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DNA-Binding and Cytotoxicity of Copper(I) Complexes Containing Functionalized Dipyridylphenazine Ligands

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DNA-Binding and Cytotoxicity of Copper(I) Complexes Containing Functionalized Dipyridylphenazine Ligands pharmaceutics Article DNA-Binding and Cytotoxicity of Copper(I) Complexes Containing Functionalized Dipyridylphenazine Ligands Sammar Alsaedi 1, Bandar A. Babgi 1,* , Magda H. Abdellattif 2 , Muhammad N. Arshad 3 , Abdul-Hamid M. Emwas 4 , Mariusz Jaremko 5, Mark G. Humphrey 6 , Abdullah M. Asiri 1,3 and Mostafa A. Hussien 1,7 1 Department of Chemistry, Faculty of Science, King Abdulaziz University, P.O. Box 80203, Jeddah 21589, Saudi Arabia; [email protected] (S.A.); [email protected] (A.M.A.); [email protected] (M.A.H.) 2 Chemistry Department, Deanship of Scientific Research, College of Sciences, Taif University, Al-Haweiah, P.O. Box 11099, Taif 21944, Saudi Arabia; [email protected] 3 Center of Excellence for Advanced Materials Research (CEAMR), King Abdulaziz University, P.O. Box 80203, Jeddah 21589, Saudi Arabia; [email protected] 4 Core Labs, King Abdullah University of Science and Technology (KAUST), Thuwal, 23955-6900, Saudi Arabia; [email protected] 5 Biological and Environmental Science and Engineering (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal 23955-6900, Saudi Arabia; [email protected] 6 Research School of Chemistry, Australian National University, Canberra, ACT 2601, Australia; [email protected] Citation: Alsaedi, S.; Babgi, B.A.; 7 Department of Chemistry, Faculty of Science, Port Said University, Port Said 42521, Egypt Abdellattif, M.H.; Arshad, M.N.; * Correspondence: [email protected]; Tel.: +966-555563702 Emwas, A.-H.M.; Jaremko, M.; Humphrey, M.G.; Asiri, A.M.; Abstract: A set of copper(I) coordination compounds with general formula [CuBr(PPh3)(dppz-R)] Hussien, M.A. DNA-Binding and (dppz-R = dipyrido[3,2-a:2’,3’-c]phenazine (Cu-1), 11-nitrodipyrido[3,2-a:2’,3’-c]phenazine (Cu-2), Cytotoxicity of Copper(I) Complexes 11-cyanodipyrido[3,2-a:2’,3’-c]phenazine (Cu-3), dipyrido[3,2-a:2’,3’-c]phenazine-11-phenone (Cu-4), Containing Functionalized 11,12-dimethyldipyrido[3,2-a:2’,3’-c]phenazine (Cu-5)) have been prepared and characterized by Dipyridylphenazine Ligands. elemental analysis, 1H-NMR and 31P-NMR spectroscopies as well as mass spectrometry. The structure Pharmaceutics 2021, 13, 764. of Cu-1 was confirmed by X-ray crystallography. The effect of incorporating different functional https://doi.org/10.3390/ groups on the dppz ligand on the binding into CT-DNA was evaluated by absorption spectroscopy, pharmaceutics13050764 fluorescence quenching of EtBr-DNA adducts, and viscosity measurements. The functional groups Academic Editors: Wukun Liu and affected the binding modes and hence the strength of binding affinities, as suggested by the changes in Damiano Cirri the relative viscosity. The differences in the quenching constants (Ksv) obtained from the fluorescence quenching assay highlight the importance of the functional groups in altering the binding sites on Received: 7 April 2021 the DNA. The molecular docking data support the DNA-binding studies, with the sites and mode Accepted: 27 April 2021 of interactions against B-DNA changing with the different functional groups. Evaluation of the Published: 20 May 2021 anticancer activities of the five copper compounds against two different cancer cell lines (M-14 and MCF-7) indicated the importance of the functional groups on the dppz ligand on the anticancer Publisher’s Note: MDPI stays neutral activities. Among the five copper complexes, the cyano-containing complex (Cu-3) has the best with regard to jurisdictional claims in anticancer activities. published maps and institutional affil- iations. Keywords: Copper(I); dipyridophenazine; DNA-binding; anticancer properties; molecular docking Copyright: © 2021 by the authors. 1. Introduction Licensee MDPI, Basel, Switzerland. The field of metallodrugs has been under scrutiny since the discovery of the an- This article is an open access article ticancer properties of cis-diamminedichloroplatinum(II) (cisplatin). Although cisplatin distributed under the terms and has been widely applied as a chemotherapeutic agent, it causes severe side effects [1–4], conditions of the Creative Commons Attribution (CC BY) license (https:// so there have been intensive efforts to find more effective metal-based anticancer drugs. creativecommons.org/licenses/by/ In the search for new and more effective anticancer drugs, a wide range of transition 4.0/). metal complexes have been synthesized and tested as anticancer agents [5,6]. Copper Pharmaceutics 2021, 13, 764. https://doi.org/10.3390/pharmaceutics13050764 https://www.mdpi.com/journal/pharmaceutics Pharmaceutics 2021, 13, x 2 of 15 Pharmaceutics 2021, 13, 764 2 of 14 complexes have been synthesized and tested as anticancer agents [5,6]. Copper com- pounds attractedcompounds special interest attracted as possible special candidates interest as [7–11] possible because candidates copper [ 7exists–11] because in copper ex- many biological systemsists in many and is biological involved in systems many biological and is involved processes in manysuch as biological energy me- processes such as tabolism and oxygenenergy transportation. metabolism andIn this oxygen regard, transportation. the interest in copper(I) In this regard, complexes the interest as in copper(I) potential chemotherapeuticcomplexes agents as potential have grown chemotherapeutic enormously in agents the past have three grown decades enormously (Fig- in the past ure 1) [12]. Recently,three a decades copper( (FigureI) phosphine1)[ 12 ].complex, Recently, [Cu(PR a copper(I)3)4][PF phosphine6] (R = CH2 complex,OH), has [Cu(PR3)4][PF6] attracted special (Rinterest = CH due2OH), to its has strong attracted anticancer special effects. interest The due complex to its strongshows particu- anticancer effects. The larly strong effectscomplex against shows human particularly colon cancer strong cells; effectsit is even against more human efficient colon than cancer plati- cells; it is even num-based drugsmore and efficientdisplays thanminimal platinum-based effects on non-tumo drugs andr cells displays [13,14]. minimal Hydrophilic effects on non-tumor phosphines suchcells as [13 ,tris(2-cyanoethyl)ph14]. Hydrophilic phosphinesosphine such(L1) asand tris(2-cyanoethyl)phosphine bis(2-cyanoethyl)phe- (L1) and bis(2- nylphosphine (L2)cyanoethyl)phenylphosphine were employed in synthesizing (L2) were the employed Cu(I) complexes in synthesizing [Cu(L1) the2]+, Cu(I) complexes + + + [Cu(MeCN)(L1)][Cu(L1)+, [CuX(L1)],2] , [Cu(MeCN)(L1)] and [Cu(L2)2]+. The, [CuX(L1)], new copper(I) and complexes [Cu(L2)2] .were The tested new copper(I) for complexes their cytotoxic propertieswere tested against for their a suite cytotoxic of human properties cancer cell against lines aand suite were of humanhighlighted cancer cell lines and for their ability towere alter highlighted the mitochondrial for their me abilitymbrane to alterpotential the mitochondrial and production membrane of reactive potential and pro- oxygen species (ROS)duction [15]. of Recently, reactive oxygen complexe speciess were (ROS) reported [15]. with Recently, 1,10-phenanthroline complexes were reported with (phen) or 2,9-dimethyl-1,10-phenanthroline1,10-phenanthroline (phen) (d ormp) 2,9-dimethyl-1,10-phenanthroline copper(I) iodide complexes and (dmp) one of copper(I) iodide complexes and one of three hydrophilic phosphine ligands: P(CH N(CH CH ) NCH ) , three hydrophilic phosphine ligands: P(CH2N(CH2CH2)2NCH3)3, P(CH2N(CH2CH22)2O)3 2 2 2 3 3 P(CH N(CH CH ) O) and P(CH N(CH )CH CH OH) . The complexes exhibit a strong and P(CH2N(CH3)CH22CH2OH)2 3. The2 2 complexes3 exhibit2 a 3strong2 in 2vitro 3antitumor activ- in vitro antitumor activity against human ovarian carcinoma cell lines (MDAH2774 and ity against human ovarian carcinoma cell lines (MDAH2774 and SCOV3) with IC50 values µ in the range 2–7 μSCOV3)M [16]. withKomarnicka IC50 values et al. in employed the range a 2–7phosphineM[16 ].ligand Komarnicka decorated et al.with employed a phos- a sparfloxacin moietyphine (an ligand antibiotic decorated agent) with in the a sparfloxacin synthesis of moietycomplexes (an antibioticwith the general agent) in the synthesis formula [CuXP(NN)].of complexes Evaluation with of the the general in vitro formula anticancer [CuXP(NN)]. activity Evaluationof these complexes of the in vitro anticancer activity of these complexes against mouse colon carcinoma (CT26) and human lung adeno- against mouse colon carcinoma (CT26) and human lung adenocarcinoma (A549) revealed carcinoma (A549) revealed that the complexes generate reactive oxygen species in the cancer that the complexes generate reactive oxygen species in the cancer cells, inducing apoptosis cells, inducing apoptosis and leading to cell death [17]. Despite the negligible cytotoxic ef- and leading to cell death [17]. Despite the negligible cytotoxic effects of varying the fects of varying the diimine ligand in such complexes, diimines have important roles in the diimine ligand in such complexes, diimines have important roles in the complex-DNA complex-DNA interactions. For example, biquinoline-containing complexes are proposed interactions. For example, biquinoline-containing complexes are proposed to bind via in- to bind via intercalation, while groove-binding was suggested for the complexes with a tercalation, while groove-binding was suggested for the complexes with a 2,9-dime- 2,9-dimethylphenanthroline ligand [17,18]. Complexes [CuBr(1,10-phenanthroline)(PPh3)] thylphenanthroline ligand [17,18]. Complexes [CuBr(1,10-phenanthroline)(PPh+ 3)] and and [Cu(1,10-phenanthroline)(P(4-methoxyphenyl)3)2]
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