Review

The mechanical responses of cell to electrical stimulation

  • SUN Weihao ,
  • MA Jianli ,
  • LIU Hailong ,
  • WU Chengwei ,
  • ZHANG Wei ,
  • PENGPAT Kamonpan
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  • 1. Department of Engineering Mechanics, State Key Laboratory of Structural Analysis for Industrial Equipment, Dalian University of Technology, Dalian 116024, China;
    2. Department of Biomedical Engineering, Dalian University of Technology, Dalian 116024, China;
    3. Department of Physics and Materials Science, Faculty of Science, Chiang Mai University, Chiang Mai 50202, Thailand

Received date: 2019-11-15

  Revised date: 2020-05-11

  Online published: 2021-01-14

Abstract

In the past 40 years, the electrical stimulation is widely applied in biomedicine, largely due to the progress achieved in the experimental studies of electrical stimulation of cells. The obtained results are valuable for developing novel diagnosis and therapy techniques for diseases. Recent studies focused on the mechanism by which electrical stimulation alters cellular biological behavior, but the interpretation of many of related phenomena is difficult and controversial. We discuss the experimental equipment for electrical stimulation of cells from three aspects:the direct current electric field, the sinusoidal electric field and the pulsed electric field, and the effects of electrical stimulation on the mechanical properties of cells, including the elasticity modulus, the intercellular stress, the cell adhesion and the cell membrane tether force, as well as the corresponding biological mechanism and the application of electrical stimulation in inducing the cell differentiation, the apoptosis and changing the cell migration direction. The correlations among the electrical stimulation, the mechanical characteristics of cells and the biological behavior of cells are analyzed. Finally, we highlight the existing problems in the electrical stimulation of cells and put forward some suggestions for the future development.

Cite this article

SUN Weihao , MA Jianli , LIU Hailong , WU Chengwei , ZHANG Wei , PENGPAT Kamonpan . The mechanical responses of cell to electrical stimulation[J]. Science & Technology Review, 2020 , 38(22) : 114 -122 . DOI: 10.3981/j.issn.1000-7857.2020.22.013

References

[1] Polk C. Biological applications of large electric fields:Some history and fundamentals[J]. IEEE Transactions on Plasma Science, 2000, 28(1):6-14.
[2] Malmivuo J, Plonsey R. Bioelectromagnetism[M]. Oxford:Oxford University Press, 1995:2-3.
[3] Geddes L A. Historical highlights in cardiac pacing[J]. IEEE Engineering in Medicine and Biology Magazine, 1990, 9(2):12-18.
[4] Timms D. A review of clinical ventricular assist devices[J]. Medical Engineering and Physics, 2011, 33(9):1041-1047.
[5] Jaffe L F, Nuccitelli R. Electrical controls of development[J]. Annual Review of Biophysics and Bioengineering, 1977(6):445-476.
[6] Bai G, Li Y, Chu H K, et al. Characterization of biomechanical properties of cells through dielectrophoresisbased cell stretching and actin cytoskeleton modeling[J]. BioMedical Engineering OnLine, 2017, 16(1):41.
[7] Titushkin I, Cho M. Regulation of cell cytoskeleton and membrane mechanics by electric field:Role of linker proteins[J]. Biophysical Journal, 2009, 96(2):717-728.
[8] Titushkin I A, Cho M R. Controlling cellular biomechanics of human mesenchymal stem cells[C]. Proceedings of the 31st Annual International Conference of the IEEE Engineering in Medicine and Biology Society:Engineering the Future of Biomedicine, Piscataway, NJ:IEEE, 2009:2090-2093.
[9] Titushkin I, Cho M. Altered osteogenic commitment of human mesenchymal stem cells by ERM protein-dependent modulation of cellular biomechanics[J]. Journal of Biomechanics, 2011, 44(15):2692-2698.
[10] McBeath M, Pirone D M, Nelson C M, et al. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment[J]. Developmental Cell, 2004, 6(4):483-495.
[11] Wong P K, Tan W, Ho C M. Cell relaxation after electrodeformation:Effect of latrunculin A on cytoskeletal actin[J]. Journal of Biomechanics, 2005, 38(3):529-535.
[12] Pelling A E, Horton M A. An historical perspective on cell mechanics[J]. Pflugers Archiv-European Journal of Physiology, 2008, 456(1):3-12.
[13] Janmey P A, McCulloch C A. Cell Mechanics:Integrating cell responses to mechanical stimuli[J]. Annual Review of Biomedical Engineering, 2007(9):1-34.
[14] Meyers V E, Zayzafoon M, Douglas J T, et al. RhoA and cytoskeletal disruption mediate reduced osteoblastogenesis and enhanced adipogenesis of human mesenchymal stem cells in modeled microgravity[J]. Journal of Bone and Miner research, 2005, 20(10):1858-1866.
[15] Engler A J, Sen S, Sweeney H L, et al. Matrix elasticity directs stem cell lineage specification[J]. Cell, 2006, 126(4):677-689.
[16] Ruan J L, Tulloch N L, Razumova M V, et al. Mechanical stress conditioning and electrical stimulation promote contractility and force maturation of induced pluripotent stem cell-derived human cardiac tissue[J]. Circulation, 2016, 134(20):1557-1567.
[17] Smith P G, Deng L, Fredberg J J, et al. Mechanical strain increases cell stiffness through cytoskeletal filament reorganization[J]. Lung Cellular and Molecular Physiology, 2003, 285(2):456-463.
[18] Cho Y, Son M, Jeong M, et al. Electric field-induced migration and intercellular stress alignment in a collective epithelial monolayer[J]. Molecular Biology of the Cell, 2018(29):2243-2357.
[19] Curtze S, Dembo M, Miron M, et al. Dynamic changes in traction forces with DC electric field in osteoblast-like cells[J]. Journal of Cell Science, 2004(117):2721-2729.
[20] Steckel R R, Page E H, Geddes L A, et al. Electrical stimulation on skin wound healing in the horse:Preliminary studies[J]. Amreican Journal of Veterinary Research, 1984, 45(4):800-803.
[21] Thrivikraman G, Boda S K, Basu B. Unraveling the mechanistic effects of electric field stimulation towards directing stem cell fate and function:A tissue engineering perspective[J]. Biomaterials, 2018(150):60-86.
[22] Mobini S, Leppik L, Barker J H. Direct current electrical stimulation chamber for treating cells in vitro[J]. Biotechniques, 2016, 60(2):95-98.
[23] Yizraeli M L, Weihs D. Time-dependent micromechanical responses of breast cancer cells and adjacent fibroblasts to electric treatment[J]. Cell Biochemistry and Biophysics, 2011, 61(3):605-618.
[24] Jaatinen L, Young E, Hyttinen J. Quantifying the effect of electric current on cell adhesion studied by singlecell force spectroscopy[J]. Biointerphases, 2016, 11(4):1-8.
[25] Tambe D T, Hardin C C, Angelini T E, et al. Collective cell guidance by cooperative intercellular forces[J]. Nature Materials, 2011(10):469-475.
[26] Sun S, Titushkin I, Cho M. Regulation of mesenchymal stem cell adhesion and orientation in 3D collagen scaffold by electrical stimulus[J]. Bioelectrochemistry, 2006, 69(2):133-141.
[27] Sun S, Liu Y, Lipsky S, et al. Physical manipulation of calcium oscillations facilitates osteodifferentiation of human mesenchymal stem cells[J]. The FASEB Journal, 2007, 21(7):1472-1480.
[28] Kim J H, Serra-Picamal X, Tambe D T, et al. Propulsion and navigation within the advancing monolayer sheet[J]. Nature Materials, 2013(12):856-863.
[29] Salipante P F, Shapiro M L, Vlahovska PM. Electric field induced deformations of biomimetic fluid membranes[J]. Procedia Iutam, 2015(16):60-69.
[30] Portet T, Mauroy C, Demery V, et al. Destabilizing giant vesicles with electric fields:An overview of current applications[J]. The Journal of Membrane Biology, 2012, 245(9):555-564.
[31] Kummrow M, Helfrich W. Deformation of giant lipid vesicles by electric fields[J]. Physical Review A, 1991, 44(12):8356-8361.
[32] Li Z, Anvari B, Takashima M, et al. Membrane tether formation from outer hair cells with optical tweezers[J]. Biophysical Journal, 2002, 82(3):1386-1395.
[33] Qian F, Ermilov S, Murdock D, et al. Combining optical tweezers and patch clamp for studies of cell membrane electromechanics[J]. Review of Scientific Instruments, 2004, 75(9):2937-2942.
[34] Brownell W E, Qian F, Anvari B. Cell membrane tethers generate mechanical force in response to electrical stimulation[J]. Biophysical Journal, 2010, 99(3):845-852.
[35] Qian F, William E B, Bahman A. Effect of ionic strength on electrically evoked membrane tether force:An optical tweezers study[J]. Proceedings of SPIE, 2004(5514):626-631.
[36] Beebe S, Sain N, Ren W. Induction of cell death mechanisms and apoptosis by nanosecond pulsed electric fields (nsPEFs)[J]. Cells, 2013, 2(1):136-162.
[37] 郑超. 低温等离子体和脉冲电场灭菌技术[D]. 杭州:浙江大学, 2013.
[38] 黄康. 高压脉冲电场处理室内多物理场对微生物灭活作用的研究[D]. 杭州:浙江大学, 2013.
[39] Pillet F, Formosa-Dague C, Baaziz H, et al. Cell wall as a target for bacteria inactivation by pulsed electric fields[J]. Science Reports, 2016, 6(1):19778-19778.
[40] Schoenbach K H, Beebe S J, Buescher E S. Intracellular effect of ultrashort electrical pulses[J]. Bioelectromagnetics, 2001, 22(6):440-448.
[41] Kolb J F, Kono S, Schoenbach K H. Nanosecond pulsed electric field generators for the study of subcellular effects[J]. Bioelectromagnetics, 2006, 27(3):172-187.
[42] Berghöfer T, Eing C, Flickinger B, et al. Nanosecond electric pulses trigger actin responses in plant cells[J]. Biochemical and Biophysical Research Communications, 2009, 387(3):590-595.
[43] Dutta D, Asmar A, Stacey M. Effects of nanosecond pulse electric fields on cellular elasticity[J]. Micron, 2015(72):15-20.
[44] Hohenberger P, Eing C, Straessner R, et al. Plant actin controls membrane permeability[J]. Biochimica Biophysica Acta(BBA) -Biomembranes, 2011, 1808(9):2304-2312.
[45] Xiao D, Tang L, Zeng C, et al. Effect of actin cytoskeleton disruption on electric pulse-induced apoptosis and electroporation in tumour cells[J]. Cell Biology International, 2011, 35(2):99-104.
[46] Thompson G L, Roth C, Tolstykh G, et al. Disruption of the actin cortex contributes to susceptibility of mammalian cells to nanosecond pulsed electric fields[J]. Bioelectromagnetics, 2014, 35(4):262-272.
[47] Stacey M, Fox P, Buescher S, et al. Nanosecond pulsed electric field induced cytoskeleton, nuclear membrane and telomere damage adversely impact cell survival[J]. Bioelectrochemistry, 2011, 82(2):131-134.
[48] Louise C, Etienne D, Marie-Pierre R. AFM sensing cortical actin cytoskeleton destabilization during plasma membrane electropermeabilization[J]. Cytoskeleton, 2014, 71(10):587-594.
[49] Chopinet L, Roduit C, Rols M P, et al. Destabilization induced by electropermeabilization analyzed by atomic force microscopy[J]. Biochimica et Biophysica Acta (BBA)-Biomembranes, 2013, 1828(9):2223-2229.
[50] Chopinet L, Rols M P. Nanosecond electric pulses:A mini-review of the present state of the art[J]. Bioelectrochemistry, 2015(103):2-6.
[51] Nuccitelli R, Pliquett U, Chen X, et al. Nanosecond pulsed electric fields cause melanomas to self-destruct[J]. Biochemical and Biophysical Research Communication, 2006, 343(2):351-360.
[52] Nuccitelli R, Chen X, Pakhomov A G, et al. A new pulsed electric field therapy for melanoma disrupts the tumor's blood supply and causes complete remission without recurrence[J]. International Journal of Cancer, 2009, 125(2):438-445.
[53] 张仁民, 姚陈果, 陈新, 等. ns级陡脉冲诱导肿瘤细胞凋亡的实验研究[J]. 高电压技术, 2007(2):106-108.
[54] 姚青, 宋治远, 马显光. 脉冲微交流电刺激促进体外诱导大鼠骨髓间充质干细胞向心肌分化[J]. 第三军医大学学报, 2008(5):410-413.
[55] Timoshkin I V, MacGregor S J, Fouracre R A, et al. Forces acting on biological cells in external electrical fields[C]. IEEE Conference on Electrical Insulation and Dielectric Phenomena. Piscataway, NJ:IEEE, 2006.
[56] Teissie J, Golzio M, Rols M P. Mechanisms of cell membrane electropermeabilization:A minireview of our present (lack of?) knowledge[J]. Biochimica et Biophysica Acta(BBA)-General Subjects, 2005, 1724(3):270-280.
[57] Neumann E, Kakorin S, Tœnsing K. Fundamentals of electroporative delivery of drugs and genes[J]. Bioelectrochemistry Bioenerg, 1999, 48(1):3-16.
[58] Sack M, Sigler J, Frenzel S, et al. Research on industrial-scale electroporation devices fostering the extraction of substances from biological tissue[J]. Food Engineering Reviews, 2010, 2(2):147-156.
[59] Knorr D, Angersbach A, Eshtiaghi M N, et al. Processing concepts based on high intensity electric field pulses[J]. Trends in Food Science and Technology, 2001, 12(3/4):129-135.
[60] Gusbeth C, Frey W, Volkmann H, et al. Pulsed electric field treatment for bacteria reduction and its impact on hospital wastewater[J]. Chemosphere, 2009, 75(2):228-233.
[61] Toepfl S, Heinz V, Knorr D. High intensity pulsed electric fields applied for food preservation[J]. Chemical Engineering and Processing:Process Intensification, 2007, 46(6):537-546.
[62] Sun X, Nunes S S. Biowire platform for maturation of human pluripotent stem cell-derived cardiomyocytes[J]. Methods, 2016, 101(15):21-26.
[63] Poo M M, Poo W J H, Lam J W. Lateral electrophoresis and diffusion of concanavalin:A receptors in the membrane of embryonic muscle cell[J]. Journal of Cell Biology, 1978, doi:10.1083/jcb.76.2.483.on cell migration and actin filament distribution in bovine vascular endothelial cells[J]. Journal of Vascular Research, 2002(39):391-404.
[65] Li Y, Xu T, Chen X, et al. Effects of direct current electric fields on lung cancer cell electrotaxis in a PMMAbased microfluidic device[J]. Analytical and Bioanalytical Chemistry, 2017, 409(8):2163-2178.
[66] Kotnik T, Pucihar G, Reberšek M, et al. Role of pulse shape in cell membrane electropermeabilization[J]. Biochimica et Biophysica Acta(BBA)-Biomembranes, 2003, 1614(2):193-200.
[67] Miklavcic D, Towhidi L. Numerical study of the electroporation pulse shape effect on molecular uptake of biological cells[J]. Radiology & Oncology, 2010, 44(1):34-41.
[64] Li X, Kolega J. Effects of direct current electric fields
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