Heat shock increases expression of NAD(P)H:quinone oxidoreductase (NQO1), mediator of β-lapachone cytotoxicity, by increasing NQO1 gene activity and via Hsp70-mediated stabilisation of NQO1 protein

International Journal of Hyperthermia

Volumn 25, Issue 6, 2009, Pages 477-487

  Dong, Guang Zhi ^a   Youn, Hyewon ^a   Park, Moon Taek ^a   Oh, Eun Taex ^a   Park, Kyung Hee ^a   Song, Chang Won ^b   Kyung Choi, Eun ^c   Park, Heon Joo ^a,b  

^a Inha University School of Medicine   (South Korea)

^b UNIVERSITY OF MINNESOTA   (United States)

^c University of Ulsan   (South Korea)

Author keywords

Betalapachone; Hsp70; Hyperthermia; NQO1

Indexed keywords

BETA LAPACHONE; HEAT SHOCK PROTEIN 70; MESSENGER RNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; CANCER CELL; CELL DEATH; CONTROLLED STUDY; CYTOTOXICITY; GENE ACTIVITY; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HEAT SHOCK; HEATING; HUMAN; HUMAN CELL; PROMOTER REGION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; TURNOVER TIME; WESTERN BLOTTING; XENOBIOTIC METABOLISM;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; CELL DEATH; CELL LINE, TUMOR; CYCLOHEXIMIDE; DACTINOMYCIN; GENE EXPRESSION REGULATION, NEOPLASTIC; HEAT-SHOCK RESPONSE; HSP70 HEAT-SHOCK PROTEINS; HUMANS; HYPERTHERMIA, INDUCED; NAD(P)H DEHYDROGENASE (QUINONE); NAPHTHOQUINONES;

EID: 70849106184     PISSN: 02656736     EISSN: 14645157     Source Type: Journal    
DOI: 10.1080/02656730903049836     Document Type: Article

References (55)

1. Begleiter A, Fourie J. Induction of NQO1 in cancer cells. Methods Enzymol 2004;382:320-351.
2. Joseph P, Jaiswal AK. NAD(P)H: Quinone oxidoreductase1 (DT diaphorase) specifically prevents the formation of benzo[a]pyrene quinone-DNA adducts generated by cytochrome P4501A1 and P450 reductase. Proc Natl Acad Sci USA 1994;91:8413-8417.
3. Ross D, Siegel D. NAD(P)H: Quinone oxidoreductase 1 (NQO1, DT-diaphorase), functions and pharmacogenetics. Methods Enzymol 2004;382:115-144.
4. Talalay P, Dinkova-Kostova AT. Role of nicotinamide quinone oxidoreductase 1 (NQO1) in protection against toxicity of electrophiles and reactive oxygen intermediates. Methods Enzymol 2004;382:355-364.
5. Rauth AM, Goldberg Z, Misra V. DT-diaphorase: Possible roles in cancer chemotherapy and carcinogenesis. Oncol Res 1997;9:339-349.
6. Robertson N, Stratford IJ, Houlbrook S, Carmichael J, Adams GE. The sensitivity of human tumour cells to quinone bioreductive drugs: What role for DT-diaphorase? Biochem Pharmacol 1992;44:409-412.
7. Begleiter A, Leith MK, Thliveris JA, Digby T. Dietary induction of NQO1 increases the antitumour activity of mitomycin C in human colon tumours in vivo. Br J Cancer 2004;91:1624-1631.
8. Siegel D, Beall H, Senekowitsch C, et al. Bioreductive activation of mitomycin C by DT-diaphorase. Biochemistry 1992;31:7879-7885.
9. Keyes SR, Fracasso PM, Heimbrook DC, et al. Role of NADPH:cytochrome c reductase and DT-diaphorase in the biotransformation of mitomycin C1. Cancer Res 1984;44:5638-5643.
10. Loadman PM, Bibby MC, Phillips RM. Pharmacological approach towards the development of indolequinone bioreductive drugs based on the clinically inactive agent EO9. Br J Pharmacol 2002;137:701-709.
11. Winski SL, Swann E, Hargreaves RH, et al. Relationship between NAD(P)H: Quinone oxidoreductase 1 (NQO1) levels in a series of stably transfected cell lines and susceptibility to antitumor quinones. Biochem Pharmacol 2001;61: 1509-1516.
12. Fitzsimmons SA, Workman P, Grever M, et al. Reductase enzyme expression across the National Cancer Institute Tumor cell line panel: Correlation with sensitivity to mitomycin C and EO9. J Natl Cancer Inst 1996;88:259-269.
13. Pink JJ, Planchon SM, Tagliarino C, et al. NAD(P)H: Quinone oxidoreductase activity is the principal determinant of beta-lapachone cytotoxicity. J Biol Chem 2000;275:5416-5424.
14. Planchon SM, Pink JJ, Tagliarino C, et al. beta-Lapachoneinduced apoptosis in human prostate cancer cells: Involvement of NQO1/xip3. Exp Cell Res 2001;267:95-106.
15. Bey EA, Bentle MS, Reinicke KE, et al. An NQO1- and PARP-1-mediated cell death pathway induced in non-smallcell lung cancer cells by beta-lapachone. Proc Natl Acad Sci USA 2007;104:11832-11837.
16. Cruz FS, Docampo R, Boveris A. Generation of superoxide anions and hydrogen peroxide from beta-lapachone in bacteria. Antimicrob Agents Chemother 1978;14:630-633.
17. Docampo R, Cruz FS, Boveris A, Muniz RP, Esquivel DM. beta-Lapachone enhancement of lipid peroxidation and superoxide anion and hydrogen peroxide formation by sarcoma 180 ascites tumor cells. Biochem Pharmacol 1979; 28:723-728.
18. Pardee AB, Li YZ, Li CJ. Cancer therapy with betalapachone. Curr Cancer Drug Targets 2002;2: 27-242.
19. Li Y, Sun X, LaMont JT, Pardee AB, Li CJ. Selective killing of cancer cells by beta -lapachone: Direct checkpoint activation as a strategy against cancer. Proc Natl Acad Sci USA 2003;100:2674-2678.
20. Tagliarino C, Pink JJ, Dubyak GR, Nieminen AL, Boothman DA. Calcium is a key signaling molecule in beta-lapachonemediated cell death. J Biol Chem 2001;276:19150-19159.
21. Bentle MS, Reinicke KE, Bey EA, Spitz DR, Boothman DA. Calcium-dependent modulation of poly(ADP-ribose) polymerase- 1 alters cellular metabolism and DNA repair. J Biol Chem 2006;281:33684-33696.
22. Park HJ, Ahn KJ, Ahn SD, et al. Susceptibility of cancer cells to beta-lapachone is enhanced by ionizing radiation. Int J Radiat Oncol Biol Phys 2005;61:212-219.
23. Suzuki M, Amano M, Choi J, et al. Synergistic effects of radiation and beta-lapachone in DU-145 human prostate cancer cells in vitro. Radiat Res 2006;165:525-531.
24. Choi EK, Terai K, Ji IM, et al. Upregulation of NAD(P)H: Quinone oxidoreductase by radiation potentiates the effect of bioreductive beta-lapachone on cancer cells. Neoplasia 2007;9:634-642.
25. Park HJ, Choi EK, Choi J, et al. Heat-induced up-regulation of NAD(P)H: Quinone oxidoreductase potentiates anticancer effects of beta-lapachone. Clin Cancer Res 2005;11: 8866-8871.
26. Song CW, Chae JJ, Choi EK, et al. Anti-cancer effect of bio-reductive drug beta-lapachon is enhanced by activating NQO1 with heat shock. Int J Hyperthermia 2008;24:161-169.
27. Siegel D, Franklin WA, Ross D. Immunohistochemical detection of NAD(P)H: Quinone oxidoreductase in human lung and lung tumors. Clin Cancer Res 1998;4:2065-2070.
28. Belinsky M, Jaiswal AK. NAD(P)H: Quinone oxidoreductase1 (DT-diaphorase) expression in normal and tumor tissues. Cancer Metastasis Rev 1993;12:103-117.
29. Cresteil T, Jaiswal AK. High levels of expression of the NAD(P)H: Quinone oxidoreductase (NQO1) gene in tumor cells compared to normal cells of the same origin. Biochem Pharmacol 1991;42:1021-1027.
30. Beall HD, Murphy AM, Siegel D, et al. Nicotinamide adenine dinucleotide (phosphate): Quinone oxidoreductase (DT-diaphorase) as a target for bioreductive antitumor quinones: Quinone cytotoxicity and selectivity in human lung and breast cancer cell lines. Mol Pharmacol 1995;48:499-504.
31. Kepa JK, Ross D. Differential expression of the antioxidant response element within the hNQO1 promoter in NSCLC versus SCLC. Biochem Biophys Res Commun 2003;311: 446-453.
32. Boothman DA, Trask DK, Pardee AB. Inhibition of potentially lethal DNA damage repair in human tumor cells by betalapachone, an activator of topoisomerase I. Cancer Res 1989;49:605-612.
33. Bentle MS, Reinicke KE, Dong Y, Bey EA, Boothman DA. Nonhomologous end joining is essential for cellular resistance to the novel antitumor agent, beta-lapachone. Cancer Res 2007;67:6936-6945.
34. Khong HT, Dreisbach L, Kindler HL, et al. A phase 2 study of ARQ 501 in combination with gemcitabine in adult patients with treatment naïve, unresectable pancreatic adenocarcinoma. ASCO Annual Meeting Proceedings Part I. J Clin Oncol 2007;25:15017.
35. Blanco E, Bey EA, Dong Y, et al. Beta-lapachone-containing PEG-PLA polymer micelles as novel nanotherapeutics against NQO1-overexpressing tumor cells. J Control Release 2007;122:365-374.
36. Dong Y, Chin SF, Blanco E, et al. Intratumoral delivery of beta-lapachone via polymer implants for prostate cancer therapy. Clin Cancer Res 2009;15:131-139.
37. Long DJ, II, Gaikwad A, Multani A, et al. Disruption of the NAD(P)H: Quinone oxidoreductase 1 (NQO1) gene in mice causes myelogenous hyperplasia. Cancer Res 2002;62: 3030-3036.
38. Dhakshinamoorthy S, Jaiswal AK. Functional characterization and role of INrf2 in antioxidant response element-mediated expression and antioxidant induction of NAD(P)H: Quinone oxidoreductase1 gene. Oncogene 2001;20:3906-3917.
39. Nioi P, Hayes JD. Contribution of NAD(P)H: Quinone oxidoreductase 1 to protection against carcinogenesis, and regulation of its gene by the Nrf2 basic-region leucine zipper and the arylhydrocarbon receptor basic helix-loop-helix transcription factors. Mutat Res 2004;555:149-171.
40. Jaiswal AK. Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic Biol Med 2004; 36:1199-1207.
41. Xie T, Belinsky M, Xu Y, Jaiswal AK. ARE- and TREmediated regulation of gene expression. Response to xenobiotics and antioxidants. J Biol Chem 1995;270:6894-6900.
42. Anwar A, Siegel D, Kepa JK, Ross D. Interaction of the molecular chaperone Hsp70 with human NAD(P)H: Quinone oxidoreductase 1. J Biol Chem 2002;277:14060-14067.
43. Elegbeleye OO. Cavernous sinus thrombosis in Nigerians. West Indian Med J 1975;24:94-96.
44. Ma Q, Kinneer K, Bi Y, Chan JY, Kan YW. Induction of murine NAD(P)H: Quinone oxidoreductase by 2,3,7,8-tetrachlorodibenzo- p-dioxin requires the CNC (cap 'n' collar) basic leucine zipper transcription factor Nrf2 (nuclear factor erythroid 2-related factor 2): cross-interaction between AhR (aryl hydrocarbon receptor) and Nrf2 signal transduction. Biochem J 2004;377:205-213.
45. Reddy AJ, Christie JD, Aplenc R, et al. Association of Human Nad(P)H: Quinone Oxidoreductase 1 (Nqo1) Polymorphism with Development of Acute Lung Injury. J Cell Mol Med 2008.
46. Tirumalai R, Rajesh Kumar T, Mai KH, Biswal S. Acrolein causes transcriptional induction of phase II genes by activation of Nrf2 in human lung type II epithelial (A549) cells. Toxicol Lett 2002;132:27-36.
47. Dhakshinamoorthy S, Jaiswal AK. c-Maf negatively regulates ARE-mediated detoxifying enzyme genes expression and anti-oxidant induction. Oncogene 2002;21: 5301-5312.
48. Yang XY, Yang TT, Schubert W, Factor SM, Chow CW. Dosage-dependent transcriptional regulation by the calcineurin/ NFAT signaling in developing myocardium transition. Dev Biol 2007;303:825-837.
49. Kolesar JM, Rizzo JD, Kuhn JG. Quantitative analysis of NQO1 gene expression by RT-PCR and CE-LIF. J Capillary Electrophor 1995;2:287-290.
50. Fritsche E, Schafer C, Calles C, et al. Lightening up the UV response by identification of the arylhydrocarbon receptor as a cytoplasmatic target for ultraviolet B radiation. Proc Natl Acad Sci USA 2007;104:8851-8856.
51. Pontrelli P, Ursi M, Ranieri E, et al. CD40L proinflammatory and profibrotic effects on proximal tubular epithelial cells: Role of NF-kappaB and lyn. J Am Soc Nephrol 2006; 17:627-636.
52. Kolesar JM, Rizzo JD, Kuhn JG. Quantitative analysis of NQO1 gene expression by RT-PCR and CE-LIF. J Capillary Electrophor 1995;2:287-290.
53. Haemi Lee, Hee-Jin Kwak, Il-taeg Cho, Seok Hee Park, Chang-Hun Lee. S1219 residue of 53BP1 is phosphorylated by ATM kinase upon DNA damage and required for proper execution of DNA damage response. Biochem Biophys Res Comm 2009;378:32-36.
54. + T cell-mediated cell death. Immunol Lett 2009;122:58-67.
55. Korashy HM, El-Kadi AO. Transcriptional regulation of the NAD(P)H: Quinone oxidoreductase 1 and glutathione S-transferase ya genes by mercury, lead, and copper. Drug Metab Dispos 2006;34:152-165.