najoNanosystems: Physics, Chemistry, MathematicsНаносистемы: физика, химия, математика2220-80542305-7971Университет ИТМО10.17586/2220-8054-2021-12-1-22-31najo-374Research ArticlePHYSICSФИЗИКАMechanism of gas molecule transport through erythrocytes’ membranes by kinks-solitonsМеханизм транспорта молекул газа через мембраны эритроцитов кинк-солитонамиMokrushnikovP. V.MokrushnikovP. V.

Leningradskaya, 113, Novosibirsk, 630008

Leningradskaya, 113, Novosibirsk, 630008

pavel.mokrushnikov@bk.ruRudyakV. Ya.RudyakV. Ya.

Leningradskaya, 113, Novosibirsk, 630008; Pirogova, 1, Novosibirsk, 630090

Leningradskaya, 113, Novosibirsk, 630008; Pirogova, 1, Novosibirsk, 630090

valery.rudyak@mail.ruLezhnevE. V.LezhnevE. V.

Leningradskaya, 113, Novosibirsk, 630008

Leningradskaya, 113, Novosibirsk, 630008

lionlev@yandex.ruNovosibirsk State University of Architecture and Civil EngineeringNovosibirsk State University of Architecture and Civil EngineeringNovosibirsk State University of Architecture and Civil Engineering; Novosibirsk State UniversityNovosibirsk State University of Architecture and Civil Engineering; Novosibirsk State University2021280720251212231Copyright © Mokrushnikov P.V., Rudyak V.Y., Lezhnev E.V., 20252025Mokrushnikov P.V., Rudyak V.Y., Lezhnev E.V.Mokrushnikov P.V., Rudyak V.Y., Lezhnev E.V.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://nanojournal.ifmo.ru/jour/article/view/374

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.

Предложена модель возникновения кинков липидной бислойной мембраны эритроцитов, ответственных за транспорт молекул газа, в частности кислорода. Показано, что кинки возникают за счет одновременного действия поперечных и растягивающих продольных механических напряжений, сжимающих мембрану. Эта модель объясняет резкое увеличение проницаемости мембраны для газов при прохождении эритроцита по микрокапиллярной сети с резко возрастающими в ее мембране сжимающими поперечными механическими напряжениями. Установлено, что уравнение движения кинков имеет солитонное решение, поэтому в бислое мембраны эритроцита образуется кинк-солитон. Разработанная модель согласуется с ранее экспериментально установленным фактом, что естественные мембраны эритроцитов в кровотоке претерпевают структурный переход, когда небольшие изменения рН крови, концентрации гормонов и температуры резко изменяют конформацию биомембран и ее функции за счет изменения механического поля напряжений в биомембране.

биомембранадиффузиякинкимеханические напряжения в биомембранахмикрокапиллярнаносистемаэритроцитbiomembranediffusionkinksmechanical stress in biomembranesmicrocapillarynanosystemerythrocyteThis work was financially supported by the Russian Foundation for Basic Research (Grant No. 19-01-00399).ReferencesBahri 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.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.Kreuzer F., Yahr W.Z. Influence of red cell membrane on diffusion of oxygen. J. Appl. Physiol., 1960, 15, P. 1117–1122.Kreuzer F., Yahr W.Z. Influence of red cell membrane on diffusion of oxygen. J. Appl. Physiol., 1960, 15, P. 1117–1122.Blank M. Monolayer permeability and the properties of natural membranes. J. Phys. Chem., 1962, 66 (10), P. 1911–1918.Blank M. Monolayer permeability and the properties of natural membranes. J. Phys. Chem., 1962, 66 (10), P. 1911–1918.Ivanov I.I., Loktyushkin A.V., et al. Oxygen channels of the erythrocyte membrane. Doklady biochemistry and biophysics, 2007, 414 (1), P. 137–140.Ivanov I.I., Loktyushkin A.V., et al. Oxygen channels of the erythrocyte membrane. Doklady biochemistry and biophysics, 2007, 414 (1), P. 137–140.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.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.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.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.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.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.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.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.Agre P., Preston G.M., et al. Aquaporin CHIP: the archetypal molecular water channel. Am. J. Physiol., 1993, 265 (4), P. 463–476.Agre P., Preston G.M., et al. Aquaporin CHIP: the archetypal molecular water channel. Am. J. Physiol., 1993, 265 (4), P. 463–476.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.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.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.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.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.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.Träuble H. The movement of molecules across lipid membranes: A molecular theory. J. Membr. Biol., 1971, 4 (1), P. 193–208.Träuble H. The movement of molecules across lipid membranes: A molecular theory. J. Membr. Biol., 1971, 4 (1), P. 193–208.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.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.Flory P.J., Volkenstein M. Statistical mechanics of chain molecules. Biopolymers, 1969, 5, P. 699—700.Flory P.J., Volkenstein M. Statistical mechanics of chain molecules. Biopolymers, 1969, 5, P. 699—700.Secomb T.W., Pries A.R. Blood viscosity in microvessels: experiment and theory.Comptes Rendus Physique, 2013, 14 (6), P. 470–478.Secomb T.W., Pries A.R. Blood viscosity in microvessels: experiment and theory.Comptes Rendus Physique, 2013, 14 (6), P. 470–478.Rubin A.B. Biophysics, Nauka, Moscow, 2004, 469 p.Rubin A.B. Biophysics, Nauka, Moscow, 2004, 469 p.Rudyak V.Ya. Statistical Aerohydromechanics of Homogeneous and Heterogeneous Media. Vol. 2. Hydromechanics, NSUACE, Novosibirsk, 2005, 468 p.Rudyak V.Ya. Statistical Aerohydromechanics of Homogeneous and Heterogeneous Media. Vol. 2. Hydromechanics, NSUACE, Novosibirsk, 2005, 468 p.Dodd R.K., Eilbeck J.C., Gibbon J.D., Morris H.C. Solitons and Nonlinear Wave Equations. Academic Press, New York, 1982, 697 p.Dodd R.K., Eilbeck J.C., Gibbon J.D., Morris H.C. Solitons and Nonlinear Wave Equations. Academic Press, New York, 1982, 697 p.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.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.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.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.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.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.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.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.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.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.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.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.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.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.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.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.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.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.Mokrushnikov P.V., Panin L.E., et al. Interaction of corundum and quartz nanocrystals with erythrocyte membranes. Biophysics, 2011, 56 (6), P. 1074–1077.Mokrushnikov P.V., Panin L.E., et al. Interaction of corundum and quartz nanocrystals with erythrocyte membranes. Biophysics, 2011, 56 (6), P. 1074–1077.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.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.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.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.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.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.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.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.Mokrushnikov P.V. A Mechanism of the Interaction of Metal Oxide Nanoparticles with Biological Membranes. Biophysics, 2020, 65 (1), P. 65–69.Mokrushnikov P.V. A Mechanism of the Interaction of Metal Oxide Nanoparticles with Biological Membranes. Biophysics, 2020, 65 (1), P. 65–69.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.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.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.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.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.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.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.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.Mokrushnikov P.V., Panin L.E., et al. Structural transitions in erythrocyte membranes (experimental and theoretical models). NGASU, Novosibirsk, 2019, 286 p.Mokrushnikov P.V., Panin L.E., et al. Structural transitions in erythrocyte membranes (experimental and theoretical models). NGASU, Novosibirsk, 2019, 286 p.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.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.Filippov A., Oradd G., Lindblom G. Lipid lateral diffusion in ordered anddisordered phases in raft mixtures. Biophys. J., 2004, 86, P. 891–896.Filippov A., Oradd G., Lindblom G. Lipid lateral diffusion in ordered anddisordered phases in raft mixtures. Biophys. J., 2004, 86, P. 891–896.Bagayev S.N. Fomin Yu.N., et al. Investigation of transcapillary exchange by the laser method. Laser Physics, 2005, 15 (9), P. 1292–1298.Bagayev S.N. Fomin Yu.N., et al. Investigation of transcapillary exchange by the laser method. Laser Physics, 2005, 15 (9), P. 1292–1298.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.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.Mokrushnikov P.V. The influence of ðH on the surface tension of suspended erythrocytes. The Siberian Scientific Medical Journal, 2010, 1, P. 38–46.Mokrushnikov P.V. The influence of ðH on the surface tension of suspended erythrocytes. The Siberian Scientific Medical Journal, 2010, 1, P. 38–46.

The authors declare that there are no conflicts of interest present.