rev 2004; 56: 185–229
   PubMed Web of Science ®Google Scholar
• Rose PG. Pegylated liposomal doxorubicin: Optimizing the dosing schedule in ovarian cancer. Oncologist 2005; 10: 205–214
   PubMed Web of Science ®Google Scholar