Fever-range whole body thermotherapy combined with oxaliplatin: A curative regimen in a pre-clinical breast cancer model

References

• Nishimura Y, Shibamoto Y, Jo S, Akuta K, Hiraoka M, Takahashi M, Abe M. Relationship between heat-induced vascular damage and thermosensitivity in four mouse tumors. Cancer Res 1988; 48: 7226–7230
   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
• Kong G, Braun RD, Dewhirst MW. Characterization of the effect of hyperthermia on nanoparticle extravasation from tumor vasculature. Cancer Res 2001; 61: 3027–3032
   PubMed Web of Science ®Google Scholar
• Rowe RW, Strebel FR, Sumiyoshi K, Kirpotin DB, Bull JMC. Time-course of liposome uptake in MTLn3 tumors and normal tissue with and without whole body hyperthermia. Proc Am Assoc Cancer Res 2002; 43: 417, (abstract)
   Google Scholar
• Leunig M, Goetz AE, Dellian M, Zetterer G, Gamarra F, Jain RK, Mesmer K. Interstitial fluid pressure in solid tumors following hyperthermia: Possible correlation with therapeutic response. Cancer Res 1992; 52: 487–490
   PubMed Web of Science ®Google Scholar
• Sem A, Capitano M, Hylander B, Spernyak J, Schueckler J, Singh A, Repasky E. Fever-range systemic hyperthermia increases tumor vascular perfusion, decreases interstitial fluid pressure and hypoxia and sensitizes tumors to subsequent radiation therapy. Paper presented at the Society for Thermal Medicine Annual Meeting, Tucson, Arizona, (2009) (Symposium IV: Thermal Therapy, Hypoxia and the Tumor Microenvironment). Abstract available at http://stm.conference-services.net/resources/467/1527/pdf/STM(2009)_0118.pdf. Accessed March 25, 2010.
   Google Scholar
• Van der Zee J, Vernon CC. Thermoradiotherapy for advanced and recurrent breast tumors. Thermoradiotherapy and Thermochemotherapy, HM Seegenschmiedt, P Fessenden, CC Vernon. Clinical Applications Berlin, Springer. 1996; 2: 35–48
   Google Scholar
• Vernon CC, Hand JW, Field SB, Machin D, Whaley JB, van der Zee J, van Putten WL, van Rhoon GC, van Dijk JD, González González D, et al. Radiotherapy with or without hyperthermia in the treatment of superficial localized breast cancer: Results from five randomized controlled trials. International Collaborative Hyperthermia Group. Int J Radiat Oncol Biol Phys 1996; 35: 731–744
   PubMed Web of Science ®Google Scholar
• Jones EL, Marks LB, Prosnitz LR. Point: Hyperthermia with radiation for chest wall recurrences. J Natl Compr Canc Netw 2007; 5: 339–344
   PubMedGoogle Scholar
• Hehr T, Wust P, Bamberg M, Budach W. Current and potential role of thermoradiotherapy for solid tumours. Onkologie 2003; 26: 295–302
   PubMedGoogle Scholar
• Falk MH, Issels RD. Hyperthermia in oncology. Int J Hyperthermia 2001; 17: 1–18
   PubMed Web of Science ®Google Scholar
• Rowe RW. Hyperthermia, systemic. Encyclopedia of Medical Devices and Instrumentationsecond (Table 6)., JG Webster. Wiley, New York 2006; 57
   Google Scholar
• Matsuda H, Strebel FR, Kaneko T, Danhavser LL, Jenkins GN, Toyota N, Bull JM. Long duration mild whole body hyperthermia of up to 12 hours in rats: Feasibility, and efficacy on primary tumour and axillary lymph node metastases of a mammary adenocarcinoma: Implications for adjuvant therapy. Int J Hyperthermia 1997; 13: 89–98
   PubMed Web of Science ®Google Scholar
• Yamada Y, Itoh Y, Aoki S, Nakamura K, Taki T, Naruse K, Tobiume M, Zennami K, Katsuda R, Kato Y, et al. Preliminary results of M-VAC chemotherapy combined with mild hyperthermia, a new therapeutic strategy for advanced or metastatic transitional cell carcinoma of the urothelium. Cancer Chemother Pharmacol 2009; 64: 1079–1083
   PubMedGoogle Scholar
• Sakaguchi Y, Makino M, Kaneko T, Stephens LC, Strebel FR, Danhauser LL, Jenkins GN, Bull JM. Therapeutic efficacy of long duration-low temperature whole body hyperthermia when combined with tumor necrosis factor and carboplatin in rats. Cancer Res 1994; 54: 2223–2227
   PubMed Web of Science ®Google Scholar
• Toyota N, Strebel FR, Stephens LC, Matsuda H, Bull JM. Long-duration, mild whole body hyperthermia with cisplatin: Tumour response and kinetics of apoptosis and necrosis in a metastatic rat mammary adenocarcinoma. Int J Hyperthermia 1997; 13: 497–506
   PubMed Web of Science ®Google Scholar
• Nagle V, Berry J, Bull JM. Whole body hyperthermia with carboplatin (CBDCA) for treatment of advanced or metastatic GI adenocarcinomas. Proc Am Assoc Ca Res 1999; 40: 345
   Google Scholar
• Bull JM, Scott GL, Nagle VL, Strebel FR, Koch SM. Phase I study of long-duration, low-temperature whole-body hyperthermia (LL-WBH) with liposomal doxorubicin (Doxil), 5-fluorouracil (5-FU), and interferon-a (IFN-a). Proc Am Soc Clin Oncol 2002; 21, abstract No. 2126. Accessed March 25, 2010 from http://www.asco.org/ASCOv2/meetings/abstracts?&vmview=abst_detail_view&confID=16&abstractID=2126
   Google Scholar
• Bull JM, Scott GL, Strebel FR, Nagle VL, Oliver D, Redwine M, Rowe RW, Ahn CW, Koch SM. Fever-range whole-body thermal therapy combined with cisplatin, gemcitabine, and daily interferon-alpha: A description of a phase I-II protocol. Int J Hyperthermia 2008; 24: 649–662
   PubMed Web of Science ®Google Scholar
• Baba H, Siddik ZH, Strebel FR, Jenkins GN, Bull JM. Increased therapeutic gain of combined cis-diamminedichloroplatinum (II) and whole body hyperthermia therapy by optimal heat/drug scheduling. Cancer Res 1989; 49: 7041–7044
   PubMed Web of Science ®Google Scholar
• Strebel FR, Sumiyoshi K, Jenkins GN, Rowe RW, Bull JMC. Drug sequence effect on therapeutic outcome (tumor growth, toxicity, and survival) of irinotecan combined with epirubicin in the in vivo MTLn3 rat mammary adenocarcinoma. Proc Am Assoc Cancer Res 2002; 43: 587
   Google Scholar
• Bull JMC, Strebel FR, Jenkins GN, Deng W, Rowe RW. The importance of schedule in whole body thermochemotherapy. Int J Hyperthermia 2008; 24: 171–181
   PubMed Web of Science ®Google Scholar
• Skitzki JJ, Repasky EA, Evans SS. Hyperthermia as an immunotherapy strategy for cancer. Curr Opin Investig Drugs 2009; 10: 550–558
   PubMed Web of Science ®Google Scholar
• Zhang H-G, Mehta K, Cohen P, Guha C. Hyperthermia on immune regulation: A temperature's story. Cancer Lett 2008; 271: 191–204
   PubMed Web of Science ®Google Scholar
• Tulapurkar ME, Asiegbu BE, Singh IS, Hasday JD. Hyperthermia in the febrile range induces HSP72 expression proportional to exposure temperature but not to HSF-1 DNA-binding activity in human lung epithelial A549 cells. Cell Stress Chaperones 2009; 14: 499–508
   PubMed Web of Science ®Google Scholar
• Murapa P, Gandhapudi S, Skaggs HS, Sarge KD, Woodward JG. Physiological fever temperature induces a protective stress response in T lymphocytes mediated by heat shock factor-1 (HSF1). J Immunol 2007; 179: 8305–8312
   PubMed Web of Science ®Google Scholar
• Ostberg JR, Repasky EA. Emerging evidence indicates that physiologically relevant thermal stress regulates dendritic cell function. Cancer Immunol Immunother 2006; 55: 292–298
   PubMed Web of Science ®Google Scholar
• Milani V, Noessner E. Effects of thermal stress on tumor antigenicity and recognition by immune effector cells. Cancer Immunol Immunother 2006; 55: 312–319
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Burd R, Dziedzic TS, Xu Y, Caligiuri MA, Subjeck JR, Repasky EA. Tumor cell apoptosis, lymphocyte recruitment and tumor vascular changes are induced by low temperature, long duration (fever-like) whole body hyperthermia. J Cell Physiol 1998; 177: 137–147
   PubMed Web of Science ®Google Scholar
• Zhao W, An H, Zhou J, Xu H, Yu Y, Cao X. Hyperthermia differentially regulates TLR4 and TLR2-mediated innate immune response. Immunol Let 2007; 108: 137–142
   PubMed Web of Science ®Google Scholar
• Van der Most RG, Currie AJ, Robinson BWS, Lake RA. Decoding dangerous cell death: How cytotoxic chemotherapy invokes inflammation, immunity, or nothing at all. Cell Death Differ 2008; 15: 13–20
   PubMedGoogle Scholar
• Tesniere A, Panaretakis T, Kepp O, apeton L, Ghiringhelli F, Zitvogel L, Kroemer G. Molecular characteristics of immunogenic cancer cell death. Cell Death Differ 2008; 15: 3–12
   PubMed Web of Science ®Google Scholar
• Ullrich E, Bonmort M, Mignot G, Kroemer G, Zitvogel L. Tumor stress, cell death, and the ensuing immune response. Cell Death Differ 2008; 15: 21–28
   PubMed Web of Science ®Google Scholar
• Kepp O, Tesniere A, Zitvogel L, Kroemer G. The immunogenicity of tumor cell death. Current Opin Oncol 2009; 21: 71–76
   PubMed Web of Science ®Google Scholar
• Shurin GV, Tourkova IL, Kaneno R, Shurin MR. Chemotherapeutic agents in noncytotoxic concentrations increase antigen presentation by dendritic cells via an IL-12-dependent mechanism. J Immunol 2009; 183: 137–144
   PubMed Web of Science ®Google Scholar
• Tesniere A, Schlemmer F, Boige V, Kepp O, Martins I, Ghiringhelli F, Aymeric L, Michaud M, Apetoh L, Barault L, et al. Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene 2010; 29: 482–91
   PubMed Web of Science ®Google Scholar
• Raymond E, Faivre S, Chaney S, Woynarowsky J, Cvitkovic E. Cellular and molecular pharmacology of oxaliplatin. Mol Cancer Ther 2002; 1: 227–235
   PubMed Web of Science ®Google Scholar
• Apetoh L, Tesniere A, Ghiringhelli F, Kroemer G, Zitvogel L. Molecular interactions between dying tumor cells and the innate immune system determine the efficacy of conventional anticancer therapies. Cancer Res 2008; 68: 4026–4030
   PubMed Web of Science ®Google Scholar
• Dong Xda E, Ito N, Lotze MT, Demarco RA, Popovic P, Shand SH, Watkins S, Winikoff S, Brown CK, Bartlett DL, et al. High mobility group box I (HMGB1) release from tumor cells after treatment: Implications for development of targeted chemoimmunotherapy. J Immunother 2007; 30: 596–606
   PubMed Web of Science ®Google Scholar
• Matsuda H, Strebel FR, Kaneko T, Stephens LC, Danhauser LL, Jenkins GN, Toyota N, Bull JM. Apoptosis and necrosis occurring during different stages of primary and metastatic tumor growth of a rat mammary adenocarcinoma. Anticancer Res 1996; 16: 1117–1122
   PubMed Web of Science ®Google Scholar
• Siddik ZH, Boxall FE, Harrap KR. Flameless atomic absorption spectrophotometric determination of platinum in tissues solubilized in hyaminehydroxide. Anal Biochem 1987; 163: 21–26
   PubMed Web of Science ®Google Scholar
• Neri A, Welch D, Kawaguchi T, Nicolson GL. Development and biologic properties of malignant cell sublines and clones of a spontaneously metastasizing rat mammary adenocarcinoma. J Natl Cancer Inst 1982; 68: 507–517
   PubMedGoogle Scholar
• Sumiyoshi K, Strebel FR, Rowe RW, Bull JM. The effect of whole-body hyperthermia combined with ‘metronomic’ chemotherapy on rat mammary adenocarcinoma metastases. Int J Hyperthermia 2003; 19: 103–118
   PubMed Web of Science ®Google Scholar
• Thrall DE, Page RL, Dewhirst MW, Meyer RE P, Hoopes J, Kornegay JN. Temperature measurements in normal and tumor tissue of dogs undergoing whole body hyperthermia. Cancer Res 1986; 46: 6229–6235
   Google Scholar
• Wondergem J, Siddik ZH, Strebel FR, Bull JM. Effect of whole body hyperthermia on cis-diamminedichloroplatinum (II)-induced antitumour activity and tissue Pt-distribution: Do anaesthetics influence the therapeutic ratio?. Eur J Cancer 1993; 29A: 549–554
   PubMed Web of Science ®Google Scholar
• Nehmé A, Baskaran R, Nebel S, Jink D, Howell SB, Wang JY, Christen RD. Induction of JNK and c-Abl signalling by cisplatin and oxaliplatin in mismatch repair-proficient and -deficient cells. Br J Cancer 1999; 79: 1104–1110
   PubMed Web of Science ®Google Scholar
• Atallah D, Marsaud V, Radanyi C, Komprobst M, Rouzier R, Zlias D, Renoir JM. Thermal enhancement of oxaliplatin-induced inhibition of cell cycle progression in human carcinoma cell lines. Int J Hyperthermia 2004; 20: 405–419
   PubMed Web of Science ®Google Scholar
• Bischof JC, Padanilam WH, Holmes RM, et al. Dynamics of cell membrane permeability changes at supraphysiological temperatures. Biophys J 1995; 68: 2608–2614
   PubMed Web of Science ®Google Scholar
• Terunuma H, Wada A, Deng X, Yasuma Y, Onishi T, Toki A, Abe H. Mild hyperthermia modulates the relative frequency of lymphocyte cell subpopulations: an increase in a cytolytic NK cell subset and a decrease in a regulatory T cell subset. Thermal Med (Jap J Hyperthermic Oncol) 2007; 23: 41–47
   Google Scholar
• Ehrke MJ. Immunomodulation in cancer therapeutics. Int Immunopharmacol 2003; 3: 1105–1119
   PubMed Web of Science ®Google Scholar
• William-Faltaos S, Rouillard D, Lechat P, Bastian G. Cell cycle arrest by oxaliplatin on cancer cells. Fundam Clin Pharmacol 2007; 21: 165–172
   PubMed Web of Science ®Google Scholar
• Toscano F, Parmentier B, El Fajoui Z, Estornes Y, Chayvialle JA, Saurin JC, Abello J. p53 dependent and independent sensitivity to oxaliplatin of colon cancer cells. Biochem Pharmacol 2007; 74: 392–406
   PubMed Web of Science ®Google Scholar
• van Nimwegen MJ, Huigsloot M, Camier A, Tijdens IB, van de Water B. Focal adhesion kinase and protein kinase B cooperate to suppress doxorubicin-induced apoptosis of breast tumor cells. Mol Pharmacol 2006; 70: 1330–1339
   PubMed Web of Science ®Google Scholar
• Gasser S, Raule DH. The DNA damage response arouses the immune system. Cancer Res 2006; 66: 3959–3962
   PubMed Web of Science ®Google Scholar
• Egloff AM, Vella LA, Oliver JF. Cyclin B1 and other cyclins as tumor antigens in immunosurveillance and immunotherapy of cancer. Cancer Res 2006; 66: 6–9
   PubMedGoogle Scholar
• Camporeale A, Boni A, Iezzi G, Degl'Innocenti E, Grioni M, Mondino A, Bellone M. Critical impact of the kinetics of dendritic cells activation on the in vivo induction of tumor-specific T lymphocytes. Cancer Res 2003; 63: 3688–3694
   PubMed Web of Science ®Google Scholar
• Bousso P, Robey E. Dynamics of CD8+ T cell priming by dendritic cells in intact lymph nodes. Nat Immunol 2003; 4: 579–585
   PubMed Web of Science ®Google Scholar
• Roosnek E, Demotz S, Corradin G, Lanzavecchia A. Kinetics of MHC-antigen complex formation on antigen-presenting cells. J Immunol 1988; 140: 4079–4082
   PubMedGoogle Scholar
• Kelly JM, Darcy PK, Markby JL, Godfrey DI, Takeda K, Yagita H, Smyth MJ. Induction of tumor-specific T cell memory by NK cell-mediated tumor rejection. Nat Immunol 2002; 3: 83–90
   PubMed Web of Science ®Google Scholar
• Dayanc BE, Beachy SH, Ostberg JR, Repasky EA. Dissection the role of hyperthermia in natural killer cell mediated anti-tumor responses. Int J Hyperthermia 2008; 24: 41–56
   PubMed Web of Science ®Google Scholar