Abstract
The molecular mechanisms of the interaction of anticancer antibiotic doxorubicin with lipid cell membrane models have been investigated using grazing incidence X-ray diffraction (XRD) and X-ray reflectivity (XRR). The model systems were monolayers of four types of phospholipids, related to the main components of animal cell membranes. New information on the processes of damage of phospholipid monolayer lattice caused by doxorubicin is obtained. It is established that the action of doxorubicin on anionic phospholipid monolayers is determined by the electrostatic interaction: positively charged doxorubicin molecules are incorporated between negatively charged phospholipid functional groups. In the case of neutral phospholipids the key role belongs to the hydrophobic interaction: doxorubicin molecules are coordinated with phospholipid hydrocarbon tails in disordered regions.
REFERENCES
G. Brezesinski and H. Möhwald, Adv. Colloid Int. Sci. 100, 563 (2003). https://doi.org/10.1016/s0001-8686(02)00071-4
C. Stefaniu and G. Brezesinski, Curr. Opin. Colloid Int. Sci. 19, 216 (2014). https://doi.org/10.1016/j.cocis.2014.01.004
V. M. Kaganer, H. Mohwald, and P. Dutta, Rev. Modern Phys. 71 (3), 779 (1999). https://doi.org/10.1103/RevModPhys.71.779
J. Daillant and A. Gibaud, X-ray and Neutron Reflectivity: Principles and Application (Springer, Berlin, 2009).
N. N. Novikova, M. V. Koval’chuk, E. A. Yur’eva, et al., Crystallogr. Rep. 57 (5), 648 (2012).
N. Novikova, M. Kovalchuk, O. Konovalov, et al., BioNanoSci 10, 618 (2021). https://doi.org/10.1007/s12668-020-00742-0
F. Arcamone, G. Cassinelli, G. Fantini, et al., Biotechnol. Bioeng. 67, 704 (2000). https://doi.org/10.1002/bit.260110607
C. F. Thorn, C. Oshiro, S. Marsh, et al., Pharmacogenet. Genomics 21, 440 (2011). https://doi.org/10.1097/FPC.0b013e32833ffb56
S. Sritharan and N. A. Sivalingam, Life Sci. 278, 119527 (2021). https://doi.org/10.1016/j.lfs.2021.119527
M. C. Asensio-López, F. Soler, D. Pascual-Figal, et al., PLOS One 12, e0172803 (2017). https://doi.org/10.1371/journal.pone.0172803
A. C. Alves, A. Magarkar, M. Horta, et al., Sci. Rep. 7, 6343 (2017). https://doi.org/10.1038/s41598-017-06445-z
C. Peetla, R. Bhave, S. Vijayaraghavalu, et al., Mol. Pharm. 7, 2334 (2010). https://doi.org/10.1021/mp100308n
R. Dadhich and S. Kapoor, Mol. Cell. Biochem. 477, 2507 (2022). https://doi.org/10.1007/s11010-022-04459-4
A. Ramu, D. Glaubiger, I. T. Magrath, et al., Cancer Res. 43, 5533 (1983).
G. Speelmans, R. W. Staffhorst, B. de Kruijff, et al., Biochemistry 33, 13761 (1994). https://doi.org/10.1021/bi00250a029
L. Chen, H. Alrbyawi, I. Poudel, et al., AAPS PharmSciTech 20, 99 (2019). https://doi.org/10.1208/s12249-019-1316-0
A. Alves, C. Nunes, J. Lima, et al., Colloids Surf. B 160, 610 (2017). https://doi.org/10.1016/j.colsurfb.2017.09.058
T. J. Yacoub, A. S. Reddy, and I. Szleifer, Biophys. J. 101, 378 (2011). https://doi.org/10.1016/j.bpj.2011.06.015
Y. Hou, J. Li, X. Liu, et al., Chem. Phys. 541, 111036 (2021).
D. Matyszewska and S. Moczulska, Electrochim. Acta 280, 229 (2018). https://doi.org/10.1016/j.electacta.2018.05.119
M. H. Gaber, M. M. Ghannam, S. A. Ali, et al., Biophys. Chem. 70, 223 (1998). https://doi.org/10.1016/S0301-4622(97)00125-7
D. Marsh, Biochim. Biophys. Acta 1286, 183 (1996). https://doi.org/10.1016/S0304-4157(96)00009-3
A. Zameshin, I. A. Makhotkin, S. N. Yakunin, et al., J. Appl. Crystallogr. 49, 1300 (2016). https://doi.org/10.1107/S160057671601044X
O. A. Kondratev, I. A. Makhotkin, and S. N. Yakunin, Appl. Surf. Sci. 574, 151573 (2022). https://doi.org/10.1016/j.apsusc.2021.151573
Y. N. Malakhova, A. N. Korovin, D. A. Lapkin, et al., Soft Matter 13, 7300 (2017). https://doi.org/10.1039/c7sm01773a
D. L. Windt, Comput. Phys. IEEE Comput. Sci. Eng. 12, 360 (1998). https://doi.org/10.1063/1.168689
Zh. Xiao-Lin and Ch. Sow-Hsin, Phys. Rev. E 47, 3174 (1993). https://doi.org/10.1103/PhysRevE.47.3174
V. F. Selemenev, L. V. Rudakova, O. B. Rudakov, et al., Phospholipids against the Background of Natural Matrices (Nauchnaya Kniga, Voronezh, 2020).
ACKNOWLEDGMENTS
We acknowledge the European Synchrotron Radiation Facility for provision of the beam time at ID10 beamline and to the head of the ID10 beamline, O.V. Konovalov, for his help in carrying out experiments and fruitful discussion of the obtained results.
Funding
The study was supported in part by the Ministry of Science and Higher Education of the Russian Federation within a government contract, project FSSM-2022-0003.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The authors of this work declare that they have no conflicts of interest.
Additional information
Translated by Yu. Sin’kov
Publisher’s Note.
Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Novikova, N.N., Kovalchuk, M.V., Rogachev, A.V. et al. Structural Reorganization of Cell Membrane Models Caused by the Anticancer Antibiotic Doxorubicin. Crystallogr. Rep. 68, 986–996 (2023). https://doi.org/10.1134/S1063774523601156
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S1063774523601156