Induction of intrinsic and extrinsic apoptosis through oxidative stress in drug-resistant cancer by a newly synthesized Schiff base copper chelate

References

• Fojo T. Multiple paths to a drug resistance phenotype: mutations, translocations, deletions and amplification of coding genes or promoter regions, epigenetic changes and microRNAs. Drug Resist Updat 2007;10:59–67.
   PubMed Web of Science ®Google Scholar
• Maddika S, Ande SR, Panigrahi S, Paranjothy T, Weglarczyk K, Zuse A, et al. Cell survival, cell death and cell cycle pathways are interconnected: implications for cancer therapy. Drug Resist Updat 2007;10:13–29.
   PubMed Web of Science ®Google Scholar
• Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005;5:275–284.
   PubMed Web of Science ®Google Scholar
• Assaraf YG. The role of multidrug resistance efflux transporters in antifolate resistance and folate homeostasis. Drug Resist Update 2006;9:227–246.
   PubMed Web of Science ®Google Scholar
• Burchert A. Roots of imatinib resistance: a question of self-renewal? Drug Resist Updat 2007;10:152–161.
   PubMed Web of Science ®Google Scholar
• Mimeault M, Hauke R, Mehta PP, Batra SK. Recent advances in cancer stem/progenitor cell research: therapeutic implications for overcoming resistance to the most aggressive cancers. J Cell Mol Med 2007;11:981–1011.
   PubMed Web of Science ®Google Scholar
• Majumder S, Dutta P, Mookerjee A, Choudhuri SK. The role of a novel copper complex in overcoming doxorubicin resistance in Ehrlich ascites carcinoma cells in vivo. Chem Biol Interact 2006;159:90–103.
   PubMed Web of Science ®Google Scholar
• Rassool FV, Gaymes TJ, Omidvar N, Brady N, Beurlet S, Pla M, et al. Reactive oxygen species, DNA damage, and error-prone repair: a model for genomic instability with progression in myeloid leukemia? Cancer Res 2007;67:8762–8771.
   PubMed Web of Science ®Google Scholar
• Park MT, Kim MJ, Kang YH, Choi SY, Lee JH, Choi JA, et al. Phytosphingosine in combination with ionizing radiation enhances apoptotic cell death in radiation-resistant cancer cells through ROS dependent and -independent AIF release. Blood 2005;105:1724–1733.
   PubMed Web of Science ®Google Scholar
• Hwang JT, Ha J, Park OJ. Combination of 5-fluorouracil and genistein induces apoptosis synergistically in chemo-resistant cancer cells through the modulation of AMPK and COX-2 signaling pathways. Biochem Biophys Res Commun 2005;332:433–440.
   PubMed Web of Science ®Google Scholar
• Rosenberg B, Vancamp L, Krigas T. Inhibition of cell division in Escherichia coli by electrolysis products from a platinum electrode. Nature 1965;205:698–699.
   PubMed Web of Science ®Google Scholar
• Rosenberg B, VanCamp L, Trosko JE, Mansour VH. Platinum compounds: a new class of potent antitumour agents. Nature 1969;222:385–386.
   PubMed Web of Science ®Google Scholar
• Kelland L. Broadening the clinical use of platinum drug-based chemotherapy with new analogues. Satraplatin and picoplatin. Expert Opin Investig Drugs 2007;16:1009–1021.
   PubMed Web of Science ®Google Scholar
• Stewart DJ. Mechanisms of resistance to cisplatin and carboplatin. Crit Rev Oncol Hematol 2007;63:12–31.
   PubMed Web of Science ®Google Scholar
• Stordal B, Pavlakis N, Davey R. Oxaliplatin for the treatment of cisplatin-resistant cancer: a systematic review. Cancer Treat Rev 2007;33:347–357.
   PubMed Web of Science ®Google Scholar
• Basu S, Ganguly A, Chakraborty P, Sen R, Banerjee K, Chatterjee M, et al. Targeting the mitochondrial pathway to induce apoptosis/necrosis through ROS by a newly developed Schiff’s base to overcome MDR in cancer. Biochimie 2012;94:166–183.
   PubMed Web of Science ®Google Scholar
• Ganguly A, Basu S, Banerjee K, Chakraborty P, Sarkar A, Chatterjee M, Choudhuri SK. Redox active copper chelate overcomes multidrug resistance in T-lymphoblastic leukemia cell by triggering apoptosis. Mol Biosyst 2011;7:1701–1712.
   PubMed Web of Science ®Google Scholar
• Chatterjee S, Mookerjee A, Basu JM, Chakraborty P, Ganguly A, Adhikary A, et al. A novel copper chelate modulates tumor associated macrophages to promote anti-tumor response of T cells. PLoS One 2009;4:e7048.
   PubMed Web of Science ®Google Scholar
• Majumder S, Panda GS, Kumar Choudhuri S. Synthesis, characterization and biological properties of a novel copper complex. Eur J Med Chem 2003;38:893–898.
   PubMed Web of Science ®Google Scholar
• Efferth T, Konkimalla VB, Wang YF, Sauerbrey A, Meinhardt S, Zintl F, et al. Prediction of broad spectrum resistance of tumors towards anticancer drugs. Clin Cancer Res 2008;14:2405–2412.
   PubMed Web of Science ®Google Scholar
• Gillet JP, Efferth T, Steinbach D, Hamels J, de Longueville F, Bertholet V, Remacle J. Microarray based detection of multidrug resistance in human tumor cells by expression profiling of ATP binding cassette transporter genes. Cancer Res 2004;64:8987–8993.
   PubMed Web of Science ®Google Scholar
• Choudhuri SK, Chatterjee A. Reversal of resistance against doxorubicin by a newly developed compound, oxalyl bis(N-phenyl)hydroxamic acid in vitro. Anticancer Drugs 1994;9:825–832.
   Web of Science ®Google Scholar
• Ganguly A, Basu S, Chakraborty P, Chatterjee S, Sarkar A, Chatterjee M, Choudhuri SK. Targeting mitochondrial cell death pathway to overcome drug resistance with a newly developed iron chelate. PLoS One 2010;5:e11253.
   PubMed Web of Science ®Google Scholar
• Banerjee K, Ganguly A, Chakraborty P, Sarkar A, Singh S, Chatterjee M, et al. ROS and RNS induced apoptosis through p53 and iNOS mediated pathway by a dibasic hydroxamic acid molecule in leukemia cells. Eur J Pharm Sci 2014;52:146–164.
   PubMed Web of Science ®Google Scholar
• White CC, Viernes H, Krejsa CM, Botta D, Kavanagh TJ. Fluorescence-based microtiter plate assay for glutamate-cysteine ligase activity. Anal Biochem 2003;318:175–180.
   PubMed Web of Science ®Google Scholar
• Mulherin DM, Thurnham DI, Situnayake RD. Glutathione reductase activity, riboflavin status, and disease activity in rheumatoid arthritis. Ann Rheum Dis 1996;55:837–840.
   PubMed Web of Science ®Google Scholar
• Sedlack J, Lindsay RN. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 1968;25:192–205.
   PubMed Web of Science ®Google Scholar
• Lowry OH, Rosenberg NJ, Farr AL, Randal RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265–271.
   PubMed Web of Science ®Google Scholar
• LeBel CP, Ischiropoulos H, Bondy SC. Evaluation of the probe 2',7'-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 1992;5:227–231.
   PubMed Web of Science ®Google Scholar
• Petit JM, Maftah A, Ratinaud MH, Julien R. 10N-nonyl acridine orange interacts with cardiolipin and allows the quantification of this phospholipid in isolated mitochondria. Eur J Biochem 1992;209:267–273.
   PubMedGoogle Scholar
• Green DR, Kroemer G. The pathophysiology of mitochondrial cell death. Science 2004;305:626–629.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Tozzi F, Chen J, Fan F, Xia L, Wang J, et al. Intracellular ATP levels are a pivotal determinant of chemoresistance in colon cancer cells. Cancer Res 2012;72:304–314.
   PubMed Web of Science ®Google Scholar
• Latchoumycandane C, Seah QM, Tan RC, Sattabongkot J, Beerheide W, Boelsterli UA. Leflunomide or A77 1726 protect from acetaminophen-induced cell injury through inhibition of JNK-mediated mitochondrial permeability transition in immortalized human hepatocytes. Toxicol Appl Pharmacol 2006;217:125–133.
   PubMed Web of Science ®Google Scholar
• Sorenson RJR. (ed.). Biology of copper complexes. Clifton, NJ: Humana Press; 1987.
   Google Scholar
• Basu Baul TS, Dutta S, Rivarola E, Scopelliti M, Choudhuri SK. Synthesis, characterization of diorganotin(IV) complexes of N-(2-hydroxyarylidine)aminoacetic acid and antitumour screening in vivo in Ehrlich ascites carcinoma cells. Appl Organometal Chem 2001;15:947–953.
   Web of Science ®Google Scholar
• Procter IM, Hathaway BJ, Nicholls P. The electronic properties and stereochemistry of the copper (II) ion. Part I. Bis(ethylenediamine) copper(II) complexes. J Chem Soc A 1968;1678–1684. DOI: 10.1039/J19680001678.
   PubMed Web of Science ®Google Scholar
• Davis FJ, Gilbert BC, Norman ROC, Symons MCR. Electron spin resonance studies. Part 66. Characterization of copper(II) complexes in the oxidation of D-penicillamine, L-cysteine, and related sulphur-containing compounds. J Chem Soc Perkin Trans 2 1983;1763–1771. DOI: 10.1039/P29830001763.
   Google Scholar
• Chandra Patra S, Saha Roy A, Manivannan V, Weyhermüller T, Ghosh P. Ruthenium, osmium and rhodium complexes of 1,4-diaryl 1,4-diazabutadiene: radical versus non-radical states. Dalton Trans 2014;43:13731–13741.
   PubMed Web of Science ®Google Scholar
• Hay PJ, Wadt WR. Ab initio effective core potentials for molecular calculations. Potentials for the transition metal atoms Sc to Hg. J Chem Phys 1985;82:270–283.
   Web of Science ®Google Scholar
• Wadt WR, Hay PJ. Ab initio effective core potentials for molecular calculations. Potentials for main group elements Na to Bi. J Chem Phys 1985;82:284.
   Web of Science ®Google Scholar
• Hay PJ, Wadt WR. Ab initio effective core potentials for molecular calculations. Potentials for K to Au including the outermost core orbitals. J Chem Phys 1985;82:299.
   Web of Science ®Google Scholar
• Garribba E, Micera G. The determination of the geometry of Cu(II) complexes: an EPR spectroscopy experiment. J Chem Educ 2006;83:1229–1232.
   Web of Science ®Google Scholar
• Chandra S, Sangeetika S. Synthesis and spectral studies on copper(II) and cobalt(II) complexes of macrocyclic ligand containing thiosemicarbazone moiety. Ind J Chem 2002;41A:1629–1633.
   Google Scholar
• Koval IA, van der Schilden K, Schuitema AM, Gamez P, Belle C, Pierre JL, et al. Proton NMR spectroscopy and magnetic properties of a solution-stable dicopper(II) complex bearing a single mu-hydroxo bridge. Inorg Chem 2005;44:4372–4382.
   PubMed Web of Science ®Google Scholar
• Ly JD, Grubb DR, Lawen A. The mitochondrial membrane potential (deltapsi(m)) in apoptosis; an update. Apoptosis 2003;8:115–128.
   PubMed Web of Science ®Google Scholar
• Trachootham D, Alexandre J, Huang P. Targeting cancer cells by ROS mediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov 2009;8:579–591.
   PubMed Web of Science ®Google Scholar
• Franco JL, Posser T, Dunkley PR, Dickson PW, Mattos JJ, Martins R, et al. Methylmercury neurotoxicity is associated with inhibition of the antioxidant enzyme glutathione peroxidase. Free Radic Biol Med 2009;47:449–457.
   PubMed Web of Science ®Google Scholar
• Lu SC. Regulation of glutathione synthesis. Mol Aspects Med 2009;30:42–59.
   PubMed Web of Science ®Google Scholar
• Lowe SW, Lin AW. Apoptosis in cancer. Carcinogenesis 2000;21:485–495.
   PubMed Web of Science ®Google Scholar
• Jiang C, Wang Z, Ganther H, Lu J. Caspases as key executors of methyl selenium-induced apoptosis (anoikis) of DU145 prostate cancer cells. Cancer Res 2001;61:3062–3070.
   PubMed Web of Science ®Google Scholar
• Ghavami S, Hashemi M, Ande SR, Yeganeh B, Xiao W, Eshraghi M, et al. Apoptosis and cancer: mutations within caspase genes. J Med Genet 2009;46:497–510.
   PubMed Web of Science ®Google Scholar
• Slee EA, Adrain C, Martin SJ. Executioner caspase-3, -6, and -7 perform distinct, non-redundant roles during the demolition phase of apoptosis. J Biol Chem 2001;276:7320–7326.
   PubMed Web of Science ®Google Scholar
• Carmody RJ, Cotter TG. Signalling apoptosis: a radical approach. Redox Rep 2001;6:77–90.
   PubMed Web of Science ®Google Scholar
• Fleury C, Mignotte B, Vayssiere JL. Mitochondrial reactive oxygen species in cell death signaling. Biochimie 2002;84:131–141.
   PubMed Web of Science ®Google Scholar
• Kagan VE, Tyurin VA, Jiang J, Tyurina YY, Ritov VB, Amoscato AA, et al. Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat Chem Biol 2005;1:223–232.
   PubMed Web of Science ®Google Scholar
• Longley DB, Johnston PG. Molecular mechanisms of drug resistance. J Pathol 2005;205:275–292.
   PubMed Web of Science ®Google Scholar
• Pommier Y, Sordet O, Antony S, Hayward RL, Kohn KW. Apoptosis defects and chemotherapy resistance: molecular interaction maps and networks. Oncogene 2004;23:2934–2949.
   PubMed Web of Science ®Google Scholar
• Ghosh RD, Chakraborty P, Banerjee K, Adhikary A, Sarkar A, Chatterjee M, et al. The molecular interaction of a copper chelate with human P-glycoprotein. Dalton Trans 2012;364:309–320.
   Google Scholar
• Giovannini C, Matarreseb P, Scazzocchioa B, Sanchezc M, Masellaa R, Malorni W. Mitochondria hyperpolarization is an early event in oxidized low-density lipoprotein-induced apoptosis in Caco-2 intestinal cells. FEBS Lett 2002;523:200–206.
   PubMed Web of Science ®Google Scholar
• Baell J, Huang D. Prospects for targeting the Bcl-2 family of proteins to develop novel cytotoxic drugs. Biochem Pharmacol 2002;64:851–863.
   PubMed Web of Science ®Google Scholar
• Machida K, Tanaka T. Farnesol-induced generation of reactive oxygen species dependent on mitochondrial transmembrane potential hyperpolarization mediated by F(0)F(1)-ATPase in yeast. FEBS Lett 1999;462:108–112.
   PubMed Web of Science ®Google Scholar
• Gergely P Jr, Grossman C, Niland B, Puskas F, Neupane H, Allam F, et al. Mitochondrial hyperpolarization and ATP depletion in patients with systemic lupus erythematosus. Arthritis Rheum 2002;46:175–190.
   PubMed Web of Science ®Google Scholar
• Verhagen AM, Ekert PG, Pakusch M, Silke J, Connolly LM, Reid GE, et al. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 2000;102:43–53.
   PubMed Web of Science ®Google Scholar
• Filomeni G, Cerchiaro G, Da Costa Ferreira AM, De Martino A, Pedersen JZ, Rotilio G, Ciriolo MR. Pro-apoptotic activity of novel Isatin-Schiff base copper(ii) complexes depends on oxidative stress induction and organelle-selective damage. J Biol Chem 2007;282:12010–12021.
   PubMed Web of Science ®Google Scholar
• Gough DR, Cotter TG. Hydrogen peroxide: a Jekyll and Hyde signalling molecule. Cell Death Dis 2011;2:e213.
   PubMed Web of Science ®Google Scholar
• Seshiah PN, Weber DS, Rocic P, Valppu L, Taniyama Y, Griendling KK. Angiotensin II stimulation of NAD(P)H oxidase activity: upstream mediators. Circ Res 2002;91:406–413.
   PubMed Web of Science ®Google Scholar
• Nielsen D, Maare C, Eriksen J, Litman T, Skovsgaard T. Expression of P-glycoprotein and multidrug resistance associated protein in Ehrlich ascites tumor cells after fractionated irradiation. Int J Radiat Oncol Biol Phys 2001;51:1050–1057.
   PubMed Web of Science ®Google Scholar
• Ganguly A, Chakraborty P, Banerjee K, Choudhuri SK. The role of a Schiff base scaffold, N-(2-hydroxy acetophenone) glycinate-in overcoming multidrug resistance in cancer. Eur J Pharm Sci 2014;51:96–109.
   PubMed Web of Science ®Google Scholar
• Dang TN, Arseneault M, Ramassamy C. Regulation of redox-sensitive signaling pathways in rat primary astrocytes following acrolein exposure. J Alzheimers Dis 2011;25:263–277.
   PubMed Web of Science ®Google Scholar
• Wiley JS, Taupin J, Jamieson GP, Snook M, Sawyer WH, Finch LR. Cytosine arabinoside transport and metabolism in acute leukemias and T cell lymphoblastic lymphoma. J Clin Invest 1985;75:632–642.
   PubMed Web of Science ®Google Scholar
• Shewach DS, Mitchell BS. Differential metabolism of 9-beta-D-arabinofuranosylguanine in human leukemic cells. Cancer Res 1989;49:6498–6502.
   PubMed Web of Science ®Google Scholar
• Ott M, Zhivotovsky B, Orrenius S. Role of cardiolipin in cytochrome c release from mitochondria. Cell Death Differ 2007;14:1243–1247.
   PubMed Web of Science ®Google Scholar
• Yamauchi R, Morita A, Yasuda Y, Grether-Beck S, Klotz LO, Tsuji T, Krutmann J. Different susceptibility of malignant versus nonmalignant human T cells toward ultraviolet A-1 radiation-induced apoptosis. J Invest Dermatol 2004;122:477–483.
   PubMed Web of Science ®Google Scholar
• Chatterjee S, Chakraborty P, Banerjee K, Sinha A, Adhikary A, Das T, Choudhuri SK. Selective induction of apoptosis in various cancer cells irrespective of drug sensitivity through a copper chelate, copper N-(2 hydroxy acetophenone) glycinate: crucial involvement of glutathione. Biometals 2013;26:517–534.
   PubMed Web of Science ®Google Scholar