DFT studies of camptothecins cytotoxicity III: camptothecin, irinotecan and SN-38

Štekláč, Marek; Breza, Martin

doi:10.2478/acs-2022-0009

Abstract

Geometries of camptothecin, irinotecan, SN-38, and of their hypothetical Cu(II) complexes were optimized at the B3LYP/6-311G* level of theory. Their electron structure, evaluated in terms of Mulliken population analysis and Quantum Theory of Atoms-in-Molecule, was subsequently related to in vitro cytotoxicity. Electron density transfer from the relevant active sites to Cu decreases in the sequence irinotecan > SN-38 > camptothecin. The absolute values of their metal-ligand interaction energies exhibit the same trend. Discrepancy with the least relative in vitro cytotoxicity of irinotecan can be explained by differences in its pharmacokinetics.

References

Alagona G, Ghio C (2009) Antioxidant Properties of Pterocarpans through Their Copper(II) Coordination Ability. A DFT Study in Vacuo and in Aqueous Solution. J Phys Chem A 113: 15206—15216.10.1021/jp905521u19831341
Search in Google Scholar Back to article
Alagona G, Ghio C (2009a) Plicatin B conformational landscape and affinity to copper (I and II) metal cations. A DFT study. Phys Chem Chem Phys 11: 776—790.10.1039/B813464B19290324
Search in Google Scholar Back to article
Babu PC, Sundaraganesan N, Sudha S, Aroulmoji V, Murano E (2012) Molecular structure and vibrational spectra of Irinotecan: A density functional theoretical study. Spectrochim Acta A 98: 1—6.10.1016/j.saa.2012.08.00522982380
Search in Google Scholar Back to article
Bader RFW (1990) Atoms in Molecules: A Quantum Theory. Claredon Press, Oxford.
Search in Google Scholar Back to article
Bailly Ch (2019) Irinotecan: 25 years of cancer treatment. Pharmacol Res 148: 104398.10.1016/j.phrs.2019.10439831415916
Search in Google Scholar Back to article
Becke AD (1993) Density-functional thermochemistry. III. The role of exact exchange. J Chem Phys 98: 5648—5652.10.1063/1.464913
Search in Google Scholar Back to article
Biegler-Konig F, Schonbohm J, Bayles D (2001) AIM2000 — A Program to Analyze and Visualize Atoms in Molecules. J Comput Chem 22: 545—559.
Search in Google Scholar Back to article
Breza M (2018) DFT studies of camptothecin aggregation in solutions. Comp Theor Chem 1143: 1—8.10.1016/j.comptc.2018.09.008
Search in Google Scholar Back to article
Breza M (2021) Quantum-chemical studies of rutile nanoparticles toxicity II. Comparison of B3LYP and PM6 data. Acta Chim Slovaca 14: 38—50.10.2478/acs-2021-0006
Search in Google Scholar Back to article
Breza M, Simon P (2019) Quantum-chemical studies of rutile nanoparticles toxicity I. Defect-free rod-like model clusters. Acta Chim Slovaca 12: 168—174.10.2478/acs-2019-0023
Search in Google Scholar Back to article
Breza M, Simon P (2020) On shape dependence of the toxicity of rutile nanoparticles. J Nanopart Res 22: 0058.10.1007/s11051-020-4773-1
Search in Google Scholar Back to article
Bruns RE, Haidukea RLA, do Amaral AT (2002) The Linear Relationship Between Koopmans’ and Hydrogen Bond Energies for some Simple Carbonyl Molecules. J Braz Chem Soc 13: 800—805.10.1590/S0103-50532002000600011
Search in Google Scholar Back to article
Carbonero RG, Supko JG (2002) Current Perspectives on the Clinical Experience, Pharmacology, and Continued Development of the Camptothecins. Clin Cancer Res 8: 641—661.
Search in Google Scholar Back to article
Dvoranova D, Bobenicova M, Soralova S, Breza M (2013) On UV-Vis spectra and structure of the anticancer drug camptothecin in solutions. Chem Phys Let 580: 141—144.10.1016/j.cplett.2013.07.001
Search in Google Scholar Back to article
Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR et al. (2013) Gaussian 09, Revision D.01, Gaussian, Inc., Wallingford, CT.
Search in Google Scholar Back to article
Hsiang YH, Liu LF (1988) Identification of Mammalian DNA Topoisomerase I as an Intracellular Target of the Anticancer Drug Camptothecin. Cancer Res 48: 1722—1726.
Search in Google Scholar Back to article
Hussain I, Bania KK, Gour NK, Deka RC (2016) Application of Physicochemical and DFT Based Descriptors for QSAR Study of Camptothecin Derivatives. ChemistrySelect 1: 4973—4978.10.1002/slct.201600609
Search in Google Scholar Back to article
Ivanova B, Spiteller M (2012) Physical Properties and Molecular Conformations of Indole Alkaloids and Model Protein Interactions — Theoretical vs. Experimental Study. Natural Products Commun 7: 157—164.10.1177/1934578X1200700206
Search in Google Scholar Back to article
Ivanova B, Spiteller M (2012a) Structure and Properties of Camptothecin Derivatives, Their Protonated Forms, and Model Interaction with the Topoisomerase I–DNA Complex. Biopolymers 97: 134—144.10.1002/bip.2171421898362
Search in Google Scholar Back to article
Ivanova B, Spiteller M (2012b) Experimental and theoretical spectroscopic and structural study of A-ring substituted camptothecins. J Mol Struct 1012: 189—197.10.1016/j.molstruc.2012.01.001
Search in Google Scholar Back to article
Jelemenska I, Breza M (2021) Comparative DFT study of the effectiveness of p-phenylenediamine antioxidants through their coordination ability towards the late 1st row transition metals. Polym Degrad Stab 183: 109438.10.1016/j.polymdegradstab.2020.109438
Search in Google Scholar Back to article
Jena NR, Mishra PC (2007) A theoretical study of some new analogues of the anti-cancer drug camptothecin. J Mol Model 13: 267—274.
Search in Google Scholar Back to article
Kabanda MM, Tran VT, Seema KM, Serobatse KRN, Tsiepe TJ, Tran QT, Ebenso EE (2014) Conformational, electronic and antioxidant properties of lucidone, linderone and methyllinderone: DFT, QTAIM and NBO studies. Mol Phys 113: 683—697.10.1080/00268976.2014.969343
Search in Google Scholar Back to article
Keith TA (2017) AIMAll, Version 17.11.14, TK Gristmill Software Overland Park, KS. Available from aim. tkgristmill.com.
Search in Google Scholar Back to article
Khaiwa N, Maarouf NR, Darwish MH, Alhamad DWM, Sebastian A, Hamad M, Omar HA, Orive G, Al-Tel TH (2021) Camptothecin’s journey from discovery to WHO Essential Medicine: Fifty years of promise. Eur J Med Chem 223: 113639.10.1016/j.ejmech.2021.11363934175539
Search in Google Scholar Back to article
Kochanek SE, Clymer TM, Pakkala VS, Hebert SP, Reeping K, Firestine SM, Evanseck JD (2015) Intramolecular Charge-Assisted Hydrogen Bond Strength in Pseudochair Carboxyphosphate. J Phys Chem B 119: 1184—1191.10.1021/jp506796r430650025405523
Search in Google Scholar Back to article
Kohn KW, Pommier Y (2000) Molecular and biological determinants of the cytotoxic actions of camptothecins: perspective for the development of new topoisomerase I inhibitors. Ann N Y Acad Sci 922: 11—26.
Search in Google Scholar Back to article
Kostjukov VV (2021) Theoretical analysis of lactone and carboxylate forms of camptothecin in aqueous solution: Electronic states, absorption spectra, and hydration. J Mol Liquids 344: 117804.10.1016/j.molliq.2021.117804
Search in Google Scholar Back to article
Liao H-Y, Chu S-Y (2015) Hydrogen bond acceptor capability of carbonyl p-electrons — case study of the hydrogen-bonded urea dimer. J Phys Chem B 119: 1184—1191.
Search in Google Scholar Back to article
Lu W, Wang Y, Wang L, Zhao F, Yang Sh, Xi Ch, Yang Y, Xu L, Chi X (2018) Synthesis, crystal structure and antitumor activities of water soluble protonated salt of 20(S)-camptothecin. J Mol Struct 1155: 623—627.10.1016/j.molstruc.2017.10.113
Search in Google Scholar Back to article
Mammino L (2013) Investigation of the antioxidant properties of hyperjovinol A through its Cu(II) coordination ability. J Mol Model 19: 2127—2142.10.1007/s00894-012-1684-923212237
Search in Google Scholar Back to article
Mi Z, Burke TG (1994) Differential Interactions of Camptothecin Lactone and Carboxylate Forms with Human Blood Components. Biochemistry 33: 10325—10336.10.1021/bi00200a0138068669
Search in Google Scholar Back to article
Mulliken RS (1955) Electronic Population Analysis on LCAO-MO Molecular Wave Functions. J Phys Chem 23: 1833—1840.10.1063/1.1740588
Search in Google Scholar Back to article
Mulliken RS (1955a) Electronic population analysis on LCAO-MO molecular wave functions 2. Overlap populations, bond orders, and covalent bond energies. J Phys Chem 23: 1841—1846.10.1063/1.1740589
Search in Google Scholar Back to article
Puskarova I, Breza M (2016) DFT studies of the effectiveness of p-phenylenediamine antioxidants through their Cu(II) coordination ability. Polym Degrad Stab 128: 15—21.10.1016/j.polymdegradstab.2016.02.028
Search in Google Scholar Back to article
Puskarova I, Breza M (2017) DFT studies of the effectiveness of p-substituted diphenyl amine antioxidants in styrene-butadiene rubber through their Cu(II) coordination ability. Chem Phys Let 680: 78—82.10.1016/j.cplett.2017.05.036
Search in Google Scholar Back to article
Redinbo MR, Stewart L, Kuhn P, Champoux JJ, Hol WGJ (1998) Crystal structure of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 279: 1504—1513.10.1126/science.279.5356.15049488644
Search in Google Scholar Back to article
Sanna N, Chillemi G, Gontrani L, Grandi A, Mancini G, Castelli S, Zagotto G, Zazza C, Barone V, Desideri A (2009) UV-Vis Spectra of the Anticancer Campothecin Family Drugs in Aqueous Solution: Specific Spectroscopic Signatures Unraveled by a Combined Computational and Experimental Study. J Phys Chem B 113: 5369—5375.10.1021/jp809801y19334673
Search in Google Scholar Back to article
Serobatse KRN, Kabanda MM (2016) Antioxidant and antimalarial properties of butein and homobutein based on their ability to chelate iron (II and III) cations: a DFT study in vacuo and in solution. Eur Food Res Technol 242: 71—90.10.1007/s00217-015-2520-0
Search in Google Scholar Back to article
Serobatse KRN, Kabanda MM (2016a) A theoretical study on the antioxidant properties of methoxy-substituted chalcone derivatives: A case study of kanakugiol and pedicellin through their Fe (II and III) coordination ability. J Theor Comput Chem 15: 1650048.10.1142/S0219633616500486
Search in Google Scholar Back to article
Staker BL, Feese MD, Cushman M, Pommier Y, Zembower D, Stewart L, Burgin AB (2005) Structures of Three Classes of Anticancer Agents Bound to the Human Topoisomerase I-DNA Covalent Complex. J Med Chem 48: 2336—2345.10.1021/jm049146p15801827
Search in Google Scholar Back to article
Steklac M, Breza M (2018) Quantum-chemical study of the active sites of camptothecin through their Cu(II) coordination ability. Acta Chim Slovaca 11: 6—10.10.2478/acs-2018-0002
Search in Google Scholar Back to article
Steklac M, Breza M (2021) DFT studies of camptothecins cytotoxicity I. Active and inactive forms of camptothecin. Comput Theor Chem 1206: 113461.10.1016/j.comptc.2021.113461
Search in Google Scholar Back to article
Steklac M, Breza M (2021a) DFT studies of the toxicity of alkylphenols to Tetrahymena pyriformis. Polyhedron 207: 115360.10.1016/j.poly.2021.115360
Search in Google Scholar Back to article
Steklac M, Breza M (2021b) DFT Studies of Substituted Phenols Cytotoxicity I. Para-substituted Phenols. ChemistrySelect 6: 7049—7055.10.1002/slct.202101568
Search in Google Scholar Back to article
Steklac M, Breza M (2021c) DFT studies of the toxicity of 4-substituted 1,2-benzoquinones. Polyhedron 210: 115532.10.1016/j.poly.2021.115532
Search in Google Scholar Back to article
Steklac M, Breza M (2022) DFT studies of camptothecins cytotoxicity II. Protonated lactone forms of camptothecin. Comput Theor Chem 1211: 113677.10.1016/j.comptc.2022.113677
Search in Google Scholar Back to article
Subramanian N, Sundaraganesan N, Sudha S, Aroulmoji V, Sockalingam GD, Bergamin M (2011) Experimental and theoretical investigation of the molecular and electronic structure of anticancer drug camptothecin. Spectrochim Acta A 78: 1058—1067.10.1016/j.saa.2010.12.04921233010
Search in Google Scholar Back to article
Tanizawa A, Fujimori A, Fujimori Y, Pommier Y (1994) Comparison of Topoisomerase I Inhibition, DNA Damage, and Cytotoxicity of Camptothecin Derivatives Presently in Clinical Trials. J Natl Cancer Inst 86: 836—842.10.1093/jnci/86.11.8368182764
Search in Google Scholar Back to article
Tsiepe TJ, Kabanda MM, Serobatse KRN (2015) Antioxidant Properties of Kanakugiol Revealed Through the Hydrogen Atom Transfer, Electron Transfer and M2+ (M2+ = Cu(II) or Co(II) Ion) Coordination Ability Mechanisms. A DFT Study In Vacuo and in Solution. Food Biophys 10: 342—359.10.1007/s11483-015-9397-0
Search in Google Scholar Back to article
Ugliengo P (2006) MOLDRAW: A Program to Display and Manipulate Molecular and Crystal Structures. University Torino, Torino. Available from: www.moldraw.software.informer.com.
Search in Google Scholar Back to article
Urbic T (2014) Ions increase strength of hydrogen bond in water. Chem Phys Lett 610-611: 159—162.10.1016/j.cplett.2014.06.054417543525267857
Search in Google Scholar Back to article
Wall ME, Wani MC, Cook CE, Palmer KH, McPhail HT, Sim GA (1966) Plant Antitumor Agents I. The Isolation and Structure of Camptothecin, a Novel Alkaloidal Leukemia and Tumor Inhibitor from Camptotheca acuminate. J Am Chem Soc. 88: 3888—3890.10.1021/ja00968a057
Search in Google Scholar Back to article
Zhou HY, Zhao DX, Yang ZZ (2013) A theoretical study on mechanism of the anticancer drug camptothecin’s E-ring-opening. J Mol Grahics Model 43: 58—65.10.1016/j.jmgm.2013.03.00423727896
Search in Google Scholar Back to article

DFT studies of camptothecins cytotoxicity III: camptothecin, irinotecan and SN-38

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