Mechanism of gas molecule transport through erythrocytes’ membranes by kinks-solitons
https://doi.org/10.17586/2220-8054-2021-12-1-22-31
Abstract
A model of kinks appearance in the lipid bilayer membrane of erythrocytes, which are responsible for gas molecule transport, in particular, oxygen, is proposed. It was shown that the kinks arise due to the simultaneous action of transverse and tensile longitudinal mechanical stresses compressing the membrane. This model explains the membrane’s permeability sharp increase for gases during an erythrocyte passage through the microcapillary network with the compressive transverse mechanical stresses sharply increasing in its membrane. It was found that the equation of kinks motion has a soliton solution, so that a kink-soliton is formed in the bilayer of the erythrocyte membrane. The developed model is consistent with the previously experimentally established fact that the native erythrocyte membranes in the bloodstream undergo a structural transition, when small changes in blood pH, hormone concentration, and temperature dramatically change the conformation of the biomembranes and its functions by changing the mechanical stress field in the biomembrane.
Keywords
biomembrane,
diffusion,
kinks,
mechanical stress in biomembranes,
microcapillary,
nanosystem,
erythrocyte
Supporting agencies: This work was financially supported by the Russian Foundation for Basic Research (Grant No. 19-01-00399).
About the Authors
P. V. Mokrushnikov
Novosibirsk State University of Architecture and Civil Engineering
Russian Federation
Russian Federation
Leningradskaya, 113, Novosibirsk, 630008
V. Ya. Rudyak
Novosibirsk State University of Architecture and Civil Engineering; Novosibirsk State University
Russian Federation
Russian Federation
Leningradskaya, 113, Novosibirsk, 630008; Pirogova, 1, Novosibirsk, 630090
E. V. Lezhnev
Novosibirsk State University of Architecture and Civil Engineering
Russian Federation
Russian Federation
Leningradskaya, 113, Novosibirsk, 630008
References
1. Bahri M.A., Heine B.J, Hans P., et al. Quantification of lipid bilayer effective microviscosity and fluidity effect induced by propofol. Biophys. Chem., 2005, 114, P. 53–61.
2. Kreuzer F., Yahr W.Z. Influence of red cell membrane on diffusion of oxygen. J. Appl. Physiol., 1960, 15, P. 1117–1122.
3. Blank M. Monolayer permeability and the properties of natural membranes. J. Phys. Chem., 1962, 66 (10), P. 1911–1918.
4. Ivanov I.I., Loktyushkin A.V., et al. Oxygen channels of the erythrocyte membrane. Doklady biochemistry and biophysics, 2007, 414 (1), P. 137–140.
5. Denker B.M., Smith B.L., Kuhajda F.P., Agre P. Identification, purification, and partial characterization of a novel Mr 28,000 integral membrane protein from erythrocytes and renal tubules. J. Biol. Chem., 1988, 263 (30), P. 15634–15642.
6. Preston G.M., Carroll T.P., Guggino W.B., Agre P. Appearance of water channels in Xenopus oocytes expressing red cell CHIP 28 protein. Science, 1992, 256 (5055), P. 385–387.
7. Saparov S.M., Liu K., Agre P., Pohl P. Fast and selective ammonia transport by aquaporin-8. J. Biol. Chem., 2007, 282 (8), P. 5296–5301.
8. Endeward V., Cartron J.P., Ripoche P., Gros G. RhAG protein of the Rhesus complex is a CO2 channel in the human red cell membrane. FASEB J., 2008, 22 (1), P. 64–73.
9. Agre P., Preston G.M., et al. Aquaporin CHIP: the archetypal molecular water channel. Am. J. Physiol., 1993, 265 (4), P. 463–476.
10. Cooper G.J., Boron W.F. Effect of PCMBS on CO2 permeability of Xenopus oocytes expressing aquaporin 1 or its C189S mutant. Am. J. Physiol., 1998, 275 (6), P. 1481–1486.
11. Endeward V., Musa-Aziz R., et al. Evidence that aquaporin 1 is a major pathway for CO2 transport across the human erythrocyte membrane. FASEB J., 2006, 20 (12), P. 1974–1981.
12. Endeward V., Gros G. Low carbon dioxide permeability of the apical epithelial membrane of guinea-pig colon. J. Physiol., 2005, 567 (1), P. 253–265.
13. Träuble H. The movement of molecules across lipid membranes: A molecular theory. J. Membr. Biol., 1971, 4 (1), P. 193–208.
14. Subczynski W.K., Hyde J.S., Kusumi A. Effect of alkyl chain unsaturation and cholesterol intercalation on oxygen transport in membranes: a pulse ESR spin labeling study. Biochemistry, 1991, 30 (35), P. 8578–8590.
15. Flory P.J., Volkenstein M. Statistical mechanics of chain molecules. Biopolymers, 1969, 5, P. 699—700.
16. Secomb T.W., Pries A.R. Blood viscosity in microvessels: experiment and theory.Comptes Rendus Physique, 2013, 14 (6), P. 470–478.
17. Rubin A.B. Biophysics, Nauka, Moscow, 2004, 469 p.
18. Rudyak V.Ya. Statistical Aerohydromechanics of Homogeneous and Heterogeneous Media. Vol. 2. Hydromechanics, NSUACE, Novosibirsk, 2005, 468 p.
19. Dodd R.K., Eilbeck J.C., Gibbon J.D., Morris H.C. Solitons and Nonlinear Wave Equations. Academic Press, New York, 1982, 697 p.
20. Panin L.E., Mokrushnikov P.V., Kunitsyn V.G., Zaitsev B.N. The interaction mechanism of cortisol and catecholamines with structural components of erythrocyte membranes. Journal of physical chemistry B, 2010, 114, P. 9462–9473.
21. Angles G., Dotson R., Bueche K., Pias S.C. Predicted Decrease in Membrane Oxygen Permeability with Addition of Cholesterol. Adv. Exp. Med. Biol., 2017, 977, P. 9–14.
22. Subczynski W.K., Widomska J., Mainali L. Factors Determining the Oxygen Permeability of Biological Membranes: Oxygen Transport Across Eye Lens Fiber-Cell Plasma Membranes. Adv. Exp. Med. Biol., 2017, 977, P. 27–34.
23. Widomska J., Raguz M., Subczynski W.K. Oxygen permeability of the lipid bilayer membrane made of calf lens lipids. Biochim. Biophys. Acta, 2007, 1768 (10), P. 2635–2645.
24. Subczynski W.K., Widomska J., Feix J.B. Physical properties of lipid bilayers from EPR spin labeling and their influence on chemical reactions in a membrane environment. Free Radic. Biol. Med., 2009, 46 (6), P. 707–718.
25. Subczynski W.K., Raguz M., et al. Functions of cholesterol and the cholesterol bilayer domain specific to the fiber-cell plasma membrane of the eye lens. J. Membr. Biol., 2012, 245 (1), P. 51–68.
26. Mainali L., Raguz M., O’Brien W.J., Subczynski W.K. Properties of membranes derived from the total lipids extracted from the human lens cortex and nucleus. Biochim. Biophys. Acta, 2013, 1828 (6), P. 1432–1440.
27. Khan N., Shen J., et al. Plasma membrane cholesterol: a possible barrier to intracellular oxygen in normal and mutant CHO cells defective in cholesterol metabolism. Biochemistry, 2003, 42 (1), P. 23–29.
28. Kawasaki K., Yin J.J., et al. Pulse EPR detection of lipid exchange between protein-rich raft and bulk domains in the membrane: Methodology development and its application to studies of influenza viral membrane. Biophys. J., 2001, 80 (2), P. 738–748.
29. Mokrushnikov P.V., Panin L.E., et al. Interaction of corundum and quartz nanocrystals with erythrocyte membranes. Biophysics, 2011, 56 (6), P. 1074–1077.
30. Kozelskaya A.I., Panin A.V., et al. Morphological changes of the red blood cells treated with metal oxide nanoparticles. Toxicology in Vitro, 2016, 37, P. 34–40.
31. Panin L.E., Mokrushnikov P.V., Kunitsyn V.G., Zaitsev B.N. Interaction mechanism of anabolic steroid hormones with structural components of erythrocyte membranes. Journal of physical chemistry B, 2011, 115, P. 14969–14979.
32. Bagayev S.N., Zakharov V.N., et al. Transcapillary exchange regulation by pulse blood pressure. Russian Journal of Biomechanics, 2008, 12 (3), P. 7–14.
33. Mokrushnikov P.V., Dudarev A.N., et al. Effects of native and oxidized apolipoprotein A–I on lipid bilayer microviscosity of erythrocyte plasma membrane. Journal Biochemistry (Moscow), Supplement Series A: Membrane and Cell Biology, 2017, 11 (1), P. 48–53.
34. Mokrushnikov P.V. A Mechanism of the Interaction of Metal Oxide Nanoparticles with Biological Membranes. Biophysics, 2020, 65 (1), P. 65–69.
35. Popov A.L., Savintseva I.V., et al. Cytotoxicity analysis of gadolinium doped cerium oxide nanoparticles on human mesenchymal stem cells. Nanosystems: physics, chemistry, mathematics, 2018, 9 (3), P. 430–438.
36. Popov A.L., Savintseva I.V., et al. PVP-stabilized tungsten oxide nanoparticles (WO3) nanoparticles cause hemolysis of human erythrocytes in a dose-dependent manner. Nanosystems: physics, chemistry, mathematics, 2019, 10 (2), P. 199–205.
37. Poteryaeva O.N., Russkikh G.S., et al. Hormonal status, lipid profile and membranes microviscosity of north residents. Journal of Ural Medical Academic Science, 2014, 2 (48), P. 149–152.
38. Mokrushnikov P.V., Osipova L.P., Gol’tsova T.V., Rozumenko A.A. Erythrocyte membranes microviscosity in the population of Samburg village Yamalo-Nenets Autonomous Okrug. Yakut medical journal, 2016, 2 (54), P. 15–16.
39. Mokrushnikov P.V., Panin L.E., et al. Structural transitions in erythrocyte membranes (experimental and theoretical models). NGASU, Novosibirsk, 2019, 286 p.
40. Mokrushnikov P.V. Mechanical Stresses in the Lipid Bilayer of Erythrocyte Membranes. In: “Lipid Bilayers: Properties, Behavior and Interactions” edited by Mohammad Ashrafuzzaman, Nova Science Publishers, NY, 2019, P. 43–91.
41. Filippov A., Oradd G., Lindblom G. Lipid lateral diffusion in ordered anddisordered phases in raft mixtures. Biophys. J., 2004, 86, P. 891–896.
42. Bagayev S.N. Fomin Yu.N., et al. Investigation of transcapillary exchange by the laser method. Laser Physics, 2005, 15 (9), P. 1292–1298.
43. Bagaev S.N., Zakharov V.N., et al. Investigation of the physical mechanisms of blood microcirculation and transcapillary exchange using a phase-sensitive laser method. Russian Journal of Biomechanics, 2006, 10 (3), P. 22–40.
44. Mokrushnikov P.V. The influence of ðH on the surface tension of suspended erythrocytes. The Siberian Scientific Medical Journal, 2010, 1, P. 38–46.
Review
For citations:
Mokrushnikov P.V., Rudyak V.Ya., Lezhnev E.V. Mechanism of gas molecule transport through erythrocytes’ membranes by kinks-solitons. Nanosystems: Physics, Chemistry, Mathematics. 2021;12(1):22-31. https://doi.org/10.17586/2220-8054-2021-12-1-22-31
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