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Estimation of the physical properties of neurons and glial cells using dielectrophoresis crossover frequency

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Abstract

We successfully determine the ranges of dielectric permittivity, cytoplasm conductivity, and specific membrane capacitance of mouse hippocampal neuronal and glial cells using dielectrophoresis (DEP) crossover frequency (CF). This methodology is based on the simulation of CF directly from the governing equation of a dielectric model of mammalian cells, as well as the measurements of DEP CFs of mammalian cells in different suspension media with different conductivities, based on a simple experimental setup. Relationships between the properties of cells and DEP CF, as demonstrated by theoretical analysis, enable the simultaneous estimation of three properties by a straightforward fitting procedure based on experimentally measured CFs. We verify the effectiveness and accuracy of this approach for primary mouse hippocampal neurons and glial cells, whose dielectric properties, previously, have not been accurately determined. The estimated neuronal properties significantly narrow the value ranges available from the literature. Additionally, the estimated glial cell properties are a valuable addition to the scarce information currently available about this type of cell. This methodology is applicable to any type of cultured cell that can be subjected to both positive and negative dielectrophoresis.

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References

  1. Chitwood, R.A., Hubbard, A., Jaffe, D.B.: Passive electrotonic properties of rat hippocampal CA3 interneurones. J. Physiol. 515(3), 743–756 (1999)

    Article  Google Scholar 

  2. Major, G., Larkman, A.U., Jonas, P., Sakmann, B., Jack, J.B.: Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices. J. Neurosci. 14(8), 4613–4638 (1994)

    Google Scholar 

  3. Mainen, Z.F., Carnevale, N.T., Zador, A.M., Claiborne, B.J., Brown, T.H.: Electrotonic architecture of hippocampal CA1 pyramidal neurons based on three-dimensional reconstructions. J. Neurophysiol. 76(3), 1904–1923 (1996)

    Google Scholar 

  4. Carnevale, N.T., Tsai, K.Y., Claiborne, B.J., Brown, T.H.: Comparative electrotonic analysis of three classes of rat hippocampal neurons. J. Neurophysiol. 78(2), 703–720 (1997)

    Google Scholar 

  5. Rall, W.: Theory of physiological properties of dendrites. Ann. N. Y. Acad. Sci. 96, 1071–1092 (1962)

    Article  ADS  Google Scholar 

  6. Miles, R.: Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea-pig in vitro. J. Physiol. 428, 61–77 (1990)

    Article  Google Scholar 

  7. Traub, R.D., Miles, R.: Pyramidal cell-to-inhibitory cell spike transduction explicable by active dendritic conductances in inhibitory cell. J. Comput. Neurosci. 2(4), 291–298 (1995)

    Article  Google Scholar 

  8. Gentet, L.J., Stuart, G.J., Clement, J.D.: Direct measurement of specific membrane capacitance in neurons. Biophys. J. 79, 314–320 (2000)

    Article  Google Scholar 

  9. Pilwat, G., Zimmermann, U.: Determination of intracellular conductivity from electrical breakdown measurements. Biochim. Biophys. Acta 820, 305–314 (1985)

    Article  Google Scholar 

  10. Heida, T., Rutten, W.L.C., Marani, E.: Dielectrophoretic trapping of dissociated fetal cortical rat neurons. IEEE Trans. Biomed. Eng. 48(8), 921–930 (2001)

    Article  Google Scholar 

  11. Flanagan, L.A., Lu, J., Wang, L., Marchenko, S.A., Jeon, N.L., Lee, A.P., Monuki, E.S.: Unique dielectric properties distinguish stem cells and their differentiated progeny. Stem Cells 26(3), 656–665 (2008)

    Article  Google Scholar 

  12. Pethig, R., Menachery, A., Pells, S., Sousa, P.D.: Dielectrophoresis: a review of applications for stem cell research. J. Biomed. Biotechnol. 2010, 182581 (2010)

    Article  Google Scholar 

  13. Jaber, F.T., Labeed, F.H., Hughes, M.P.: Action potential recording from dielectrophoretically positioned neurons inside micro-wells of a planar microelectrode array. J. Neurosci. Methods 182, 225–235 (2009)

    Article  Google Scholar 

  14. Sano, M.B., Henslee, E.A., Schmelz, E., Davalos, R.V.: Contactless dielectrophoretic spectroscopy: examination of the dielectric properties of cells found in blood. Electrophoresis 32(22), 3164–3171 (2011)

    Article  Google Scholar 

  15. Gagnon, Z.R.: Cellular dielectrophoresis: applications to the characterization, manipulation, separation and patterning of cells. Electrophoresis 32, 2466–2487 (2011)

    Article  Google Scholar 

  16. Morgan, H., Sun, T., Holmes, D., Gawad, S., Green, N.G.: Single cell dielectric spectroscopy. J. Phys. D Appl. Phys. 40, 61–70 (2007)

  17. Pethig, R.: Dielectrophoresis: status of the theory, technology, and applications. Biomicrofluidics 4, 022811 (2010)

  18. Mahaworasilpa, T.L., Coster, H.G.L., George, E.P.: Forces on biological cells due to applied alternating (AC) electric fields. I. Dielectrophoresis. Biochim. Biophys. Acta 1193, 118–126 (1994)

    Article  Google Scholar 

  19. Gascoyne, P., Pethig, R., Satayavivad, J., Becker, F.F., Ruchirawat, M.: Dielectrophoretic detection of changes in erythrocyte membranes following malarial infection. Biochim. Biophys. Acta 1323, 240–252 (1997)

    Article  Google Scholar 

  20. Vykoukal, D.M., Gascoyne, P.R., Vykoukal, J.: Dielectric characterization of complete mononuclear and polymorphonuclear blood cell subpopulations for label-free discrimination. Integr. Biol. 1(7), 477–484 (2009)

    Article  Google Scholar 

  21. Vahey, M.D., Voldman, J.: An equilibrium method for continuous-flow cell sorting using dielectrophoresis. Anal. Chem. 80, 3135–3143 (2008)

    Article  Google Scholar 

  22. Vahey, M.D., Voldman, J.: High-throughput cell and particle characterization using isodielectric separation. Anal. Chem. 81(7), 2446–2455 (2009)

    Article  Google Scholar 

  23. Gagnon, Z., Gordon, J., Sengupta, S., Chang, H.-C.: Bovine red blood cell starvation age discrimination through a glutaraldehyde-amplified dielectrophoretic approach with buffer selection and membrane cross-linking. Electrophoresis 29, 2272–2279 (2008)

    Article  Google Scholar 

  24. Gascoyne, P.R.C., Shim, S., Noshari, J., Becker, F.F., Stemke-Hale, K.: Correlations between the dielectric properties and exterior morphology of cells revealed by dielectrophoretic field-flow fractionation. Electrophoresis 34, 1042–1050 (2013)

    Article  Google Scholar 

  25. Schwan, H.P.: Electrical properties of tissue and cell suspensions. Adv. Biol. Med. Phys. 5, 147–209 (1957)

    Article  Google Scholar 

  26. Lei, U., Sun, P.-H., Pethig, R.: Refinement of the theory for extracting cell dielectric properties from dielectrophoresis and electrorotation experiments. Biomicrofluidics 5(4), 44109–4410916 (2011)

    Article  Google Scholar 

  27. Huang, Y., Wang, X.B., Becker, F.F., Gascoyne, P.R.C.: Membrane changes associated with the temperature-sensitive P85gag-mos-dependent transformation of rat kidney cells as determined by dielectrophoresis and electrorotation. Biochim. Biophys. Acta 1282, 76–84 (1996)

    Article  Google Scholar 

  28. Jones, T.B.: Electromechanics of Particles, pp. 34–81. Cambridge University Press, New York (1995)

  29. Zhou, T., Tatic-Lucic, S.: On application of positive dielectrophoresis and microstructure confinement on multielectrode array with sensory applications. Proc. Sensors, IEEE, Taipei, 1–4 (2012)

  30. Pohl, H.A.: Dielectrophoresis: the Behavior of Neutral Matter in Nonuniform Electric Fields. Cambridge University Press, New York (1978)

  31. Yu, Z., Xiang, G., Pan, L., Huang, L., Yu, Z., Xing, W., Cheng, J.: Negative dielectrophoretic force assisted construction of ordered neuronal networks on cell positioning bioelectronic chips. Biomed. Microdevices 6(4), 311–324 (2004)

    Article  Google Scholar 

  32. Huang, Y., Wang, X.B., Becker, F.F., Gascoyne, P.R.: Introducing dielectrophoresis as a new force field for field-flow fractionation. Biophys. J. 73(2), 1118–1129 (1997)

    Article  Google Scholar 

  33. Gagnon, Z., Senapati, S., Gordon, J., Chang, H.-C.: Dielectrophoretic detection and quantification of hybridized DNA molecules on nano-genetic particles. Electrophoresis 29, 4808–4812 (2008)

    Article  Google Scholar 

  34. Prasad, S., Zhang, X., Yang, M., Ni, Y., Parpura, V., Ozkan, C.S., Ozkan, M.: Separation of individual neurons using dielectrophoretic alternative current fields. J. Neurosci. Methods 135, 79–88 (2004)

    Article  Google Scholar 

  35. Asami, K., Takahashi, Y., Takashima, S.: Dielectric properties of mouse lymphocytes and erythrocytes. Biochim. Biophys. Acta Mol. Cell. Res. 1010, 49–55 (1989)

  36. Peters, M., Stinstra, J., Leveles, I.: Modeling and imaging of bioelectrical activity principles and applications. In: He, B. (ed.) Bioelectric Engineering, pp. 281–319. Springer, New York (2005)

  37. Okada, Y.C., Huang, J., Rice, M.E., Tranchina, D., Nicholson, C.: Origin of the apparent tissue conductivity in the molecular and granular layers of the in vitro turtle cerebellum and the interpretation of current source-density analysis. J. Neurophysiol. 72(2), 742–753 (1994)

    Google Scholar 

  38. Wang, X.-B., Huang, Y., Gascoyne, P.R.C., Becker, F.F., Holzel, R., Pethig, R.: Changes in Friend murine erythroleukaemia cell membranes during induced differentiation determined by electrorotation. Biochim. Biophys. Acta Biomembr. 1193(2), 330–344 (1994)

  39. Zhou, T., Perry, S.F., Tatic-Lucic, S.: On combining the dielectrophoresis and microdevices: Investigation of hippocampal neuronal viability after implementing dielectrophoretic positioning on multi-electrode arrays. BIODEVICES 2015, Proceedings of the International Conference on Biomedical Electronics and Devices, Lisbon, Portugal, 71–77 (2015)

  40. Zhou, T., Perry, S.F., Ming, Y., Petryna, S., Fluck, V., Tatic-Lucic, S.: Separation and assisted patterning of hippocampal neurons from glial cells using positive dielectrophoresis. Biomed. Microdevices 17(3), 9965 (2015). doi:10.1007/s10544-015-9965-6

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Acknowledgments

This work was funded by The National Science Foundation (NSF) through grant NSF ECCS-1321356.

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Authors and Affiliations

  1. Department of Electrical and Computer Engineering, Lehigh University, 16A Memorial Dr. East, Bethlehem, PA, 18015, USA

    Tianyi Zhou, Yixuan Ming & Svetlana Tatic-Lucic

  2. Bioengineering Program, Lehigh University, Bethlehem, PA, 18015, USA

    Susan F. Perry & Svetlana Tatic-Lucic

  3. Department of Chemical Engineering, Lehigh University, Bethlehem, PA, 18015, USA

    Susan F. Perry

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  1. Tianyi Zhou
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  2. Yixuan Ming
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  4. Svetlana Tatic-Lucic
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Correspondence to Tianyi Zhou or Svetlana Tatic-Lucic.

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Zhou, T., Ming, Y., Perry, S.F. et al. Estimation of the physical properties of neurons and glial cells using dielectrophoresis crossover frequency. J Biol Phys 42, 571–586 (2016). https://doi.org/10.1007/s10867-016-9424-5

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  • DOI: https://doi.org/10.1007/s10867-016-9424-5

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