DT-diaphorase: A target for new anticancer drugs

Cancer Treatment Reviews

Volumn 30, Issue 5, 2004, Pages 437-449

  Danson, S ^a,b   Ward, T H ^a   Butler, J ^c   Ranson, M ^a,b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b CHRISTIE HOSPITAL   (United Kingdom)

^c UNIVERSITY OF SALFORD   (United Kingdom)

Author keywords

Bioreductive; Diaziridinylquinones; DT diaphorase; Induction; Resistance; RH1

Indexed keywords

2,5 DIAZIRIDINYL 3 HYDROXYMETHYL 6 METHYL 1,4 BENZOQUINONE; 2,5 DIAZIRIDINYL 3,6 BIS(2 HYDROXYETHYLAMINO) 1,4 BENZOQUINONE; 2,5 DIAZIRIDINYL 3,6 DIMETHYL 1,4 BENZOQUINONE; 3 HYDROXY 5 AZIRIDINYL 1 METHYL 2(1H INDOLE 4,7 DIONE)PROP BETA EN ALPHA OL; 5 (1 AZIRIDINYL) 2,4 DINITROBENZAMIDE; ACETYLSALICYLIC ACID; ALPHA TOCOPHEROL; ANTICOAGULANT AGENT; ANTINEOPLASTIC AGENT; BENZOQUINONE DERIVATIVE; BETA NAPHTHOFLAVONE; BUTYLATED HYDROXYANISOLE; CYCLODEXTRIN; DIAZIQUONE; DICOUMAROL; DIHYDROLIPOAMIDE DEHYDROGENASE; FISETIN; HEAT SHOCK PROTEIN 70; MITOMYCIN C; MITOMYCIN DERIVATIVE; OLTIPRAZ; OXIDOREDUCTASE; QUERCETIN; QUINONE DERIVATIVE; RETINOIC ACID; SULFONE DERIVATIVE; SULFORAPHANE; UBIQUINONE; UNCLASSIFIED DRUG; UNINDEXED DRUG; WARFARIN;

ANTINEOPLASTIC ACTIVITY; BONE MARROW SUPPRESSION; BRAIN TUMOR; CELLULAR DISTRIBUTION; CLINICAL TRIAL; DRUG METABOLISM; DRUG RESISTANCE; DRUG RESPONSE; DRUG SOLUBILITY; DRUG TARGETING; HEAD AND NECK CANCER; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INJECTION SITE; INJECTION SITE REACTION; KIDNEY CANCER; LIVER CANCER; NEPHROTOXICITY; NONHUMAN; PH; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN POLYMORPHISM; PROTEIN STRUCTURE; PROTEIN TARGETING; REVIEW; SIDE EFFECT; SINGLE NUCLEOTIDE POLYMORPHISM; SOLID TUMOR; STOMACH CANCER; STRUCTURE ANALYSIS; TISSUE DISTRIBUTION;

EID: 3242742185     PISSN: 03057372     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ctrv.2004.01.002     Document Type: Article

References (145)

1. Ernster L. Navazio F. Soluble diaphorase in animal tissues Acta Chemica Scandanavia 12 1958 595-602
2. Gutierrez P.L. The role of NAD(P)H oxidoreductase (DT-diaphorase) in the bioactivation of quinone-containing antitumour agents: a review Free Rad. Biol. Med. 29 2000 263-275
3. Ross D. Kepa J. Winski S. Beall H.D. Anwar A. Siegel D. NAD(P)H: quinone oxidoreductase 1 (NQO1): chemoprotection, gene regulation and genetic polymorphisms Chem-Biol. Int. 129 2000 77-97
4. Rauth A.M. Goldberg Z. Misra V. DT-diaphorase: possible roles in cancer chemotherapy and carcinogenesis Oncol. Res. 9 1997 339-349
5. Ross D. Beall H. Traver R. Siegel D. Phillips R.M. Gibson N.W. Bioactivation of quinones by DT-diaphorase, molecular, biochemical and chemical studies Oncol. Res. 6 1994 493-500
6. Ross D. Siegel D. Beall H. Prakash A.S. Mulcahy R.T. Gibson N.W. DT-diaphorase in activation and detoxification of quinones. Bioreductive activation of mitomycin C Cancer Metastasis Rev. 12 1993 83-101
7. Riley R.J. Workman P. DT-diaphorase and cancer chemotherapy Biochem. Pharmacol. 43 1992 1657-1669
8. Eliasson M. Bostrom M. Depierre J.W. Levels and subcellular distributions of detoxifying enzymes in the ovarian corpus luteum of the pregnant and non-pregnant pig Biochem. Pharmacol. 58 1999 1287-1292
9. Danielson L. Ernster L. Ljunggren M. Selective extraction of DT-diaphorase from mitochondria and microsomes Acta Chem. Scand. 14 1960 1837-1838
10. Conover T.E. Ernster L. DT-diaphorase IV. Coupling of extramitochondrial reduced pyridine nucleotide oxidation to mitochondrial respiratory chain Biochem. Biophys. Acta 67 1968 268-280
11. Edlund C. Elhrmammer A. Dallner G. Distribution of newly synthesised DT-diaphorase in rat liver Biosci. Rep. 2 1982 861-865
12. Winski S.L. Koutalos Y. Bentley D.L. Ross D. Subcellular localisation of NAD(P)H:quinone oxidoreductase 1 in human cancer cells Cancer Res. 62 2002 1420-1424
13. Siegel D. Gibson N.W. Preusch P.C. Ross D. Metabolism of NAD(P)H: (quinone acceptor) oxidoreductase (DT-diaphorase): role in diaziquone-induced DNA damage and cytotoxicity in human colon carcinoma cells Cancer Res. 50 1990 7293-7300
14. Beyer R.E. Segura-Aguilar J. Di Bernardo S. et al. The role of DT-diaphorase in the maintenance of the reduced antioxidant form of coenzyme Q in membrane systems PNAS 93 1996 2528-2532
15. Siegel D. Bolton E.M. Burr J.A. Liebler D.C. Ross D. The reduction of alpha-tocopherolquinone by human NAD(P)H:quinone oxidoreductase: the role of alpha-tocopherolhydroquinone as a cellular antioxidant Mol. Pharmacol. 52 1997 300-305
16. Jaiswal A.K. Regulation of genes encoding NAD(P)H:quinone oxidoreductases Free Rad. Biol. Med. 29 2000 254-262
17. Benson A.N. Hunckler M.J. Talalay P. Increase of NAD(P)H:quinone reductase by dietary antioxidants: possible role in protection against carcinogenesis and toxicity PNAS 77 1980 5216-5220
18. Schlager J.J. Powis G. Cytosolic NAD(P)H:(quinone-acceptor) oxidoreductase in human and normal tissue: effects of cigarette smoking and alcohol Int. J. Cancer 45 1990 403-409
19. Chen S. Knox R. Wu K. Deng P.S.K. Zhou D. Molecular basis of the catalytic differences among DT-diaphorase of human, rat, and mouse J. Biol. Chem. 272 1997 1437-1439
20. Edwards Y.H. Potter J. Hopkinson D.S. Human FAD-dependent NAD(P)H diaphorase Biochem. J. 187 1980 429-436
21. Jaiswal A.K. McBride O.W. Adesnik M. Nebert D.W. Human dioxin-inducible cytosolic NAD(P)H:menadione oxidoreductase cDNA sequence and localization of gene to chromosome 16 J. Biol. Chem. 263 1988 13572-13578
22. Jaiswal A.K. Human NAD(P)H:quinone oxidoreductase (NQO1) gene structure and induction by dioxin Biochemistry 30 1991 10647-10653
23. Joseph P. Xie T. Xu Y. Jaiswal A.K. NAD(P)H:quinone oxidoreductase 1 (DT-diaphorase): expression, regulation and role in cancer Oncol. Res. 6 1994 525-532
24. Yao K. O'Dwyer P.J. Involvement of NF-kB in the induction of NAD(P)H:quinone oxidoreductase (DT-diaphorase) by hypoxia, oltipraz and mitomycin C Biochem. Pharmacol. 49 1995 275-282
25. Montano M.M. Jaiswal A.K. Katzenellenbogen B.S. Transcriptional regulation of the human quinone reductase gene by antioestrogen-liganded oestrogen receptor-α and oestrogen receptor-β Oncogene 273 1998 25443-25449
26. Jaiswal A.K. Burnet P. Adesnik M. McBride O.W. Nucleotide and deduced amino acid sequence of a human cDNA(NQO2) corresponding to a second member of the NAD(P)H:quinone oxidoreductase gene family. Extensive polymorphism at the NQO2 gene locus on chromosome 6 Biochemistry 29 1990 1899-1906
27. Chen S. Wu K. Knox R. Structure-function studies of DT-diaphorase (NQO1) and NRH:quinone oxidoreductase (NQO2) Free Rad. Biol. Med. 29 2000 276-284
28. Long D.J. II Jaiswal A.K. NRH:quinone oxidoreductase 2 (NQO2) Chem. Biol. Int. 129 2000 99-112
29. Traver R.D. Horikoshi T. Danenberg K.D. et al. NAD(P)H:quinone oxidoreductase gene expression in human colon carcinoma cells: characterisation of a mutation which modulates DT-diaphorase activity and mitomycin sensitivity Cancer Res. 52 1992 797-802
30. Siegel D. Anwar A Winski S.L. Kepa J.K. Zolman K.L. Ross D. Rapid polyubiquination and proteosomal degradation of a mutant form of NAD(P)H:quinone oxidoreductase 1 Mol. Pharmacol. 59 2001 263-268
31. Li R. Bianchet M.A. Talalay P. Amzel L.M. The three-dimentional structure of NAD(P)H:quinone reductase, a flavoprotein involved in cancer chemoprotection and chemotherapy: mechanism of the two-electron reduction PNAS 92 1995 8846-8850
32. Kelsey K.T. Ross D. Traver R.D. et al. Ethnic variation in the prevalence of a common NAD(P)H quinone oxidoreductase polymorphism and its implications for anticancer chemotherapy Br. J. Cancer 76 1997 852-854
33. Misra V. Grondin A. Klamut H.J. Rauth A.M. Assessment of the relationship between genotypic status of a DT-diaphorase point mutation and enzymatic activity Br. J. Cancer 83 2000 998-1002
34. Gaedigk A. Tyndale R.F. Jurima-Fomet M. Sellers E.M. Grant D.M. Leeder J.S. NAD(P)H:quinone oxidoreductase: polymorphisms and allele frequencies in Caucasian, Chinese and Canadian Native Indian and Inuit populations Pharmacogenetics 8 1998 305-313
35. Pan S.S. Han Y. Farabaugh P. Xia H. Implication of alternative splicing for expression of a variant NAD(P)H:quinone oxidoreductase-1 with a single nucleotide polymorphism at 465C>T Pharmacogenetics 12 2002 479-488
36. Yoneda Y. Hieda M. Nagoshi E. Miyamoto Y. Nucleocytoplasmic protein transport and recycling of Ran Cell Struct. Funct. 24 1999 425-433
37. Anwar A. Siegel D. Kepa J.K. Ross D. Interaction of the molecular chaperone HSP70 with human NAD(P)H:quinone oxidoreductase 1 J. Biol. Chem. 277 2002 14060-14067
38. Qiu X. Schonthal A.H. Cadenas E. Anticancer quinones induce pRb-preventable G2/M cell cycle arrest and apoptosis Free Rad. Biol. Med. 24 1998 848-854
39. Ngo E.O. Nutter L.M. Sura T. Gutierrez P.L. Induction of p53 by the concerted actions of aziridine and quinone moieties of diaziquone Chem. Res. Toxixol. 11 1988 360-368
40. Asher G. Lotem J. Kama R. Sachs L. Shaul Y. NQO1 stabilises p53 through a distinct pathway PNAS 99 2002 3099-3104
41. Schor N.A. Rice B.F. Huseby R.A. Dehydrogenation of reduced pyridine nucleotides by leydig cell tumours of the rat testis Proc. Soc. Exp. Biol. Med. 151 1976 418-421
42. Schor N.A. Morris H.P. The activity of DT-diaphorase in experimental hepatomas Biochem. Biophys. Acta 2 1977 5-9
43. Schor N.A. Ogawa K. Lee G. Farber E. The use of the DT-diaphorase for the detection of foci of early neoplastic transformation in rat liver Cancer Lett. 5 1978 167-171
44. Becker F.F. Stout D.L. A constitutive deficiency in the monooxygenase system of spontaneous mouse liver tumours Carcinogenesis 5 1984 785-788
45. Berger M.S. Talcott R.E. Rosenblum M.L. Use of quinones in brain tumour therapy: preliminary results of preclinical laboratory investigations J. Toxicol. Env. Health 16 1985 713-719
46. Beyer R.E. Segura-Aguilar J.E. Ernster L. The anticancer enzyme DT-diaphorase is induced selectively in the liver during ascites hepatoma growth Anticancer Res. 8 1988 233-238
47. Schor N.A. Cornelisse C.J. Biochemical and quantitative histochemical study of reduced pyridine nucleotide dehydrogenation by human colon carcinomas Cancer Res. 43 1983 4850-4855
48. Batist K. Cowan K.H. Curt G. Kathi A.G. Increased glutathione S-transferase activity (GST) in drug-treated human breast cancer cells Proc. Am. Assoc. Cancer Res. 26 1985 1362a
49. Cresteil T. Jaiswal A.K. High levels of expression of the NAD(P)H:quinone oxidoreductase (NQO1) gene in tumour cells compared to normal cells of the same origin Biochem. Pharm. 42 1991 1021-1027
50. Malkinson A.M. Siegel D. Forrest G.L. et al. Elevated DT-diaphorase activity and messanger RNA content in human non-small cell lung carcinomas - relationship to the response of human tumour xenografts to mitomycin C Cancer Res. 52 1992 4752-4757
51. Eickelmann P. Ebert T. Warskulat U. Schulz W.A. Sies H. Expression of NAD(P)H:quinone oxidoreductase and glutathione S-transferase alpha and pi in human renal cell carcinoma and in kidney cancer-derived cell lines Carcinogenesis 15 1994 219-225
52. Smitskamp-Wilms E. Giaccone G. Pinedo H.M. van der Laun B.F.A.M. Peters G.J. DT-diaphorase activity in normal and neoplastic human tissues; an indicator for sensitivity to bioreductive agents Br. J. Cancer 72 1995 917-921
53. Marin A. Lopez de Cerain A. Hamilton E. et al. DT-diaphorase and cytochrome B5 reductase in human lung and breast tumours Br. J. Cancer 76 1997 923-929
54. Williams J.B. Lu A.Y.H. Cameron R.G. Pickett C.B. Rat liver NAD(P)H:quinone reductase. Construction of a quinone reductase cDNA clone and regulation of quinone reductase mRNA by 3-methylcholanthrene and in persistent hepatocyte nodules induced by chemical carcinogens J. Biol. Chem. 261 1986 5524-5528
55. Workman P. Enzyme-directed bioreductive drug development revisited: a commentary on recent progress and future prospects with emphasis on quinone anticancer agents and quinone metabolising enzymes, particularly DT-diaphorase Oncol. Res. 6 1994 461-475
56. Sistonen L. Holtta E. Makela T.P. Keski-Oje J. Alitalo K. The cellular response to induction of the p21 c-Ha-ras oncoprotein includes stimulation of jun gene expression EMBO 8 1989 815-822
57. Mikami K. Naito M. Ishiguro T. et al. Immunological quantification of DT-diaphorase in carcinoma cell lines and clinical colon cancer cases: advanced tumours express greater levels of DT-diaphorase Jpn. J. Cancer Res. 89 1998 910-915
58. Schulz W.A. Krummeck A. Rosinger I. et al. Increased frequency of a null-allele for NAD(P)H:quinone oxidoreductase in patients with urological malignancies Pharmacogenetics 7 1977 235-239
59. Rosvold E.A. Mcglynn K.A. Lustbader E.D. Buetow K.H. Identification of an NAD(P)H:quinone oxidoreductase polymorphism and its association with lung cancer and smoking Pharmacogenetics 5 1995 199-206
60. Lafuente M.J. Casterad X. Trias M. et al. NAD(P)H:quinone oxidoreductase-dependent risk for colorectal cancer and its association with the presence of k-ras mutations in tumours Carcinogenesis 21 2000 1813-1819
61. Zhang J.-.H. Li Y. Wang R. et al. NQO1 C609T polymorphism associated with esophageal and gastric cardiac carcinoma in North China World J. Gastroenterol. 9 2003 1390-1393
62. Longuemaux S. Delomenie C. Gallon C. et al. Candidate genetic modifiers of individual susceptibility to renal cell carcinoma: a study of polymorphic human xenobiotic-metabolizing enzymes Cancer Res. 59 1999 2903-2908
63. Yin L. Pu Y. Liu T.-Y. Tung Y.-H. Chen K.-W. Lin P. Genetic polymorphisms of NAD(P)H quinone oxidoreductase, CYP1A1 and microsomal epoxide hydrolase and lung cancer risk in Nanjing, China Lung Cancer 33 2001 133-141
64. Hamajima N. Matsuo K. Ewato H. et al. NAD(P)H:quinone oxidoreductase 1 (NQO1) C609T polymorphism and the risk of eight cancers for Japanese Int. J. Clin. Oncol. 7 2002 103-108
65. Harth V. Donat S. Ko Y. Abel J. Vetter H. Bruning T. NAD(P)H quinone oxidoreductase 1 codon 609 polymorphism and its association to colorectal cancer Arch. Toxicol. 73 2000 528-531
66. Peters E.S. Kelsey K.T. Wiencke J.K. et al. NAT2 and NQO1 polymorphisms are not associated with adult glioma Cancer Epidemiol. Biomark. Prev. 10 2001 151-152
67. Soucek P. Sarmanova J. Kristensen V.N. Apltauerova M. Gut I. Genetic polymorphisms of biotransformation enzymes in patients with Hodgkin's and non-Hodgkin's lymphomas Int. Arch. Occup. Environ. Health 75 2002 S86-S92
68. Steiner M. Hillenbrand M. Borkowski M. Seiter H. Schuff-Werner P. 609 CaT polymorphism in NAD(P)H:quinone oxidoreductase gene in patients with prostatic adenocarcinoma or benign prostatic hyperplasia Cancer Lett. 135 1999 67-71
69. Smith M.T. Wang Y. Kane R. et al. Low NAD(P)H:quinone oxidoreductase 1 activity is associated with increased risk of acute leukaemia in adults Blood 97 2001 1422-1426
70. Wiemels J.L. Pagnamenta A. Taylor G.M. Eden O.B. Alexander F.E. Greaves M.F. A lack of a functional NAD(P)H:quinone oxidoreductase allele is selectively associated with paediatric leukaemias that have MLL fusions Cancer Res. 59 1999 4095-4099
71. Krajinovic M. Sinnett H. Richer C. Labuda D. Sinnett D. Role of NQO1, MPO and CYP2E1 genetic polymorphisms in the susceptibility to childhood acute lymphoblastic leukaemia Int. J. Cancer 97 2002 230-236
72. Larson R.A. Wang Y. Banerjee M. et al. Prevalence of the inactivating 609C->T polymorphism in the NAD(P)H:quinone oxidoreductase (NQO1) gene in patients with primary and therapy-related myeloid leukemia Blood 94 1999 803-807
73. Blanco J.G. Edick M.J. Hancock M.L. et al. Genetic polymorphisms in CYP3A5 CYP3A4 and NQO1 in children who developed therapy-related malignancies Pharmacogenetics 12 2002 605-611
74. Rothman N. Smith M.T. Hayes R.B. et al. Benzene poisoning, a risk factor for haematological malignancy, is associated with the NQO1 609C>T mutation and rapid fractional excretion of chlorzoxazone Cancer Res. 57 1997 2839-2842
75. Radjendirane V. Joseph P. Lee Y.H. et al. Disruption of the DT-diaphorase (NQO1) gene in mice leads to increased menadione toxicity J. Biol. Chem. 273 1998 7382-7389
76. Walton M.I. Smith P.J. Workman P. The role of NAD(P)H:quinone oxidoreductase (EC 1.6.99.2, DT-diaphorase) in the reductive bioactivation of the novel indoloquinone antitumour agent E09 Cancer Commun. 3 1991 199-206
77. Pardee A.B. Li Y.Z. Li C.J. Cancer therapy with β-lapachone Curr. Cancer Drug Targets 2 2002 227-242
78. Siegel D. Gibson N.W. Preusch P.C. Ross D. Metabolism of mitomycin C by DT-diaphorase: role in mitomycin C-induced DNA damage and cytotoxicity in human colon carcinoma cells Cancer Res. 50 1990 7483-7489
79. Tudor G. Gutierrez P. Aguilera-Gutierrez A. Sausville E.A. Cytotoxicity and apoptosis of benzoquinones: redox cycling, cytochrome release, and BAD protein expression Biochem. Pharmacol. 65 2003 1061-1075
80. Nemeikaite-Ceniene A. Sarlauskas J. Anusevicius Z. Nivinskas H. Cenas N. Cytotoxity of RH1 and related aziridinylbenzoquinones: involvement of activation by NAD(P)H:quinone oxidoreductase (NQO1) and oxidative stress Arch. Biochem. Biophys. 416 2003 110-118
81. Hoey B.M. Butler J.B. Swallow A.J. Reductive activation of mitomycin C Biochemistry 27 1988 2608-2614
82. Fitzsimmons S.A. Workman P. Grever M. Paull K. Camalier R. Lewis A.D. Reductase enzyme expression across the national cancer institute tumour cell line panel: correlation with sensitivity to mitomycin C and E09 J. Natl. Cancer Inst. 83 1996 259-269
83. Gustafson D.L. Beal H.D. Bolton E.M. Ross D. Waldren C.A. Expression of human NAD(P)H: quinone oxoreductase (DT-diaphorase) in chinese hamster ovary cells; effects on the cytotoxicity of antitumour quinones Mol. Pharmacol. 50 1996 728-735
84. Nishiyama M. Saeki S. Aogi K. Hirabayashi N. Toge T. Relevance of DT-diaphorase activity to mitomycin C efficacy on human cancer cells: differences in in vitro and in vivo systems Int. J. Cancer 53 1993 1013-1016
85. Phillips R.M. Burger A.M. Loadman P.M. Jarrett C.M. Swaine D.J. Fiebig H.-.H. Predicting tumour responses to mitomycin C on the basis of DT-diaphorase activity or drug metabolism by tumour homogenates: implications for enzyme-directed bioreductive drug development Cancer Res. 60 2000 6384-6390
86. Marshall R.S. Paterson M.C. Rauth A.M. DT-diaphorase activity and mitomycin C sensitivity in non-transformed cell strains derived from members of a cancer-prone family Biochem. Pharmacol. 12 1991 1175-1180
87. Beall H.D. Murphy A.M. Siegel D. Hargreaves R.H. Butler J. Ross D. Nicotinamide adenine dinucleotide (Phosphate):quinone oxidoreductase (DT-diaphorase) as a target for bioreductive antitumour quinones; quinone cytotoxicity and selectivity in human lung and breast cancer cell lines Mol. Pharmacol. 48 1995 499-504
88. Siegel D. Beall H. Kasai M. Atal H. Gibson N.W. Ross D. pH-dependent inactivation of DT-diaphorase by mitomycin C and porfiromycin Mol. Pharmacol. 44 1993 1128-1134
89. Robertson N. Stratford I.J. Houlbrook S. Carmichael J. Adams G.E. The sensitivity of human tumour cells to quinone bioreductive drugs: what role for DT-diaphorase Biochem. Pharm. 44 1992 409-412
90. Schellens J.H.M. Planting A.S. van Acker B.A.C. et al. Phase I and pharmacologic study of the novel indoloquinone bioreductive alkylating cytotoxic drug E09 J. Natl. Cancer Inst. 86 1994 906-912
91. Knox R.J. Friedlos F. Jarman M. Roberts J.J. A new cytotoxic DNA interstrand crosslinking agent 5-(aziridin-1-yl)-4-hydroxylamino-2-nitrobenzamide is formed from 5-(aziridin-1-yl-2,4-dinitrobenzamide (CB1954) by a nitroreductase enzyme in walker carcinoma cells Biochem. Pharmacol. 37 1988 4661-4669
92. Boland M.P. Knox R.J. Roberts J.J. The differences in kinetics of rat and human DT-diaphorase result in a differential sensitivity of derived cell lines to CB1954 (5-(aziridin-1-yl)-2,4-dinitrobenzamide) Biochem. Pharmacol. 41 1991 867-875
93. Knox R.J. Jenkins T.C. Hobbs S.M. Chen S. Melton R.G. Burke P.J. Bioactivation of 5-(aziridin--yl)-2,4-dinitrobenzamide (CB1954) by human NAD(P)H:quinone oxidoreductase. 2. A novel co-substrate-mediated antitumour prodrug therapy Cancer Res. 60 2000 4179-4186
94. Butler J. Dzielendziak A. Lea J.S. Ward T.H. Hoey B.M. Contrasting cytotoxic mechanisms of similar antitumour diaziridinylbenzoquinones Free Rad. Res. Comms. 8 1990 231-239
95. Gibson N.W. Hartley J.A. Butler J. Siegel D. Ross D. Relationship between DT-diaphorase mediated metabolism of a series of aziridinylbenzoquinones and DNA damage and cytotoxicity Mol. Pharmacol. 42 1992 531-536
96. Haid M. Khandekhar J.D. Christ M. et al. Aziridinylbenzoquinone in recurrent, progressive glioma of the central nervous system. A Phase II study by the Illinois Cancer Council Cancer 56 1985 1311-1315
97. Case D.C. Jr. Hayes D.M. Phase II study of aziridinylbenzoquinone in refractory lymphoma Cancer Treat Rep. 67 1983 993-996
98. Lee C.S. Hartley J.A. Beradini M.D. et al. Alteration in DNA cross-linking and sequence selectivity of a series of aziridinylbenzoquinones after enzymatic reduction by DT-diaphorase Biochemistry 31 1992 3019-3025
99. Berardini M.D. Souhami R.L. Lee C.S. Gibson N.W. Butler J. Hartley J.A. Two structurally related diaziridinylbenzoquinones preferentially cross-link DNA at different sites upon reduction with DT-diaphorase Biochemistry 32 1993 3306-3312
100. Naylor M.A. Swann E. Everett J. et al. Indolequinone antitumor agents: reductive activation and elimination from (5-methoxy-1-methyl-4,7-dioxoindol-3-yl)methyl derivatives and hypoxia-selective cytotoxicity in vitro J. Med. Chem. 41 1998 2720-2731
101. Xing C. Skibo E.B. Sigmatropic reactions of the aziridinyl semiquinone species. Why aziridinyl benzoquinones are metabolically more stable than aziridinyl indoloquinones Biochemistry 39 2000 10770-10780
102. Loadman P.M. Phillips R.M. Lim L.E. Bibby M.C. Pharmaocological properties of a new aziridinylbenzoquinone, RH1 (2,5-diaziridinyl-3-(hydroxyl)-6-methyl-1,4-benzoquinone) in mice Biochem. Pharmacol. 59 2000 831-837
103. Winski S.L. Hargreaves R.H. Butler J. Ross D. A new screening system for NAD(P)H:quinone oxidoreductase (NQO1)-directed antitumour quinones: identification of a new aziridinylbenzoquinone, RH1, as a NQO1-directed antitumour agent Clin. Cancer Res. 4 1998 3083-3088
104. Sausville E. NCI developmental therapeutics program (personal communication)
105. Hollander P.M. Ernster L. Studies on the reaction mechanism of DT diaphorase. Action of dead-end inhibitors and effects of phospholipids Arch. Biochem. Biophys. 169 1975 560-567
106. Chen S. Wu K. Zhang D. Sherman M. Knox R. Yang C.S. Molecular characterisation of binding of substrates and inhibitors to DT-diaphorase: combined approach involving site-directed mutagenesis, inhibitor-binding analysis and computer modelling Mol. Pharmacol. 56 1999 272-278
107. Winski S.L. Faig M. Bianchet M.A. et al. Characterization of a mechanism-based ingibitor of NAD(P)H:quinone oxidoreductase 1 by biochemical, X-ray crystallographic and mass spectrometric approaches Biochemistry 40 2001 15135-15142
108. Begleiter A. Leith M.K. Curphey T.J. Induction of DT-diaphorase by 1,2-dithiole-3-thione and increase of anticancer activity of bioreductive agents Br. J. Cancer 27 1996 S9-S14
109. Twerdok L.E. Rembish S.J. Trush M.A. Induction of quinone reductase and glutathione in bone marrow cells by 1,2-dithiole-3-thione: effect on hydroquinone-induced cytotoxicity Toxicol. Appl. Pharmacol. 112 1992 273-281
110. Li Y. Lafuente A. Trush M.A. Characterisation of quinone oxidoreductase, glutathione and glutathione S-transferase in human myeloid cell lines: induction by 1,2-dithiole-3-thione and effects on hydroquinone-induced cytotoxicity Life Sci. 54 1994 901-916
111. Doherty G.P. Leith M.K. Wang X. Curphey T.J. Begleiter A. Induction of DT-diaphorase by 1,2-dithiole-3-thiones in human tumour and normal cells and effect on anti-tumour activity of bioreductive agents Br. J. Cancer 77 1998 1241-1252
112. Begleiter A. Leith M.K. Doherty G.P. Digby T.J. Pan S. Factors influencing the induction of DT-diaphorase activity by 1,2-dithiole-3-thione in human tumour cell lines Biochem. Pharmacol. 61 2001 955-964
113. Wang X. Doherty G.P. Leith M.K. Curphey T.J. Begleiter A. Enhanced cytotoxicity of mitomycin C in human tumour cells with inducers of DT-diaphorase Br. J. Cancer 80 1999 1223-1230
114. Carr B.A. Franklin M.R. Induction of drug metabolising enzymes by 1,7-phenanthroline and oltipraz in mice is unrelated to Ah-responsiveness J. Biochem. Toxicol. 13 1999 77-82
115. Kensler T.W. Egner P.A. Dolan P.M. Groopman J.D. Roebuck B.D. Mechanism of protection against aflatoxin tumourigenecity in rats fed 5-(2-pyrazinyl)-4-methyl-1,2-dithiol-3-thione (oltipraz) and related 1,2-dithiol-3-thiones and 1,2-dithiol-3-ones Cancer Res. 47 1987 4271-4277
116. O'Dwyer P.J. Clayton M. Halbherr T. Myers C.B. Yao K. Cellular kinetics of induction by oltipraz and its keto derivative of detoxification enzymes in human colon adenocarcinoma cells Clin. Cancer Res. 3 1997 783-791
117. Jiang Z.-.Q. Chen C. Yang B. Habbar V. Kong A.-.N.T. Differential responses from seven mammalian cell lines to the treatments of detoxifying enzyme inducers Life Sci. 72 2003 2243-2253
118. Gordon G.B. Prochaska H.J. Yang L.Y.-S. Induction of NAD(P)H:quinone reductase in human peripheral blood lymphocytes Carcinogenesis 12 1991 2393-2396
119. Zhang Y. Talalay P. Cho C.G. Posner G.H. A major inducer of anticarcinogenic protective enzymes from broccoli: isolation and elucidation of structure PNAS 89 1992 2399-2403
120. Flescher E. Snyder C.A. Aspirin-like drugs can protect human T lymphocytes against benzoquinone cytotoxicity Arch. Toxicol. 69 1995 684-689
121. Hou D.-.X. Fukuda M. Johnson J.A. Miyamori K. Ushikai M. Fujii M. Fisetin induces transcription of NADPH:quinone oxidoreductase gene through an antioxidant responsive element-involved activation Int. J. Oncol. 18 2001 1175-1179
122. Heo Y.H. Kim S. Park J.E. Jeong L.S. Lee S.K. Induction of quinone reductase activity by stilbene analogs in mouse Hepa 1c1c7 cells Arch. Pharm. Res. 24 2001 597-600
123. Valerio Jr L.G. Kepa J.K. Peckwell G.V. Quattrochi L.C. Induction of human NAD(P)H:quinone oxidoreductase (NQO1) gene expression by the flavenol quercetin Toxicol. Lett. 119 2001 49-57
124. McMahon M. Itoh K. Yamamoto M. et al. The Cap'n'Collar basic leucine zipper transcription factor Nrf2 (NF-E2 p45-related factor2) controls both constitutive and inducible expression of intestinal detoxification and glutathione biosynthetic enzymes Cancer Res. 61 2001 3299-3307
125. Begleiter A. Leith M.K. Induction of DT-diaphorase by doxorubicin and combination therapy with mitomycin C in vitro Biochem. Pharmacol. 50 1995 1281-1286
126. Gonzalez S. Labombarda F. Deniselle M.C.G. Saravia F.E. Roig P. De Nicola A.F. Glucocorticoid effects on fos immunoreactivity and NADPH-diaphorase histochemical staining following spinal cord injury Brain Res. 912 2001 144-153
127. Yao K.S. Clayton M. O'Dwyer P.J. Interaction of heat and hypoxia in modulating transcription of DT diaphorase in human colon adenocarcinoma cells Cell Growth Differ. 5 1994 125-131
128. Alvarez S. Boveria A. Induction of antioxidant enzymes and DT-diaphorase in human blood mononuclear cells by light stress Arch. Biochem. Biophy. 305 1993 247-251
129. Kolesar J. Miller J. Duan W. et al. T1 induction in PBMC by mitomycin C predicts response to irinotecan Proc. ASCO 22 2002 456a
130. Begleiter A. Leith M.K. Curphey T.J. Doherty G.P. Induction of DT-diaphorase in cancer chemoprevention and chemotherapy Oncol. Res. 9 1997 371-382
131. Kepa J.K. Ross D. DT-diaphorase activity in NSCLC and SCLC cell lines: a role for fos/jun regulation Br. J. Cancer 79 1999 1679-1684
132. Yu R. Lei W. Mandlekar S. et al. Role of a mitogen-activated protein kinase pathway in the induction of phase II detoxifying enzymes by chemicals J. Biol. Chem. 274 1999 27545-27552
133. Watternberg L.W. Bueding E. Inhibitory effects of 5-(2-pyrazinyl)-4-methyl-1,2-dithiol-3-thione (Oltipraz) on carcinogenesis induced by benzo[a]pyrene, diethylnitrosamine and uracil mustard Carcinogenesis 7 1986 1379-1381
134. Egner P.A. Kensler T.W. Prestera T. et al. Regulation of phase 2 enzyme induction by oltipraz and other dithiolethiones Carcinogenesis 15 1994 177-181
135. Szarka C.E. Yao K.S. Pfeiffer G.R. et al. Chronic dosing of oltipraz in people at increased risk for colorectal cancer Cancer Detect Prev. 25 2001 352-361
136. Morrow C.S. Cowan K.H. Mechanisms and clinical significance of multidrug resistance Oncology 2 1988 55-63
137. Mikami K. Naito M. Tomida A. Yamada M. Sirakusa T. Tsuruo T. DT-diaphorase as a critical determinant of sensitivity to mitomycin C in human colon and gastric carcinoma cell lines Cancer Res. 56 1996 2823-2826
138. Sagara N. Katoh M. Mitomycin C resistance is induced by TCF-3 overexpression in gastric cancer cell line MKN28 is associated with DT-diaphorase down-regulation Cancer Res. 60 2000 5959-5962
139. Lambert P.A. Kang Y. Greaves B. Perry R.R. The importance of DT-diaphorase in mitomycin C resistance in human colon cancer cell lines J. Surg. Res. 80 1998 177-181
140. Singh S.V. Scalamogna D. Xia H. et al. Biochemical characterisation of a mitomycin C resistant human bladder cancer cell line Int. J. Cancer 65 1996 852-857
141. Baumann P. Hodnick W.F. Scow H.A. et al. Reversal of mitomycin C resistance by overexpression of bioreductive enzymes in Chinese hamster ovary cells Cancer Res. 61 2001 7770-7776
142. O'Dwyer P.J. Perez R.P. Yao K.S. Godwin A.K. Hamilton T.C. Increased DT-diaphorase expression and cross-resistance to mtomycin C in a series of cisplatin-resistant human ovarian cancer cell lines Biochem. Pharmacol. 52 1996 21-27
143. Wakusawa S. Nalamura S. Miyamoto K. Establishment by adriamycin exposure of multidrug-resistant rat ascites hepatoma AH130 cells showing low DT-diaphorase activity and high cross resistance to mitomycins Jpn. J. Cancer Res. 88 1997 88-96
144. Ward T.H. Haran M.S. Whittaker D. Watson A.J. Howard T.D. Butler J. Cross-resistance studies on two K562 sublines resistant to diaziridinylbenzoquinones Biochem. Pharmacol. 50 1995 459-464
145. Danson S. Ranson M. Denneny O. Jones N. Ward T.H. Drug resistance studies on two paired cell lines resistant to the diaziridinylbenzoquinone, RH1. British Oncological Association Annual Meeting, 2003