Effects of High Magnetic Fields on the Diffusion of Biologically Active Molecules

. 2021 Dec 28 ; 11 (1) : . [epub] 20211228

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid35011642

Grantová podpora
SOLID21 - CZ.02.1.01/0.0/0.0/16_019/0000760 Operational Programme Research, Development and Education, financed by the European Structural and Investment Funds and the Czech Ministry of Education, Youth and Sports

The diffusion of biologically active molecules is a ubiquitous process, controlling many mechanisms and the characteristic time scales for pivotal processes in living cells. Here, we show how a high static magnetic field (MF) affects the diffusion of paramagnetic and diamagnetic species including oxygen, hemoglobin, and drugs. We derive and solve the equation describing diffusion of such biologically active molecules in the presence of an MF as well as reveal the underlying mechanism of the MF's effect on diffusion. We found that a high MF accelerates diffusion of diamagnetic species while slowing the diffusion of paramagnetic molecules in cell cytoplasm. When applied to oxygen and hemoglobin diffusion in red blood cells, our results suggest that an MF may significantly alter the gas exchange in an erythrocyte and cause swelling. Our prediction that the diffusion rate and characteristic time can be controlled by an MF opens new avenues for experimental studies foreseeing numerous biomedical applications.

Zobrazit více v PubMed

Sharma S., Sharma R. 21 Tesla Mri Microscopy of Mice Kidney, Heart and Skin: Quantitation of Mri Visible Features. Nat. Preced. 2009 doi: 10.1038/npre.2009.3484.1. DOI

Magdoom K.N., Brown A., Rey J., Mareci T.H., King M.A., Sarntinoranont M. Mri of Whole Rat Brain Perivascular Network Reveals Role for Ventricles in Brain Waste Clearance. Sci. Rep. 2019;9:11480. doi: 10.1038/s41598-019-44938-1. PubMed DOI PMC

Waskaas M. Short-Term Effects of Magnetic Fields on Diffusion in Stirred and Unstirred Paramagnetic Solutions. J. Phys. Chem. 1993;97:6470–6476. doi: 10.1021/j100126a023. DOI

Kinouchi Y., Tanimoto S., Ushita T., Sato K., Yamaguchi H., Miyamoto H. Effects of Static Magnetic Fields on Diffusion in Solutions. Bioelectromagnetics. 1988;9:159–166. doi: 10.1002/bem.2250090207. PubMed DOI

Xin Z., Yarema K., Xu A. Biological Effects of Static Magnetic Fields. Springer; Singapore: 2017. Impact of Static Magnetic Fields (Smfs) on Cells; pp. 81–131. DOI

Miyakoshi J. Effects of Static Magnetic Fields at the Cellular Level. Prog. Biophys. Mol. Biol. 2005;87:213–223. doi: 10.1016/j.pbiomolbio.2004.08.008. PubMed DOI

Hideki H., Nakahara T., Zhang Q., Yonei S., Miyakoshi J. Static Magnetic Field with a Strong Magnetic Field Gradient (47.7 T/M) Induces C-Jun Expression in Hl-60 Cells. Vitr. Cell. Dev. Biol.-Anim. 2003;39:348–352. doi: 10.1290/1543-706X(2003)0392.0.CO;2. PubMed DOI

Tian X.F., Wang D.M., Feng S., Zhang L., Ji X.M., Wang Z., Lu Q.Y., Xi C.Y., Pi L., Zhang X. Effects of 3.5–23.0 T Static Magnetic Fields on Mice: A Safety Study. Neuroimage. 2019;199:273–280. doi: 10.1016/j.neuroimage.2019.05.070. PubMed DOI

Oliveira F.T.P., Diedrichsen J., Verstynen T., Duque J., Ivry R.B. Transcranial Magnetic Stimulation of Posterior Parietal Cortex Affects Decisions of Hand Choice. Proc. Natl. Acad. Sci. USA. 2010;107:17751–17756. doi: 10.1073/pnas.1006223107. PubMed DOI PMC

Zablotskii V., Lunov O., Novotna B., Churpita O., Trosan P., Holan V., Sykova E., Dejneka A., Kubinova S. Down-Regulation of Adipogenesis of Mesenchymal Stem Cells by Oscillating High-Gradient Magnetic Fields and Mechanical Vibration. Appl. Phys. Lett. 2014;105:103702. doi: 10.1063/1.4895459. DOI

Jarek W., Chen W., Qin K., Ghobrial R.M., Kubiak J.Z., Kloc M. Magnetic Field Changes Macrophage Phenotype. Biophys. J. 2018;114:2001–2013. doi: 10.1016/j.bpj.2018.03.002. PubMed DOI PMC

Xingxing Y., Song C., Zhang L., Wang J., Yu X., Yu B., Zablotskii V., Zhang X. An Upward 9.4 T Static Magnetic Field Inhibits DNA Synthesis and Increases Ros-P53 to Suppress Lung Cancer Growth. Transl. Oncol. 2021;14:101103. doi: 10.1016/j.tranon.2021.101103. PubMed DOI PMC

Dini L., Abbro L. Bioeffects of Moderate-Intensity Static Magnetic Fields on Cell Cultures. Micron. 2005;36:195–217. doi: 10.1016/j.micron.2004.12.009. PubMed DOI

Yang X., Li Z., Polyakova T., Dejneka A., Zablotskii V., Zhang X. Effect of Static Magnetic Field on DNA Synthesis: The Interplay between DNA Chirality and Magnetic Field Left-Right Asymmetry. FASEB BioAdvances. 2020;2:254–263. doi: 10.1096/fba.2019-00045. PubMed DOI PMC

Ayala M.R., Syrovets T., Hafner S., Zablotskii V., Dejneka A., Simmet T. Spatiotemporal Magnetic Fields Enhance Cytosolic Ca2+ Levels and Induce Actin Polymerization Via Activation of Voltage-Gated Sodium Channels in Skeletal Muscle Cells. Biomaterials. 2018;163:174–184. doi: 10.1016/j.biomaterials.2018.02.031. PubMed DOI

Wang C.X., Hilburn I.A., Wu D.-A., Mizuhara Y., Cousté C.P., Abrahams J.N.H., Bernstein S.E., Matani A., Shimojo S., Kirschvink J.L. Transduction of the Geomagnetic Field as Evidenced from Alpha-Band Activity in the Human Brain. eNeuro. 2019;6 doi: 10.1523/ENEURO.0483-18.2019. PubMed DOI PMC

Barbic M. Possible Magneto-Mechanical and Magneto-Thermal Mechanisms of Ion Channel Activation in Magnetogenetics. eLife. 2019;8:e45807. doi: 10.7554/eLife.45807. PubMed DOI PMC

Hong L., Pan Y., Wu R., Lv Y. Innate Immune Regulation under Magnetic Fields with Possible Mechanisms and Therapeutic Applications. Front. Immunol. 2020;11:2705. doi: 10.3389/fimmu.2020.582772. PubMed DOI PMC

Grant A., Metzger G.J., Van de Moortele P.-F., Adriany G., Olman C., Zhang L., Koopermeiners J., Eryaman Y., Koeritzer M., Adams M.E., et al. 10.5 t Mri Static Field Effects on Human Cognitive, Vestibular, and Physiological Function. Magn. Reson. Imaging. 2020;73:163–176. doi: 10.1016/j.mri.2020.08.004. PubMed DOI PMC

Ivan T., Benneyworth M.A., Nichols-Meade T., Steuer E.L., Larson S.N., Metzger G.J., Uğurbil K. Long-Term Behavioral Effects Observed in Mice Chronically Exposed to Static Ultra-High Magnetic Fields. Magn. Reson. Med. 2021;86:1544–1559. doi: 10.1002/mrm.28799. PubMed DOI PMC

Zhang L., Hou Y., Li Z., Ji X., Wang Z., Wang H., Tian X., Yu F., Yang Z., Pi L., et al. 27 T Ultra-High Static Magnetic Field Changes Orientation and Morphology of Mitotic Spindles in Human Cells. eLife. 2017;6:e22911. doi: 10.7554/eLife.22911. PubMed DOI PMC

Yue L., Fan Y., Tian X., Yu B., Song C., Feng C., Zhang L., Ji X., Zablotskii V., Zhang X. The Anti-Depressive Effects of Ultra-High Static Magnetic Field. J. Magn. Reson. Imaging. 2021 doi: 10.1002/jmri.28035. PubMed DOI

Hinds G., Coey J.M.D., Lyons M.E.G. Influence of Magnetic Forces on Electrochemical Mass Transport. Electrochem. Commun. 2001;3:215–218. doi: 10.1016/S1388-2481(01)00136-9. DOI

Zablotskii V., Lunov O., Kubinova S., Polyakova T., Sykova E., Dejneka A. Effects of High-Gradient Magnetic Fields on Living Cell Machinery. J. Phys. D Appl. Phys. 2016;49:493003. doi: 10.1088/0022-3727/49/49/493003. DOI

Zablotskii V., Polyakova T., Dejneka A. Cells in the Non-Uniform Magnetic World: How Cells Respond to High-Gradient Magnetic Fields. BioEssays. 2018;40:1800017. doi: 10.1002/bies.201800017. PubMed DOI

Dunne P., Mazza L., Coey J.M.D. Magnetic Structuring of Electrodeposits. Phys. Rev. Lett. 2011;107:024501. doi: 10.1103/PhysRevLett.107.024501. PubMed DOI

Leventis N., Dass A. Demonstration of the Elusive Concentration-Gradient Paramagnetic Force. J. Am. Chem. Soc. 2005;127:4988–4989. doi: 10.1021/ja043169b. PubMed DOI

Vitalii Z., Polyakova T., Dejneka A. Modulation of the Cell Membrane Potential and Intracellular Protein Transport by High Magnetic Fields. Bioelectromagnetics. 2021;42:27–36. doi: 10.1002/bem.22309. PubMed DOI

Ayansiji A.O., Dighe A.V., Linninger A.A., Singh M.R. Constitutive Relationship and Governing Physical Properties for Magnetophoresis. Proc. Natl. Acad. Sci. USA. 2020;117:30208–30214. doi: 10.1073/pnas.2018568117. PubMed DOI PMC

Waskaas M. On the Origin of the Magnetic Concentration Gradient Force and Its Interaction Mechanisms with Mass Transfer in Paramagnetic Electrolytes. Fluids. 2021;6:114. doi: 10.3390/fluids6030114. DOI

Sear R.P. Diffusiophoresis in Cells: A General Nonequilibrium, Nonmotor Mechanism for the Metabolism-Dependent Transport of Particles in Cells. Phys. Rev. Lett. 2019;122:128101. doi: 10.1103/PhysRevLett.122.128101. PubMed DOI

McRobbie D.W. 3.01—Fundamentals of Mr Imaging. In: Brahme A., editor. Comprehensive Biomedical Physics. Elsevier; Oxford, UK: 2014. pp. 1–19.

Tikhonov A.N. Equations of Mathematical Physics. Pergamon Press; Oxford, UK: 1963.

Lifshitz E.M., Pitaevskii L.P. Physical Kinetics: Volume 10. Elsevier Science; Amsterdam, The Netherlands: 1995.

Hardt S., Hartmann J., Zhao S.C., Bandopadhyay A. Electric-Field-Induced Pattern Formation in Layers of DNA Molecules at the Interface between Two Immiscible Liquids. Phys. Rev. Lett. 2020;124:064501. doi: 10.1103/PhysRevLett.124.064501. PubMed DOI

Crank J. The Mathematics of Diffusion. Oxford University Press; Oxford, UK: 1975.

Wolfram Research, Inc. Mathematica. [(accessed on 23 December 2021)]. Available online: https://www.wolfram.com/mathematica.

Kang M.-Y., Katz I., Sapoval B. A New Approach to the Dynamics of Oxygen Capture by the Human Lung. Respir. Physiol. Neurobiol. 2015;205:109–119. doi: 10.1016/j.resp.2014.11.001. PubMed DOI

Miller D.G. Some Comments on Multicomponent Diffusion: Negative Main Term Diffusion Coefficients, Second Law Constraints, Solvent Choices, and Reference Frame Transformations. J. Phys. Chem. 1986;90:1509–1519. doi: 10.1021/j100399a010. DOI

Clark W.M., Rowley R.L. Ternary Liquid Diffusion Coefficients near Plait Points. Int. J. Thermophys. 1985;6:631–642. doi: 10.1007/BF00500335. DOI

Daniela B., Buzatu F.D., Paduano L., Sartorio R. Diffusion Coefficients for the Ternary System Water + chloroform + acetic Acid at 25 °C. J. Solut. Chem. 2007;36:1373–1384. doi: 10.1007/s10953-007-9200-z. DOI

Vitagliano V., Sartorio R., Scala S., Spaduzzi D. Diffusion in a Ternary System and the Critical Mixing Point. J. Solut. Chem. 1978;7:605–622. doi: 10.1007/BF00646038. DOI

Kozlova S., Mialdun A., Ryzhkov I., Janzen T., Vrabec J., Shevtsova V. Do Ternary Liquid Mixtures Exhibit Negative Main Fick Diffusion Coefficients? Phys. Chem. Chem. Phys. 2019;21:2140–2152. doi: 10.1039/C8CP06795C. PubMed DOI

Reguera G. When Microbial Conversations Get Physical. Trends Microbiol. 2011;19:105–113. doi: 10.1016/j.tim.2010.12.007. PubMed DOI PMC

Spees W.M., Yablonskiy D.A., Oswood M.C., Ackerman J.J.H. Water Proton Mr Properties of Human Blood at 1.5 Tesla: Magnetic Susceptibility, T-1, T-2, T-2* and Non-Lorentzian Signal Behavior. Magn. Reson. Med. 2001;45:533–542. doi: 10.1002/mrm.1072. PubMed DOI

Jin X., Yazer M.H., Chalmers J.J., Zborowski M. Quantification of Changes in Oxygen Release from Red Blood Cells as a Function of Age Based on Magnetic Susceptibility Measurements. Analyst. 2011;136:2996–3003. doi: 10.1039/c0an01018a. PubMed DOI PMC

Voitländer J. Diamagnétisme et Paramagnétisme, von G. Foëx. Relaxation Paramagnétique, von C.-J. Gorter und L.-J. Smits. Reihe: Tables de Constantes et Données Numériques, begründet v. Ch. Marie. Verlag Masson & Cie., Paris 1957. 1. Aufl., 317 S., geb. Ffrs. 9.700.- Angew. Chem. 1959;71:204.

Rosensweig R.E. Ferrohydrodynamics. Dover Books on Physics, Dover Publications; Mineola, NY, USA: 2014.

Longeville S., Stingaciu L.R. Hemoglobin Diffusion and the Dynamics of Oxygen Capture by Red Blood Cells. Sci. Rep. 2017;7:10448. doi: 10.1038/s41598-017-09146-9. PubMed DOI PMC

Adams L.R., Fatt I. The Diffusion Coefficient of Human Hemoglobin at High Concentrations. Respir. Physiol. 1967;2:293–301. doi: 10.1016/0034-5687(67)90034-5. PubMed DOI

Wang Y.M., Austin R.H., Cox E.C. Single Molecule Measurements of Repressor Protein 1d Diffusion on DNA. Phys. Rev. Lett. 2006;97:048302. doi: 10.1103/PhysRevLett.97.048302. PubMed DOI

Hook C., Yamaguchi K., Scheid P., Piiper J. Oxygen-Transfer of Red Blood-Cells—Experimental-Data and Model Analysis. Respir. Physiol. 1988;72:65–82. doi: 10.1016/0034-5687(88)90080-1. PubMed DOI

Piiper J., Hook C., Yamaguchi K., Scheid P. Modeling of Oxygen-Transfer Kinetics of Red Blood-Cells. FASEB J. 1988;2:A925.

Di Caprio G., Stokes C., Higgins J.M., Schonbrun E. Single-Cell Measurement of Red Blood Cell Oxygen Affinity. Proc. Natl. Acad. Sci. USA. 2015;112:9984–9989. doi: 10.1073/pnas.1509252112. PubMed DOI PMC

Peterson D.R., Bronzino J.D. Biomechanics: Principles and Practices. CRC Press; Boca Raton, FL, USA: 2014.

Yamaguchi K., Nguyen-Phu D., Scheid P., Piiper J. Kinetics of O2 Uptake and Release by Human Erythrocytes Studied by a Stopped-Flow Technique. J. Appl. Physiol. 1985;58:1215–1224. doi: 10.1152/jappl.1985.58.4.1215. PubMed DOI

Earl D.R., Geis I. Hemoglobin: Structure, Function, Evolution, and Pathology. Benjamin/Cummings Pub. Co.; Menlo Park, CA, USA: 1983.

Cerdonio M., Congiu-Castellano A., Calabrese L., Morante S., Pispisa B., Vitale S. Room-Temperature Magnetic Properties of Oxy- and Carbonmonoxyhemoglobin. Proc. Natl. Acad. Sci. USA. 1978;75:4916–4919. doi: 10.1073/pnas.75.10.4916. PubMed DOI PMC

Hillman R., Finch C. The Red Cell Manual. F.A. Davis, Co.; Philadelphia, PA, USA: 1996.

Wei X., Moore L.R., Nakano N., Chalmers J.J., Zborowski M. Single Cell Magnetometry by Magnetophoresis Vs. Bulk Cell Suspension Magnetometry by Squid-Mpms—A Comparison. J. Magn. Magn. Mater. 2019;474:152–160. doi: 10.1016/j.jmmm.2018.10.108. PubMed DOI PMC

Hongyuan J., Sun S.X. Cellular Pressure and Volume Regulation and Implications for Cell Mechanics. Biophys. J. 2013;105:609–619. doi: 10.1016/j.bpj.2013.06.021. PubMed DOI PMC

Stewart M.P., Helenius J., Toyoda Y., Ramanathan S.P., Muller D.J., Hyman A.A. Hydrostatic Pressure and the Actomyosin Cortex Drive Mitotic Cell Rounding. Nature. 2011;469:226–230. doi: 10.1038/nature09642. PubMed DOI

Li F.F., Chan C.U., Ohl C.D. Yield Strength of Human Erythrocyte Membranes to Impulsive Stretching. Biophys. J. 2013;105:872–879. doi: 10.1016/j.bpj.2013.06.045. PubMed DOI PMC

Iwasaka M. Deformation of Cellular Components of Bone Forming Cells When Exposed to a Magnetic Field. AIP Adv. 2019;9:035327. doi: 10.1063/1.5079635. DOI

Zablotskii V., Syrovets T., Schmidt Z.W., Dejneka A., Simmet T. Modulation of Monocytic Leukemia Cell Function and Survival by High Gradient Magnetic Fields and Mathematical Modeling Studies. Biomaterials. 2014;35:3164–3171. doi: 10.1016/j.biomaterials.2013.12.098. PubMed DOI

Nouri S., Sharif M.R., Sahba S. The Effect of Ferric Chloride on Superficial Bleeding. Trauma Mon. 2015;20:e18042. doi: 10.5812/traumamon.18042. PubMed DOI PMC

Eckly A., Hechler B., Freund M., Zerr M., Cazenave J.-P., Lanza F., Mangin P.H., Gachet C. Mechanisms Underlying Fecl3-Induced Arterial Thrombosis. J. Thromb. Haemost. 2011;9:779–789. doi: 10.1111/j.1538-7836.2011.04218.x. PubMed DOI

Li Q., Liao Z., Gu L., Zhang L., Zhang L., Tian X., Li J., Fang Z., Zhang X. Moderate Intensity Static Magnetic Fields Prevent Thrombus Formation in Rats and Mice. Bioelectromagnetics. 2020;41:52–62. doi: 10.1002/bem.22232. PubMed DOI

Merbach A.E., Toth E. The Chemistry of Contrast Iagents in Medical Magnetic Resonance Imaging. John Wiley & Sons, Ltd.; New York, NY, USA: 2001.

Klaassen N.J.M., Arntz M.J., Gil Arranja A., Roosen J., Nijsen J.F.W. The Various Therapeutic Applications of the Medical Isotope Holmium-166: A Narrative Review. EJNMMI Radiopharm. Chem. 2019;4:19. doi: 10.1186/s41181-019-0066-3. PubMed DOI PMC

Cristea D., Krishtul S., Kuppusamy P., Baruch L., Machluf M., Blank A. New Approach to Measuring Oxygen Diffusion and Consumption in Encapsulated Living Cells, Based on Electron Spin Resonance Microscopy. Acta Biomater. 2020;101:384–394. doi: 10.1016/j.actbio.2019.10.032. PubMed DOI

Tamagno P., Costa-Almeida R., Gomes M.E. Magnetotherapy: The Quest for Tendon Regeneration. J. Cell. Physiol. 2018;233:6395–6405. doi: 10.1002/jcp.26637. PubMed DOI

Lv Y., Shi Y., Scientific Committee of the First International Conference of Magnetic Surgery Xi’an Consensus on Magnetic Surgery. Hepatobiliary Surg. Nutr. 2019;8:177–178. doi: 10.21037/hbsn.2019.03.01. PubMed DOI PMC

Parfenov V.A., Khesuani Y.D., Petrov S.V., Karalkin P.A., Koudan E.V., Nezhurina E.K., DAS Pereira F., Krokhmal A.A., Gryadunova A.A., Bulanova E.A., et al. Magnetic Levitational Bioassembly of 3d Tissue Construct in Space. Sci. Adv. 2020;6:eaba4174. doi: 10.1126/sciadv.aba4174. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...