Skip to main content
Cellular & Molecular Biology Letters logoLink to Cellular & Molecular Biology Letters
. 2013 Mar 7;18(2):187–199. doi: 10.2478/s11658-013-0082-3

The role of passive calcium influx through the cell membrane in galvanotaxis

Przemysław Borys 1,
PMCID: PMC6275758  PMID: 23468381

Abstract

Passive calcium influx is one of the theories to explain the cathodal galvanotaxis of cells that utilize the electric field to guide their motion. When exposed to an electric field, the intracellular fluid becomes polarized, leading to positive charge accumulation on the cathodal side and negative charge accumulation on the anodal side. The negative charge on the anodal side attracts extracellular calcium ions, increasing the anodal calcium concentration, which is supposed to decrease the mobile properties of this side. Unfortunately, this model does not capture the Ca2+ dynamics after its presentation to the intracellular fluid. The ions cannot permanently accumulate on the anodal side because that would build a potential drop across the cytoplasm leading to an ionic current, which would carry positive ions (not only Ca2+) from the anodal to the cathodal part through the cytoplasm. If the cytoplasmic conductance for Ca2+ is low enough compared to the membrane conductance, the theory could correctly predict the actual behavior. If the ions move through the cytoplasm at a faster rate, compensating for the passive influx, this theory may fail. This paper contains a discussion of the regimes of validity for this theory.

Key words: Galvanotaxis, Electrotaxis, Passive influx, Leak current, PNP equation, Electrodiffusion, Motility

Full Text

The Full Text of this article is available as a PDF (396.6 KB).

Abbreviations used

PMCA

plasma membrane Ca2+ ATPase

PNP equation

Poisson-Nernst-Planck equation

SERCA

sarco/endoplasmic reticulum Ca2+ ATPase

TRPC

transient receptor potential cation channels

VGCC

voltage-gated calcium channel

References

  • 1.Ananthakrishnan R, Ehrlicher A. The forces behind cell movement. Int. J. Biol. Sci. 2007;3:303–317. doi: 10.7150/ijbs.3.303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Korohoda W, Kucia M, Wybieralska E, Wianecka-Skoczeń M, Waligórska A, DrukaŁa J, Madeja Z. Solute-dependent activation of cell motility in strongly hypertonic solutions in Dictyostelium discoideum, Human Melanoma HTN-140 cells and Walker 256 Carcinosarcoma cells. Cell. Mol. Biol. Lett. 2011;16:412–430. doi: 10.2478/s11658-011-0015-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Shanley LJ, Walczysko P, Bain M, MacEwan DJ, Zhao M. Influx of extracellular Ca2+ is necessary for electrotaxis in Dictyostelium. J. Cell Sci. 2006;119:4741–4748. doi: 10.1242/jcs.03248. [DOI] [PubMed] [Google Scholar]
  • 4.Djamgoz MBA. Directional movement of rat prostate cancer cells in direct-current electric field: involvement of voltage-gated Na+ channel activity. J. Cell Sci. 2001;114:2697–2705. doi: 10.1242/jcs.114.14.2697. [DOI] [PubMed] [Google Scholar]
  • 5.Alt W, Deutsch A, Dunn G. Dynamics of cell and tissue motion. Basel: Birkhauser; 1997. [Google Scholar]
  • 6.Bray D. Cell movements: from molecules to motility. 2nd edition. New York: Garland Publishing; 2000. [Google Scholar]
  • 7.Barnes FS, Greenbaum B, editors. Handbook of biological effects of electromagnetic fields. Boca Raton: CRC press; 2007. [Google Scholar]
  • 8.Nuccitelli R. A role for endogenous electric fields in wound healing. Curr. Top. Dev. Biol. 2003;58:1–26. doi: 10.1016/s0070-2153(03)58001-2. [DOI] [PubMed] [Google Scholar]
  • 9.McCaig CD, Rajnicek AM, Song B, Zhao M. Controlling cell behavior electrically: current views and future potential. Physiol. Rev. 2005;85:943–978. doi: 10.1152/physrev.00020.2004. [DOI] [PubMed] [Google Scholar]
  • 10.Mycielska ME, Djamgoz MBA. Cellular mechanisms of directcurrent electric field effects: galvanotaxis and metastatic disease. J. Cell Sci. 2004;117:1631–1639. doi: 10.1242/jcs.01125. [DOI] [PubMed] [Google Scholar]
  • 11.Fang KS, Behnom F, Nuccitelli R, Isseroff RR. Migration of human keratinocytes in electric fields requires growth factors and extracellular calcium. J. Invest. Dermatol. 1998;111:751–756. doi: 10.1046/j.1523-1747.1998.00366.x. [DOI] [PubMed] [Google Scholar]
  • 12.Trollinger DR, Isseroff RR, Nuccitelli R. Calcium channel blockers inhibit galvanotaxis in human keratinocytes. J. Cell. Physiol. 2002;193:1–9. doi: 10.1002/jcp.10144. [DOI] [PubMed] [Google Scholar]
  • 13.Aonuma M, Kadano T, Kawano T. Inhibition of anodic galvanotaxis of Green Paramecia by T-type calcium channel inhibitors. Z. Naturforsch. 2007;62c:93–102. doi: 10.1515/znc-2007-1-217. [DOI] [PubMed] [Google Scholar]
  • 14.Wang GX, Poo MM. Requirement of TRPC channels in netrin-1-induced chemotropic turning of nerve growth cones. Nature. 2005;434:898–904. doi: 10.1038/nature03478. [DOI] [PubMed] [Google Scholar]
  • 15.Torossian F, Bisson A, Vannier JP, Boyer O, Lamacz M. TRPC expression in mesenchymal cells. Cell. Mol. Biol. Lett. 2010;15:600–610. doi: 10.2478/s11658-010-0031-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Cooper MS, Keller RE. Perpendicular orientation and directional migration of amphibian neural crest cells in dc electrical fields. Proc. Natl. Acad. Sci. USA. 1984;81:160–164. doi: 10.1073/pnas.81.1.160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Chen TH, Jaffe LF. Effects of membrane potential on calcium fluxes of pelvetia eggs. Planta. 1978;140:63–67. doi: 10.1007/BF00389381. [DOI] [PubMed] [Google Scholar]
  • 18.Robinson KR. The responses of cells to electrical fields: a review. J. Cell Biol. 1985;101:2023–2027. doi: 10.1083/jcb.101.6.2023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Isaacson BM, Bloebaum RD. Bone bioelectricity: what have we learned in the past 160 years? J. Biomed. Mat. Res. A. 2010;95A:1270–1279. doi: 10.1002/jbm.a.32905. [DOI] [PubMed] [Google Scholar]
  • 20.Gao RCh, Zhang XD, Sun YH, Kamimura Y, Mogilner A, Devreotes PN, Zhao M. Different roles of membrane potentials in electrotaxis and chemotaxis of Dictyostelium cells. Eukaryot. Cell. 2011;10:1251–1256. doi: 10.1128/EC.05066-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Borys P. On the biophysics of cathodal galvanotaxis in rat prostate cancer cells: Poisson-Nernst-Planck equation approach. Eur. Biophys. J. 2012;41:527–534. doi: 10.1007/s00249-012-0807-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Coalson RD, Kurnikova MG. Poisson-Nernst-Planck theory of ion permeation through biological channels. In: Chung SH, Andersen OS, Krishnamurthy V, editors. Biological membrane ion channels. New York: Springer; 2007. pp. 449–485. [Google Scholar]
  • 23.Kurnikova MG, Coalson RD, Graf P, Nitzan A. A lattice relaxation algorithm for three-dimensional Poisson-Nernst-Planck theory with application to ion transport through the Gramicidin A channel. Biophys. J. 1999;76:642–656. doi: 10.1016/S0006-3495(99)77232-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Rubinstein I. SIAM studies in applied mathematics. 1990. Electro-diffusion of ions. [Google Scholar]
  • 25.Ni MJ, Tao WQ, Wang SJ. Stability controllable second-order difference scheme for convection term. J. Therm. Sci. 1998;7:119–130. [Google Scholar]
  • 26.Abelson PH, Duryee WR. Radioactive sodium permeability and exchange in frog eggs. Biol. Bull. 1949;96:205–217. [PubMed] [Google Scholar]
  • 27.Hodgkin AL, Keynes RD. The mobility and diffusion coefficient of potassium in giant axons from Sepia. J. Physiol. 1953;119:513–528. doi: 10.1113/jphysiol.1953.sp004863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Donahue BS, Abercrombie RF. Free diffusion coefficient of ionic calcium in cytoplasm. Cell Calcium. 1987;8:437–448. doi: 10.1016/0143-4160(87)90027-3. [DOI] [PubMed] [Google Scholar]
  • 29.Lodish HF, Berk A, Matsudaira P, Kaiser CA, Krieger M, Scott MP, Zipursky L, Darnell J. Molecular Cell Biology. W.H. New York: Freeman; 2003. [Google Scholar]
  • 30.Neher E, Sakmann B. Single channel recording. New York: Plenum; 1995. [Google Scholar]
  • 31.Kager H, Wasman WJ, Somjen GG. Simulated seizures and spreading depression in a neuron model incorporating interstitial space and ion concentrations. J. Neurophysiol. 2000;84:495–512. doi: 10.1152/jn.2000.84.1.495. [DOI] [PubMed] [Google Scholar]
  • 32.Zeng J, Borchman D, Paterson CA. Calcium permeability in large unilamellar vesicles prepared from bovine lens cortical lipids. Exp. Eye Res. 1997;64:115–120. doi: 10.1006/exer.1996.0186. [DOI] [PubMed] [Google Scholar]
  • 33.Obejero-Paz CA, Jones SW, Scarpa A. Multiple channels mediate calcium leakage in the A7r5 smooth muscle-derived cell line. Biophys. J. 1998;32:12–21. doi: 10.1016/S0006-3495(98)74047-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Di Leva F, Domi T, Fedrizzi L, Lim D, Carafoli E. The plasmamembrane Ca2+ ATPase of animal cells: Structure, function and regulation. Arch. Biochem. Biophys. 2008;476:65–74. doi: 10.1016/j.abb.2008.02.026. [DOI] [PubMed] [Google Scholar]

Articles from Cellular & Molecular Biology Letters are provided here courtesy of BMC

RESOURCES