Dept. of Cell Culture - Molecular Modeling & Drug Design, Symeonidion

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Dept. of Cell Culture - Molecular Modeling & Drug Design, Symeonidion Research Center, Theagenion Cancer Hospital, Thessaloniki, Greece 2 1 Department of Chemistry, Aristotle University, Thessaloniki, Greece Understanding the molecular basis of a drug action and exploring the chemical interactions involved in the complex processes of drug delivery and reaction with a variety of biological molecules, are among the most important goals of contemporary drug design. We have thus developed a copper (II) chelate complex of the formula Cu(SalNEt2)citrate, where SalNEt2 stands for the anion of the N-(2-(diethylamino)ethyl)salicylidenaminato (Figure 1). We have focused in one hand in the study of the possible anticancer activity of the compound through in vitro experiments, and in the other hand, in the theoretical study of this complex and its binding to various biological molecules. In previous experiments, this complex has shown a potent cytotoxic activity against a panel of human cancer cell lines. Micromolar concentrations could induce inhibition of cellular growth, apoptotic cell death via DNA fragmentation and blocking of cells in the cell cycle. In the present study, molecular modeling computations, incorporating molecular docking approaches, have been adopted, in order to investigate the hypothesis that the mechanism of action of this complex involves binding to DNA and RNA and also interference in the signal transduction pathway of DNA topoisomerases I and II. Our in vitro results revealed that Cu(SalNEt2)Citrate complex, caused a dose-dependent inhibition of cell proliferation. The found IC50 values (microg/ml) are: 68.8 (HeLa), 52.5 (HT29), 64.0 (L929), 156.0 (A-549) and 98.0 (SK-N-MC). The elucidation of Cu(SalNEt2)Citrate’s molecular mechanism of action regarding DNA topoisomerase pathway was attempted via molecular docking studies with the crystallographic structures of the proteins. Cu(SalNEt2)Citrate complex found to be positioned inside the binding cavity of both proteins. Some of the best possible binding modes of copper (II) complex in DNA topo I & II are displayed in Figures 2-11. The interactions between Cu(SalNEt2)Citrate complex and DNA topo I are mainly governed by hydrogen bonds and polar contacts with residues Asn722 [(3.84 Å: carbonyl O (Asn)-H1/carboxyl, 3.55 Å: N (side chain Asn)-O1/carboxyl, 4.21 Å: N (side chain Asn)-H1/carboxyl)], Thr718 (3.53 Å between OG1 of the amino acid and the adjacent to Cu atom carbonyl O), and Glu332 (3.12 Å: N (side chain Glu)-H/hydroxyl. Furthermore, the Cu-citrate complex interacted with nucleobases G12 (4.11 Å: O/carboxyl of G12-H2/carboxyl), T10 (3.81Å: O1 of T10-carbonyl O adjacent to Cu & 4.20 Å: O2 of T10-H1/hydroxyl). Binding with DNA to II, are mediated through residues Glu31 (2.17, 2.79 Å between hydroxyl O of Glu & H or O/hydroxyl, respectively), also Glu31 (4.12 Å: side chain N of Glu & H/hydroxyl), Tyr186 (3.48, 3.31 Å: aromatic O of Tyr-carboxylic O1, O2), Lys131 (3.52, 3.40, 3.08, 3.21, 3.54 Å between side chain N of Lys and H1, H2, O1, O2, salicylate O of complex), Glu185 (4.12 Å: O carboxyl of Glu-H2), and Val30 (3.67 Å: side chain N of Val- H/hydroxyl). Hydrophobic contacts are mediated through C112 & Cu-citrate complex (2.81 Å). The aim of this study was to investigate the in vitro activity of Cu(SalNEt2)citrate, against a panel of 4 human cancer cell lines: HeLa (cervical), HT29 (colon), A-549 (lung) and SK-N-MC (neuroblastoma) and one normal mouse fibroblast (L929) cell line. Experiments were performed on cells grown in adherence in 96-well microplates and cytotoxicity was evaluated by means of SRB, XTT, WST-1 and BrdU metabolic assays. The drug concentrations that induce cytotoxicity on 50% of cells (IC50) were calculated for each cell line (Table I, Figure 2). Beyond the in vitro activity assessment of this compound, we aimed at the elucidation of the underlying mechanism of action carrying out molecular docking calculations via BioMedCaChe program, which is part of the CaChe package. The molecule was built in 3D coordinates and its best (lower energy) conformation was detected, by geometrical optimization of its structure as implemented in the same molecular modeling program suite. Geometry optimization was accomplished via PM3 semi-empirical calculations. To identify molecular determinants responsible for the binding mode of this molecule, we have used in our calculations the determined X-ray crystal structures of human DNA topoisomerases I (2.1 Å resolution, PDB entry code: 1K4T) & II (2.51 Å resolution, PDB entry code: 1ZXN), obtained from the Brookhaven Protein Data Bank (RCSB). Undertaken docking approach could be informative in pointing out the mechanism of action of the complex in a molecular level. Docking studies revealed the functional role of residues ASN722, GLU332 and Thr718, and nucleobases G12, T9, T10 and C112 in DNA topo I, and residues GLU31, TYR186, LYS131, GLU185 and VAL30 in DNA topo II, for Cu(SalNEt2)Citrate complexation with the proteins. These findings represent a prompting to search systematically for the possible interaction of the complex with other cellular elements in signal transduction which are of fundamental importance in cell proliferation. New insights in the mechanism of interaction may come into light through further molecular modeling experimentation which are underway. Cu(SalNEt2)citrate docked onto DNA topo IIA ATPase-ADP (1ZXN) (solid surface colored by chainbow, copper complex is represented in CPK spheres) Cu(SalNEt2)citrate complex docked into DNA topo I (1K4T). The molecule which is bound in the ligand binding cavity is shown in stick respresentation, while helices are depicted as cartoons colored by chain Cu(SalNEt2)citrate complex docked into DNA topo I (1K4T). Cu(SalNEt2) citrate is shown in stick respresentation, while protein is depicted as ribbons Cu(SalNEt2)citrate (depicted as stick) docked onto DNA topo I (solid protein & DNA surface) Cu(SalNEt2)citrate molecular structure Cu(SalNEt2)citrate (depicted as stick) docked onto DNA topo I (semitransparent protein & DNA surface Cu(SalNEt2)citrate (in stick) docked with target 1K4T (human DNA topo I without bound TPT). A close up view of the ligand binding cavity of the protein (represented as solid surface colored by chain) Binding interactions between Cu(SalNEt2) citrate and the aminoacids of the binding site of DNA topo II A close up view of the ligand binding pocket of Cu(SalNEt2)citrate complex docked into DNA topo I (1K4T). Cu(SalNEt2)citrate is shown in stick respresentation, while the binding site is illustrated as a mesh surface Cu(SalNEt2)citrate docked onto DNA topo IIA ATPase-ADP (helices are represented as cartoon, and colored according to secondary structure (helix: red, sheet: yellow, loop: green) Dose-effect curves of Cu(SalNEt2)citrate complex against a panel of cell lines Cu(SalNEt2)Citrate concentration (microg/ml) Survival Fraction (SF) Top view of Cu(SalNEt2)citrate complex docked into DNA topo I