Inhibition of Hsp90 and 70 sensitizes melanoma cells to hyperthermia using ferromagnetic particles with a low Curie temperature

International Journal of Clinical Oncology

Volumn 19, Issue 4, 2014, Pages 722-730

  Miyagawa, Tomoyuki ^a   Saito, Hajime ^a   Minamiya, Yoshihiro ^a   Mitobe, Kazutaka ^b   Takashima, Shinogu ^a   Takahashi, Naoko ^a   Ito, Aki ^a   Imai, Kazuhiro ^a   Motoyama, Satoru ^a   Ogawa, Junichi ^a  

^a AKITA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b AKITA UNIVERSITY   (Japan)

Author keywords

Heat shock protein; Hyperthermia; Melanoma

Indexed keywords

ALVESPIMYCIN; FERROMAGNETIC MATERIAL; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; PROTEIN KINASE B; QUERCETIN; 17-(DIMETHYLAMINOETHYLAMINO)-17-DEMETHOXYGELDANAMYCIN; BENZOQUINONE DERIVATIVE; MACROCYCLIC LACTAM;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CURIE TEMPERATURE; DRUG EFFECT; DRUG INHIBITION; FEMALE; HYPERTHERMIA; IN VITRO STUDY; IN VIVO STUDY; INCIDENCE; LUNG METASTASIS; MAGNETIC FIELD; MELANOMA B16; MELANOMA CELL; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SURVIVAL RATE; TEMPERATURE; TUMOR CELL INOCULATION; TUMOR GROWTH; TUMOR VOLUME; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; DRUG EFFECTS; GENE EXPRESSION REGULATION; HUMAN; HYPERTHERMIC THERAPY; MAGNET; MELANOMA; METABOLISM; PATHOLOGY;

ANIMALS; APOPTOSIS; BENZOQUINONES; GENE EXPRESSION REGULATION, NEOPLASTIC; HSP70 HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; HYPERTHERMIA, INDUCED; LACTAMS, MACROCYCLIC; MAGNETS; MELANOMA; MICE; QUERCETIN;

EID: 84906334146     PISSN: 13419625     EISSN: 14377772     Source Type: Journal    
DOI: 10.1007/s10147-013-0606-x     Document Type: Article

References (50)

1. Overgaard K, Overgaard J (1972) Investigations on the possibility of a thermic tumour therapy. I. Short-wave treatment of a transplanted isologous mouse mammary carcinoma. Eur J Cancer 8:65-78
2. Hiraoka M, Jo S, Akuta K et al (1987) Radiofrequency capacitive hyperthermia for deep-seated tumors I. studies on thermometry. Cancer 60:121-127 (Pubitemid 17083563)
3. van der Zee J (2002) Heating the patient: a promising approach? Ann Oncol 13:1173-1184
4. Abe M, Hiraoka M, Takahashi M et al (1986) Multi-institutional studies on hyperthermia using an 8-MHz radiofrequency capacitive heating device (Thermotron RF-8) in combination with radiation for cancer therapy. Cancer 58:1589-1595 (Pubitemid 16032134)
5. Shinkai M, Yanase M, Honda H et al (1996) Intracellular hyperthermia for cancer using magnetite cationic liposomes: in vitro study. Jpn J Cancer Res 87:1179-1183 (Pubitemid 26420027)
6. Minamimura T, Sato H, Kasaoka S et al (2000) Tumor regression by inductive hyperthermia combined with hepatic embolization using dextran magnetite-incorporated microspheres in rats. Int J Oncol 16:1153-1158
7. Ito A, Tanaka K, Kondo K et al (2003) Tumor regression by combined immunotherapy and hyperthermia using magnetic nanoparticles in an experimental subcutaneous murine melanoma. Cancer Sci 94:308-313 (Pubitemid 36575900)
8. Tanaka K, Ito A, Kobayashi T et al (2005) Intratumoral injection of immature dendritic cells enhances antitumor effect of hyperthermia using magnetic nanoparticles. Int J Cancer 116:624-633 (Pubitemid 41099200)
9. Johannsen M, Gneveckow U, Eckelt L et al (2005) Clinical hyperthermia of prostate cancer using magnetic nanoparticles: presentation of a new interstitial technique. Int J Hyperthermia 21:637-647 (Pubitemid 41684238)
10. Lilly MB, Brezovich IA, Atkinson WJ (1985) Hyperthermia induction with thermally self-regulated ferromagnetic implants. Radiology 154:243-244 (Pubitemid 15196326)
11. Kobayashi T, Kida Y, Tanaka T et al (1986) Magnetic induction hyperthermia for brain tumor using ferromagnetic implant with low Curie temperature I. Experimental study. J Neurooncol 4:175-181 (Pubitemid 17206914)
12. Müller-Schulte D (1986) Means for the selective tumor therapy as well as processes for the synthesis and their application. German Patent Application DE3502998A1
13. Doerschuk CM, Allard MF, Hogg JC (1989) Neutrophil kinetics in rabbits during infusion of zymosan-activated plasma. J Appl Physiol 67:88-95 (Pubitemid 19196452)
14. Saito H, Mitobe K, Ito A et al (2008) Self-regulating hyperthermia induced using thermosensitive ferromagnetic material with a low Curie temperature. Cancer Sci 99:805-809 (Pubitemid 351448087)
15. Ito A, Saito H, Mitobe K et al (2009) Inhibition of heat shock protein 90 sensitizes melanoma cells to thermosensitive ferromagnetic particles mediated hyperthermia with low Curie temperature. Cancer Sci 100:558-564
16. Freeman BC, Morimoto RI (1996) 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 15:2969-2979
17. Schneider C, Sepp-Lorenzino L, Nimmesgern E et al (1996) Pharmacologic shifting of a balance between protein refolding and degradation mediated by Hsp90. Proc Natl Acad Sci USA 93:14536-14541 (Pubitemid 26419002)
18. Schumacher RJ, Hansen WJ, Freeman BC et al (1996) Cooperative action of Hsp70, Hsp90, and DnaJ proteins in protein renaturation. Biochemistry 35:14889-14898 (Pubitemid 26423824)
19. Smith V, Sausville EA, Camalier RF et al (2005) Comparison of 17-dimethylaminoethylamino-17-demethoxy-geldanamycin (17D MAG) and 17-allylamino-17-demethoxygeldanamycin (17AAG) in vitro: effects on Hsp90 and client proteins in melanoma models. Cancer Chemother Pharmacol 56:126-137 (Pubitemid 40884268)
20. Banerji U, O'Donnell A, Scurr M et al (2005) Phase I pharmacokinetic and pharmacodynamic study of 17-allylamino, 17-demethoxygeldanamycin in patients with advanced malignancies. J Clin Oncol 23:4152-4161 (Pubitemid 46211321)
21. Bagatell R, Paine-Murrieta GD, Taylor CW et al (2000) Induction of a heat shock factor 1-dependent stress response alters the cytotoxic activity of hsp90-binding agents. Clin Cancer Res 6:3312-3318 (Pubitemid 30637762)
22. Sittler A, Lurz R, Lueder G et al (2001) Geldanamycin activates a heat shock response and inhibits huntingtin aggregation in a cell culture model of Huntington's disease. Hum Mol Genet 10:1307-1315 (Pubitemid 32600484)
23. Prodromou C, Roe SM, O'Brien R et al (1997) Identification and structural characterization of the ATP/ADP-binding site in the Hsp90 molecular chaperone. Cell 90:65-75 (Pubitemid 28009419)
24. Mimnaugh EG, Chavany C, Neckers L (1996) Polyubiquitination and proteasomal degradation of the p185c-erbB-2 receptor protein-tyrosine kinase induced by geldanamycin. J Biol Chem 271:22796-22801 (Pubitemid 26304727)
25. Stancato LF, Silverstein AM, Owens-Grillo JK et al (1997) 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 272:4013-4020 (Pubitemid 27078462)
26. Xu W, Mimnaugh E, Rosser MF et al (2001) Sensitivity of mature Erbb2 to geldanamycin is conferred by its kinase domain and is mediated by the chaperone protein Hsp90. J Biol Chem 276:3702-3708
27. Sausville EA, Tomaszewski JE, Ivy P (2003) Clinical development of 17-allylamino, 17-demethoxygeldanamycin. Curr Cancer Drug Targ 3:377-383 (Pubitemid 37128324)
28. Pratt WB, Toft DO (1997) Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr Rev 18:306-360 (Pubitemid 27246880)
29. Ferrarini M, Heltai S, Zocchi MR et al (1992) Unusual expression and localization of heat-shock proteins in human tumor cells. Int J Cancer 51:613-619
30. Kamal A, Thao L, Sensintaffar J et al (2003) A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 425:407-410 (Pubitemid 37187270)
31. Bisht KS, Bradbury CM, Mattson D et al (2003) 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 63:8984-8995 (Pubitemid 38064080)
32. Machida H, Matsumoto Y, Shirai M et al (2003) Geldanamycin, an inhibitor of Hsp90, sensitizes human tumour cells to radiation. Int J Radiat Biol 79:973-980 (Pubitemid 38147058)
33. Machida H, Nakajima S, Shikano N et al (2005) 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 96:911-917 (Pubitemid 43056131)
34. Matsumoto Y, Machida H, Kubota N (2005) Preferential sensitization of tumor cells to radiation by heat shock protein 90 inhibitor geldanamycin. J Radiat Res 46:215-221 (Pubitemid 41190658)
35. Münster PN, Basso A, Solit D et al (2001) Modulation of Hsp90 function by ansamycins sensitizes breast cancer cells to chemotherapy-induced apoptosis in an RB- and schedule-dependent manner. Clin Cancer Res 7:2228-2236 (Pubitemid 32751619)
36. Adams J, Elliott PJ (2000) New agents in cancer clinical trials. Oncogene 19:6687-6692 (Pubitemid 32197709)
37. Grem JL, Morrison G, Guo XD et al (2005) Phase I and pharmacologic study of 17-(allylamino)-17-demethoxygeldanamycin in adult patients with solid tumors. J Clin Oncol 23:1885-1893 (Pubitemid 46211366)
38. Pacey S, Banerji U, Judson I et al (2006) Hsp90 inhibitors in the clinic. Handb Exp Pharmacol 172:331-358
39. Ciocca DR, Calderwood SK (2005) Heat shock proteins in cancer: diagnostic, prognostic, predictive, and treatment implications. Cell Stress Chaperones 10:86-103 (Pubitemid 40942470)
40. Yang X, Wang J, Zhou Y et al (2012) Hsp70 promotes chemoresistance by blocking Bax mitochondrial translocation in ovarian cancer cells. Cancer Lett 321:137-143
41. Ray S, Lu Y, Kaufmann SH et al (2004) Genomic mechanisms of p210BCR-ABL signaling: induction of heat shock protein 70 through the GATA response element confers resistance to paclitaxel-induced apoptosis. J Biol Chem 279:35604-35615 (Pubitemid 39100562)
42. Hosokawa N, Hirayoshi K, Kudo H et al (1992) Inhibition of the activation of heat shock factor in vivo and in vitro by flavonoids. Mol Cell Biol 12:3490-3498
43. Guo F, Rocha K, Bali P et al (2005) Abrogation of heat shock protein 70 induction as a strategy to increase antileukemia activity of heat shock protein 90 inhibitor 17-allylamino-demethoxy geldanamycin. Cancer Res 65:10536-10544 (Pubitemid 41743748)
44. Aalinkeel R, Bindukumar B, Reynolds JL et al (2008) The dietary bioflavonoid, quercetin, selectively induces apoptosis of prostate cancer cells by down-regulating the expression of heat shock protein 90. Prostate 68:1773-1789
45. Goetz MP, Toft DO, Ames MM et al (2003) The Hsp90 chaperone complex as a novel target for cancer therapy. Ann Oncol 14:1169-1176 (Pubitemid 37039035)
46. Zhao R, Davey M, Hsu YC et al (2005) Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone. Cell 120:715-727 (Pubitemid 40343082)
47. Suganuma T, Irie K, Fujii E et al (2002) Effect of heat stress on lipopolysaccharide-induced vascular permeability change in mice. J Pharmacol Exp Ther 303:656-663 (Pubitemid 35231238)
48. Pratt WB (1998) The hsp90-based chaperone system: involvement in signal transduction from a variety of hormone and growth factor receptors. Proc Soc Exp Biol Med 217:420-434
49. Clarke PA, Hostein I, Banerji U et al (2000) 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 19:4125-4133
50. Goloudina AR, Demidov ON, Garrido C (2012) Inhibition of HSP70: a challenging anti-cancer strategy. Cancer Lett 325:117-124