Prior Exposure of FM3A Cells to Quercetin Results in Enhanced Cytotoxic and Apoptotic Effects of Hyperthermia
Hyperthermia (HT) cancer treatments have been widely utilised, however, cancer cells develop thermotolerance following exposure to HT, and heat shock proteins (HSPs) are responsible for thermotolerance. A plant flavonoid, quercetin (QCT), has been reported to inhibit heat dependent expression of HSP...
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| Published in | Japanese Journal of Hyperthermic Oncology Vol. 16; no. 2; pp. 99 - 106 |
|---|---|
| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Japanese Society for Thermal Medicine
01.06.2000
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0911-2529 1881-9516 1881-9516 |
| DOI | 10.3191/thermalmedicine.16.99 |
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| Abstract | Hyperthermia (HT) cancer treatments have been widely utilised, however, cancer cells develop thermotolerance following exposure to HT, and heat shock proteins (HSPs) are responsible for thermotolerance. A plant flavonoid, quercetin (QCT), has been reported to inhibit heat dependent expression of HSPs. In this study, therefore, the effects of prior exposure to QCT followed by HT on the cytotoxic and apoptotic activities were evaluated in FM3A, mouse breast cancer cells. Treatment of FM3A cells to 10 μM QCT and hyperthermia at 43°C for 1 h (HT) suppressed cell proliferation only in 34% and 55%, respectively and were relatively ineffective. Combination of the two treatments (QCT+HT) synergistically inhibited cell proliferation (90% inhibition). QCT+HT also suppressed clonogenicity (80%), compared to the results of QCT (56%) and HT (41%). Apoptotic cell death occurred after each treatment in a time-dependent manner. There was 4.9 ± 0.7%, 9.6 ± 1.5% and 18.1 ± 4.3% apoptosis after QCT+HT, and 3.2 ± 0.2%, 4.6 ± 0.5% and 8.6 ± 2.8% apoptosis after QCT, 3.4 ± 0.1%, 5.1 ± 0.3% and 10.1 ± 3.1% apoptosis after HT 1, 6 and 24 h post exposure compared to control of 2.0 ± 0.1%. HT or QCT proved ineffective in suppressing cell proliferation or inducing apoptosis. QCT+HT induced an accumulation of cells in G2/M and S phases and a reduction in G0/G1phase. The increased FM3A cell killing by HT after prior exposure to QCT is probably due to suppressed HSPs expression and diminished cellular thermotolerance. QCT may play a useful adjunct role in the hyperthermic treatment of resistant tumor. |
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| AbstractList | Hyperthermia (HT) cancer treatments have been widely utilised, however, cancer cells develop thermotolerance following exposure to HT, and heat shock proteins (HSPs) are responsible for thermotolerance. A plant flavonoid, quercetin (QCT), has been reported to inhibit heat dependent expression of HSPs. In this study, therefore, the effects of prior exposure to QCT followed by HT on the cytotoxic and apoptotic activities were evaluated in FM3A, mouse breast cancer cells. Treatment of FM3A cells to 10 μM QCT and hyperthermia at 43°C for 1 h (HT) suppressed cell proliferation only in 34% and 55%, respectively and were relatively ineffective. Combination of the two treatments (QCT+HT) synergistically inhibited cell proliferation (90% inhibition). QCT+HT also suppressed clonogenicity (80%), compared to the results of QCT (56%) and HT (41%). Apoptotic cell death occurred after each treatment in a time-dependent manner. There was 4.9 ± 0.7%, 9.6 ± 1.5% and 18.1 ± 4.3% apoptosis after QCT+HT, and 3.2 ± 0.2%, 4.6 ± 0.5% and 8.6 ± 2.8% apoptosis after QCT, 3.4 ± 0.1%, 5.1 ± 0.3% and 10.1 ± 3.1% apoptosis after HT 1, 6 and 24 h post exposure compared to control of 2.0 ± 0.1%. HT or QCT proved ineffective in suppressing cell proliferation or inducing apoptosis. QCT+HT induced an accumulation of cells in G2/M and S phases and a reduction in G0/G1phase. The increased FM3A cell killing by HT after prior exposure to QCT is probably due to suppressed HSPs expression and diminished cellular thermotolerance. QCT may play a useful adjunct role in the hyperthermic treatment of resistant tumor. Hyperthermia (HT) cancer treatments have been widely utilised, however, cancer cells develop thermotolerance following exposure to HT, and heat shock proteins (HSPs) are responsible for thermotolerance. A plant flavonoid, quercetin (QCT), has been reported to inhibit heat dependent expression of HSPs. In this study, therefore, the effects of prior exposure to QCT followed by HT on the cytotoxic and apoptotic activities were evaluated in FM3A, mouse breast cancer cells. Treatment of FM3A cells to 10 μM QCT and hyperthermia at 43℃ for 1 h (HT) suppressed cell proliferation only in 34% and 55%, respectively and were relatively ineffective. Combination of the two treatments (QCT+HT) synergistically inhibited cell proliferation (90% inhibition). QCT+HT also suppressed clonogenicity (80%), compared to the results of QCT (56%) and HT (41%). Apoptotic cell death occurred after each treatment in a time-dependent manner. There was 4.9±0.7%, 9 6±1.5% and 18.1±4.3% apoptosis after QCT+HT, and 3.2±0.2%, 4.6±0.5% and 8.6±2.8% apoptosis after QCT, 3.4±0.1%, 5.1±0.3% and 10.1±3.1% apoptosis after HT 1, 6 and 24 h post exposure compared to control of 2.0±0.1%. HT or QCT proved ineffective in suppressing cell proliferation or inducing apoptosis. QCT+HT induced an accumulation of cells in G_2 /M and S phases and a reduction in G_0 /G_1 phase. The increased FM3A cell killing by HT after prior exposure to QCT is probably due to suppressed HSPs expression and diminished cellular thermotolerance. QCT may play a useful adjunct role in the hyperthermic treatment of resistant tumor. |
| Author | KOSAKA, MITSUO LEE, JEONG-BEOM GOTO, SHINJI OTHMAN, TIMOTHY NOK, ANDREW MATSUMOTO, TAKAAKI |
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| References | 6) Fujita M., Nagai M., Murata M., Kawakami K., Irino S., Takahara J. : Synergistic cytotoxic effect of quercetin and heat treatment in a lymphoid cell line (OZ) with low HSP70 expression. Leuk Res, 21 : 139-145, 1997. 12) Hansen R.K., Oesterreich S., Lemieux P., Sarge K.D., Fuqua S.A. : Quercetin inhibits heat shock protein induction but not heat shock factor DNA-binding in human breast carcinoma cells. Biochem Biophys Res Commun, 239 : 851-856, 1997. 1) 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, 89 : 463-469, 1998. 7) Ogawa A., Griffin R.J., Song C.W. : Effect of a combination of mild-temperature hyperthermia and nicotinamide on the radiation response of experimental tumors. Radiat Res, 153 : 327-31, 2000. 5) Kobayashi T. : Hyperthermia for brain tumors. Jpn J Hyperthermic Oncol, 9 : 245-249, 1993. 13) Barry M.A., Behnke C.A., Eastman A. : Activation of programmed cell death (apoptosis) by cisplatin, other anticancer drugs, toxins and hyperthermia. Biochem Pharmacol, 40 : 2353-2362, 1990. 20) Jaattela M., Wissing D., Kokholm K., Kallunki T., Egeblad M. : Hsp70 exerts its anti-apoptotic function downstream of caspase-3-like proteases. EMBO, 17 : 6124-6134, 1998. 9) Zhou Y., Lee A.S. : Mechanism for suppression of the mammalian stress response by genistein, an anticancer phytoestrogen from soy. J Nat Cancer Inst, 90 : 381-388, 1998. 10) Hosakawa N., Hirayoshi H., Kudo H., Takechi H., Aoike A., Kawai K., Nagata K. : Inhibition of the activation of heat -shock factor in vivo and in vitro by flavonoids. Mol Cell Biol, 12 : 3490-3498, 1992. 8) Benndorf R., Bielka H. : Cellular stress response : stress proteins-physiology and implications for cancer. Recent Results Cancer Res, 143 : 129-144, 1997. 19) Mosser DD., Caron AW., Bourget L., Denis-Larose C., Massie B. : Role of human heat shock protein 70 in protection against stress-induced apoptosis. Mol Cell Biol, 17 : 5317-5327, 1997. 2) Harmon B.V., Takano Y.S., Winterford C.M., Gobe G.C. : The role of apoptosis in the response of cells and tumours to mild hyperthermia. Int J Radiat Biol, 59 : 489-501, 1991. 16) Wei YQ., Zhao X., Kariya Y., Fukata H., Teshigawara K., Uchida A. : Induction of apoptosis by quercetin : involvement of heat shock protein. Cancer Res, 54 : 4952-4957, 1994. 15) So F.V., Guthrie N., Chambers A.F., Moussa M., Carroll K.K. : Inhibition of human breast cancer cell proliferation and delay of mammary tumorigenesis by flavonoids and citrus juices. Nutr Cancer, 26 : 167-181, 1996. 3) Overgaard K., Overgaard J, : Investigations on the possibility of a thermic tumor therapy. I. Short-wave treatment of transplanted isologous mouse mammary carcinoma. Eur J Cancer, 39 : 65-78, 1972. 17) Plauman B., Fritsche M., Rimpler H., Brandner G., Hess RD. : Flavonoids activates wild-type p53. Oncogene, 13 : 1605-1614, 1996. 18) Gabai VL., Meriin AB., Mosser DD., Caron AW., Rits S., Shifrin VI., Sherman MY. : Hsp70 prevents activation of stress kinases. A novel pathway of cellular thermotolerance. J Biol Chem, 272 : 18033-18037, 1997. 4) Overgaard J. : Effect of hyperthermia on malignant cells in vivo. Cancer, 39 : 2637-2646, 1977. 14) Kang TB., Liang NC. : Studies on the inhibitory effects of quercetin on the growth of HL-60 leukemia cells. Biochem Pharmacol, 54 : 1013-1018, 1997. 11) Nagai N., Nakai A., Nagata K. : Quercetin suppresses heat-shock response by down-regulation of HSF1. Biochem Biophys Res Commun, 208 : 1099-1105, 1995. |
| References_xml | – reference: 10) Hosakawa N., Hirayoshi H., Kudo H., Takechi H., Aoike A., Kawai K., Nagata K. : Inhibition of the activation of heat -shock factor in vivo and in vitro by flavonoids. Mol Cell Biol, 12 : 3490-3498, 1992. – reference: 15) So F.V., Guthrie N., Chambers A.F., Moussa M., Carroll K.K. : Inhibition of human breast cancer cell proliferation and delay of mammary tumorigenesis by flavonoids and citrus juices. Nutr Cancer, 26 : 167-181, 1996. – reference: 5) Kobayashi T. : Hyperthermia for brain tumors. Jpn J Hyperthermic Oncol, 9 : 245-249, 1993. – reference: 12) Hansen R.K., Oesterreich S., Lemieux P., Sarge K.D., Fuqua S.A. : Quercetin inhibits heat shock protein induction but not heat shock factor DNA-binding in human breast carcinoma cells. Biochem Biophys Res Commun, 239 : 851-856, 1997. – reference: 2) Harmon B.V., Takano Y.S., Winterford C.M., Gobe G.C. : The role of apoptosis in the response of cells and tumours to mild hyperthermia. Int J Radiat Biol, 59 : 489-501, 1991. – reference: 3) Overgaard K., Overgaard J, : Investigations on the possibility of a thermic tumor therapy. I. Short-wave treatment of transplanted isologous mouse mammary carcinoma. Eur J Cancer, 39 : 65-78, 1972. – reference: 9) Zhou Y., Lee A.S. : Mechanism for suppression of the mammalian stress response by genistein, an anticancer phytoestrogen from soy. J Nat Cancer Inst, 90 : 381-388, 1998. – reference: 20) Jaattela M., Wissing D., Kokholm K., Kallunki T., Egeblad M. : Hsp70 exerts its anti-apoptotic function downstream of caspase-3-like proteases. EMBO, 17 : 6124-6134, 1998. – reference: 11) Nagai N., Nakai A., Nagata K. : Quercetin suppresses heat-shock response by down-regulation of HSF1. Biochem Biophys Res Commun, 208 : 1099-1105, 1995. – reference: 17) Plauman B., Fritsche M., Rimpler H., Brandner G., Hess RD. : Flavonoids activates wild-type p53. Oncogene, 13 : 1605-1614, 1996. – reference: 6) Fujita M., Nagai M., Murata M., Kawakami K., Irino S., Takahara J. : Synergistic cytotoxic effect of quercetin and heat treatment in a lymphoid cell line (OZ) with low HSP70 expression. Leuk Res, 21 : 139-145, 1997. – reference: 7) Ogawa A., Griffin R.J., Song C.W. : Effect of a combination of mild-temperature hyperthermia and nicotinamide on the radiation response of experimental tumors. Radiat Res, 153 : 327-31, 2000. – reference: 8) Benndorf R., Bielka H. : Cellular stress response : stress proteins-physiology and implications for cancer. Recent Results Cancer Res, 143 : 129-144, 1997. – reference: 4) Overgaard J. : Effect of hyperthermia on malignant cells in vivo. Cancer, 39 : 2637-2646, 1977. – reference: 13) Barry M.A., Behnke C.A., Eastman A. : Activation of programmed cell death (apoptosis) by cisplatin, other anticancer drugs, toxins and hyperthermia. Biochem Pharmacol, 40 : 2353-2362, 1990. – reference: 14) Kang TB., Liang NC. : Studies on the inhibitory effects of quercetin on the growth of HL-60 leukemia cells. Biochem Pharmacol, 54 : 1013-1018, 1997. – reference: 16) Wei YQ., Zhao X., Kariya Y., Fukata H., Teshigawara K., Uchida A. : Induction of apoptosis by quercetin : involvement of heat shock protein. Cancer Res, 54 : 4952-4957, 1994. – reference: 19) Mosser DD., Caron AW., Bourget L., Denis-Larose C., Massie B. : Role of human heat shock protein 70 in protection against stress-induced apoptosis. Mol Cell Biol, 17 : 5317-5327, 1997. – reference: 18) Gabai VL., Meriin AB., Mosser DD., Caron AW., Rits S., Shifrin VI., Sherman MY. : Hsp70 prevents activation of stress kinases. A novel pathway of cellular thermotolerance. J Biol Chem, 272 : 18033-18037, 1997. – reference: 1) 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, 89 : 463-469, 1998. |
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| Title | Prior Exposure of FM3A Cells to Quercetin Results in Enhanced Cytotoxic and Apoptotic Effects of Hyperthermia |
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