Interactions of the Anticancer Drug Tamoxifen with Lipid Membranes

Khadka, Nawal K.; Cheng, Xiaolin; Ho, Chian Sing; Katsaras, John; Pan, Jianjun

doi:10.1016/j.bpj.2015.04.010

Title: Interactions of the Anticancer Drug Tamoxifen with Lipid Membranes

Journal Article · Fri May 01 00:00:00 EDT 2015 · Biophysical Journal

DOI:https://doi.org/10.1016/j.bpj.2015.04.010· OSTI ID:1253817

Khadka, Nawal K.; Cheng, Xiaolin; Ho, Chian Sing; Katsaras, John; Pan, Jianjun

Interactions of the hydrophobic anticancer drug tamoxifen (TAM) with lipid model membranes were studied using calcein-encapsulated vesicle leakage, attenuated total reflection Fourier transform infrared (FTIR) spectroscopy, small-angle neutron scattering (SANS), atomic force microscopy (AFM) based force spectroscopy, and all-atom molecular dynamics (MD) simulations. The addition of TAM enhances membrane permeability, inducing calcein to translocate from the interior to the exterior of lipid vesicles. A large decrease in the FTIR absorption band’s magnitude was observed in the hydrocarbon chain region, suggesting suppressed bond vibrational dynamics. Bilayer thickening was determined from SANS data. Force spectroscopy measurements indicate that the lipid bilayer area compressibility modulus KA is increased by a large amount after the incorporation of TAM. MD simulations show that TAM decreases the lipid area and increases chain order parameters. Moreover, orientational and positional analyses show that TAM exhibits a highly dynamic conformation within the lipid bilayer. Lastly, our detailed experimental and computational studies of TAM interacting with model lipid membranes shed new light on membrane modulation by TAM.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). High Flux Isotope Reactor (HFIR); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Center for Structural Molecular Biology (CSMB); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-05CH11231; AC05-00OR22725

OSTI ID:: 1253817

Alternate ID(s):: OSTI ID: 1265514

Journal Information:: Biophysical Journal, Journal Name: Biophysical Journal Vol. 108 Journal Issue: 10; ISSN 0006-3495

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 45 works

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References (48)

Acyl chain length and charge effect on Tamoxifen–lipid model membrane interactions Bilge, Duygu; Kazanci, Nadide; Severcan, Feride Journal of Molecular Structure, Vol. 1040 https://doi.org/10.1016/j.molstruc.2013.02.031	journal	May 2013
Concentration Dependent Different Action of Tamoxifen on Membrane Fluidity Kazanci, Nadide; Severcan, Feride Bioscience Reports, Vol. 27, Issue 4-5 https://doi.org/10.1007/s10540-007-9050-3	journal	August 2007
Calibration of atomic‐force microscope tips Hutter, Jeffrey L.; Bechhoefer, John Review of Scientific Instruments, Vol. 64, Issue 7 https://doi.org/10.1063/1.1143970	journal	July 1993
Revisiting the bilayer structures of fluid phase phosphatidylglycerol lipids: Accounting for exchangeable hydrogens Pan, Jianjun; Marquardt, Drew; Heberle, Frederick A. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1838, Issue 11 https://doi.org/10.1016/j.bbamem.2014.08.009	journal	November 2014
Scalable molecular dynamics with NAMD Phillips, James C.; Braun, Rosemary; Wang, Wei Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802 https://doi.org/10.1002/jcc.20289	journal	January 2005
Leakage and lysis of lipid membranes induced by the lipopeptide surfactin Heerklotz, Heiko; Seelig, Joachim European Biophysics Journal, Vol. 36, Issue 4-5 https://doi.org/10.1007/s00249-006-0091-5	journal	October 2006
Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes Ryckaert, Jean-Paul; Ciccotti, Giovanni; Berendsen, Herman J. C. Journal of Computational Physics, Vol. 23, Issue 3 https://doi.org/10.1016/0021-9991(77)90098-5	journal	March 1977
Effect of Chain Length and Unsaturation on Elasticity of Lipid Bilayers Rawicz, W.; Olbrich, K. C.; McIntosh, T. Biophysical Journal, Vol. 79, Issue 1 https://doi.org/10.1016/S0006-3495(00)76295-3	journal	July 2000
Scattering Density Profile Model of POPG Bilayers As Determined by Molecular Dynamics Simulations and Small-Angle Neutron and X-ray Scattering Experiments Kučerka, Norbert; Holland, Bryan W.; Gray, Chris G. The Journal of Physical Chemistry B, Vol. 116, Issue 1 https://doi.org/10.1021/jp208920h	journal	December 2011
Cholesterol Perturbs Lipid Bilayers Nonuniversally Pan, Jianjun; Mills, Thalia T.; Tristram-Nagle, Stephanie Physical Review Letters, Vol. 100, Issue 19 https://doi.org/10.1103/PhysRevLett.100.198103	journal	May 2008
Aggregation Modulators Interfere with Membrane Interactions of β2-Microglobulin Fibrils Sheynis, Tania; Friediger, Anat; Xue, Wei-Feng Biophysical Journal, Vol. 105, Issue 3 https://doi.org/10.1016/j.bpj.2013.06.015	journal	August 2013
Lipids as a Target for Drugs Modulating Multidrug Resistance of Cancer Cells Hendrich, A.; Michalak, K. Current Drug Targets, Vol. 4, Issue 1 https://doi.org/10.2174/1389450033347172	journal	January 2003
Reversible multiple time scale molecular dynamics Tuckerman, M.; Berne, B. J.; Martyna, G. J. The Journal of Chemical Physics, Vol. 97, Issue 3 https://doi.org/10.1063/1.463137	journal	August 1992
Inside-outside transitions of phospholipids in vesicle membranes McConnell, Harden M.; Kornberg, Roger D. Biochemistry, Vol. 10, Issue 7 https://doi.org/10.1021/bi00783a003	journal	March 1971
Roles of Bilayer Material Properties in Function and Distribution of Membrane Proteins McIntosh, Thomas J.; Simon, Sidney A. Annual Review of Biophysics and Biomolecular Structure, Vol. 35, Issue 1 https://doi.org/10.1146/annurev.biophys.35.040405.102022	journal	June 2006
Tamoxifen-model membrane interactions: an FT-IR study Boyar, Handan; Severcan, Feride Journal of Molecular Structure, Vol. 408-409 https://doi.org/10.1016/S0022-2860(96)09571-3	journal	June 1997
A calorimetric and spectroscopic comparison of the effects of ergosterol and cholesterol on the thermotropic phase behavior and organization of dipalmitoylphosphatidylcholine bilayer membranes Mannock, David A.; Lewis, Ruthven N. A. H.; McElhaney, Ronald N. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1798, Issue 3 https://doi.org/10.1016/j.bbamem.2009.09.002	journal	March 2010
Effect of estradiol and tamoxifen on brain membranes: investigation by infrared and fluorescence spectroscopy Dicko, Awa; Morissette, Marc; Ben Ameur, Samir Brain Research Bulletin, Vol. 49, Issue 6 https://doi.org/10.1016/S0361-9230(99)00066-0	journal	August 1999
Constant pressure molecular dynamics simulation: The Langevin piston method Feller, Scott E.; Zhang, Yuhong; Pastor, Richard W. The Journal of Chemical Physics, Vol. 103, Issue 11 https://doi.org/10.1063/1.470648	journal	September 1995
Tamoxifen: new membrane-mediated mechanisms of action and therapeutic advances Wiseman, Helen Trends in Pharmacological Sciences, Vol. 15, Issue 3 https://doi.org/10.1016/0165-6147(94)90283-6	journal	March 1994
Use ofBacillus stearothermophilus as a model to study tamoxifen-membrane interactions Luxo, C.; Jurado, A. S.; Custo´dio, J. B. A. Toxicology in Vitro, Vol. 10, Issue 4 https://doi.org/10.1016/0887-2333(96)00019-7	journal	August 1996
The Structural Basis of Estrogen Receptor/Coactivator Recognition and the Antagonism of This Interaction by Tamoxifen Shiau, Andrew K.; Barstad, Danielle; Loria, Paula M. Cell, Vol. 95, Issue 7 https://doi.org/10.1016/S0092-8674(00)81717-1	journal	December 1998
Update of the CHARMM All-Atom Additive Force Field for Lipids: Validation on Six Lipid Types Klauda, Jeffery B.; Venable, Richard M.; Freites, J. Alfredo The Journal of Physical Chemistry B, Vol. 114, Issue 23 https://doi.org/10.1021/jp101759q	journal	June 2010
CHARMM-GUI Membrane Builder for Mixed Bilayers and Its Application to Yeast Membranes Jo, Sunhwan; Lim, Joseph B.; Klauda, Jeffery B. Biophysical Journal, Vol. 97, Issue 1 https://doi.org/10.1016/j.bpj.2009.04.013	journal	July 2009
Has tamoxifen had its day? Baum, Michael Breast Cancer Research, Vol. 4, Issue 6 https://doi.org/10.1186/bcr536	journal	December 2002
Lipid Bilayer Structure Determined by the Simultaneous Analysis of Neutron and X-Ray Scattering Data Kučerka, Norbert; Nagle, John F.; Sachs, Jonathan N. Biophysical Journal, Vol. 95, Issue 5 https://doi.org/10.1529/biophysj.108.132662	journal	September 2008
Tamoxifen for early breast cancer: an overview of the randomised trials The Lancet, Vol. 351, Issue 9114, p. 1451-1467 https://doi.org/10.1016/S0140-6736(97)11423-4	journal	May 1998
Method of separated form factors for polydisperse vesicles Pencer, Jeremy; Krueger, Susan; Adams, Carl P. Journal of Applied Crystallography, Vol. 39, Issue 3 https://doi.org/10.1107/S0021889806005255	journal	May 2006
The Molecular Structure of the Liquid-Ordered Phase of Lipid Bilayers Sodt, Alexander J.; Sandar, Michael Logan; Gawrisch, Klaus Journal of the American Chemical Society, Vol. 136, Issue 2 https://doi.org/10.1021/ja4105667	journal	January 2014
Elasticity, Strength, and Water Permeability of Bilayers that Contain Raft Microdomain-Forming Lipids Rawicz, W.; Smith, B. A.; McIntosh, T. J. Biophysical Journal, Vol. 94, Issue 12 https://doi.org/10.1529/biophysj.107.121731	journal	June 2008
The anticancer drug tamoxifen induces changes in the physical properties of model and native membranes Custódio, JoséB. A.; Almeida, Leonor M.; Madeira, Vítor M. C. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1150, Issue 2 https://doi.org/10.1016/0005-2736(93)90080-J	journal	August 1993
Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems Darden, Tom; York, Darrin; Pedersen, Lee The Journal of Chemical Physics, Vol. 98, Issue 12 https://doi.org/10.1063/1.464397	journal	June 1993
Mitochondria: The gateway for tamoxifen-induced liver injury Ribeiro, Mariana P. C.; Santos, Armanda E.; Custódio, José B. A. Toxicology, Vol. 323 https://doi.org/10.1016/j.tox.2014.05.009	journal	September 2014
Dynamic structure of fatty acyl chains in a phospholipid bilayer measured by deuterium magnetic resonance Seelig, Anna; Seelig, Joachim Biochemistry, Vol. 13, Issue 23 https://doi.org/10.1021/bi00720a024	journal	November 1974
Interactions of tamoxifen with distearoyl phosphatidylcholine multilamellar vesicles: FTIR and DSC studies Bilge, Duygu; Sahin, Ipek; Kazanci, Nadide Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, Vol. 130 https://doi.org/10.1016/j.saa.2014.04.027	journal	September 2014
Fluid phase lipid areas and bilayer thicknesses of commonly used phosphatidylcholines as a function of temperature Kučerka, Norbert; Nieh, Mu-Ping; Katsaras, John Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1808, Issue 11 https://doi.org/10.1016/j.bbamem.2011.07.022	journal	November 2011
Structural interactions of a voltage sensor toxin with lipid membranes Mihailescu, Mihaela; Krepkiy, Dmitriy; Milescu, Mirela Proceedings of the National Academy of Sciences, Vol. 111, Issue 50 https://doi.org/10.1073/pnas.1415324111	journal	December 2014
Genistein derivatives decrease liposome membrane integrity — Calcein release and molecular modeling study Środa, Kamila; Michalak, Krystyna; Maniewska, Jadwiga Biophysical Chemistry, Vol. 138, Issue 3 https://doi.org/10.1016/j.bpc.2008.09.010	journal	December 2008
Concluding remarks Back to the future: mechanics and thermodynamics of lipid biomembranes Evans, E.; Rawicz, W.; Smith, B. A. Faraday Discuss., Vol. 161 https://doi.org/10.1039/C2FD20127E	journal	January 2013
Theory of Passive Permeability through Lipid Bilayers Nagle, John F.; Mathai, John C.; Zeidel, Mark L. Journal of General Physiology, Vol. 131, Issue 1 https://doi.org/10.1085/jgp.200709849	journal	December 2007
Survival Benefit of Tamoxifen in Estrogen Receptor-Negative and Progesterone Receptor-Positive Low Grade Breast Cancer Patients Yang, Li-Heng; Tseng, Hsin-Shun; Lin, Che Journal of Breast Cancer, Vol. 15, Issue 3 https://doi.org/10.4048/jbc.2012.15.3.288	journal	January 2012
Nanoscale mechanical probing of supported lipid bilayers with atomic force microscopy Das, Chinmay; Sheikh, Khizar H.; Olmsted, Peter D. Physical Review E, Vol. 82, Issue 4 https://doi.org/10.1103/PhysRevE.82.041920	journal	October 2010
Lipid Peroxides Promote Large Rafts: Effects of Excitation of Probes in Fluorescence Microscopy and Electrochemical Reactions during Vesicle Formation Ayuyan, Artem G.; Cohen, Fredric S. Biophysical Journal, Vol. 91, Issue 6 https://doi.org/10.1529/biophysj.106.087387	journal	September 2006
PACKMOL: A package for building initial configurations for molecular dynamics simulations Martínez, L.; Andrade, R.; Birgin, E. G. Journal of Computational Chemistry, Vol. 30, Issue 13 https://doi.org/10.1002/jcc.21224	journal	October 2009
A reliable and rapid procedure to estimate drug partitioning in biomembranes Custódio, JoséB. A.; Almeida, Leonor M.; Madeira, Vitor M. C. Biochemical and Biophysical Research Communications, Vol. 176, Issue 3 https://doi.org/10.1016/0006-291X(91)90394-M	journal	May 1991
A smooth particle mesh Ewald method Essmann, Ulrich; Perera, Lalith; Berkowitz, Max L. The Journal of Chemical Physics, Vol. 103, Issue 19 https://doi.org/10.1063/1.470117	journal	November 1995
Constant pressure molecular dynamics algorithms Martyna, Glenn J.; Tobias, Douglas J.; Klein, Michael L. The Journal of Chemical Physics, Vol. 101, Issue 5 https://doi.org/10.1063/1.467468	journal	September 1994
The Condensing Effect of Cholesterol in Lipid Bilayers Hung, Wei-Chin; Lee, Ming-Tao; Chen, Fang-Yu Biophysical Journal, Vol. 92, Issue 11 https://doi.org/10.1529/biophysj.106.099234	journal	June 2007

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Tamoxifen induces toxicity, causes autophagy, and partially reverses dexamethasone resistance in Jurkat T cells Torres‐López, Liliana; Maycotte, Paola; Liñán‐Rico, Andrómeda Journal of Leukocyte Biology, Vol. 105, Issue 5 https://doi.org/10.1002/jlb.2vma0818-328r	journal	January 2019
Vibrational eigenmodes of phospholipid layers in low‐wavenumber Raman spectrum of multilamellar vesicles Dmitriev, Alexey A.; Surovtsev, Nikolay V. Journal of Raman Spectroscopy, Vol. 50, Issue 11 https://doi.org/10.1002/jrs.5684	journal	July 2019
Adsorption of galloyl catechin aggregates significantly modulates membrane mechanics in the absence of biochemical cues Matsuzaki, Takahisa; Ito, Hiroaki; Chevyreva, Veronika Physical Chemistry Chemical Physics, Vol. 19, Issue 30 https://doi.org/10.1039/c7cp02771k	journal	January 2017
Normal vibrational modes of phospholipid bilayers observed by low-frequency Raman scattering Surovtsev, N. V.; Dmitriev, A. A.; Dzuba, S. A. Physical Review E, Vol. 95, Issue 3 https://doi.org/10.1103/physreve.95.032412	journal	March 2017
C-Cbl reverses HER2-mediated tamoxifen resistance in human breast cancer cells Li, Wei; Xu, Ling; Che, Xiaofang BMC Cancer, Vol. 18, Issue 1 https://doi.org/10.1186/s12885-018-4387-5	journal	May 2018

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