765
Views
22
CrossRef citations to date
0
Altmetric
Review Article

Nanotechnology-enabled delivery of NQO1 bioactivatable drugs

, , , , &
Pages 672-680 | Received 22 May 2015, Accepted 13 Jul 2015, Published online: 09 Oct 2015

References

  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin 2015;65:5–29
  • Blanco E, Bey EA, Dong Y, et al. β-Lapachone-containing PEG–PLA polymer micelles as novel nanotherapeutics against NQO1-overexpressing tumor cells. J Control Release 2007;122:365–74
  • Blanco E, Bey EA, Khemtong C, et al. β-Lapachone micellar nanotherapeutics for non-small cell lung cancer therapy. Cancer Res 2010;70:3896–904
  • Blanco E, Kessinger CW, Sumer BD, Gao J. Multifunctional micellar nanomedicine for cancer therapy. Exp Biol Med (Maywood) 2009;234:123–31
  • Allen TM, Cullis PR. Liposomal drug delivery systems: from concept to clinical applications. Adv Drug Deliv Rev 2013;65:36–48
  • Kesharwani P, Jain K, Jain NK. Dendrimer as nanocarrier for drug delivery. Prog Polym Sci 2014;39:268–307
  • Hrkach J, Von Hoff D, Mukkaram Ali M, et al. Preclinical development and clinical translation of a PSMA-targeted docetaxel nanoparticle with a differentiated pharmacological profile. Sci Transl Med 2012;4:128ra39
  • Sutton D, Nasongkla N, Blanco E, Gao J. Functionalized micellar systems for cancer targeted drug delivery. Pharm Res 2007;24:1029–46
  • Gref R, Minamitake Y, Peracchia MT, et al. Biodegradable long-circulating polymeric nanospheres. Science 1994;263:1600–3
  • Torchilin VP. Structure and design of polymeric surfactant-based drug delivery systems. J Control Release 2001;73:137–72
  • Hashizume H, Baluk P, Morikawa S, et al. Openings between defective endothelial cells explain tumor vessel leakiness. Am J Pathol 2000;156:1363–80
  • Maeda H. The enhanced permeability and retention (EPR) effect in tumor vasculature: the key role of tumor-selective macromolecular drug targeting. Adv Enzyme Regul 2001;41:189–207
  • Ross D, Kepa JK, Winski SL, et al. NAD(P)H:quinone oxidoreductase 1 (NQO1): chemoprotection, bioactivation, gene regulation and genetic polymorphisms. Chem Biol Interact 2000;129:77–97
  • Cadenas E. Antioxidant and prooxidant functions of DT-diaphorase in quinone metabolism. Biochem Pharmacol 1995;49:127–40
  • Chou TC, Talalay P. Simple generalized equation for analysis of multiple inhibitions of Michaelis–Menten kinetic systems. J Biol Chem 1977;252:6438–42
  • Preusch PC, Siegel D, Gibson NW, Ross D. A note on the inhibition of DT-diaphorase by dicoumarol. Free Radic Biol Med 1991;11:77–80
  • Faig M, Bianchet MA, Winski S, et al. Structure-based development of anticancer drugs: complexes of NAD(P)H:quinone oxidoreductase 1 with chemotherapeutic quinones. Structure 2001;9:659–67
  • Nolan KA, Timson DJ, Stratford IJ, Bryce RA. In silico identification and biochemical characterization of novel inhibitors of NQO1. Bioorg Med Chem Lett 2006;16:6246–54
  • Belinsky M, Jaiswal AK. NAD(P)H:quinone oxidoreductase1 (DT-diaphorase) expression in normal and tumor tissues. Cancer Metastasis Rev 1993;12:103–17
  • Srivastava M, Khurana P, Sugadev R. Lung cancer signature biomarkers: tissue specific semantic similarity based clustering of digital differential display (DDD) data. BMC Res Notes 2012;5:617
  • Awadallah NS, Dehn D, Shah RJ, et al. NQO1 expression in pancreatic cancer and its potential use as a biomarker. Appl Immunohistochem Mol Morphol 2008;16:24–31
  • Siegel D, Franklin WA, Ross D. Immunohistochemical detection of NAD(P)H:quinone oxidoreductase in human lung and lung tumors. Clin Cancer Res 1998;4:2065–70
  • Schlager JJ, Powis G. Cytosolic NAD(P)H:(quinone-acceptor)oxidoreductase in human normal and tumor tissue: effects of cigarette smoking and alcohol. Int J Cancer 1990;45:403–9
  • Lewis AM, Ough M, Hinkhouse MM, et al. Targeting NAD(P)H:quinone oxidoreductase (NQO1) in pancreatic cancer. Mol Carcinog 2005;43:215–24
  • DeNicola GM, Karreth FA, Humpton TJ, et al. Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 2011;475:106–9
  • Singh A, Misra V, Thimmulappa RK, et al. Dysfunctional KEAP1-NRF2 interaction in non-small-cell lung cancer. PLoS Med 2006;3:e420
  • Cruz FS, Docampo R, Boveris A. Generation of superoxide anions and hydrogen peroxide from beta-lapachone in bacteria. Antimicrob Agents Chemother 1978;14:630–3
  • Boveris A, Docampo R, Turrens JF, Stoppani AO. Effect of beta-lapachone on superoxide anion and hydrogen peroxide production in Trypanosoma cruzi. Biochem J 1978;175:431–9
  • 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
  • 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;275:5416–24
  • Planchon SM, Pink JJ, Tagliarino C, et al. Beta-lapachone-induced apoptosis in human prostate cancer cells: involvement of NQO1/xip3. Exp Cell Res 2001;267:95–106
  • Li LS, Bey EA, Dong Y, et al. Modulating endogenous NQO1 levels identifies key regulatory mechanisms of action of beta-lapachone for pancreatic cancer therapy. Clin Cancer Res 2011;17:275–85
  • Docampo R, Cruz FS, Boveris A, et al. Beta-lapachone enhancement of lipid peroxidation and superoxide anion and hydrogen peroxide formation by sarcoma 180 ascites tumor cells. Biochem Pharmacol 1979;28:723–8
  • Imlay JA, Chin SM, Linn S. Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 1988;240:640–2
  • Bentle MS, Reinicke KE, Dong Y, et al. Nonhomologous end joining is essential for cellular resistance to the novel antitumor agent, beta-lapachone. Cancer Res 2007;67:6936–45
  • Haince JF, McDonald D, Rodrigue A, et al. PARP1-dependent kinetics of recruitment of MRE11 and NBS1 proteins to multiple DNA damage sites. J Biol Chem 2008;283:1197–208
  • Beck C, Robert I, Reina-San-Martin B, et al. Poly(ADP-ribose) polymerases in double-strand break repair: focus on PARP1, PARP2 and PARP3. Exp Cell Res 2014;329:18–25
  • Bey EA, Bentle MS, Reinicke KE, 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 USA 2007;104:11832–7
  • Tagliarino C, Pink JJ, Dubyak GR, et al. Calcium is a key signaling molecule in beta-lapachone-mediated cell death. J Biol Chem 2001;276:19150–9
  • Pink JJ, Wuerzberger-Davis S, Tagliarino C, 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
  • Tagliarino C, Pink JJ, Reinicke KE, et al. Mu-calpain activation in beta-lapachone-mediated apoptosis. Cancer Biol Ther 2003;2:141–52
  • Bey EA, Reinicke KE, Srougi MC, et al. Catalase abrogates beta-lapachone-induced PARP1 hyperactivation-directed programmed necrosis in NQO1-positive breast cancers. Mol Cancer Ther 2013;12:2110–20
  • Park EJ, Min KJ, Lee TJ, et al. Beta-lapachone induces programmed necrosis through the RIP1-PARP-AIF-dependent pathway in human hepatocellular carcinoma SK-Hep1 cells. Cell Death Dis 2014;5:e1230
  • Bentle MS, Reinicke KE, Bey EA, et al. Calcium-dependent modulation of poly(ADP-ribose) polymerase-1 alters cellular metabolism and DNA repair. J Biol Chem 2006;281:33684–96
  • Huang X, Dong Y, Bey EA, et al. An NQO1 substrate with potent antitumor activity that selectively kills by PARP1-induced programmed necrosis. Cancer Res 2012;72:3038–47
  • van Wijk SJ, Hageman GJ. Poly(ADP-ribose) polymerase-1 mediated caspase-independent cell death after ischemia/reperfusion. Free Radic Biol Med 2005;39:81–90
  • Ying W, Sevigny MB, Chen Y, Swanson RA. Poly(ADP-ribose) glycohydrolase mediates oxidative and excitotoxic neuronal death. Proc Natl Acad Sci USA 2001;98:12227–32
  • Woo HJ, Choi YH. Growth inhibition of A549 human lung carcinoma cells by beta-lapachone through induction of apoptosis and inhibition of telomerase activity. Int J Oncol 2005;26:1017–23
  • Park MT, Song MJ, Lee H, et al. Beta-lapachone significantly increases the effect of ionizing radiation to cause mitochondrial apoptosis via JNK activation in cancer cells. PLoS One 2011;6:e25976
  • Szejtli J. Introduction and general overview of cyclodextrin chemistry. Chem Rev 1998;98:1743–54
  • Davis ME, Brewster ME. Cyclodextrin-based pharmaceutics: past, present and future. Nat Rev Drug Discov 2004;3:1023–35
  • Nasongkla N, Wiedmann A, Bruening A, et al. Enhancement of solubility and bioavailability of β-lapachone using cyclodextrin inclusion complexes. Pharm Res 2003;20:1626–33
  • Hartner PL Rosen L, Hensley M, et al. Phase 2 dose multi-center, open-label study of ARQ 501, a checkpoint activator, in adult patients with persistent, recurrent or metastatic leiomyosarcoma (LMS). J Clin Oncol 2007;25:20521
  • Torchilin VP, Lukyanov AN, Gao Z, Papahadjopoulos-Sternberg B. Immunomicelles: targeted pharmaceutical carriers for poorly soluble drugs. Proc Natl Acad Sci USA 2003;100:6039–44
  • Jones M-C, Leroux J-C. Polymeric micelles – a new generation of colloidal drug carriers. Eur J Pharm Biopharm 1999;48:101–11
  • Savić R, Luo L, Eisenberg A, Maysinger D. Micellar nanocontainers distribute to defined cytoplasmic organelles. Science 2003;300:615–18
  • Reinicke KE, Bey EA, Bentle MS, 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
  • Ma X, Huang X, Huang G, et al. Prodrug strategy to achieve lyophilizable, high drug loading micelle formulations through diester derivatives of β-lapachone. Adv Healthcare Mater 2014;3:1210–16
  • Rautio J, Kumpulainen H, Heimbach T, et al. Prodrugs: design and clinical applications. Nat Rev Drug Discov 2008;7:255–70
  • Perez C, Daniel KB, Cohen SM. Evaluating prodrug strategies for esterase-triggered release of alcohols. ChemMedChem 2013;8:1662–7
  • Hooker SC. The constitution of lapachol and its derivatives. Part IV.1 Oxidation with potassium permanganate2,3. J Am Chem Soc 1936;58:1168–73
  • Xu G, Zhang W, Ma MK, McLeod HL. Human Carboxylesterase 2 is commonly expressed in tumor tissue and is correlated with activation of irinotecan. Clin Cancer Res 2002;8:2605–11
  • Lu X, Howard MD, Talbert DR, et al. Nanoparticles containing anti-inflammatory agents as chemotherapy adjuvants II: role of plasma esterases in drug release. AAPS J 2009;11:120–2
  • Ma X, Huang X, Moore Z, et al. Esterase-activatable β-lapachone prodrug micelles for NQO1-targeted lung cancer therapy. J Control Release 2015;200:201–11
  • Dong Y, Bey EA, Li L-S, et al. Prostate cancer radiosensitization through poly(ADP-ribose) polymerase-1 hyperactivation. Cancer Res 2010;70:8088–96
  • Cenas N, Ollinger K. Redox conversions of methemoglobin during redox cycling of quinones and aromatic nitrocompounds. Arch Biochem Biophys 1994;315:170–6
  • 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;61:212–19
  • Reddy S, Li L, Boothman DA, et al. NQO1-mediated synergistic lethality in combination with β-lapachone (β-lap) and ionizing radiation (IR) in head-and-neck cancer (HNC). Int J Radiat Oncol Biol Phys 2013;87:S139
  • D'Anneo A, Augello G, Santulli A, et al. Paclitaxel and beta-lapachone synergistically induce apoptosis in human retinoblastoma Y79 cells by downregulating the levels of phospho-Akt. J Cell Physiol 2010;222:433–43
  • Terai K, Dong GZ, Oh ET, et al. Cisplatin enhances the anticancer effect of beta-lapachone by upregulating NQO1. Anticancer Drugs 2009;20:901–9

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.