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The FMO2 analysis of the ligand-receptor binding energy: the Biscarbene-Gold(I)/DNA G-Quadruplex case study

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Abstract

In this work, the ab initio fragment molecular orbital (FMO) method was applied to calculate and analyze the binding energy of two biscarbene-Au(I) derivatives, [Au(9-methylcaffein-8-ylidene)2]+ and [Au(1,3-dimethylbenzimidazol-2-ylidene)2]+, to the DNA G-Quadruplex structure. The FMO2 binding energy considers the ligand-receptor complex as well as the isolated forms of energy-minimum state of ligand and receptor, providing a better description of ligand-receptor affinity compared with simple pair interaction energies (PIE). Our results highlight important features of the binding process of biscarbene-Au(I) derivatives to DNA G-Quadruplex, indicating that the total deformation-polarization energy and desolvation penalty of the ligands are the main terms destabilizing the binding. The pair interaction energy decomposition analysis (PIEDA) between ligand and nucleobases suggest that the main interaction terms are electrostatic and charge-transfer energies supporting the hypothesis that Au(I) ion can be involved in π-cation interactions further stabilizing the ligand-receptor complex. Moreover, the presence of polar groups on the carbene ring, as C = O, can improve the charge-transfer interaction with K+ ion. These findings can be employed to design new powerful biscarbene-Au(I) DNA-G quadruplex binders as promising anticancer drugs. The procedure described in this work can be applied to investigate any ligand-receptor system and is particularly useful when the binding process is strongly characterized by polarization, charge-transfer and dispersion interactions, properly evaluated by ab initio methods.

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Data availability

The 3D coordinates of Gq, Gq-13, Gq-1(I), Gq-1(II), Gq-1(III), Gq-2(I), Gq-1(II), Gq-2(III), ligands 1 and 2 structures reported in this study are also available in the pdb and xyz file formats at the following link https://doi.org/10.5281/zenodo.7102260.

Abbreviations

CADD:

Computer-assisted drug discovery

Gq:

G-quadruplex

DNA:

Deoxyribonucleic acid;

FF:

Force field

FE:

Fragment efficiency

FMO:

Fragment molecular orbital method

FRET:

Fluorescence resonance energy transfer assay

F2LE:

FMO2 ligand efficiency

L:

Ligand

LR:

Ligand-receptor complex

MD:

Molecular dynamics

MEP:

Molecular electrostatic potential

MM:

Molecular mechanics

MM/GBSA:

Molecular mechanics/generalized Born surface area method

MM/PBSA:

Molecular mechanics/ Poisson-Boltzmann surface area method

PIE:

Pair interaction energy

PIEDA:

Pair interaction energy decomposition analysis

QM:

Quantum mechanics

R:

Receptor

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Acknowledgements

We are thankful to Loriano Storchi of the Department of Pharmacy for computer support.

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No funding was received to assist with the preparation of this manuscript.

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Authors and Affiliations

  1. Department of Pharmacy, Università “G. D’Annunzio” Di Chieti-Pescara, Chieti, Italy

    Roberto Paciotti, Cecilia Coletti, Alessandro Marrone & Nazzareno Re

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  1. Roberto Paciotti
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  2. Cecilia Coletti
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  3. Alessandro Marrone
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  4. Nazzareno Re
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Conceptualization: RP; Formal analysis and investigation: RP; Writing—original draft preparation: RP; Writing—review and editing: CC, AM, NR, RP; Supervision: NR. All authors read and approved the final manuscript.

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Correspondence to Roberto Paciotti.

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Paciotti, R., Coletti, C., Marrone, A. et al. The FMO2 analysis of the ligand-receptor binding energy: the Biscarbene-Gold(I)/DNA G-Quadruplex case study. J Comput Aided Mol Des 36, 851–866 (2022). https://doi.org/10.1007/s10822-022-00484-z

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