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Review Article

Drug metabolizing enzymes-associated chemo resistance and strategies to overcome it

, , , &
Pages 196-223 | Received 13 Feb 2019, Accepted 10 Jun 2019, Published online: 01 Jul 2019

References

  • mHurley TD, Matei D. 2015. Compositions of aldh1a1 inhibitors and methods of use in treating cancer. Google Patents.
  • Adegoke OJ, Shu XO, Gao Y-T, Cai Q, Breyer J, Smith J, Zheng W. 2004. Genetic polymorphisms in uridine diphospho-glucuronosyltransferase 1A1 (UGT1A1) and risk of breast cancer. Breast Cancer Res Treat. 85:239–245.
  • Aksoy M, Küfrevioglu I. 2018. Inhibition of human erythrocyte glutathione S-transferase by some flavonoid derivatives. Toxin Rev. 37:251–257.
  • Álvarez P, Marchal JA, Boulaiz H, Carrillo E, Vélez C, Rodríguez-Serrano F, Melguizo C, Prados J, Madeddu R, Aranega A. 2012. 5-Fluorouracil derivatives: a patent review. Expert Opin Ther Pat. 22:107–123.
  • Andersson B, Murray D. 2002. Clinically relevant resistance in cancer chemotherapy. Vol. 112. Berlin (Germany): Springer Science & Business Media.
  • Arafa HM. 2009. Possible contribution of β-glucosidase and caspases in the cytotoxicity of glufosfamide in colon cancer cells. Eur J Pharmacol. 616:58–63.
  • Ashwanikumar N, Kumar NA, Nair SA, Kumar GV. 2012. Methacrylic-based nanogels for the pH-sensitive delivery of 5-fluorouracil in the colon. Int J Nanomed. 7:5769.
  • Baccanari DP, Davis ST, Knick VC, Spector T. 1993. 5-Ethynyluracil (776C85): a potent modulator of the pharmacokinetics and antitumor efficacy of 5-fluorouracil. Proc Natl Acad Sci USA. 90:11064–11068.
  • Blagosklonny MV. 2004. Analysis of FDA approved anticancer drugs reveals the future of cancer therapy. Cell Cycle. 3:1033–1040.
  • Blossey HC, Wander HE, Koebberling J, Nagel GA. 1984. Pharmacokinetic and pharmacodynamic basis for the treatment of metastatic breast cancer with high‐dose medroxyprogesterone acetate. Cancer. 54:1208–1215.
  • Borch RF, Liu J, Schmidt JP, Marakovits JT, Joswig C, Gipp JJ, Mulcahy RT. 2000. Synthesis and evaluation of nitroheterocyclic phosphoramidates as hypoxia-selective alkylating agents. J Med Chem. 43:2258–2265.
  • Borch RF, Valente RR. 1991. Synthesis, activation, and cytotoxicity of aldophosphamide analogs. J Med Chem. 34:3052–3058.
  • Brocker C, Lassen N, Estey T, Pappa A, Cantore M, Orlova VV, Chavakis T, Kavanagh KL, Oppermann U, Vasiliou V. 2010. Aldehyde dehydrogenase 7A1 (ALDH7A1) is a novel enzyme involved in cellular defense against hyperosmotic stress. J Biol Chem. 285:18452–18463.
  • Buchman CD, Hurley TD. 2017. Inhibition of the aldehyde dehydrogenase 1/2 family by psoralen and coumarin derivatives. J Med Chem. 60:2439–2455.
  • Buchman CD, Mahalingan KK, Hurley TD. 2015. Discovery of a series of aromatic lactones as ALDH1/2-directed inhibitors. Chem Biol Interact. 234:38–44.
  • Burg D, Filippov DV, Hermanns R, van der Marel GA, van Boom JH, Mulder GJ. 2002. Peptidomimetic glutathione analogues as novel gammaGT stable GST inhibitors. Bioorg Med Chem. 10:195–205.
  • Calderaro J, Nault J-C, Bioulac-Sage P, Laurent A, Blanc J-F, Decaens T, Zucman-Rossi J. 2014. ALDH3A1 is overexpressed in a subset of hepatocellular carcinoma characterised by activation of the Wnt/ß-catenin pathway. Virchows Arch. 464:53–60.
  • Caudle K, Thorn C, Klein T, Swen J, McLeod H, Diasio RB, Schwab M. 2013. Clinical pharmacogenetics implementation consortium guidelines for dihydropyrimidine dehydrogenase genotype and fluoropyrimidine dosing. Clin Pharmacol Ther. 94:640–645.
  • Chen L, She X, Wang T, He L, Shigdar S, Duan W, Kong L. 2015. Overcoming acquired drug resistance in colorectal cancer cells by targeted delivery of 5-FU with EGF grafted hollow mesoporous silica nanoparticles. Nanoscale. 7:14080–14092.
  • Chen Y, Zhu J-Y, Hong KH, Mikles DC, Georg GI, Goldstein AS, Amory JK, Schönbrunn E. 2018. Structural basis of ALDH1A2 inhibition by irreversible and reversible small molecule inhibitors. ACS Chem Biol. 13:582–590.
  • Chintala L, Vaka S, Baranda J, Williamson SK. 2011. Capecitabine versus 5-fluorouracil in colorectal cancer: where are we now? Oncol Rev. 5:129–140.
  • Cronin KA, Lake AJ, Scott S, Sherman RL, Noone AM, Howlader N, Henley SJ, Anderson RN, Firth AU, Ma J. 2018. Annual report to the nation on the status of cancer, part I: national cancer statistics. Cancer. 124(13):2785–2800.
  • Crooke ST, Prestayko AW. 2013. Antineoplastic agents. Amsterdam (Netherlands): Elsevier.
  • Cui J, Meng Q, Zhang X, Cui Q, Zhou W, Li S. 2015. Design and synthesis of new α-naphthoflavones as cytochrome P450 (CYP) 1B1 inhibitors to overcome docetaxel-resistance associated with CYP1B1 overexpression. J Med Chem. 58:3534–3547.
  • Di L. 2014. The role of drug metabolizing enzymes in clearance. Expert Opin Drug Metab Toxicol. 10:379–393.
  • Diasio RB. 1998. The role of dihydropyrimidine dehydrogenase (DPD) modulation in 5-FU pharmacology. Oncol-Huntington. 12:23–27.
  • Diasio RB, Johnson MR. 1999. Dihydropyrimidine dehydrogenase: its role in 5-fluorouracil clinical toxicity and tumor resistance. Clin Cancer Res. 5:2672–2673.
  • D'Incalci M, Bolis G, Facchinetti T, Mangioni C, Morasca L, Morazzoni P, Salmona M. 1979. Decreased half life of cyclophosphamide in patients under continual treatment. Eur J Cancer. 15:7–10.
  • Dobritzsch D, Schneider G, Schnackerz KD, Lindqvist Y. 2001. Crystal structure of dihydropyrimidine dehydrogenase, a major determinant of the pharmacokinetics of the anti‐cancer drug 5‐fluorouracil. EMBO J. 20:650–660.
  • Dutour R, Cortés-Benítez F, Roy J, Poirier D. 2017. Structure-based design and synthesis of newestrane-pyridine derivatives as cytochrome P450 (CYP) 1B1 inhibitors. ACS Med Chem Lett. 8:1159–1164.
  • Dutour R, Poirier D. 2017. Inhibitors of cytochrome P450 (CYP) 1B1. Eur J Med Chem. 135:296–306.
  • Eaton DL, Bammler TK. 1999. Concise review of the glutathione S-transferases and their significance to toxicology. Toxicol Sci Off J Soc Toxicol. 49:156–164.
  • El-Hammadi MM, Delgado ÁV, Melguizo C, Prados JC, Arias JL. 2017. Folic acid-decorated and PEGylated PLGA nanoparticles for improving the antitumour activity of 5-fluorouracil. Int J Pharma. 516:61–70.
  • Endo M, Miwa M, Eda H, Ura M, Tanimura H, Ishikawa T, Miyazaki-Nose T, Hattori K, Shimma N, Yamada-Okabe H, et al. 2003. Augmentation of the antitumor activity of capecitabine by a tumor selective dihydropyrimidine dehydrogenase inhibitor, RO0094889. Int J Cancer. 106:799–805.
  • Etienne-Grimaldi M-C, Boyer J-C, Beroud C, Mbatchi L, van Kuilenburg A, Bobin-Dubigeon C, Thomas F, Chatelut E, Merlin J-L, Pinguet F, et al. 2017. New advances in DPYD genotype and risk of severe toxicity under capecitabine. PloS One. 12:e0175998.
  • Flader C, Liu J, Borch RF. 2000. Development of novel quinone phosphorodiamidate prodrugs targeted to DT-diaphorase. J Med Chem. 43:3157–3167.
  • Franco M, Man S, Chen L, Emmenegger U, Shaked Y, Cheung AM, Brown AS, Hicklin DJ, Foster FS, Kerbel RS. 2006. Targeted anti-vascular endothelial growth factor receptor-2 therapy leads to short-term and long-term impairment of vascular function and increase in tumor hypoxia. Cancer Res. 66:3639–3648.
  • Fu J, Liu L, Huang Z, Lai Y, Ji H, Peng S, Tian J, Zhang Y. 2013. Hybrid molecule from O2-(2,4-dinitrophenyl)diazeniumdiolate and oleanolic acid: a glutathione S-transferase π-activated nitric oxide prodrug with selective anti-human hepatocellular carcinoma activity and improved stability. J Med Chem. 56:4641–4655.
  • Gaikwad NW, Rogan EG, Cavalieri EL. 2007. Evidence from ESI-MS for NQO1-catalyzed reduction of estrogen ortho-quinones. Free Radic Biol Med. 43:1289–1298.
  • Galluzzi L, Senovilla L, Vitale I, Michels J, Martins I, Kepp O, Castedo M, Kroemer G. 2012. Molecular mechanisms of cisplatin resistance. Oncogene. 31:1869.
  • Gatti L, Zunino F. 2005. Overview of tumor cell chemoresistance mechanisms. Chemosensitivity: Vol. II. Berlin (Germany): Springer; p. 127–148.
  • Gauthier-Landry L, Bélanger A, Barbier O. 2015. Multiple roles for UDP-glucuronosyltransferase (UGT)2B15 and UGT2B17 enzymes in androgen metabolism and prostate cancer evolution. J Steroid Biochem Mol Biol. 145:187–192.
  • Godwin AK, Meister A, O'Dwyer PJ, Huang CS, Hamilton TC, Anderson ME. 1992. High resistance to cisplatin in human ovarian cancer cell lines is associated with marked increase of glutathione synthesis. Proc Natl Acad Sci USA. 89:3070–3074.
  • Gottesman MM, Fojo T, Bates SE. 2002. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer. 2:48.
  • Guengerich FP. 2008. Cytochrome p450 and chemical toxicology. Chem Res Toxicol. 21:70–83.
  • Guillemette C. 2003. Pharmacogenomics of human UDP-glucuronosyltransferase enzymes. Pharmacogenom J. 3:136.
  • Guillemette C, Lévesque É, Rouleau M. 2014. Pharmacogenomics of human uridine diphospho-glucuronosyltransferases and clinical implications . Clin Pharmacol Ther. 96:324–339.
  • Gupta V, Jani JP, Jacobs S, Levitt M, Fields L, Awasthi S, Xu BH, Sreevardhan M, Awasthi YC, Singh SV. 1995. Activity of melphalan in combination with the glutathione transferase inhibitor sulfasalazine. Cancer Chemoth Pharm. 36:13–19.
  • Haas J, Roth S, Arnold K, Kiefer F, Schmidt T, Bordoli L, Schwede T. 2013. The protein model portal—a comprehensive resource for protein structure and model information. Database. 2013:2013.
  • Hattori K, Kohchi Y, Oikawa N, Suda H, Ura M, Ishikawa T, Miwa M, Endoh M, Eda H, Tanimura H, et al. 2003. Design and synthesis of the tumor-activated prodrug of dihydropyrimidine dehydrogenase (DPD) inhibitor, RO0094889 for combination therapy with capecitabine. Bioorg Med Chem Lett. 13:867–872.
  • Hilton J. 1984. Role of aldehyde dehydrogenase in cyclophosphamide-resistant L1210 leukemia. Cancer Res. 44:5156–5160.
  • Holohan C, Van Schaeybroeck S, Longley DB, Johnston PG. 2013. Cancer drug resistance: an evolving paradigm. Nat Rev Cancer. 13:714.
  • Horley NJ, Beresford KJM, Chawla T, McCann GJP, Ruparelia KC, Gatchie L, Sonawane VR, Williams IS, Tan HL, Joshi P, et al. 2017. Discovery and characterization of novel CYP1B1 inhibitors based on heterocyclic chalcones: overcoming cisplatin resistance in CYP1B1-overexpressing lines. Eur J Med Chem. 129:159–174.
  • Huddle BC, Grimley E, Buchman CD, Chtcherbinine M, Debnath B, Mehta P, Yang K, Morgan CA, Li S, Felton J, et al. 2018. Structure-based optimization of a novel class of aldehyde dehydrogenase 1A (ALDH1A) subfamily-selective inhibitors as potential adjuncts to ovarian cancer chemotherapy. J Med Chem. 61:8754–8773.
  • Ishii Y, An K, Nishimura Y, Yamada H. 2012. ATP Serves as an Endogenous Inhibitor of UDP-Glucuronosyltransferase (UGT): a new insight into the'latency'of UGT. Drug Metab Disposit. 40:2081. 112.046862.
  • Jain M, Fan J, Baturay NZ, Kwon C-H. 2004. Sulfonyl-containing aldophosphamide analogues as novel anticancer prodrugs targeted against cyclophosphamide-resistant tumor cell lines. J Med Chem. 47:3843–3852.
  • Jaramillo AC, Al Saig F, Cloos J, Jansen G, Peters GJ. 2018. How to overcome ATP-binding cassette drug efflux transporter-mediated drug resistance. CDR. 1:6–29.
  • Jedinak A, Loughlin KR, Moses MA. 2018. Approaches to the discovery of non-invasive urinary biomarkers of prostate cancer. Oncotarget. 9:32534.
  • Johnstone TC, Suntharalingam K, Lippard SJ. 2016. The next generation of platinum drugs: targeted Pt(II) agents, nanoparticle delivery, and Pt(IV) prodrugs. Chem Rev. 116:3436–3486.
  • Kasherman Y, Sturup S, Gibson D. 2009. Is glutathione the major cellular target of cisplatin? A study of the interactions of cisplatin with cancer cell extracts. J Med Chem. 52:4319–4328.
  • Kastan MB, Schlaffer E, Russo J-E, Colvin OM, Civin CI, Hilton J. 1990. Direct demonstration of elevated aldehyde dehydrogenase in human hematopoietic progenitor cells. Blood. 75:1947–1950.
  • Kazmi F, Yerino P, Barbara JE, Parkinson A. 2015. Further characterization of the metabolism of desloratadine and its cytochrome P450 and UDP-glucuronosyltransferase (UGT) inhibition potential: Identification of desloratadine as a relatively selective UGT2B10 inhibitor. Drug Metabolism and Disposition.dmd. 115.065011.
  • Kelland L. 2007. The resurgence of platinum-based cancer chemotherapy. Nat Rev Cancer. 7:573.
  • Keller MA, Zander U, Fuchs JE, Kreutz C, Watschinger K, Mueller T, Golderer G, Liedl KR, Ralser M, Kräutler B, et al. 2014. A gatekeeper helix determines the substrate specificity of Sjögren-Larsson syndrome enzyme fatty aldehyde dehydrogenase. Nat Commun. 5:4439.
  • Ketterer B. 1998. Glutathione S-transferases and prevention of cellular free radical damage. Free Radic Res. 28:647–658.
  • Khanna M, Chen C-H, Kimble-Hill A, Parajuli B, Perez-Miller S, Baskaran S, Kim J, Dria K, Vasiliou V, Mochly-Rosen D. 2011a. Discovery of a novel class of covalent inhibitor for aldehyde dehydrogenases. J Biol Chem. M111:293597.
  • Khanna M, Chen C-H, Kimble-Hill A, Parajuli B, Perez-Miller S, Baskaran S, Kim J, Dria K, Vasiliou V, Mochly-Rosen D, et al. 2011b. Discovery of a novel class of covalent inhibitor for aldehyde dehydrogenases. J Biol Chem. 286:43486–43494.
  • Kikuchi O, Ohashi S, Nakai Y, Nakagawa S, Matsuoka K, Kobunai T, Takechi T, Amanuma Y, Yoshioka M, Ida T, et al. 2015. Novel 5-fluorouracil-resistant human esophageal squamous cell carcinoma cells with dihydropyrimidine dehydrogenase overexpression. Am J Cancer Res. 5:2431.
  • Kim YG, Lee S, Kwon OS, Park SY, Lee SJ, Park BJ, Kim KJ. 2009. Redox-switch modulation of human SSADH by dynamic catalytic loop . EMBO J. 28:959–968.
  • Kimble-Hill AC, Parajuli B, Chen C-H, Mochly-Rosen D, Hurley TD. 2014. Development of selective inhibitors for aldehyde dehydrogenases based on substituted indole-2,3-diones. J Med Chem. 57:714–722.
  • Kindler HL, Schilsky RL. 2000. Eniluracil: an irreversible inhibitor of dihydropyrimidine dehydrogenase. Expert Opin Investig Drugs. 9:1635–1649.
  • Kirihara Y, Yamamoto W, Toge T, Nishiyama M. 1999. Dihydropyrimidine dehydrogenase, multidrug resistance-associated protein, and thymidylate synthase gene expression levels can predict 5-fluorouracil resistance in human gastrointestinal cancer cells. Int J Oncol. 14:551–557.
  • Koch MF, Harteis S, Blank ID, Pestel G, Tietze LF, Ochsenfeld C, Schneider S, Sieber SA. 2015. Structural, biochemical, and computational studies reveal the mechanism of selective aldehyde dehydrogenase 1A1 inhibition by cytotoxic duocarmycin analogues. Angew Chem Int Ed Engl. 54:13550–13554.
  • Kuin A, Aalders M, Lamfers M, Van Zuidam D, Essers M, Beijnen J, Smets L. 1999. Potentiation of anti-cancer drug activity at low intratumoral pH induced by the mitochondrial inhibitor m-iodobenzylguanidine (MIBG) and its analogue benzylguanidine (BG). Br J Cancer. 79:793.
  • Kumar R, Kaur M, Bahia MS, Silakari O. 2014. Synthesis, cytotoxic study and docking based multidrug resistance modulator potential analysis of 2-(9-oxoacridin-10(9H)-yl)-N-phenyl acetamides. Eur J Med Chem. 80:83–91.
  • Kursula P, Schüler H, Flodin S, Nilsson-Ehle P, Ogg DJ, Savitsky P, Nordlund P, Stenmark P. 2006. Structures of the hydrolase domain of human 10-formyltetrahydrofolate dehydrogenase and its complex with a substrate analogue. Acta Crystallogr D Biol Crystallogr. 62:1294–1299.
  • Larsson H, Mattson H, Sundell G, Carlsson E. 1985. Animal pharmacodynamics of omeprazole. A survey of its pharmacological properties in vivo. Scand J Gastroenterol Suppl. 108:23–35.
  • Lawler M, Johnston PG. 2011. The approval of Teysuno™/S-1 by the European medicines agency: a potentially important advance for gastric cancer patients. The Oncologist. 16:e1–e4.
  • Lee KGZ, Babak MV, Weiss A, Dyson PJ, Nowak‐Sliwinska P, Montagner D, Ang WH. 2018. Development of an efficient dual‐action GST‐inhibiting anticancer platinum (IV) prodrug. Chem Med Chem. 13:1210.
  • Li S, Li C, Jin S, Liu J, Xue X, Eltahan AS, Sun J, Tan J, Dong J, Liang X-J. 2017. Overcoming resistance to cisplatin by inhibition of glutathione S-transferases (GSTs) with ethacraplatin micelles in vitro and in vivo. Biomaterials. 144:119–129.
  • Li Y, Steppi A, Zhou Y, Mao F, Miller PC, He MM, Zhao T, Sun Q, Zhang J. 2017. Tumoral expression of drug and xenobiotic metabolizing enzymes in breast cancer patients of different ethnicities with implications to personalized medicine. Sci Rep. 7:4747.
  • Lin C, Xie L, Lu Y, Hu Z, Chang J. 2018. miR-133b reverses cisplatin resistance by targeting GSTP1 in cisplatin-resistant lung cancer cells. Int J Mol Med. 41:2050–2058.
  • Lin X, Chen X, Riddell IA, Tao W, Wang J, Hollett G, Lippard SJ, Farokhzad OC, Shi J, Wu J. 2018. Glutathione-scavenging poly (disulfide amide) nanoparticles for effective delivery of Pt (IV) prodrugs and reversal of cisplatin resistance. Nano Lett.
  • Liu J, Liu J, Zhao D, Ma N, Luan Y. 2016. Highly enhanced leukemia therapy and oral bioavailability from a novel amphiphilic prodrug of cytarabine. RSC Adv. 6:35991–35999.
  • Liu Y, Zhao D, Sun M, Wei W, Wang Y, Zhou J, Zhang R, Wang J, Zhang H, He Z, et al. 2018. Covalently mucoadhesive amphiphilic prodrug of 5-fluorouracil for enhanced permeation and improved oral absorption. Drug Deliv Transl Res. 8:645–656.
  • Luciani F, Spada M, De Milito A, Molinari A, Rivoltini L, Montinaro A, Marra M, Lugini L, Logozzi M, Lozupone F, et al. 2004. Effect of proton pump inhibitor pretreatment on resistance of solid tumors to cytotoxic drugs. J Natl Cancer Inst. 96:1702–1713.
  • Ludeman SM, Boyd VL, Regan JB, Gallo KA, Zon G, Ishii K. 1986. Synthesis and antitumor activity of cyclophosphamide analogues. 4. Preparation, kinetic studies, and anticancer screening of "phenylketophosphamide" and similar compounds related to the cyclophosphamide metabolite aldophosphamide. J Med Chem. 29:716–727.
  • Luo M, Gates KS, Henzl MT, Tanner JJ. 2015. Diethylaminobenzaldehyde is a covalent, irreversible inactivator of ALDH7A1. ACS Chem Biol. 10:693–697.
  • Luo M, Tanner JJ. 2015. Structural basis of substrate recognition by aldehyde dehydrogenase 7A1. Biochemistry. 54:5513–5522.
  • Lyttle MH, Hocker MD, Hui HC, Caldwell CG, Aaron DT, Engqvist-Goldstein A, Flatgaard JE, Bauer KE. 1994. Isoenzyme-specific glutathione-S-transferase inhibitors: design and synthesis. J Med Chem. 37:189–194.
  • Ma I, Allan AL. 2011. The role of human aldehyde dehydrogenase in normal and cancer stem cells. Stem Cell Rev.7:292–306.
  • Mannervik B, Helena Danielson U, Ketterer B. 1988. Glutathione transferases—structure and catalytic activit. Crit Rev Biochem. 23:283–337.
  • Massaad L, de Waziers I, Ribrag V, Janot F, Beaune PH, Morizet J, Gouyette A, Chabot GG. 1992. Comparison of mouse and human colon tumors with regard to phase I and phase II drug-metabolizing enzyme systems. Cancer Res. 52:6567–6575.
  • Mathew N, Kalyanasundaram M, Balaraman K. 2006. Glutathione S-transferase (GST) inhibitors. Exp Opin Therap Patents. 16:431–444.
  • Burg D, Mulder GJ. 2004. Peptidomimetic glutathione analogs. U. S. Patent No. 6, 747, 009.
  • McFadyen MC, McLeod HL, Jackson FC, Melvin WT, Doehmer J, Murray GI. 2001. Cytochrome P450 CYP1B1 protein expression: a novel mechanism of anticancer drug resistance1. Biochem Pharmacol. 62:207–212.
  • McFadyen MC, Murray GI. 2005. Cytochrome P450 1B1: a novel anticancer therapeutic target. Future Med. 1(2):259–263.
  • Meng X, Sun H, Yang L, Yin R, Qi L. 2017. A hydroxylated flavonol, fisetin inhibits the formation of a carcinogenic estrogen metabolite. Steroids. 119:53–56.
  • Miao R, Yang G, Miao Y, Mei Y, Hong J, Zhao C, Zhu L. 2005. Interactions of platinum (II) complexes with sulfur‐containing peptides studied by electrospray ionization mass spectrometry and tandem mass spectrometry. Rapid Commun Mass Spectrom.19:1031–1040.
  • Michael M, Doherty M. 2005. Tumoral drug metabolism: overview and its implications for cancer therapy. J Clin Oncol. 23:205–229.
  • Mikstacka R, Przybylska D, Rimando AM, Baer‐Dubowska W. 2007. Inhibition of human recombinant cytochromes P450 CYP1A1 and CYP1B1 by trans-resveratrol methyl ethers. Mol Nutr Food Res. 51:517–524.
  • Miners JO, Chau N, Rowland A, Burns K, McKinnon RA, Mackenzie PI, Tucker GT, Knights KM, Kichenadasse G. 2017. Inhibition of human UDP-glucuronosyltransferase enzymes by lapatinib, pazopanib, regorafenib and sorafenib: implications for hyperbilirubinemia. Biochem Pharmacol. 129:85–95.
  • Jones AD, Mitchell AE, Hammock BD, Zheng J. 1998. Inhibition of glutathione transferase by haloenol lactones. U. S. Patent No. 5,767,147.
  • Kauvar LM, Lyttle MH, Morgan AS, Borch RF. 1998. Bone marrow stimulation by certain glutathione analogs. U. S. Patent No. 5,767,086.
  • Oliver Y-P, Hsiong C-H, Wang M-T, Pao L-H. 2006. Inhibitors and enhancers of uridine diphosphate-glucuronosyltransferase 2B (UGT2B). U. S. Patent No. 9,415,034.
  • Moretti A, Li J, Donini S, Sobol RW, Rizzi M, Garavaglia S. 2016. Crystal structure of human aldehyde dehydrogenase 1A3 complexed with NAD + and retinoic acid. Sci Rep. 6:35710.
  • Morgan CA, Hurley TD. 2015a. Characterization of two distinct structural classes of selective aldehyde dehydrogenase 1A1 inhibitors. J Med Chem. 58:1964–1975.
  • Morgan CA, Hurley TD. 2015b. Development of a high-throughput in vitro assay to identify selective inhibitors for human ALDH1A1. Chem-Biol Interact. 234:29–37.
  • Morgan CA, Parajuli B, Buchman CD, Dria K, Hurley TD. 2015. N,N-diethylaminobenzaldehyde (DEAB) as a substrate and mechanism-based inhibitor for human ALDH isoenzymes . Chem Biol Interact. 234:18–28.
  • Organization W.H.Global health observatory data repository. 2011. Number of deaths (World) by cause. 2017.
  • Organization W. H. Guide to cancer early diagnosis. 2018.
  • Spector T. 2014. Methods for preventing or reducing neurotoxicity associated with administering DPD inhibitors in combination with 5-FU and 5-FU prodrugs. U. S. Patent No. 8,658,618.
  • Mulder GJ, Ouwerkerk-Mahadevan S. 1997. Modulation of glutathione conjugation in vivo: how to decrease glutathione conjugation in vivo or in intact cellular systems in vitro. Chem-Biol Interact. 105:17–34.
  • Murray GI, Taylor MC, McFadyen MC, McKay JA, Greenlee WF, Burke MD, Melvin WT. 1997. Tumor-specific expression of cytochrome P450 CYP1B1. Cancer Res. 57:3026–3031.
  • Wu Y-C, Lee K-H, Chang F-R, Chuang D-W, Juan-Cheng Y. 2014. Compound for inhibiting glutathione s-transferase omega 1 activity, pharmaceutical composition containing thereof, and method for synthesizing the same. U. S. Patent No. 13,845,119.
  • Yao Z, Wardell S, Spasojevic I, Norris J, Katzenellenbogen J, McDonnell D, Josan JS. 2018. Development of a selective androgen receptor degrader (SARD) for treatment of castration-resistant prostate cancer. Cancer Res. 78:1805.
  • Napier M, Sharma S, Springer C, Bagshawe K, Green A, Martin J, Stribbling S, Cushen N, O’Malley D, Begent R. 2000. Antibody-directed enzyme prodrug therapy: efficacy and mechanism of action in colorectal carcinoma. Clin Cancer Res. 6:765–772.
  • Negoita S, Feuer EJ, Mariotto A, Cronin KA, Petkov VI, Hussey SK, Benard V, Henley SJ, Anderson RN, Fedewa S. 2018. Annual report to the nation on the status of cancer, part II: recent changes in prostate cancer trends and disease characteristics. Cancer. 124(13):2801–2814.
  • Newcomb M, Shen R, Choi S-Y, Toy PH, Hollenberg PF, Vaz AD, Coon MJ. 2000. Cytochrome P450-catalyzed hydroxylation of mechanistic probes that distinguish between radicals and cations. Evidence for cationic but not for radical intermediates. J Am Chem Soc. 122:2677–2686.
  • Ogino S, Konishi H, Ichikawa D, Matsubara D, Shoda K, Arita T, Kosuga T, Komatsu S, Shiozaki A, Okamoto K, et al. 2019. Glutathione S-transferase Pi 1 is a valuable predictor for cancer drug resistance in esophageal squamous cell carcinoma . Cancer Sci. 110:795.
  • Oguri T, Takahashi T, Miyazaki M, Isobe T, Kohno N, Mackenzie PI, Fujiwara Y. 2004. UGT1A10 is responsible for SN-38 glucuronidation and its expression in human lung cancers. Anticancer Res. 24:2893–2896.
  • Olsen L, Oostenbrink C, Jørgensen FS. 2015. Prediction of cytochrome P450 mediated metabolism. Adv Drug Deliv Rev. 86:61–71.
  • Osborne CK, Wiebe VJ, McGuire WL, Ciocca DR, DeGregorio MW. 1992. Tamoxifen and the isomers of 4-hydroxytamoxifen in tamoxifen-resistant tumors from breast cancer patients. J Clin Oncol. 10:304–310.
  • Pan S, Yu F, Hipsher C. 1993. Enzymatic and pH modulation of mitomycin C-induced DNA damage in mitomycin C-resistant HCT 116 human colon cancer cells. Mol Pharmacol. 43:870–877.
  • Parajuli B, Fishel ML, Hurley TD. 2014. Selective ALDH3A1 inhibition by benzimidazole analogues increase mafosfamide sensitivity in cancer cells. J Med Chem. 57:449–461.
  • Parajuli B, Georgiadis TM, Fishel ML, Hurley TD. 2014. Development of selective inhibitors for human aldehyde dehydrogenase 3A1 (ALDH3A1) for the enhancement of cyclophosphamide cytotoxicity. Chembiochem. 15:701–712.
  • Park H-G, Lim Y-R, Han S, Jeong D, Kim D. 2017. Enhanced purification of recombinant rat NADPH-P450 reductase by using a hexahistidine-tag. J Microbiol Biotechnol. 27:983–989.
  • Parkinson A, Kazmi F, Buckley DB, Yerino P, Ogilvie BW, Paris BL. 2010. System-dependent outcomes during the evaluation of drug candidates as inhibitors of cytochrome P450 (CYP) and uridine diphosphate glucuronosyltransferase (UGT) enzymes: human hepatocytes versus liver microsomes versus recombinant enzymes. Drug Metab Pharmacokinet. 25:16–27.
  • Patel M, Lu L, Zander DS, Sreerama L, Coco D, Moreb JS. 2008. ALDH1A1 and ALDH3A1 expression in lung cancers: correlation with histologic type and potential precursors. Lung Cancer. 59:340–349.
  • Pathak D, Chadha N, Silakari O. 2016. Identification of non-resistant ROS-1 inhibitors using structure based pharmacophore analysis. J Mol Graph Model. 70:85–93.
  • Pathak RK, Wen R, Kolishetti N, Dhar S. 2017. A prodrug of two approved drugs, cisplatin and chlorambucil, for chemo war against cancer. Mol Cancer Therap. 0445:2016.
  • Pathania S, Bhatia R, Baldi A, Singh R, Rawal RK. 2018. Drug metabolizing enzymes and their inhibitors' role in cancer resistance. Biomed Pharmacother. 105:53–65.
  • Pattanawongsa A, Chau N, Rowland A, Miners JO. 2015. The inhibition of human UDP-glucuronosyltransferase (UGT) enzymes by canagliflozin and dapagliflozin: implications for drug-drug interactions. Drug Metab Disposit. 43(10):1468–76. 115.065870.
  • Pemberton TA, Srivastava D, Sanyal N, Henzl MT, Becker DF, Tanner JJ. 2014. Structural studies of yeast Δ1-pyrroline-5-carboxylate dehydrogenase (ALDH4A1): active site flexibility and oligomeric state. Biochemistry. 53:1350–1359.
  • Penner N, Woodward C, Prakash C. 2012. Drug metabolizing enzymes and biotransformation reactions. In: Zhang D, Surapaneni S, editors. ADME-enabling technologies in drug design and development. Hoboken (NJ): Wiley.
  • Persi E, Duran-Frigola M, Damaghi M, Roush WR, Aloy P, Cleveland JL, Gillies RJ, Ruppin E. 2018. Systems analysis of intracellular pH vulnerabilities for cancer therapy. Nat Commun. 9:2997.
  • Pohl J, Bertram B, Hilgard P, Nowrousian M, Stüben J, Wiessler M. 1995. D-19575-a sugar-linked isophosphoramide mustard derivative exploiting transmembrane glucose transport. Cancer Chemother Pharmacol. 35:364–370.
  • Poirier D, Roy J, Cortés-Benítez F, Dutour R. 2016. Targeting cytochrome P450 (CYP) 1B1 with steroid derivatives. Bioorg Med Chem Lett. 26:5272–5276.
  • Projan SJ. 2003. Why is big Pharma getting out of antibacterial drug discovery? Curr Opin Microbiol. 6:427–430.
  • Radominska-Pandya A, Bratton SM, Redinbo MR, Miley MJ. 2010. The crystal structure of human UDP-glucuronosyltransferase 2B7 C-terminal end is the first mammalian UGT target to be revealed: the significance for human UGTs from both the 1A and 2B families. Drug Metab Rev. 42:133–144.
  • Ranson H, Rossiter L, Ortelli F, Jensen B, Wang X, Roth CW, Collins FH, Hemingway J. 2001. Identification of a novel class of insect glutathione S-transferases involved in resistance to DDT in the malaria vector Anopheles gambiae. Biochem J. 359:295–304.
  • Rochat B, Morsman JM, Murray GI, Figg WD, McLeod HL. 2001. Human CYP1B1 and anticancer agent metabolism: mechanism for tumor-specific drug inactivation?. J Pharmacol Exp Ther. 296:537–541.
  • Ross D, Kepa JK, Winski SL, Beall HD, Anwar A, Siegel D. 2000. NAD(P)H:quinone oxidoreductase 1 (NQO1): chemoprotection, bioactivation, gene regulation and genetic polymorphisms. Chem Biol Interact. 129:77–97.
  • Santi DV, Schneider EL, Ashley GW. 2014. Macromolecular prodrug that provides the irinotecan (CPT-11) active-metabolite SN-38 with ultralong half-life, low C max, and low glucuronide formation. J Med Chem. 57:2303–2314.
  • Sawada S, Yokokura T, Miyasaka T. 1996. Synthesis of CPT‐11 (irinotecan hydrochloride trihydrate). Ann NY Acad Sci. 803:13–28.
  • Seow HA, Belcourt MF, Penketh PG, Hodnick WF, Tomasz M, Rockwell S, Sartorelli AC. 2005. Nuclear localization of NADPH:cytochrome c (P450) reductase enhances the cytotoxicity of mitomycin C to Chinese hamster ovary cells. Mol Pharmacol. 67:417–423.
  • Seow HA, Penketh PG, Baumann RP, Sartorelli AC. 2004. Bioactivation and resistance to mitomycin C. Methods in enzymology. Amsterdam (Netherlands): Elsevier; p. 221–233.
  • Shelton J, Lu X, Hollenbaugh JA, Cho JH, Amblard F, Schinazi RF. 2016. Metabolism, biochemical actions, and chemical synthesis of anticancer nucleosides, nucleotides, and base analogs. Chem Rev. 116:14379–14455.
  • Shi W-J, Gao J-B. 2016. Molecular mechanisms of chemoresistance in gastric cancer. World J Gastrointest Oncol. 8:673.
  • Shimada S, Sano D, Hyakusoku H, Hatano T, Takahashi H, Isono Y, Sawakuma K, Takada K, Okudela K, Oridate N. 2018. Dihydropyrimidine dehydrogenase overexpression correlates with potential resistance to 5-fluorouracil-based treatment in head and neck squamous cell carcinoma. Transl Cancer Res. 7:411–419.
  • Siegel D, Beall H, Kasai M, Arai H, Gibson NW, Ross D. 1993. pH-dependent inactivation of DT-diaphorase by mitomycin C and porfiromycin. Mol Pharmacol. 44:1128–1134.
  • Siegel D, Ross D. 2000. Immunodetection of NAD(P)H:quinone oxidoreductase 1 (NQO1) in human tissues. Free Radic Biol Med. 29:246–253.
  • Siegel D, Yan C, Ross D. 2012. NAD(P)H:quinone oxidoreductase 1 (NQO1) in the sensitivity and resistance to antitumor quinones. Biochem Pharmacol. 83:1033–1040.
  • Sladek NE, Kollander R, Sreerama L, Kiang DT. 2002. Cellular levels of aldehyde dehydrogenases (ALDH1A1 and ALDH3A1) as predictors of therapeutic responses to cyclophosphamide-based chemotherapy of breast cancer: a retrospective study. Rational individualization of oxazaphosphorine-based cancer chemotherapeutic regimens. Cancer Chemoth Pharm. 49:309–321.
  • Sládek NE, Rekha GK, Lee MJ, Nagasawa HT. 2001. Inhibition of ALDH3A1-catalyzed oxidation by chlorpropamide analogues. Chem Biol Interact. 138:201–215.
  • Srivastava D, Singh RK, Moxley MA, Henzl MT, Becker DF, Tanner JJ. 2012. The three-dimensional structural basis of type II hyperprolinemia. J Mol Biol. 420:176–189.
  • Strassburg CP, Strassburg A, Nguyen N, Qing L, Manns MP, Tukey RH. 1999. Regulation and function of family 1 and family 2 UDP-glucuronosyltransferase genes (UGT1A, UGT2B) in human oesophagus. Biochem J. 338:489–498.
  • Swanson HI, Njar VCO, Yu Z, Castro DJ, Gonzalez FJ, Williams DE, Huang Y, Kong A-NT, Doloff JC, Ma J, et al. 2010. Targeting drug-metabolizing enzymes for effective chemoprevention and chemotherapy. Drug Metab Disposit. 38:539–544.
  • Takahashi T, Fujiwara Y, Yamakido M, Katoh O, Watanabe H, Mackenzie PI. 1997. The role of glucuronidation in 7-ethyl-10-hydroxycamptothecin resistance in vitro . Jpn J Cancer Res. 88:1211–1217.
  • Takechi T, Fujioka A, Matsushima E, Fukushima M. 2002. Enhancement of the antitumour activity of 5-fluorouracil (5-FU) by inhibiting dihydropyrimidine dehydrogenase activity (DPD) using 5-chloro-2,4-dihydroxypyridine (CDHP) in human tumour cells. Eur J Cancer. 38:1271–1277.
  • Tao N-N, Zhou H-Z, Tang H, Cai X-F, Zhang W-L, Ren J-H, Zhou L, Chen X, Chen K, Li W-Y, et al. 2016. Sirtuin 3 enhanced drug sensitivity of human hepatoma cells through glutathione S-transferase pi 1/JNK signaling pathway. Oncotarget. 7:50117.
  • Teicher BA. 2007. Cancer drug resistance. Berlin (Germany): Springer Science & Business Media.
  • Todorović-Raković N, Nešković-Konstantinović Z, Nikolić-Vukosavljević D. 2006. Cross-talk between ER and HER2 in breast carcinoma. Arch Oncol. 14:146–150.
  • Tomita H, Tanaka K, Tanaka T, Hara A. 2016. Aldehyde dehydrogenase 1A1 in stem cells and cancer. Oncotarget. 7:11018.
  • Tong CW, Wu M, Cho WC, To KK. 2018. Recent advances in the treatment of breast cancer. Front Oncol. 8: 227.
  • Trunzer K, Pavlick AC, Schuchter L, Gonzalez R, McArthur GA, Hutson TE, Moschos SJ, Flaherty KT, Kim KB, Weber JS, et al. 2013. Pharmacodynamic effects and mechanisms of resistance to vemurafenib in patients with metastatic melanoma. J Clin Oncol. 31:1767–1774.
  • Vallböhmer D, Yang DY, Kuramochi H, Shimizu D, Danenberg KD, Lindebjerg J, Nielsen JN, Jakobsen A, Danenberg PV. 2007. DPD is a molecular determinant of capecitabine efficacy in colorectal cancer. Int J Oncol. 31:413–418.
  • van Kuilenburg AB. 2004. Dihydropyrimidine dehydrogenase and the efficacy and toxicity of 5-fluorouracil. Eur J Cancer. 40:939–950.
  • Varshosaz J, Hassanzadeh F, Sadeghi H, Andalib S. 2012. Synthesis of octadecylamine-retinoic acid conjugate for enhanced cytotoxic effects of 5-FU using LDL targeted nanostructured lipid carriers. Eur J Med Chem. 54:429–438.
  • Wang C-H, Wu HT, Cheng HM, Yen T-J, Lu I-H, Chang HC, Jao S-C, Shing TK, Li W-S. 2011. Inhibition of glutathione S-transferase M1 by new gabosine analogues is essential for overcoming cisplatin resistance in lung cancer cells. J Med Chem. 54:8574–8581.
  • Wenzel M, Casini A. 2017. Mass spectrometry as a powerful tool to study therapeutic metallodrugs speciation mechanisms: current frontiers and perspectives. Coord Chem Rev. 352:432–460.
  • Werck-Reichhart D, Feyereisen R. 2000. Cytochromes P450: a success story. Genome Biol. 1:REVIEWS3003–REVIEWS3001.
  • Williams IS, Joshi P, Gatchie L, Sharma M, Satti NK, Vishwakarma RA, Chaudhuri B, Bharate SB. 2017. Synthesis and biological evaluation of pyrrole-based chalcones as CYP1 enzyme inhibitors, for possible prevention of cancer and overcoming cisplatin resistance. Bioorg Med Chem Lett. 27:3683–3687.
  • Wilson T, Johnston P, Longley D. 2009. Anti-apoptotic mechanisms of drug resistance in cancer. Curr Cancer Drug Targets. 9:307–319.
  • Wirth T, Schmuck K, Tietze LF, Sieber SA. 2012. Duocarmycin analogues target aldehyde dehydrogenase 1 in lung cancer cells. Angew Chem Int Ed Engl. 51:2874–2877.
  • Wong P, Kleemann H, Tannock I. 2002. Cytostatic potential of novel agents that inhibit the regulation of intracellular pH. Br J Cancer. 87:238.
  • Wong P, Lee C, Tannock IF. 2005. Reduction of intracellular pH as a strategy to enhance the pH-dependent cytotoxic effects of melphalan for human breast cancer cells. Clin Cancer Res. 11:3553–3557.
  • Wu Z, Minhas GS, Wen D, Jiang H, Chen K, Zimniak P, Zheng J. 2004. Design, synthesis, and structure-activity relationships of haloenol lactones: site-directed and isozyme-selective glutathione S-transferase inhibitors. J Med Chem. 47:3282–3294.
  • Yang Y, Yin F, Hang Q, Dong X, Chen J, Li L, Cao P, Yin Z, Luo L. 2018. Regulation of endothelial permeability by glutathione S-transferase Pi against actin polymerization. Cell Physiol Biochem. 45:406–418.
  • Yang S-M, Martinez NJ, Yasgar A, Danchik C, Johansson C, Wang Y, Baljinnyam B, Wang AQ, Xu X, Shah P, et al. 2018. Discovery of orally bioavailable, quinoline-based aldehyde dehydrogenase 1A1 (ALDH1A1) inhibitors with potent cellular activity. J Med Chem. 61:4883.
  • Yang S-M, Yasgar A, Miller B, Lal-Nag M, Brimacombe K, Hu X, Sun H, Wang A, Xu X, Nguyen K, et al. 2015. Discovery of NCT-501, a potent and selective theophylline-based inhibitor of aldehyde dehydrogenase 1A1 (ALDH1A1). J Med Chem. 58:5967–5978.
  • Yarden Y, Elkabets M. 2018. Resistance to anti-cancer therapeutics targeting receptor tyrosine kinases and downstream pathways. Vol. 15. Berlin (Germany): Springer.
  • Zhang X, Dong D, Wang H, Ma Z, Wang Y, Wu B. 2015. Stable knock-down of efflux transporters leads to reduced glucuronidation in UGT1A1-overexpressing HeLa cells: the evidence for glucuronidation-transport interplay. Mol Pharm. 12:1268–1278.
  • Zhou X, Zhuo X, Xie F, Kluetzman K, Shu Y-Z, Humphreys WG, Ding X. 2010. Role of CYP2A5 in the clearance of nicotine and cotinine: insights from studies on a Cyp2a5-null mouse model. J Pharmacol Exp Ther. 332:578–587.
  • Zhu Z, Mu Y, Qi C, Wang J, Xi G, Guo J, Mi R, Zhao F. 2015. CYP1B1 enhances the resistance of epithelial ovarian cancer cells to paclitaxel in vivo and in vitro. Int J Mol Med. 35:340–348.

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