Inhibition of heat shock protein 90 sensitizes melanoma cells to thermosensitive ferromagnetic particle-mediated hyperthermia with low Curie temperature

Cancer Science

Volumn 100, Issue 3, 2009, Pages 558-564

  Ito, Aki ^a   Saito, Hajime ^a   Mitobe, Kazutaka ^a   Minamiya, Yoshihiro ^a   Takahashi, Naoko ^a   Maruyama, Kiyotomi ^a   Motoyama, Satoru ^a   Katayose, Yoshihisa ^a   Ogawa, Jun Ichi ^a  

^a AKITA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FERROMAGNETIC MATERIAL; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; PROTEIN KINASE B; ANTINEOPLASTIC ANTIBIOTIC; BENZOQUINONE DERIVATIVE; FERRIC ION; FERRITE; MACROCYCLIC LACTAM;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOREGULATION; C57BL 6 MOUSE; CANCER CELL CULTURE; CONTROLLED STUDY; FEMALE; HEAT SENSITIVITY; HYPERTHERMIC THERAPY; IN VIVO STUDY; LOW TEMPERATURE PROCEDURES; MAGNETIC FIELD; MELANOMA; MELANOMA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSITIVITY ANALYSIS; TUMOR REGRESSION; ANIMAL; C57BL MOUSE; DRUG ANTAGONISM; EXPERIMENTAL MELANOMA; METABOLISM; METHODOLOGY; MULTIMODALITY CANCER THERAPY; NICK END LABELING; SKIN TUMOR; TUMOR CELL LINE; WESTERN BLOTTING;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; BENZOQUINONES; BLOTTING, WESTERN; CELL LINE, TUMOR; COMBINED MODALITY THERAPY; FEMALE; FERRIC COMPOUNDS; HSP90 HEAT-SHOCK PROTEINS; HYPERTHERMIA, INDUCED; IN SITU NICK-END LABELING; LACTAMS, MACROCYCLIC; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; PROTO-ONCOGENE PROTEINS C-AKT; SKIN NEOPLASMS;

EID: 62849085178     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/j.1349-7006.2008.01072.x     Document Type: Article

References (61)

1. Cavaliere R, Ciocatto EC, Giovanella BC et al. Selective heat sensitivity of cancer cells. Biochemical and clinical studies. Cancer 1967; 20: 1351-81.
2. Overgaard K, Overgaard J. Investigations on the possibility of a thermic tumour therapy. I. Short-wave treatment of a transplanted isologous mouse mammary carcinoma. Eur J Cancer 1972; 8: 65-78.
3. Lefor AT, Makohon S, Ackerman NB. The effects of hyperthermia on vascular permeability in experimental liver metastasis. J Surg Oncol 1985; 28: 297-300.
4. Hiraoka M, Jo S, Akuta K, Nishimura Y, Takahashi M, Abe M. Radiofrequency capacitive hyperthermia for deep-seated tumors. I. Studies on thermometry. Cancer 1987; 60: 121-7.
5. van der Zee J. Heating the patient: A promising approach? Ann Oncol 2002; 13: 1173-84.
6. Abe M, Hiraoka M, Takahashi M et al. Multi-institutional studies on hyperthermia using an 8-MHz radiofrequency capacitive heating device (Thermotron RF-8) in combination with radiation for cancer therapy. Cancer 1986; 58: 1589-95.
7. Hiraoka M, Nishimura Y, Nagata Y et al. Site-specific phase I, II trials of hyperthermia at Kyoto University. Int J Hyperthermia 1994; 10: 403-10.
8. Jordan A, Wust P, Fahling H, John W, Hinz A, Felix R. Inductive heating of ferrimagnetic particles and magnetic fluids: Physical evaluation of their potential for hyperthermia. Int J Hyperthermia 1993; 9: 51-68.
9. Shinkai M, Yanase M, Honda H, Wakabayashi T, Yoshida J, Kobayashi T. Intracellular hyperthermia for cancer using magnetite cationic liposomes: In vitro study. Jpn J Cancer Res 1996; 87: 1179-83.
10. Yanase M, Shinkai M, Honda H, Wakabayashi T, Yoshida J, Kobayashi T. Intracellular hyperthermia for cancer using magnetite cationic liposomes: An in vivo study. Jpn J Cancer Res 1998; 89: 463-9.
11. Minamimura T, Sato H, Kasaoka S et al. Tumor regression by inductive hyperthermia combined with hepatic embolization using dextran magnetite-incorporated microspheres in rats. Int J Oncol 2000; 16: 1153-8.
12. Jordan A, Scholz R, Maier-Hauff K et al. Presentation of a new magnetic field therapy system for the treatment of human solid tumors with magnetic fluid hyperthermia. J Magnetism Magn Mater 2001; 225: 118-26.
13. Ito A, Tanaka K, Kondo 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.
14. Tanaka K, Ito A, Kobayashi T et al. Intratumoral injection of immature dendritic cells enhances antitumor effect of hyperthermia using magnetic nanoparticles. Int J Cancer 2005; 116: 624-33.
15. Johannsen M, Gneveckow U, Eckelt L et al. Clinical hyperthermia of prostate cancer using magnetic nanoparticles: Presentation of a new interstitial technique. Int J Hyperthermia 2005; 21: 637-47.
16. Wust P, Gneveckow U, Johannsen M et al. Magnetic nanoparticles for interstitial thermotherapy: Feasibility, tolerance and achieved temperatures. Int J Hyperthermia 2006; 22: 673-85.
17. Jordan A, Scholz R, Maier-Hauff K et al. The effect of thermotherapy using magnetic nanoparticles on rat malignant glioma. J Neurooncol 2006; 78: 7-14.
18. Lilly MB, Brezovich IA, Atkinson WJ. Hyperthermia induction with thermally self-regulated ferromagnetic implants. Radiology 1985; 154: 243-4.
19. Kobayashi T, Kida Y, Tanaka T, Kageyama N, Kobayashi H, Amemiya Y. Magnetic induction hyperthermia for brain tumor using ferromagnetic implant with low Curie temperature. I. Experimental study. J Neurooncol 1986; 4: 175-81.
20. Müller-Schulte D. Means for the selective tumor therapy as well as processes for the synthesis and their application. German Patent DE3502998A1. 1986.
21. Doerschuk CM, Allard MF, Hogg JC. Neutrophil kinetics in rabbits during infusion of zymosan-activated plasma. J Appl Physiol 1989; 67: 88-95.
22. Saito H, Mitobe K, Ito A et al. Self-regulating hyperthermia induced using thermosensitive ferromagnetic material with a low Curie temperature. Cancer Sci 2008; 99: 805-9.
23. Freeman BC, Morimoto RI. The human cytosolic molecular chaperones hsp90, hsp70 (hsc70) and hdj-1 have distinct roles in recognition of a non-native protein and protein refolding. EMBO J 1996; 15: 2969-79.
24. Schneider C, Sepp-Lorenzino L, Nimmesgern E et al. Pharmacologic shifting of a balance between protein refolding and degradation mediated by Hsp90. Proc Natl Acad Sci U S A 1996; 93: 14 536-41.
25. Schumacher RJ, Hansen WJ, Freeman BC, Alnemri E, Litwack G, Toft DO. Cooperative action of Hsp70, Hsp90, and DnaJ proteins in protein renaturation. Biochemistry 1996; 35: 14 889-98.
26. Prodromou C, Roe SM, O'Brien R, Ladbury JE, Piper PW, Pearl LH. Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 1997; 90: 65-75.
27. Stebbins CE, Russo AA, Schneider C, Rosen N, Hartl FU, Pavletich NP. Crystal structure of an Hsp90-geldanamycin complex: Targeting of a protein chaperone by an antitumor agent. Cell 1997; 89: 239-50.
28. Mimnaugh EG, Chavany C, Neckers L. Polyubiquitination and proteasomal degradation of the p185c-erbB-2 receptor protein-tyrosine kinase induced by geldanamycin. J Biol Chem 1996; 271: 22 796-801.
29. Stancato LF, Silverstein AM, Owens-Grillo JK, Chow YH, Jove R, Pratt WB. The hsp90-binding antibiotic geldanamycin decreases Raf levels and epidermal growth factor signaling without disrupting formation of signaling complexes or reducing the specific enzymatic activity of Raf kinase. J Biol Chem 1997; 272: 4013-20.
30. Xu W, Mimnaugh E, Rosser MF et al. Sensitivity of mature Erbb2 to geldanamycin is conferred by its kinase domain and is mediated by the chaperone protein Hsp90. J Biol Chem 2001; 276: 3702-8.
31. Pratt WB, Toft DO. Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev 1997; 18: 306-60.
32. Blagosklonny MV, Schulte TW, Nguyen P, Mimnaugh EG, Trepel J, Neckers L. Taxol induction of p21WAF1 and p53 requires c-raf-1. Cancer Res 1995; 55: 4623-6.
33. Xu Y, Lindquist S. Heat-shock protein hsp90 governs the activity of pp60v-src kinase. Proc Natl Acad Sci USA 1993; 90: 7074-8.
34. Stancato LF, Chow YH, Hutchison KA, Perdew GH, Jove R, Pratt WB. Raf exists in a native heterocomplex with hsp90 and p50 that can be reconstituted in a cell-free system. J Biol Chem 1993; 268: 21 711-16.
35. Ozes ON, Mayo LD, Gustin JA, Pfeffer SR, Pfeffer LM, Donner DB. NF-κB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 1999; 401: 82-5.
36. Romashkova JA, Makarov SS. NF-κB is a target of AKT in anti-apoptotic PDGF signalling. Nature 1999; 401: 86-90.
37. Brunet A, Bonni A, Zigmond MJ et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 1999; 96: 857-68.
38. Cardone MH, Roy N, Stennicke HR et al. Regulation of cell death protease caspase-9 by phosphorylation. Science 1998; 282: 1318-21.
39. Datta SR, Dudek H, Tao X et al. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 1997; 91: 231-41.
40. del Peso L, González-García M, Page C, Herrera R, Nuñez G. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 1997; 278: 687-9.
41. Pratt WB. The hsp90-based chaperone system: Involvement in signal transduction from a variety of hormone and growth factor receptors. Proc Soc Exp Biol Med 1998; 217: 420-34.
42. Ferrarini M, Heltai S, Zocchi MR, Rugarli C. Unusual expression and localization of heat-shock proteins in human tumor cells. Int J Cancer 1992; 51: 613-19.
43. Kamal A, Thao L, Sensintaffar J et al. A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 2003; 425: 407-10.
44. Bisht KS, Bradbury CM, Mattson D et al. Geldanamycin and 17-allylamino-17-demethoxygeldanamycin potentiate the in.vitro and in.vivo radiation response of cervical tumor cells via the heat shock protein 90-mediated intracellular signaling and cytotoxicity. Cancer Res 2003; 63: 8984-95.
45. Machida H, Matsumoto Y, Shirai M, Kubota N. Geldanamycin, an inhibitor of Hsp90, sensitizes human tumour cells to radiation. Int J Radiat Biol 2003; 79: 973-80.
46. Machida H, Nakajima S, Shikano N et al. Heat shock protein 90 inhibitor 17-allylamino-17-demethoxygeldanamycin potentiates the radiation response of tumor cells grown as monolayer cultures and spheroids by inducing apoptosis. Cancer Sci 2005; 96: 911-17.
47. Matsumoto Y, Machida H, Kubota N. Preferential sensitization of tumor cells to radiation by heat shock protein 90 inhibitor geldanamycin. J Radiat Res 2005; 46: 215-21.
48. Münster PN, Basso A, Solit D, Norton L, Rosen N. Modulation of Hsp90 function by ansamycins sensitizes breast cancer cells to chemotherapy-induced apoptosis in an RB- and schedule-dependent manner. Clin Cancer Res 2001; 7: 2228-36.
49. Adams J, Elliott PJ. New agents in cancer clinical trials. Oncogene 2000; 19: 6687-92.
50. Sausville EA, Tomaszewski JE, Ivy P. Clinical development of 17-allylamino, 17-demethoxygeldanamycin. Curr Cancer Drug Targets 2003; 3: 377-83.
51. Banerji U, O'Donnell A, Scurr M et al. Phase I pharmacokinetic and pharmacodynamic study of 17-allylamino, 17-demethoxygeldanamycin in patients with advanced malignancies. J Clin Oncol 2005; 23: 4152-61.
52. Grem JL, Morrison G, Guo XD et al. Phase I and pharmacologic study of 17-(allylamino)-17-demethoxygeldanamycin in adult patients with solid tumors. J Clin Oncol 2005; 23: 1885-93.
53. Suganuma T, Irie K, Fujii E, Yoshioka T, Muraki T. Effect of heat stress on lipopolysaccharide-induced vascular permeability change in mice. J Pharmacol Exp Ther 2002; 303: 656-63.
54. Fajardo LF, Prionas SD. Endothelial cells and hyperthermia. Int J Hyperthermia 1994; 10: 347-53.
55. Neckers L, Schulte TW, Mimnaugh E. Geldanamycin as a potential anti-cancer agent: Its molecular target and biochemical activity. Invest New Drugs 1999; 17: 361-73.
56. Clarke PA, Hostein I, Banerji U et al. Gene expression profiling of human colon cancer cells following inhibition of signal transduction by 17-allylamino-17-demethoxygeldanamycin, an inhibitor of the hsp90 molecular chaperone. Oncogene 2000; 19: 4125-33.
57. Brognard J, Clark AS, Ni Y, Dennis PA. Akt/protein kinase B is constitutively active in non-small cell lung cancer cells and promotes cellular survival and resistance to chemotherapy and radiation. Cancer Res 2001; 61: 3986-97.
58. Schulte TW, Blagosklonny MV, Ingui C, Neckers L. Disruption of the Raf-1-Hsp90 molecular complex results in destabilization of Raf-1 and loss of Raf-1-Ras association. J Biol Chem 1995; 270: 24 585-8.
59. Sato S, Fujita N, Tsuruo T. Modulation of Akt kinase activity by binding to Hsp90. Proc Natl Acad Sci USA 2000; 97: 10 832-7.
60. Amin K, Ip C, Jimenez L, Tyson C, Behrsing H. In vitro detection of differential and cell-specific hepatobiliary toxicity induced by geldanamycin and 17-allylaminogeldanamycin using dog liver slices. Toxicol Sci 2005; 87: 442-50.
61. Eustace BK, Sakurai T, Stewart JK et al. Functional proteomic screens reveal an essential extracellular role for hsp90α in cancer cell invasiveness. Nat Cell Biol 2004; 6: 507-14.