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

International Journal of Hyperthermia

Volumn 26, Issue 6, 2010, Pages 565-576

  Rowe, R Wanda ^a   Strebel, Frederick R ^a   Proett, Jesse M ^a   Deng, Wanleng ^a   Chan, Diana ^a   He, Guangan ^b   Siddik, Zahid ^b   Bull, Joan M C ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Breast cancer; Cell death; Hyperthermia; Immune stimulation; Low dose chemotherapy; Oxaliplation; Schedule; Thermal therapy; Thermochemotherapy; Tumour cure

Indexed keywords

OXALIPLATIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AXILLARY LYMPH NODE; BREAST ADENOCARCINOMA; CANCER CHEMOTHERAPY; CANCER MODEL; CANCER REGRESSION; CANCER SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; DNA ADDUCT; DRUG EFFICACY; FEMALE; HYPERTHERMIC THERAPY; IC 50; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INGUINAL LYMPH NODE; LYMPH NODE METASTASIS; NONHUMAN; RAT; THERAPY EFFECT; TREATMENT OUTCOME; TREATMENT RESPONSE; TUMOR CELL LINE; TUMOR GROWTH;

ADENOCARCINOMA; ANIMALS; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; COMBINED MODALITY THERAPY; DISEASE MODELS, ANIMAL; DNA ADDUCTS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; FEMALE; FEVER; HYPERTHERMIA, INDUCED; ORGANOPLATINUM COMPOUNDS; PLATINUM; RATS; RATS, INBRED F344; TREATMENT OUTCOME;

EID: 77955645240     PISSN: 02656736     EISSN: 14645157     Source Type: Journal    
DOI: 10.3109/02656736.2010.483635     Document Type: Article

References (61)

1. 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.
2. 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.
3. Kong G, Braun RD, Dewhirst MW. Characterization of the effect of hyperthermia on nanoparticle extravasation from tumor vasculature. Cancer Res 2001;61:3027-3032.
4. 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).
5. 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.
6. 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.
7. Van der Zee J, Vernon CC. Thermoradiotherapy for advanced and recurrent breast tumors. In: Seegenschmiedt HM, Fessenden P, and Vernon CC, editors. Thermoradiotherapy and Thermochemotherapy. Vol.2. Clinical Applications Berlin: Springer; 1996. pp 35-48.
8. 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.
9. Jones EL, Marks LB, Prosnitz LR. Point: Hyperthermia with radiation for chest wall recurrences. J Natl Compr Canc Netw 2007;5:339-344.
10. Hehr T, Wust P, Bamberg M, Budach W. Current and potential role of thermoradiotherapy for solid tumours. Onkologie 2003;26:295-302.
11. Falk MH, Issels RD. Hyperthermia in oncology. Int J Hyperthermia 2001;17:1-18.
12. Rowe RW. Hyperthermia, systemic. In: Webster JG, editor. Encyclopedia of Medical Devices and Instrumentationsecond (Table 6). New York: Wiley; 2006. p 57.
13. 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.
14. 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.
15. 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 hyper-thermia when combined with tumor necrosis factor and carboplatin in rats. Cancer Res 1994;54:2223-2227.
16. 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.
17. 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.
18. Bull JM, Scott GL, Nagle VL, Strebel FR, Koch SM. Phase I study of long-duration, low-temperature whole-body hyper-thermia (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.
19. 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.
20. Baba H, Siddik ZH, Strebel FR, Jenkins GN, Bull JM. Increased therapeutic gain of combined cis-diamminedichlor-oplatinum (II) and whole body hyperthermia therapy by optimal heat/drug scheduling. Cancer Res 1989; 49:7041-7044.
21. 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.
22. 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.
23. Skitzki JJ, Repasky EA, Evans SS. Hyperthermia as an immunotherapy strategy for cancer. Curr Opin Investig Drugs 2009;10:550-558.
24. Zhang H-G, Mehta K, Cohen P, Guha C. Hyperthermia on immune regulation: A temperature's story. Cancer Lett 2008;271:191-204.
25. 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.
26. 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.
27. Ostberg JR, Repasky EA. Emerging evidence indicates that physiologically relevant thermal stress regulates dendritic cell function. Cancer Immunol Immunother 2006;55:292-298.
28. Milani V, Noessner E. Effects of thermal stress on tumor antigenicity and recognition by immune effector cells. Cancer Immunol Immunother 2006;55:312-319.
29. 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.
30. 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.
31. 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.
32. 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.
33. Tesniere A, Panaretakis T, Kepp O, apeton L, Ghiringhelli F, Zitvogel L, Kroemer G. Molecular characteristics of immu-nogenic cancer cell death. Cell Death Differ 2008;15:3-12.
34. 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.
35. Kepp O, Tesniere A, Zitvogel L, Kroemer G. The immuno-genicity of tumor cell death. Current Opin Oncol 2009;21:71-76.
36. 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.
37. 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;29:482-491
38. Raymond E, Faivre S, Chaney S, Woynarowsky J, Cvitkovic E. Cellular and molecular pharmacology of oxaliplatin. Mol Cancer Ther 2002;1:227-235.
39. 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.
40. 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.
41. 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.
42. Siddik ZH, Boxall FE, Harrap KR. Flameless atomic absorption spectrophotometric determination of platinum in tissues solubilized in hyaminehydroxide. Anal Biochem 1987; 163:21-26.
43. Neri A, Welch D, Kawaguchi T, Nicolson GL. Development and biologic properties of malignant cell sublines and clones of a spontaneously metastasizing rat mammary adenocarci-noma. J Natl Cancer Inst 1982;68:507-517.
44. 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.
45. 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.
46. 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.
47. 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.
48. 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.
49. Bischof JC, Padanilam WH, Holmes RM, et al. Dynamics of cell membrane permeability changes at supraphysiological temperatures. Biophys J 1995;68:2608-2614.
50. 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.
51. Ehrke MJ. Immunomodulation in cancer therapeutics. Int Immunopharmacol 2003;3:1105-1119.
52. William-Faltaos S, Rouillard D, Lechat P, Bastian G. Cell cycle arrest by oxaliplatin on cancer cells. Fundam Clin Pharmacol 2007;21:165-172.
53. 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.
54. 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.
55. Gasser S, Raule DH. The DNA damage response arouses the immune system. Cancer Res 2006;66:3959-3962.
56. 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.
57. 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.
58. \+ T cell priming by dendritic cells in intact lymph nodes. Nat Immunol 2003;4:579-585.
59. Roosnek E, Demotz S, Corradin G, Lanzavecchia A. Kinetics of MHC-antigen complex formation on antigen-presenting cells. J Immunol 1988;140:4079-4082.
60. 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.
61. 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.