Modulating endogenous NQO1 levels identifies key regulatory mechanisms of action of β-lapachone for pancreatic cancer therapy

Clinical Cancer Research

Volumn 17, Issue 2, 2011, Pages 275-285

  Li, Long Shan ^a,b   Bey, Erik A ^a,b   Dong, Ying ^a,b   Meng, Jieru ^a,b   Patra, Biswanath ^a,b   Yan, Jingsheng ^a   Xie, Xian Jin ^a   Brekken, Rolf A ^a   Barnett, Carlton C ^a   Bornmann, William G ^c   Gao, Jinming ^a   Boothman, David A ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BETA LAPACHONE; DEXTRAN DERIVATIVE; HYDROXYPROPYL BETA CYCLODEXTRAN; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; DRUG EFFICACY; DRUG MECHANISM; FEMALE; HUMAN; HUMAN CELL; METASTASIS; MOUSE; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; SINGLE STRANDED DNA BREAK;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL DEATH; CELL LINE, TUMOR; DNA DAMAGE; DRUG EVALUATION, PRECLINICAL; GENE KNOCKDOWN TECHNIQUES; HUMANS; MICE; MICE, NUDE; NAD(P)H DEHYDROGENASE (QUINONE); NAPHTHOQUINONES; PANCREATIC NEOPLASMS; REACTIVE OXYGEN SPECIES;

EID: 79251521028     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-10-1983     Document Type: Article

References (49)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J Clin 2009;59:225-49.
2. Chua YJ, Zalcberg JR. Pancreatic cancer-is the wall crumbling?Ann Oncol 2008;19:1224-30.
3. Pliarchopoulou K, Pectasides D. Pancreatic cancer: current and future treatment strategies. Cancer Treat Rev 2009;35:431-6.
4. Wong HH, Lemoine NR. Pancreatic cancer: molecular pathogenesis and new therapeutic targets. Nat Rev Gastroenterol Hepatol 2009;6:412-22.
5. 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 U S A 2003;100:2674-8.
6. Belinsky M, Jaiswal AK. NAD(P)H:quinone oxidoreductase1 (DT-diaphorase) expression in normal and tumor tissues. Cancer Metastasis Rev 1993;12:103-17.
7. Siegel D, Ross D. Immunodetection of NAD(P)H: quinone oxidoreductase 1 (NQO1) in human tissues. Free Radic Biol Med 2000;29:246-53.
8. Lyn-Cook BD, Yan-Sanders Y, Moore S, Taylor S, Word B, Hammons GJ. Increased levels of NAD(P)H: quinone oxidoreductase 1 (NQO1) in pancreatic tissues from smokers and pancreatic adenocarcinomas: A potential biomarker of early damage in the pancreas. Cell Biol Toxicol 2006;22:73-80.
9. Lewis AM, Ough M, Hinkhouse MM, Tsao MS, Oberley LW, Cullen JJ. Targeting NAD(P)H:quinone oxidoreductase (NQO1) in pancreatic cancer. Mol Carcinog 2005;43:215-24.
10. Logsdon CD, Simeone DM, Binkley C, Arumugam T, Greenson JK, Giordano TJ, et al. Molecular profiling of pancreatic adenocarcinoma and chronic pancreatitis identifies multiple genes differentially regulated in pancreatic cancer. Cancer Res 2003;63:2649-57.
11. Awadallah NS, Dehn D, Shah RJ, Russell Nash S, Chen YK, Ross D, et al. NQO1 expression in pancreatic cancer and its potential use as a biomarker. Appl Immunohistochem Mol Morphol 2008;16:24-31.
12. Ross D, Siegel D. NAD(P)H: quinone oxidoreductase 1 (NQO1, DT-diaphorase), functions and pharmacogenetics. Methods Enzymol 2004;382:115-44.
13. Radjendirane V, Joseph P, Lee YH, Kimura S, Klein-Szanto AJ, Gonzalez FJ, et al. Disruption of the DT diaphorase (NQO1) gene in mice leads to increased menadione toxicity. J Biol Chem 1998; 273:7382-9.
14. Ross D, Kepa JK, Winski SL, Beall HD, Anwar A, Siegel D. NAD(P)H: quinone oxidoreductase 1 (NQO1): chemoprotection, bioactivation, gene regulation and genetic polymorphisms. Chem Biol Interact 2000;129:77-97.
15. Lown JW, Begleiter A, Johnson D, Morgan AR. Studies related to antitumor antibiotics. Part V. Reactions of mitomycin C with DNA examined by ethidium fluorescence assay. Can J Biochem 1976;54:110-9.
16. Moynahan ME, Cui TY, Jasin M. Homology-directed DNA repair, mitomycin-C resistance, and chromosome stability is restored with correction of a Brca1 mutation. Cancer Res 2001;61:4842-50. (Pubitemid 32691900)
17. Cheung RY, Rauth AM, Yu Wu X. In vivo efficacy and toxicity of intratumorally delivered mitomycin C and its combination with doxorubicin using microsphere formulations. Anticancer Drugs 2005;16:423-33.
18. Pink JJ, Planchon SM, Tagliarino C, Varnes ME, Siegel D, Boothman DA. NAD(P)H:quinone oxidoreductase activity is the principal determinant of beta-lapachone cytotoxicity. J Biol Chem 2000;275:5416-24.
19. 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;281:33684-96.
20. Tagliarino C, Pink JJ, Dubyak GR, Nieminen AL, Boothman DA. Calcium is a key signaling molecule in beta-lapachone-mediated cell death. J Biol Chem 2001;276:19150-9.
21. Bey EA, Bentle MS, Reinicke KE, Dong Y, Yang CR, Girard L, et al. An NQO1- and PARP-1-mediated cell death pathway induced in non-small- cell lung cancer cells by beta-lapachone. Proc Natl Acad Sci U S A 2007;104:11832-7.
22. Pink JJ, Wuerzberger-Davis S, Tagliarino C, Planchon SM, Yang X, Froelich CJ, et al. Activation of a cysteine protease in MCF-7 and T47D breast cancer cells during beta-lapachone-mediated apoptosis. Exp Cell Res 2000;255:144-55.
23. Savage RE, Tyler AN, Miao XS, Chan TC. Identification of a novel glucosylsulfate conjugate as a metabolite of 3,4-dihydro-2,2- dimethyl-2H-naphtho[1,2-b]pyran-5,6-dione (ARQ 501, beta-lapachone) in mammals. Drug Metab Dispos 2008;36:753-8.
24. Cullen JJ, Hinkhouse MM, Grady M, Gaut AW, Liu J, Zhang YP, et al. Dicumarol inhibition of NADPH: quinone oxidoreductase induces growth inhibition of pancreatic cancer via a superoxide-mediated mechanism. Cancer Res 2003;63:5513-20. (Pubitemid 37139871)
25. Ough M, Lewis A, Bey EA, Gao J, Ritchie JM, Bornmann W, et al. Efficacy of beta-lapachone in pancreatic cancer treatment: exploiting the novel, therapeutic target NQO1. Cancer Biol Ther 2005;4:95-102. (Pubitemid 41350938)
26. Planchon SM, Pink JJ, Tagliarino C, Bornmann WG, Varnes ME, Boothman DA. Beta-lapachone-induced apoptosis in human prostate cancer cells: involvement of NQO1/xip3.Exp Cell Res 2001;267:95-106.
27. Nasongkla N, Wiedmann AF, Bruening A, Beman M, Ray D, Bornmann WG, et al. Enhancement of solubility and bioavailability of beta-lapachone using cyclodextrin inclusion complexes. Pharm Res 2003; 20:1626-33. (Pubitemid 37268279)
28. Li LS, Morales JC, Hwang A, Wagner MW, Boothman DA. DNA mismatch repair-dependent activation of c-Abl/p73alpha/GADD45alpha- mediated apoptosis.J Biol Chem 2008;283:21394-403.
29. Blanco E, Bey EA, Khemtong C, Yang SG, Setti-Guthi J, Chen H, et al. Beta-lapachone micellar nanotherapeutics for non-small cell lung cancer therapy. Cancer Res 2010;70:3896-904.
30. Fitzsimmons SA, Workman P, Grever M, Paull K, Camalier R, Lewis AD. 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;88:259-69.
31. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265-75.
32. Lee YJ, Galoforo SS, Berns CM, Chen JC, Davis BH, Sim JE, et al. Glucose deprivation-induced cytotoxicity and alterations in mitogen-activated protein kinase activation are mediated by oxidative stress in multidrug-resistant human breast carcinoma cells. J Biol Chem 1998;273:5294-9.
33. Sawada F, Inoguchi T, Tsubouchi H, Sasaki S, Fujii M, Maeda Y, et al. Differential effect of sulfonylureas on production of reactive oxygen species and apoptosis in cultured pancreatic beta-cell line, MIN6. Metabolism 2008;57:1038-45.
34. Wagner MW, Li LS, Morales JC, Galindo CL, Garner HR, Bornmann WG, et al. Role of c-Abl kinase in DNA mismatch repair-dependent G2 cell cycle checkpoint arrest responses. J Biol Chem 2008;283:21382-93.
35. Bey EA, Wuerzberger-Davis SM, Pink JJ, Yang CR, Araki S, Reinicke KE, et al. Mornings with Art, lessons learned: feedback regulation, restriction threshold biology, and redundancy govern molecular stress responses. J Cell Physiol 2006;209:604-10.
36. Jimenez RE, Hartwig W, Antoniu BA, Compton CC, Warshaw AL, Fernandez-Del Castillo C. Effect of matrix metalloproteinase inhibition on pancreatic cancer invasion and metastasis: an additive strategy for cancer control. Ann Surg 2000;231:644-54. (Pubitemid 30249825)
37. Tagliarino C, Pink JJ, Reinicke KE, Simmers SM, Wuerzberger-Davis SM, Boothman DA. Mu-calpain activation in beta-lapachone-mediated apoptosis. Cancer Biol Ther 2003;2:141-52.
38. Reinicke KE, Bey EA, Bentle MS, Pink JJ, Ingalls ST, Hoppel CL, et al. Development of beta-lapachone prodrugs for therapy against human cancer cells with elevated NAD(P)H:quinone oxidoreductase 1 levels. Clin Cancer Res 2005;11:3055-64.
39. Zhang J, Chatterjee K, Alano CC, Kalinowski MA, Honbo N, Karliner JS. Vincristine attenuates N-methyl-N′-nitro-N-nitrosoguanidine-induced poly-(ADP) ribose polymerase activity in cardiomyocytes. J Cardiovasc Pharmacol 2010;55:219-26.
40. Fagerholm R, Hofstetter B, Tommiska J, Aaltonen K, Vrtel R, Syrjakoski K, et al. NAD(P)H: quinone oxidoreductase 1 NQO1*2 genotype (P187S) is a strong prognostic and predictive factor in breast cancer. Nat Genet 2008;40:844-53.
41. Burris HA III, Moore MJ, Andersen J, Green MR, Rothenberg ML, Modiano MR, et al. Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J Clin Oncol 1997;15:2403-13.
42. Mini E, Nobili S, Caciagli B, Landini I, Mazzei T. Cellular pharmacology of gemcitabine. Ann Oncol 2006;17(Suppl 5):v7-12.
43. Ewald B, Sampath D, Plunkett W. H2AX phosphorylation marks gemcitabine-induced stalled replication forks and their collapse upon S-phase checkpoint abrogation. Mol Cancer Ther 2007;6:1239-48.
44. Doyle TH, Mornex F, McKenna WG. The clinical implications of gemcitabine radiosensitization. Clin Cancer Res 2001;7:226-8.
45. Shewach DS, Hahn TM, Chang E, Hertel LW, Lawrence TS. Metabolism of 2′,2′-difluoro-2′-deoxycytidine and radiation sensitization of human colon carcinoma cells. Cancer Res 1994;54:3218-23. (Pubitemid 24208931)
46. Boothman DA, Pardee AB. Inhibition of radiation-induced neoplastic transformation by beta-lapachone. Proc Natl Acad Sci USA 1989; 86:4963-7.
47. Boothman DA, Trask DK, Pardee AB. Inhibition of potentially lethal DNA damage repair in human tumor cells by beta-lapachone, an activator of topoisomerase I. Cancer Res 1989;49:605-12.
48. Dong Y, Bey EA, Li LS, Kabbani W, Yan J, Xie XJ, et al. Prostate cancer radiosensitization through poly(ADP-Ribose) polymerase-1 hyperactivation. Cancer Res 2010;70:8088-96.
49. Dong Y, Chin SF, Blanco E, Bey EA, Kabbani W, Xie XJ, et al. Intratumoral delivery of beta-lapachone via polymer implants for prostate cancer therapy. Clin Cancer Res 2009;15:131-9.