Molecular mechanism and binding free energy of doxorubicin intercalation in DNA

Jawad, Bahaa; Poudel, Lokendra; Podgornik, Rudolf; Steinmetz, Nicole F.; Ching, Wai -Yim

doi:10.1039/c8cp06776g

Title: Molecular mechanism and binding free energy of doxorubicin intercalation in DNA

Journal Article · Fri Jan 18 00:00:00 EST 2019 · Physical Chemistry Chemical Physics. PCCP

DOI:https://doi.org/10.1039/c8cp06776g· OSTI ID:1543801

Jawad, Bahaa ^[1]; Poudel, Lokendra ^[2]; Podgornik, Rudolf ^[3]; Steinmetz, Nicole F. ^[4];

^[2]

Univ. of Missouri-Kansas City, Kansas City, MO (United States); Univ. of Technology, Baghdad (Iraq)
Univ. of Missouri-Kansas City, Kansas City, MO (United States)
Univ. of Chinese Academy of Sciences, Beijing (China); Chinese Academy of Sciences, Beijing (China)
Univ. of California-San Diego, La Jolla, CA (United States)

The intercalation process of binding doxorubicin (DOX) in DNA is studied by extensive MD simulations. Many molecular factors that control the binding affinity of DOX to DNA to form a stable complex are inspected and quantified by employing continuum solvation models for estimating the binding free energy. The modified MM-PB(GB)SA methodology provides a complete energetic profile of ΔG_ele, ΔG_vDW, ΔG_polar, ΔG_non-polar, TΔS_total, ΔG_deform, ΔG_con, and ΔG_ion. To identify the sequence specificity of DOX, two different DNA sequences, d(CGATCG) or DNA1 and d(CGTACG) or DNA2, with one molecule (1 : 1 complex) or two molecule (2 : 1 complex) configurations of DOX were selected in this study. Our results show that the DNA deformation energy (ΔG_deform), the energy cost from translational and rotational entropic contributions (TΔS_tran+rot), the total electrostatic interactions (ΔG_polar-PB/GB + ΔG_ele) of incorporation, the intramolecular electrostatic interactions (ΔG_ele) and electrostatic polar solvation interactions (ΔG_polar-PB/GB) are all unfavorable to the binding of DOX to DNA. However, they are overcome by at least five favorable interactions: the van der Waals interactions (ΔG_vDW), the non-polar solvation interaction (ΔG_non-polar), the vibrational entropic contribution (TΔS_vib), and the standard concentration dependent free energies of DOX (ΔG_con) and the ionic solution (ΔG_ion). Specifically, the van der Waals interaction appears to be the major driving force to form a stable DOX–DNA complex. We also predict that DOX has stronger binding to DNA1 than DNA2. The DNA deformation penalty and entropy cost in the 2 : 1 complex are less than those in the 1 : 1 complex, thus they indicate that the 2 : 1 complex is more stable than the 1 : 1 complex. Here, we have calculated the total binding free energy (BFE) (ΔG_t-sim) using both MM-PBSA and MM-GBSA methods, which suggests a more stable DOX–DNA complex at lower ionic concentration. The calculated BFE from the modified MM-GBSA method for DOX–DNA1 and DOX–DNA2 in the 1 : 1 complex is –9.1 and –5.1 kcal mol^–1 respectively. The same quantities from the modified MM-PBSA method are –12.74 and –8.35 kcal mol^–1 respectively. The value of the total BFE ΔG_t-sim in the 1 : 1 complex is in reasonable agreement with the experimental value of –7.7 ± 0.3 kcal mol^–1.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, San Diego, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC03-76SF00098

OSTI ID:: 1543801

Journal Information:: Physical Chemistry Chemical Physics. PCCP, Vol. 21, Issue 7; ISSN 1463-9076

Publisher:: Royal Society of ChemistryCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 61 works

Citation information provided by
Web of Science

References (97)

Kinetics of the daunomycin-DNA interaction Chaires, Jonathan B.; Dattagupta, Nanibhushan; Crothers, Donald M. Biochemistry, Vol. 24, Issue 2 https://doi.org/10.1021/bi00323a004	journal	January 1985
Intercalation of Daunomycin into Stacked DNA Base Pairs. DFT Study of an Anticancer Drug Barone, Giampaolo; Guerra, Célia Fonseca; Gambino, Noemi Journal of Biomolecular Structure and Dynamics, Vol. 26, Issue 1 https://doi.org/10.1080/07391102.2008.10507229	journal	August 2008
MMPBSA.py : An Efficient Program for End-State Free Energy Calculations Miller, Bill R.; McGee, T. Dwight; Swails, Jason M. Journal of Chemical Theory and Computation, Vol. 8, Issue 9 https://doi.org/10.1021/ct300418h	journal	August 2012
Free energy calculation on base specificity of drug - DNA interactions: Application to daunomycin and acridine intercalation into DNA Cieplak, Piotr; Rao, Shashidhar N.; Grootenhuis, Peter D. J. Biopolymers, Vol. 29, Issue 4-5 https://doi.org/10.1002/bip.360290406	journal	March 1990
Kinetic studies of anthracycline-DNA interaction by fluorescence stopped flow confirm a complex association mechanism Rizzo, Vincenzo; Sacchi, Nereo; Menozzi, Milena Biochemistry, Vol. 28, Issue 1 https://doi.org/10.1021/bi00427a038	journal	January 1989
Intercalation of antitumor drug doxorubicin and its analogue by DNA duplex: Structural features and biological implications Agudelo, Daniel; Bourassa, Philippe; Bérubé, Gervais International Journal of Biological Macromolecules, Vol. 66 https://doi.org/10.1016/j.ijbiomac.2014.02.028	journal	May 2014
Rigorous Free Energy Calculations in Structure-Based Drug Design Michel , Julien; Foloppe, Nicolas; Essex, Jonathan W. Molecular Informatics, Vol. 29, Issue 8-9 https://doi.org/10.1002/minf.201000051	journal	July 2010
pH-controlled doxorubicin anticancer loading and release from carbon nanotube noncovalently modified by chitosan: MD simulations Rungnim, Chompoonut; Rungrotmongkol, Thanyada; Poo-arporn, Rungtiva P. Journal of Molecular Graphics and Modelling, Vol. 70 https://doi.org/10.1016/j.jmgm.2016.09.011	journal	November 2016
Interactions between an anthracycline antibiotic and DNA: molecular structure of daunomycin complexed to d(CpGpTpApCpG) at 1.2-.ANG. resolution Wang, Andrew H. J.; Ughetto, Giovanni; Quigley, Gary J. Biochemistry, Vol. 26, Issue 4 https://doi.org/10.1021/bi00378a025	journal	February 1987
Unravelling Hot Spots: a comprehensive computational mutagenesis study Moreira, Irina S.; Fernandes, Pedro A.; Ramos, Maria J. Theoretical Chemistry Accounts, Vol. 117, Issue 1 https://doi.org/10.1007/s00214-006-0151-z	journal	July 2006
Analysis of cooperativity and ion effects in the interaction of quinacrine with DNA Wilson, W. David; Lopp, Irene G. Biopolymers, Vol. 18, Issue 12 https://doi.org/10.1002/bip.1979.360181210	journal	December 1979
A review of methods for the calculation of solution free energies and the modelling of systems in solution Skyner, R. E.; McDonagh, J. L.; Groom, C. R. Physical Chemistry Chemical Physics, Vol. 17, Issue 9 https://doi.org/10.1039/C5CP00288E	journal	January 2015
Molecular Mechanism of MBX2319 Inhibition of Escherichia coli AcrB Multidrug Efflux Pump and Comparison with Other Inhibitors Vargiu, Attilio V.; Ruggerone, Paolo; Opperman, Timothy J. Antimicrobial Agents and Chemotherapy, Vol. 58, Issue 10 https://doi.org/10.1128/AAC.03283-14	journal	August 2014
Studies on interaction of anthracycline antibiotics and deoxyribonucleic acid: equilibrium binding studies on the interaction of daunomycin with deoxyribonucleic acid Chaires, Jonathan B.; Dattagupta, Nanibhushan; Crothers, Donald M. Biochemistry, Vol. 21, Issue 17 https://doi.org/10.1021/bi00260a005	journal	August 1982
Accurate Estimation of the Standard Binding Free Energy of Netropsin with DNA Zhang, Hong; Gattuso, Hugo; Dumont, Elise Molecules, Vol. 23, Issue 2 https://doi.org/10.3390/molecules23020228	journal	January 2018
Energetics of drug–DNA interactions Chaires, Jonathan B. Biopolymers, Vol. 44, Issue 3 https://doi.org/10.1002/(SICI)1097-0282(1997)44:3<201::AID-BIP2>3.0.CO;2-Z	journal	January 1997
Restrained molecular dynamics studies on complex of adriamycin with DNA hexamer sequence d-CGATCG Jain, Monica; Barthwal, Sudhir Kumar; Barthwal, Ritu Archives of Biochemistry and Biophysics, Vol. 439, Issue 1 https://doi.org/10.1016/j.abb.2005.05.009	journal	July 2005
A Computational Model for Anthracycline Binding to DNA: Tuning Groove-Binding Intercalators for Specific Sequences Cashman, Derek J.; Kellogg, Glen E. Journal of Medicinal Chemistry, Vol. 47, Issue 6 https://doi.org/10.1021/jm030529h	journal	March 2004
Sequence-selective DNA recognition by synthetic ligands Nielsen, Peter E. Bioconjugate Chemistry, Vol. 2, Issue 1 https://doi.org/10.1021/bc00007a001	journal	January 1991
Energetics of intercalation specificity. I. Backbone unwinding Ornstein, Rick L.; Rein, Robert Biopolymers, Vol. 18, Issue 5 https://doi.org/10.1002/bip.1979.360180517	journal	May 1979
Predicted mode of intercalation of doxorubicin with dinucleotide dimers Nakata, Y.; Hopfinger, A. J. Biochemical and Biophysical Research Communications, Vol. 95, Issue 2 https://doi.org/10.1016/0006-291X(80)90824-4	journal	July 1980
Early stage intercalation of doxorubicin to DNA fragments observed in molecular dynamics binding simulations Lei, Hongxing; Wang, Xiaofeng; Wu, Chun Journal of Molecular Graphics and Modelling, Vol. 38 https://doi.org/10.1016/j.jmgm.2012.05.006	journal	September 2012
Free Energy Simulations Mezei, M.; Beveridge, D. L. Annals of the New York Academy of Sciences, Vol. 482, Issue 1 Computer Simu https://doi.org/10.1111/j.1749-6632.1986.tb20933.x	journal	December 1986
Assessing the Performance of MM/PBSA and MM/GBSA Methods. 3. The Impact of Force Fields and Ligand Charge Models Xu, Lei; Sun, Huiyong; Li, Youyong The Journal of Physical Chemistry B, Vol. 117, Issue 28 https://doi.org/10.1021/jp404160y	journal	July 2013
Assessing the performance of MM/PBSA and MM/GBSA methods. 7. Entropy effects on the performance of end-point binding free energy calculation approaches Sun, Huiyong; Duan, Lili; Chen, Fu Physical Chemistry Chemical Physics, Vol. 20, Issue 21 https://doi.org/10.1039/C7CP07623A	journal	January 2018
Doxorubicin as a Molecular Nanotheranostic Agent: Effect of Doxorubicin Encapsulation in Micelles or Nanoemulsions on the Ultrasound-Mediated Intracellular Delivery and Nuclear Trafficking Mohan, Praveena; Rapoport, Natalya Molecular Pharmaceutics, Vol. 7, Issue 6 https://doi.org/10.1021/mp100269f	journal	September 2010
The intercalation of DNA double helices with doxorubicin and nagalomycin Box, Vernon G. S. Journal of Molecular Graphics and Modelling, Vol. 26, Issue 1 https://doi.org/10.1016/j.jmgm.2006.09.005	journal	July 2007
Nanopore Single-Molecule Analysis of DNA–Doxorubicin Interactions Yao, Fujun; Duan, Jing; Wang, Ying Analytical Chemistry, Vol. 87, Issue 1 https://doi.org/10.1021/ac503926g	journal	December 2014
Conformational diversity of anthracycline anticancer antibiotics: A density functional theory calculation Zhu, Suhua; Yan, Liuming; Ji, Xiaobo Journal of Molecular Structure: THEOCHEM, Vol. 951, Issue 1-3 https://doi.org/10.1016/j.theochem.2010.04.008	journal	July 2010
Electronic Structure and Partial Charge Distribution of Doxorubicin in Different Molecular Environments Poudel, Lokendra; Wen, Amy M.; French , Roger H. ChemPhysChem, Vol. 16, Issue 7 https://doi.org/10.1002/cphc.201402893	journal	February 2015
The statistical-thermodynamic basis for computation of binding affinities: a critical review Gilson, M. K.; Given, J. A.; Bush, B. L. Biophysical Journal, Vol. 72, Issue 3 https://doi.org/10.1016/S0006-3495(97)78756-3	journal	March 1997
Free Energy Calculations by the Molecular Mechanics Poisson−Boltzmann Surface Area Method Homeyer, Nadine; Gohlke, Holger Molecular Informatics, Vol. 31, Issue 2 https://doi.org/10.1002/minf.201100135	journal	January 2012
Molecular structure of an anticancer drug-DNA complex: daunomycin plus d(CpGpTpApCpG). Quigley, G. J.; Wang, A. H.; Ughetto, G. Proceedings of the National Academy of Sciences, Vol. 77, Issue 12 https://doi.org/10.1073/pnas.77.12.7204	journal	December 1980
Combined virtual screening, MMPBSA, molecular docking and dynamics studies against deadly anthrax: An in silico effort to inhibit Bacillus anthracis nucleoside hydrolase Karami, Masoumeh; Jalali, Chiya; Mirzaie, Sako Journal of Theoretical Biology, Vol. 420 https://doi.org/10.1016/j.jtbi.2017.03.010	journal	May 2017
Electronic Structure Methods for Complex Materials Ching, Wai-Yim; Rulis, Paul https://doi.org/10.1093/acprof:oso/9780199575800.001.0001	book	May 2012
Association of anthracyclines and synthetic hexanucleotides. Structural factors influencing sequence specificity Rizzo, Vincenzo; Battistini, Carlo; Vigevani, Aristide Journal of Molecular Recognition, Vol. 2, Issue 3 https://doi.org/10.1002/jmr.300020306	journal	November 1989
Energetics of DNA Intercalation Reactions ^† Ren, Jinsong; Jenkins, Terence C.; Chaires, Jonathan B. Biochemistry, Vol. 39, Issue 29 https://doi.org/10.1021/bi000474a	journal	July 2000
Doxorubicin pathways: pharmacodynamics and adverse effects Thorn, Caroline F.; Oshiro, Connie; Marsh, Sharon Pharmacogenetics and Genomics, Vol. 21, Issue 7 https://doi.org/10.1097/FPC.0b013e32833ffb56	journal	January 2011
Structure of a B-DNA dodecamer Dickerson, Richard E.; Drew, Horace R. Journal of Molecular Biology, Vol. 149, Issue 4 https://doi.org/10.1016/0022-2836(81)90357-0	journal	July 1981
Assessing the performance of MM/PBSA and MM/GBSA methods. 5. Improved docking performance using high solute dielectric constant MM/GBSA and MM/PBSA rescoring Sun, Huiyong; Li, Youyong; Shen, Mingyun Phys. Chem. Chem. Phys., Vol. 16, Issue 40 https://doi.org/10.1039/C4CP03179B	journal	January 2014
Free energy calculations of protein–ligand interactions de Ruiter, Anita; Oostenbrink, Chris Current Opinion in Chemical Biology, Vol. 15, Issue 4 https://doi.org/10.1016/j.cbpa.2011.05.021	journal	August 2011
Parsing the Free Energy of Anthracycline Antibiotic Binding to DNA ^† Chaires, Jonathan B.; Satyanarayana, S.; Suh, Dongchul Biochemistry, Vol. 35, Issue 7 https://doi.org/10.1021/bi952812r	journal	January 1996
β-Arm flexibility of HU from Staphylococcus aureus dictates the DNA-binding and recognition mechanism Kim, Do-Hee; Im, Hookang; Jee, Jun-Goo Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 12 https://doi.org/10.1107/S1399004714023931	journal	November 2014
Hydration Changes for DNA Intercalation Reactions Qu, Xiaogang; Chaires, Jonathan B. Journal of the American Chemical Society, Vol. 123, Issue 1 https://doi.org/10.1021/ja002793v	journal	January 2001
Assessing the performance of the MM/PBSA and MM/GBSA methods. 6. Capability to predict protein–protein binding free energies and re-rank binding poses generated by protein–protein docking Chen, Fu; Liu, Hui; Sun, Huiyong Physical Chemistry Chemical Physics, Vol. 18, Issue 32 https://doi.org/10.1039/C6CP03670H	journal	January 2016
Hydropathic analysis of the free energy differences in anthracycline antibiotic binding to DNA Cashman, D. J. Nucleic Acids Research, Vol. 31, Issue 15 https://doi.org/10.1093/nar/gkg645	journal	August 2003
Anthracyclines: Molecular Advances and Pharmacologic Developments in Antitumor Activity and Cardiotoxicity Minotti, Giorgio; Menna, Pierantonio; Salvatorelli, Emanuela Pharmacological Reviews, Vol. 56, Issue 2 https://doi.org/10.1124/pr.56.2.6	journal	May 2004
Understanding the co-loading and releasing of doxorubicin and paclitaxel using chitosan functionalized single-walled carbon nanotubes by molecular dynamics simulations Karnati, Konda Reddy; Wang, Yixuan Physical Chemistry Chemical Physics, Vol. 20, Issue 14 https://doi.org/10.1039/C8CP00124C	journal	January 2018
Efficiency of ab-initio total energy calculations for metals and semiconductors using a plane-wave basis set Kresse, G.; Furthmüller, J. Computational Materials Science, Vol. 6, Issue 1, p. 15-50 https://doi.org/10.1016/0927-0256(96)00008-0	journal	July 1996
DNA-drug interactions Nunn, Christine M.; Van Meervelt, Luc; Zhang, Shude Journal of Molecular Biology, Vol. 222, Issue 2 https://doi.org/10.1016/0022-2836(91)90203-I	journal	November 1991
3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures Lu, X. -J. Nucleic Acids Research, Vol. 31, Issue 17 https://doi.org/10.1093/nar/gkg680	journal	September 2003
Thermodynamics of the daunomycin-DNA interaction: Ionic strength dependence of the enthalpy and entropy Chaires, Jonathan B. Biopolymers, Vol. 24, Issue 2 https://doi.org/10.1002/bip.360240208	journal	February 1985
New Insights into the Mechanism of the DNA/Doxorubicin Interaction Pérez-Arnaiz, Cristina; Busto, Natalia; Leal, José M. The Journal of Physical Chemistry B, Vol. 118, Issue 5 https://doi.org/10.1021/jp411429g	journal	January 2014
Calculating protein-ligand binding affinities with MMPBSA: Method and error analysis: Calculating Protein-Ligand Binding Affinities Wang, Changhao; Nguyen, Peter H.; Pham, Kevin Journal of Computational Chemistry, Vol. 37, Issue 27 https://doi.org/10.1002/jcc.24467	journal	August 2016
Theoretical studies of drug-dinucleotide interactions. Empirical energy function calculations on the interaction of ethidium, 9-aminoacridine, and proflavin cations with the base-paired dinucleotides GpC and CpG Nuss, Merrill E.; Marsh, Frederick J.; Kollman, Peter A. Journal of the American Chemical Society, Vol. 101, Issue 4 https://doi.org/10.1021/ja00498a008	journal	February 1979
An extended conformational analysis of doxorubicin Nakata, Yoshiro; Hopfinger, Anton J. FEBS Letters, Vol. 117, Issue 1-2 https://doi.org/10.1016/0014-5793(80)80957-4	journal	August 1980
Molecular dynamics simulation studies for DNA sequence recognition by reactive metabolites of anticancer compounds: DNA SEQUENCE RECOGNITION FOR REACTIVE METABOLITES Tumbi, Khaled M.; Nandekar, Prajwal P.; Shaikh, Naeem Journal of Molecular Recognition, Vol. 27, Issue 3 https://doi.org/10.1002/jmr.2342	journal	January 2014
Experimental and Simulation Identification of Xanthohumol as an Inhibitor and Substrate of ABCB1 Liu, Fangming; Hoag, Hannah; Wu, Chun Applied Sciences, Vol. 8, Issue 5 https://doi.org/10.3390/app8050681	journal	April 2018
Structural comparison of anticancer drug-DNA complexes: adriamycin and daunomycin Frederick, Christine A.; Williams, Loren Dean; Ughetto, Giovanni Biochemistry, Vol. 29, Issue 10 https://doi.org/10.1021/bi00462a016	journal	March 1990
Harmonic analysis of large systems. I. Methodology Brooks, Bernard R.; Jane?i?, Du?anka; Karplus, Martin Journal of Computational Chemistry, Vol. 16, Issue 12 https://doi.org/10.1002/jcc.540161209	journal	December 1995
Coupling of local folding to site-specific binding of proteins to DNA Spolar, R.; Record, M. Science, Vol. 263, Issue 5148 https://doi.org/10.1126/science.8303294	journal	February 1994
The MM/PBSA and MM/GBSA methods to estimate ligand-binding affinities Genheden, Samuel; Ryde, Ulf Expert Opinion on Drug Discovery, Vol. 10, Issue 5 https://doi.org/10.1517/17460441.2015.1032936	journal	February 2015
Bio3d: an R package for the comparative analysis of protein structures Grant, B. J.; Rodrigues, A. P. C.; ElSawy, K. M. Bioinformatics, Vol. 22, Issue 21 https://doi.org/10.1093/bioinformatics/btl461	journal	August 2006
Efficient iterative schemes for ab initio total-energy calculations using a plane-wave basis set Kresse, G.; Furthmüller, J. Physical Review B, Vol. 54, Issue 16, p. 11169-11186 https://doi.org/10.1103/PhysRevB.54.11169	journal	October 1996
Polyelectrolyte effects on site-binding equilibria with application to the intercalation of drugs into DNA Friedman, Richard A. G.; Manning, Gerald S. Biopolymers, Vol. 23, Issue 12 https://doi.org/10.1002/bip.360231202	journal	December 1984
Energetic and structural aspects of ethidium cation intercalation into DNA minihelices Ornstein, Rick L.; Rein, Robert Biopolymers, Vol. 18, Issue 11 https://doi.org/10.1002/bip.1979.360181112	journal	November 1979
Converging free energy estimates: MM-PB(GB)SA studies on the protein-protein complex Ras-Raf Gohlke, Holger; Case, David A. Journal of Computational Chemistry, Vol. 25, Issue 2 https://doi.org/10.1002/jcc.10379	journal	January 2003
The Study of the Interaction between Doxorubicin and Single-Stranded DNA Chen, Xing; Zhou, Lu; Wang, Jine ChemistrySelect, Vol. 1, Issue 13 https://doi.org/10.1002/slct.201600473	journal	August 2016
On the Molecular Mechanism of Drug Intercalation into DNA: A Simulation Study of the Intercalation Pathway, Free Energy, and DNA Structural Changes Mukherjee, Arnab; Lavery, Richard; Bagchi, Biman Journal of the American Chemical Society, Vol. 130, Issue 30 https://doi.org/10.1021/ja8001666	journal	July 2008
³¹ P NMR study of daunorubicin-d(CGTACG) complex in solution Evidence of the intercalation sites Ragg, E.; Mondelli, R.; Battistini, C. FEBS Letters, Vol. 236, Issue 1 https://doi.org/10.1016/0014-5793(88)80320-X	journal	August 1988
A Computational Approach to Enzyme Design: Predicting ω-Aminotransferase Catalytic Activity Using Docking and MM-GBSA Scoring Sirin, Sarah; Kumar, Rajesh; Martinez, Carlos Journal of Chemical Information and Modeling, Vol. 54, Issue 8 https://doi.org/10.1021/ci5002185	journal	July 2014
Intercalators. 1. Nature of Stacking Interactions between Intercalators (Ethidium, Daunomycin, Ellipticine, and 4‘,6-Diaminide-2-phenylindole) and DNA Base Pairs. Ab Initio Quantum Chemical, Density Functional Theory, and Empirical Potential Study Řeha, David; Kabeláč, Martin; Ryjáček, Filip Journal of the American Chemical Society, Vol. 124, Issue 13 https://doi.org/10.1021/ja011490d	journal	April 2002
Structural elucidation of 4′-epiadriamycin by nuclear magnetic resonance spectroscopy and comparison with adriamycin and daunomycin using quantum mechanical and restrained molecular dynamics approach Barthwal, Ritu; Agrawal, Prashansa; Tripathi, A. N. Archives of Biochemistry and Biophysics, Vol. 474, Issue 1 https://doi.org/10.1016/j.abb.2008.02.039	journal	June 2008
A theoretical investigation on the sequence selective binding of adriamycin to double-stranded polynucleotides Chen, Kai-Xian; Gresh, Nohad; Pullman, Bernard Nucleic Acids Research, Vol. 14, Issue 5 https://doi.org/10.1093/nar/14.5.2251	journal	January 1986
Targeting Ceramide Metabolism--a Strategy for Overcoming Drug Resistance Senchenkov, A.; Litvak, D. A.; Cabot, M. C. JNCI Journal of the National Cancer Institute, Vol. 93, Issue 5 https://doi.org/10.1093/jnci/93.5.347	journal	March 2001
Multistep Drug Intercalation: Molecular Dynamics and Free Energy Studies of the Binding of Daunomycin to DNA Wilhelm, Matthieu; Mukherjee, Arnab; Bouvier, Benjamin Journal of the American Chemical Society, Vol. 134, Issue 20 https://doi.org/10.1021/ja301649k	journal	May 2012
Doxorubicin, DNA torsion, and chromatin dynamics Yang, Fan; Teves, Sheila S.; Kemp, Christopher J. Biochimica et Biophysica Acta (BBA) - Reviews on Cancer, Vol. 1845, Issue 1 https://doi.org/10.1016/j.bbcan.2013.12.002	journal	January 2014
Studies on self-aggregation of anthracycline drugs by restrained molecular dynamics approach using nuclear magnetic resonance spectroscopy supported by absorption, fluorescence, diffusion ordered spectroscopy and mass spectrometry Agrawal, Prashansa; Barthwal, Sudhir Kumar; Barthwal, Ritu European Journal of Medicinal Chemistry, Vol. 44, Issue 4 https://doi.org/10.1016/j.ejmech.2008.09.037	journal	April 2009
Assessing the performance of the molecular mechanics/Poisson Boltzmann surface area and molecular mechanics/generalized Born surface area methods. II. The accuracy of ranking poses generated from docking Hou, Tingjun; Wang, Junmei; Li, Youyong Journal of Computational Chemistry, Vol. 32, Issue 5 https://doi.org/10.1002/jcc.21666	journal	October 2010
Adriamycin and daunorubicin bind in a cooperative manner to deoxyribonucleic acid Graves, David E.; Krugh, Thomas R. Biochemistry, Vol. 22, Issue 16 https://doi.org/10.1021/bi00285a033	journal	August 1983
Dissection of the free energy of anthracycline antibiotic binding to DNA: electrostatic contributions Chaires, J. B.; Priebe, W.; Graves, D. E. Journal of the American Chemical Society, Vol. 115, Issue 13 https://doi.org/10.1021/ja00066a002	journal	June 1993
Implicit Solvation Models: Equilibria, Structure, Spectra, and Dynamics Cramer, Christopher J.; Truhlar, Donald G. Chemical Reviews, Vol. 99, Issue 8 https://doi.org/10.1021/cr960149m	journal	August 1999
A Combined Molecular Docking/Dynamics Approach to Probe the Binding Mode of Cancer Drugs with Cytochrome P450 3A4 Panneerselvam, Suresh; Yesudhas, Dhanusha; Durai, Prasannavenkatesh Molecules, Vol. 20, Issue 8 https://doi.org/10.3390/molecules200814915	journal	August 2015
Review on the binding of anticancer drug doxorubicin with DNA and tRNA: Structural models and antitumor activity Agudelo, D.; Bourassa, P.; Bérubé, G. Journal of Photochemistry and Photobiology B: Biology, Vol. 158 https://doi.org/10.1016/j.jphotobiol.2016.02.032	journal	May 2016
Virtual screening-driven repositioning of etoposide as CD44 antagonist in breast cancer cells Aguirre‑Alvarado, Charmina; Segura‑Cabrera, Aldo; Velázquez‑Quesada, Inés Oncotarget, Vol. 7, Issue 17 https://doi.org/10.18632/oncotarget.8180	journal	March 2016
An RNA Molecular Switch: Intrinsic Flexibility of 23S rRNA Helices 40 and 68 5′-UAA/5′-GAN Internal Loops Studied by Molecular Dynamics Methods Réblová, Kamila; Střelcová, Zora; Kulhánek, Petr Journal of Chemical Theory and Computation, Vol. 6, Issue 3 https://doi.org/10.1021/ct900440t	journal	January 2010
Molecular dynamics simulation of the sliding of distamycin anticancer drug along DNA: interactions and sequence selectivity Jalili, Seifollah; Maddah, Mina Journal of the Iranian Chemical Society, Vol. 14, Issue 3 https://doi.org/10.1007/s13738-016-1001-0	journal	November 2016
Binding of daunomycin to calf thymus nucleosomes Chaires, Jonathan B.; Dattagupta, Nanibhushan; Crothers, Donald M. Biochemistry, Vol. 22, Issue 2 https://doi.org/10.1021/bi00271a009	journal	January 1983
Assessing the performance of MM/PBSA and MM/GBSA methods. 4. Accuracies of MM/PBSA and MM/GBSA methodologies evaluated by various simulation protocols using PDBbind data set Sun, Huiyong; Li, Youyong; Tian, Sheng Phys. Chem. Chem. Phys., Vol. 16, Issue 31 https://doi.org/10.1039/C4CP01388C	journal	January 2014
Equilibrium binding of daunomycin and adriamycin to calf thymus DNA Barcelo, Francisca; Martorell, Jordi; Gavilanes, Francisco Biochemical Pharmacology, Vol. 37, Issue 11 https://doi.org/10.1016/0006-2952(88)90571-0	journal	June 1988
VMD: Visual molecular dynamics Humphrey, William; Dalke, Andrew; Schulten, Klaus Journal of Molecular Graphics, Vol. 14, Issue 1 https://doi.org/10.1016/0263-7855(96)00018-5	journal	February 1996
Germacrone derivatives: synthesis, biological activity, molecular docking studies and molecular dynamics simulations Wu, Jie; Feng, Yu; Han, Chao Oncotarget, Vol. 8, Issue 9 https://doi.org/10.18632/oncotarget.14832	journal	January 2017
A simple model for predicting the free energy of binding between anthracycline antibiotics and DNA. Rudnicki, W. R.; Kurzepa, M.; Szczepanik, T. Acta Biochimica Polonica, Vol. 47, Issue 1 https://doi.org/10.18388/abp.2000_4057	journal	March 2000
Intercalators. 1. Nature of Stacking Interactions between Intercalators (Ethidium, Daunomycin, Ellipticine, and 4‘,6‘-Diaminide-2-phenylindole) and DNA Base Pairs. Ab Initio Quantum Chemical, Density Functional Theory, and Empirical Potential Study [ J. Am. Chem. Soc. 2002 , 124 , 3366−3367]. Řeha, David; Kabeláč, Martin; Ryjáček, Filip Journal of the American Chemical Society, Vol. 125, Issue 18 https://doi.org/10.1021/ja033983j	journal	May 2003
High-resolution X-ray luminescence extension imaging Ou, Xiangyu; Qin, Xian; Huang, Bolong Nature, Vol. 590, Issue 7846 https://doi.org/10.1038/s41586-021-03251-6	journal	February 2021
Analysis of cooperativity and ion effects in the interaction of quinacrine with DNA Wilson, W. David; Lopp, Irene G. Biopolymers, Vol. 19, Issue 6 https://doi.org/10.1002/bip.1980.360190610	journal	June 1980
Structure of a B-DNA dodecamer Drew, Horace R.; Dickerson, Richard E. Journal of Molecular Biology, Vol. 151, Issue 3 https://doi.org/10.1016/0022-2836(81)90009-7	journal	September 1981

Cited By (2)

Ultrasensitive photoelectrochemical microRNA biosensor based on doxorubicin sensitized graphitic carbon nitride assisted by a target-activated enzyme-free DNA walker Wang, Yanlin; Xia, Lingying; Wei, Chongyao Chemical Communications, Vol. 55, Issue 87 https://doi.org/10.1039/c9cc06556c	journal	January 2019
Deciphering the Molecular Basis of Melatonin Protective Effects on Breast Cells Treated with Doxorubicin: TWIST1 a Transcription Factor Involved in EMT and Metastasis, a Novel Target of Melatonin Menéndez-Menéndez, Javier; Hermida-Prado, Francisco; Granda-Díaz, Rocío Cancers, Vol. 11, Issue 7 https://doi.org/10.3390/cancers11071011	journal	July 2019

Similar Records

Evaluation of 6-OxP-CD, an Oxime-based cyclodextrin as a viable medical countermeasure against nerve agent poisoning: Experimental and molecular dynamic simulation studies on its inclusion complexes with cyclosarin, soman and VX

Journal Article · Thu Mar 30 00:00:00 EDT 2023 · PLoS ONE · OSTI ID:1543801

Lau, Edmond Y.; Enright, Heather A.; Lao, Victoria; +4 more

Rescoring Docking Hit Lists for Model Cavity Sites: Predictions And Experimental Testing

Journal Article · Tue May 19 00:00:00 EDT 2009 · J. Mol. Biol.130:5272,2008 · OSTI ID:1543801

Graves, A P; Shivakumar, D M; Boyce, S E; +3 more

Theoretical determination of molecular structure and conformation. 17. On the existence of FH/sub 2//sup -/, OH/sub 3//sup -/, NH/sub 4//sup -/, and CH/sub 5//sup -/ in the gas phase

Journal Article · Thu Jan 02 00:00:00 EST 1986 · J. Phys. Chem.; (United States) · OSTI ID:1543801

Cremer, D; Kraka, E

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Chemistry
Physics

Title: Molecular mechanism and binding free energy of doxorubicin intercalation in DNA

Citation Formats

References (97)

Cited By (2)

Similar Records

Related Subjects