Cell-cell interactions and fluctuations in the direction of motility promote directed migration of osteoblasts in direct current electrotaxis
Under both physiological (development, regeneration) and pathological conditions (cancer metastasis), cells migrate while sensing environmental cues in the form of mechanical, chemical or electrical stimuli. In the case of bone tissue, osteoblast migration is essential in bone regeneration. Although...
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Published in: | Frontiers in bioengineering and biotechnology Vol. 10; p. 995326 |
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Abstract | Under both physiological (development, regeneration) and pathological conditions (cancer metastasis), cells migrate while sensing environmental cues in the form of mechanical, chemical or electrical stimuli. In the case of bone tissue, osteoblast migration is essential in bone regeneration. Although it is known that osteoblasts respond to exogenous electric fields, the underlying mechanism of electrotactic collective movement of human osteoblasts is unclear. Here, we present a computational model that describes the osteoblast cell migration in a direct current electric field as the motion of a collection of active self-propelled particles and takes into account fluctuations in the direction of single-cell migration, finite-range cell-cell interactions, and the interaction of a cell with the external electric field. By comparing this model with
in vitro
experiments in which human primary osteoblasts are exposed to a direct current electric field of different field strengths, we show that cell-cell interactions and fluctuations in the migration direction promote anode-directed collective migration of osteoblasts. |
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AbstractList | Under both physiological (development, regeneration) and pathological conditions (cancer metastasis), cells migrate while sensing environmental cues in the form of mechanical, chemical or electrical stimuli. In the case of bone tissue, osteoblast migration is essential in bone regeneration. Although it is known that osteoblasts respond to exogenous electric fields, the underlying mechanism of electrotactic collective movement of human osteoblasts is unclear. Here, we present a computational model that describes the osteoblast cell migration in a direct current electric field as the motion of a collection of active self-propelled particles and takes into account fluctuations in the direction of single-cell migration, finite-range cell-cell interactions, and the interaction of a cell with the external electric field. By comparing this model with in vitro experiments in which human primary osteoblasts are exposed to a direct current electric field of different field strengths, we show that cell-cell interactions and fluctuations in the migration direction promote anode-directed collective migration of osteoblasts. Under both physiological (development, regeneration) and pathological conditions (cancer metastasis), cells migrate while sensing environmental cues in the form of mechanical, chemical or electrical stimuli. In the case of bone tissue, osteoblast migration is essential in bone regeneration. Although it is known that osteoblasts respond to exogenous electric fields, the underlying mechanism of electrotactic collective movement of human osteoblasts is unclear. Here, we present a computational model that describes the osteoblast cell migration in a direct current electric field as the motion of a collection of active self-propelled particles and takes into account fluctuations in the direction of single-cell migration, finite-range cell-cell interactions, and the interaction of a cell with the external electric field. By comparing this model with in vitro experiments in which human primary osteoblasts are exposed to a direct current electric field of different field strengths, we show that cell-cell interactions and fluctuations in the migration direction promote anode-directed collective migration of osteoblasts. |
Author | van Rienen, Ursula Porath, Katrin Bader, Rainer Sellmann, Tina Köhling, Rüdiger Dawson, Jonathan Edward Appali, Revathi |
AuthorAffiliation | 4 Department of Life, Light and Matter , Interdisciplinary Faculty , University of Rostock , Rostock , Germany 1 Institute of General Electrical Engineering , University of Rostock , Rostock , Germany 7 Center for Translational Neuroscience Research , Rostock University Medical Center , Rostock , Germany 3 Oscar-Langendorff-Institute of Physiology , Rostock University Medical Center , Rostock , Germany 6 Department of Ageing of Individuals and Society , Interdisciplinary Faculty , University of Rostock , Rostock , Germany 5 Biomechanics and Implant Research Lab , Department of Orthopedics , Rostock University Medical Center , Rostock , Germany 2 Department of Chemistry and Physics , Augusta University , Augusta , GA , United States |
AuthorAffiliation_xml | – name: 3 Oscar-Langendorff-Institute of Physiology , Rostock University Medical Center , Rostock , Germany – name: 6 Department of Ageing of Individuals and Society , Interdisciplinary Faculty , University of Rostock , Rostock , Germany – name: 1 Institute of General Electrical Engineering , University of Rostock , Rostock , Germany – name: 4 Department of Life, Light and Matter , Interdisciplinary Faculty , University of Rostock , Rostock , Germany – name: 2 Department of Chemistry and Physics , Augusta University , Augusta , GA , United States – name: 5 Biomechanics and Implant Research Lab , Department of Orthopedics , Rostock University Medical Center , Rostock , Germany – name: 7 Center for Translational Neuroscience Research , Rostock University Medical Center , Rostock , Germany |
Author_xml | – sequence: 1 givenname: Jonathan Edward surname: Dawson fullname: Dawson, Jonathan Edward – sequence: 2 givenname: Tina surname: Sellmann fullname: Sellmann, Tina – sequence: 3 givenname: Katrin surname: Porath fullname: Porath, Katrin – sequence: 4 givenname: Rainer surname: Bader fullname: Bader, Rainer – sequence: 5 givenname: Ursula surname: van Rienen fullname: van Rienen, Ursula – sequence: 6 givenname: Revathi surname: Appali fullname: Appali, Revathi – sequence: 7 givenname: Rüdiger surname: Köhling fullname: Köhling, Rüdiger |
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CitedBy_id | crossref_primary_10_1016_j_mtbio_2024_101083 crossref_primary_10_1103_PhysRevE_108_064411 crossref_primary_10_1089_wound_2024_0003 |
Cites_doi | 10.1016/J.JTBI.2013.03.021 10.3390/math8111875 10.3389/fbioe.2019.00422 10.1146/annurev.cellbio.21.012704.131001 10.1016/j.cels.2020.05.009 10.1038/s41467-020-15164-5 10.1016/j.cels.2018.01.016 10.1088/1478-3975/11/2/026002 10.1074/jbc.m110.142232 10.1038/nphys1269 10.1002/term.1612 10.1002/jor.1100030310 10.1002/jcp.1041290303 10.1371/journal.pone.0122094 10.1016/j.bbrc.2011.07.004 10.3892/ijmm.2016.2590 10.1103/PhysRevE.74.061908 10.1371/journal.pcbi.1005569 10.1091/mbc.E14-12-1580 10.22203/eCM.v022a26 10.1385/cbb:33:1:33 10.1088/1361-6463/aa56fe 10.1007/BF02460652 10.1186/s12918-017-0413-5 10.1039/c3ib40137e 10.1096/fj.01-0811fje 10.1038/NPHYS3040 10.1016/j.jmb.2011.02.001 10.1016/j.bbrc.2004.11.078 10.1016/j.bpj.2021.06.034 10.1038/nmat3891 10.3389/fbioe.2020.557447 10.1073/pnas.1702526114 10.3390/app11125689 10.3892/ijmm.2011.778 10.1091/mbc.E18-01-0077 10.1016/j.bioelechem.2012.08.002 10.1016/j.bioelechem.2020.107578 10.1016/B978-0-12-814841-9.00018-X |
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Copyright | Copyright © 2022 Dawson, Sellmann, Porath, Bader, van Rienen, Appali and Köhling. 2022 Dawson, Sellmann, Porath, Bader, van Rienen, Appali and Köhling |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Reviewed by: Thomas Prescott, Bentley Systems, United Kingdom Edited by: Bin Li, Soochow University, China Paul Tsai, Okinawa Institute of Science and Technology Graduate University, Japan This article was submitted to Tissue Engineering and Regenerative Medicine, a section of the journal Frontiers in Bioengineering and Biotechnology |
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References | Waters (B36) 2005; 21 Szabó (B31) 2006; 74 Dawson (B7) 2020; 8 Zhao (B40) 2011; 22 Stains (B29) 2005 Zhao (B39) 2002; 16 Henkes (B11) 2020; 11 Lara Rodriguez (B15) 2013; 5 Brugués (B3) 2014; 10 Zajdel (B38) 2020; 10 Stains (B30) 2019; 2020 Simpson (B28) 2017; 11 Schienbein (B26) 1993; 55 Cohen (B6) 2014; 13 Gruler (B10) 2000; 33 (B19) 2021 Mousavi (B20) 2013; 329 Rohde (B24) 2019; 7 Prescott (B23) 2021; 120 Lin (B17) 2017; 114 Trepat (B33) 2009; 5 Barton (B1) 2017; 13 Kaivosoja (B14) 2015; 9 Mousavi (B22) 2015; 30 Vanegas-Acosta (B35) 2012; 88 Saltukoglu (B25) 2015 Liang (B16) 2020; 135 Hiemer (B12) 2016; 38 Lochner (B18) 2011; 28 Brighton (B2) 1985; 3 Gruening (B9) 2021; 11 Thurley (B32) 2018; 6 Wu (B37) 2011; 411 Mousavi (B21) 2014; 11 Urdeitx (B34) 2020; 8 Camley (B4) 2017; 50 Sich (B27) 2010; 285 Cho (B5) 2018; 29 Ferrier (B8) 1986; 129 Jacobs (B13) 2011; 407 |
References_xml | – volume: 329 start-page: 64 year: 2013 ident: B20 article-title: 3D computational modelling of cell migration: A mechano-chemo-thermo-electrotaxis approach publication-title: J. Theor. Biol. doi: 10.1016/J.JTBI.2013.03.021 contributor: fullname: Mousavi – volume: 8 start-page: 1875 year: 2020 ident: B34 article-title: A computational model for cardiomyocytes mechano-electric stimulation to enhance cardiac tissue regeneration publication-title: Mathematics doi: 10.3390/math8111875 contributor: fullname: Urdeitx – volume: 7 start-page: 422 year: 2019 ident: B24 article-title: Human osteoblast migration in DC electrical fields depends on store operated Ca2+-release and is correlated to upregulation of stretch-activated TRPM7 channels publication-title: Front. Bioeng. Biotechnol. doi: 10.3389/fbioe.2019.00422 contributor: fullname: Rohde – volume: 21 start-page: 319 year: 2005 ident: B36 article-title: Quorum sensing: Cell-to-cell communication in bacteria publication-title: Annu. Rev. Cell Dev. Biol. doi: 10.1146/annurev.cellbio.21.012704.131001 contributor: fullname: Waters – volume: 10 start-page: 506 year: 2020 ident: B38 article-title: Scheepdog: Programming electric cues to dynamically herd large-scale cell migration publication-title: Cell Syst. doi: 10.1016/j.cels.2020.05.009 contributor: fullname: Zajdel – volume: 11 start-page: 1405 year: 2020 ident: B11 article-title: Dense active matter model of motion patterns in confluent cell monolayers publication-title: Nat. Commun. doi: 10.1038/s41467-020-15164-5 contributor: fullname: Henkes – volume: 6 start-page: 355 year: 2018 ident: B32 article-title: Modeling cell-to-cell communication networks using response-time distributions publication-title: Cell Syst. doi: 10.1016/j.cels.2018.01.016 contributor: fullname: Thurley – volume: 11 start-page: 026002 year: 2014 ident: B21 article-title: Computational modelling of multi-cell migration in a multi-signalling substrate publication-title: Phys. Biol. doi: 10.1088/1478-3975/11/2/026002 contributor: fullname: Mousavi – volume: 285 start-page: 39150 year: 2010 ident: B27 article-title: Effects of actin-myosin kinetics on the calcium sensitivity of regulated thin filaments publication-title: J. Biol. Chem. doi: 10.1074/jbc.m110.142232 contributor: fullname: Sich – volume-title: Matlab year: 2021 ident: B19 – volume: 5 start-page: 426 year: 2009 ident: B33 article-title: Physical forces during collective cell migration publication-title: Nat. Phys. doi: 10.1038/nphys1269 contributor: fullname: Trepat – volume: 9 start-page: 31 year: 2015 ident: B14 article-title: The effect of pulsed electromagnetic fields and dehydroepiandrosterone on viability and osteo-induction of human mesenchymal stem cells publication-title: J. Tissue Eng. Regen. Med. doi: 10.1002/term.1612 contributor: fullname: Kaivosoja – volume: 3 start-page: 331 year: 1985 ident: B2 article-title: Fracture healing in the rabbit fibula when subjected to various capacitively coupled electrical fields publication-title: J. Orthop. Res. doi: 10.1002/jor.1100030310 contributor: fullname: Brighton – volume: 129 start-page: 283 year: 1986 ident: B8 article-title: Osteoclasts and osteoblasts migrate in opposite directions in response to a constant electrical field publication-title: J. Cell. Physiol. doi: 10.1002/jcp.1041290303 contributor: fullname: Ferrier – volume: 30 start-page: e0122094 year: 2015 ident: B22 article-title: Three-dimensional numerical model of cell morphology during migration in multi-signaling substrates publication-title: PLoS ONE doi: 10.1371/journal.pone.0122094 contributor: fullname: Mousavi – volume: 411 start-page: 695 year: 2011 ident: B37 article-title: A receptor-electromigration-based model for cellular electrotactic sensing and migration publication-title: Biochem. Biophysical Res. Commun. doi: 10.1016/j.bbrc.2011.07.004 contributor: fullname: Wu – volume: 38 start-page: 57 year: 2016 ident: B12 article-title: Magnetically induced electrostimulation of human osteoblasts results in enhanced cell viability and osteogenic differentiation publication-title: Int. J. Mol. Med. doi: 10.3892/ijmm.2016.2590 contributor: fullname: Hiemer – volume: 74 start-page: 061908 year: 2006 ident: B31 article-title: Phase transition in the collective migration of tissue cells: Experiment and model publication-title: Phys. Rev. E doi: 10.1103/PhysRevE.74.061908 contributor: fullname: Szabó – volume: 13 start-page: e1005569 year: 2017 ident: B1 article-title: Active Vertex Model for cell-resolution description of epithelial tissue mechanics publication-title: PLoS Comput. Biol. doi: 10.1371/journal.pcbi.1005569 contributor: fullname: Barton – year: 2015 ident: B25 article-title: Spontaneous and electric feld-controlled front-rear polarization of human keratinocytes publication-title: Mol. Biol. Cell doi: 10.1091/mbc.E14-12-1580 contributor: fullname: Saltukoglu – volume: 22 start-page: 344 year: 2011 ident: B40 article-title: Directed migration of human bone marrow mesenchymal stem cells in a physiological direct current electric field publication-title: Eur. Cell. Mat. doi: 10.22203/eCM.v022a26 contributor: fullname: Zhao – volume: 33 start-page: 33 year: 2000 ident: B10 article-title: The Galvanotaxis response mechanism of keratinocytes can be modeled as a proportional controller publication-title: Cell biochem. Biophys. doi: 10.1385/cbb:33:1:33 contributor: fullname: Gruler – volume: 50 start-page: 113002 year: 2017 ident: B4 article-title: Physical models of collective cell motility: From cell to tissue publication-title: J. Phys. D. Appl. Phys. doi: 10.1088/1361-6463/aa56fe contributor: fullname: Camley – volume: 55 start-page: 585 year: 1993 ident: B26 article-title: Langevin equation Fokker-Planck equation and cell migration publication-title: Bull. Math. Biol. doi: 10.1007/BF02460652 contributor: fullname: Schienbein – volume: 11 start-page: 39 year: 2017 ident: B28 article-title: Quantifying the roles of random motility and directed motility using advection-diffusion theory for a 3T3 fibroblast cell migration assay stimulated with an electric field publication-title: BMC Syst. Biol. doi: 10.1186/s12918-017-0413-5 contributor: fullname: Simpson – volume: 5 start-page: 1306 year: 2013 ident: B15 article-title: Directed cell migration in multi-cue environments publication-title: Integr. Biol. doi: 10.1039/c3ib40137e contributor: fullname: Lara Rodriguez – volume: 16 start-page: 857 year: 2002 ident: B39 article-title: Membrane lipidsEGF receptors and intracellular signals colocalize and are polarized in epithelial cells moving directionally in a physiological electric field publication-title: FASEB J. doi: 10.1096/fj.01-0811fje contributor: fullname: Zhao – volume: 10 start-page: 683 year: 2014 ident: B3 article-title: Forces driving epithelial wound healing publication-title: Nat. Phys. doi: 10.1038/NPHYS3040 contributor: fullname: Brugués – volume: 407 start-page: 716 year: 2011 ident: B13 article-title: Kinetics and thermodynamics of the rate-limiting conformational change in the actomyosin V mechanochemical cycle publication-title: J. Mol. Biol. doi: 10.1016/j.jmb.2011.02.001 contributor: fullname: Jacobs – year: 2005 ident: B29 article-title: Cell-to-cell interactions in bone. doi: 10.1016/j.bbrc.2004.11.078 contributor: fullname: Stains – volume: 120 start-page: 3363 year: 2021 ident: B23 article-title: Quantifying the impact of electric fields on single-cell motility publication-title: Biophysical J. doi: 10.1016/j.bpj.2021.06.034 contributor: fullname: Prescott – volume: 13 start-page: 409 year: 2014 ident: B6 article-title: Galvanotactic control of collective cell migration in epithelial monolayers publication-title: Nat. Mat. doi: 10.1038/nmat3891 contributor: fullname: Cohen – volume: 8 start-page: 557447 year: 2020 ident: B7 article-title: A general theoretical framework to study the influence of electrical fields on mesenchymal stem cells publication-title: Front. Bioeng. Biotechnol. doi: 10.3389/fbioe.2020.557447 contributor: fullname: Dawson – volume: 114 start-page: 8568 year: 2017 ident: B17 article-title: Lipid rafts sense and direct electric field-induced migration publication-title: Proc. Natl. Acad. Sci. U. S. A. doi: 10.1073/pnas.1702526114 contributor: fullname: Lin – volume: 11 start-page: 5689 year: 2021 ident: B9 article-title: Automatic actin filament quantification and cell shape modeling of osteoblasts on charged ti surfaces publication-title: Appl. Sci. doi: 10.3390/app11125689 contributor: fullname: Gruening – volume: 28 start-page: 1055 year: 2011 ident: B18 article-title: The potential role of human osteoblasts for periprosthetic osteolysis following exposure to wear particles publication-title: Int. J. Mol. Med. doi: 10.3892/ijmm.2011.778 contributor: fullname: Lochner – volume: 29 start-page: 2292 year: 2018 ident: B5 article-title: Electric field-induced migration and intercellular stress alignment in a collective epithelial monolayer publication-title: Mol. Biol. Cell doi: 10.1091/mbc.E18-01-0077 contributor: fullname: Cho – volume: 88 start-page: 134 year: 2012 ident: B35 article-title: Mathematical model of electrotaxis in osteoblastic cells publication-title: Bioelectrochemistry doi: 10.1016/j.bioelechem.2012.08.002 contributor: fullname: Vanegas-Acosta – volume: 135 start-page: 107578 year: 2020 ident: B16 article-title: Application of stable continuous external electric field promotes wound healing in pig wound model publication-title: Bioelectrochemistry doi: 10.1016/j.bioelechem.2020.107578 contributor: fullname: Liang – volume: 2020 start-page: 432 year: 2019 ident: B30 article-title: Intercellular junctions and cell-cell communication in the skeletal system publication-title: Principles of bone biology doi: 10.1016/B978-0-12-814841-9.00018-X contributor: fullname: Stains |
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SubjectTerms | Bioengineering and Biotechnology cell migration collective migration computational modeling electrotaxis osteoblasts particle based approach |
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Title | Cell-cell interactions and fluctuations in the direction of motility promote directed migration of osteoblasts in direct current electrotaxis |
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