Dielectric measurement of cell death

Enzyme and Microbial Technology

Volumn 43, Issue 7, 2008, Pages 463-470

  Patel, Pareshkumar ^a   Markx, Gerard H ^b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b HERIOT WATT UNIVERSITY   (United Kingdom)

Author keywords

Capacitance; Dielectric spectroscopy; Dielectrophoresis; Electrorotation; Permittivity; Stress; Viability

Indexed keywords

CAPACITANCE; CELL DEATH; CELL MEMBRANES; CYTOLOGY; DIELECTRIC DEVICES; DIELECTRIC PROPERTIES; DIELECTRIC SPECTROSCOPY; ELECTROPHORESIS; HIGH ENERGY PHYSICS;

CELL DIELECTRIC PROPERTIES; CELL VIABILITIES; DIELECTRIC MEASUREMENTS; DIELECTRIC TECHNIQUES; DIELECTROPHORESIS; ELECTROKINETIC; ELECTROROTATION; MAIN PARAMETERS; MEASURING CELLS; VIABILITY;

CELLS;

ANIMAL CELL; APOPTOSIS; CELL DEATH; CELL MEMBRANE CONDUCTANCE; CELL VIABILITY; ELECTRIC CAPACITANCE; ELECTROPHORESIS; HUMAN; MEASUREMENT; NONHUMAN; REVIEW; SPECTROSCOPY; TECHNIQUE;

EID: 55949087943     PISSN: 01410229     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.enzmictec.2008.09.005     Document Type: Review

References (115)

1. Maxwell J.C. A treatise on electricity and magnetism (1873), Clarendon Press, Oxford
2. Fricke H. The electrical capacity of suspensions with special reference to blood. J Gen Physiol 9 (1925) 137-152
3. Fricke H. A mathematical treatment of the electrical conductivity and capacity of disperse systems. II. The capacity of a suspension of conducting spheroids surrounded by a non-conducting membrane for a current of low frequency. Phys Rev 26 (1925) 678-681
4. Schwan H.P. Electrical properties of tissue and cell suspensions. In: Lawrence J.H., and Tobias C.A. (Eds). Advances in biological and medical physics vol. 5 (1957), Academic Press Inc., New York 147-209
5. Schwan H.P., and Foster K.R. RF-field interactions with biological systems: electrical properties and biophysical mechanisms. Proc IEEE 68 (1980) 104-113
6. Pohl H.A. Dielectrophoresis (1978), Cambridge University Press, Cambridge
7. Arnold W.M., and Zimmermann U. Electrorotation-development of a technique for dielectric measurements on individual cells and particles. J Electrostat 21 (1988) 151-191
8. Fuhr G., Fiedler S., Muller T., Schnelle T., Glasser H., Lisec T., et al. Particle micromanipulator consisting of two orthogonal channels with travelling-wave electrode structures. Sens Actuators A: Phys 41 (1994) 230-239
9. Markx G.H., and Davey C.L. The dielectric properties of biological cells at radiofrequencies: applications in biotechnology. Enzyme Microb Technol 25 (1999) 161-171
10. Pethig R., and Kell D.B. The passive electrical properties of biological systems: Their significance in physiology, biophysics and biotechnology. Phys Med Biol 32 (1987) 933-970
11. Hughes M.P. Nanoelectromechanics in engineering and biology (2002), CRC Press, Boca Raton
12. Jones T.B. Electromechanics of particles (1995), Cambridge University Press, Cambridge
13. Morgan H., and Green N.G. AC Electrokinetics: Colloids and Nanoparticles (2001), Research Studies Press, Baldock
14. Pethig R. Dielectric and Electronic Properties of Biological Materials (1979), Wiley, Chichester
15. Gascoyne P.R.C., and Vykoukal J.V. Dielectrophoresis-based sample handling in general-purpose programmable diagnostic instruments. Proc IEEE 92 (2004) 22-42
16. Pethig R., and Talary M.S. Dielectrophoretic detection of membrane morphology changes in Jurkat T-cells undergoing etoposide-induced apoptosis. IET Nanobiotechnol 1 (2007) 2-9
17. Xiao C., Lachance B., and Sunahara G. Assessment of cytotoxicity using electric cell-substrate impedance sensing: concentration and time response function approach. Anal Chem 74 (2002) 5748-5753
18. Xing J.Z., Zhu L., Jackson J.A., Gabos S., Sun X.J., Wang X.B., et al. Dynamic monitoring of cytotoxicity on microelectronic sensors. Chem Res Toxicol 18 (2005) 154-161
19. Spegel C., Heiskanen A., Skjolding L.H.D., and Emneus J. Chip based electroanalytical systems for cell analysis. Electroanalysis 20 (2008) 680-702
20. Harris C.M., Todd R.W., Bungard S.J., Lovitt R.W., Morris J.G., and Kell D.B. Dielectric permittivity of microbial suspensions at radio-frequencies-a novel method for the real-time estimation of microbial biomass. Enz Microb Technol 9 (1987) 181-186
21. Falokun C.D., and Markx G.H. Electrorotation of beads of immobilized cells. J Electrostat 65 (2007) 475-482
22. Salter G.J., Kell D.B., Ash L.A., Adams J.M., Brown A.J., and James R. Hydrodynamic deposition: a novel method of cell immobilisation. Enz Microb Technol 12 (1990) 419-430
23. Kell D.B., Markx G.H., Davey C.L., and Todd R.W. Real-time monitoring of cellular biomass: methods and applications. Trends Anal Chem 9 (1990) 190-194
24. Ducommun P., Kadouri A., von Stockar U., and Marison I.W. On-line determination of animal cell concentration in two industrial high-density culture processes by dielectric spectroscopy. Biotechnol Bioeng 77 (2002) 316-323
25. Markx G.H., Davey C.L., and Kell D.B. The permittistat: a novel type of turbidostat. J Gen Microbiol 137 (1991) 735-743
26. Carvell J.P., and Dowd J.E. On-line measurements and control of viable cell density in cell culture manufacturing processes using radio-frequency impedance. Cytotechnology 50 (2006) 35-48
27. Negrete A., Esteban G., and Kotin R.M. Process optimization of large-scale production of recombinant adeno-associated vectors using dielectric spectroscopy. Appl Microbiol Biotechnol 76 (2007) 761-772
28. Patel P.M., and Markx G.H. A comparative study of cell death using electrical capacitance measurements and dielectrophoresis. Enzymol Microb Technol 43 (2008) 523-530
29. Markx G.H., ten Hoopen H.J.G., Meijer J.J., and Vinke J.L. Dielectric spectroscopy as a novel and convenient tool for the study of the shear sensitivity of plant cells in suspension culture. J Biotechnol 19 (1991) 145-158
30. Stoicheva N.G., Davey C.L., Markx G.H., and Kell D.B. Dielectric spectroscopy: a rapid method for the determination of solvent biocompatibility during biotransformations. Biocatalysis 2 (1989) 245-255
31. Markx G.H., and Kell D.B. The use of dielectric permittivity for the control of the biomass level during biotransformations of toxic substrates in continuous culture. Biotechnol Prog 11 (1995) 64-70
32. Tileva F.P., Yotova L.K., and Markx G.H. Dielectric measurement of the resistance of Trichosporon cutaneum against toxic chemicals. African J Microbiol Res 1 (2007) 117-120
33. Huang Y., Hölzel R., Pethig R., and Wang X.B. Differences in the AC electrodynamics of viable and non-viable yeast-cells determined through combined dielectrophoresis and electrorotation studies. Phys Med Biol 37 (1992) 1499-1517
34. Pethig R. Dielectrophoresis: Using inhomogeneous AC electrical fields to separate and manipulate cells. Crit Rev Biotechnol 16 (1996) 331-348
35. Markx G.H., Talary M.S., and Pethig R. Separation of viable and non-viable yeast using dielectrophoresis. J Biotechnol 32 (1994) 29-37
36. Markx G.H., and Pethig R. Dielectrophoretic separation of cells: continuous separation. Biotechnol Bioeng 45 (1995) 337-343
37. Li H.B., and Bashir R. Dielectrophoretic separation and manipulation of live and heat-treated cells of Listeria on microfabricated devices with interdigitated electrodes. Sens Actuators B Chem 86 (2002) 215-221
38. Kaler K.V.I.S., Xie J.P., Jones T.B., and Paul R. Dual-frequency dielectrophoretic levitation of Canola protoplasts. Biophys J 63 (1992) 58-69
39. Broche L.M., Labeed F.H., and Hughes M.P. Extraction of dielectric properties of multiple populations from dielectrophoretic collection spectrum data. Phys Med Biol 50 (2005) 2267-2274
40. Fatoyinbo H.O., and Hoeftges K.F. Hughes MP Rapid-on-chip determination of dielectric properties of biological cells using imaging techniques in a dielectrophoresis dot microsystem. Electrophoresis 29 (2008) 3-10
41. Gascoyne P.R.C., Noshari J., Becker F.F., and Pethig R. Use of dielectrophoretic collection spectra for characterizing differences between normal and cancerous cells. IEEE Trans Ind Appl 30 (1994) 829-834
42. Huang Y., and Pethig R. Electrode design for negative dielectrophoresis. Meas Sci Technol 2 (1991) 1142-1146
43. Gimsa J., Marszalek P., Loewe U., and Tsong T.Y. Dielectrophoresis and electrorotation of neurospora slime and murine myeloma cells. Biophys J 60 (1991) 749-760
44. Ratanachoo K., Gascoyne P.R.C., and Ruchirawat M. Detection of cellular responses to toxicants by dielectrophoresis. Biochim Biophys Acta: Biomembr 1564 (2002) 449-458
45. Labeed F.H., Coley H.M., and Hughes M.P. Differences in the biophysical properties of membrane and cytoplasm of apoptotic cells revealed using dielectrophoresis. Biochim Biophys Acta: Gen Subj 1760 (2006) 922-929
46. Hölzel R. Non-invasive determination of bacterial single cell properties by electrorotation. Biochim Biophys Acta 1450 (1999) 53-60
47. Hölzel R., and Lamprecht I. Dielectric properties of yeast cells as determined by electrorotation. Biochim Biophys Acta 1104 (1992) 195-200
48. Wang X.B., Huang Y., Gascoyne P.R.C., Becker F.F., Hölzel R., and Pethig R. Changes in Friend murine erythroleukemia cell-membranes during induced-differentiation determined by electrorotation. Biochim Biophys Acta: Biomembr 1193 (1994) 330-344
49. Arnold W.M., Zimmermann U., Pauli W., Benzing M., Niehns C., and Ahlers J. The comparative influence of substituted phenols (especially chlorophenols) on yeast cells assayed by electro-rotation and other methods. Biochim Biophys Acta 942 (1988) 83-95
50. Dalton C., Goater A.D., Drysdale J., and Pethig R. Parasite viability by electrorotation. Colloid Surf A: Phys Eng Aspects 195 (2002) 263-268
51. Kriegmaier M., Zimmermann M., Wolf K., Zimmermann U., and Sukhorukov V.L. Dielectric spectroscopy of Schizosaccharomyces pombe using electrorotation and electroorientation. Biochim Biophys Acta: Gen Subj 1568 (2001) 135-146
52. Ivanov A.Y., Fomchenkov V.M., Khasanova L.A., Kuramshina Z.M., and Sadikov M.M. Effect of heavy-metal ions on the electrophysical properties of Anacystis nidulans and Escherichia coli. Microbiology 61 (1992) 319-326
53. Ivanov A.Y., and Fomchenkov V.M. Electrophysical analysis of the damage to Escherichia coli by silver ions. Microbiology 61 (1992) 326-332
54. Guliy O.I., Bunin V.D., O'Neil D., Ivnitski D., and Ignatov O.V. A new electro-optical approach to rapid assay of cell viability. Biosens Bioelectron 23 (2007) 583-587
55. Miller R.D., and Jones T.B. Electro-orientation of ellipsoidal erythrocytes-theory and experiment. Biophys J 64 (1993) 1588-1595
56. Markx G.H., Alp B., and McGilchrist A. Electro-orientation of Schizosaccharomyces pombe in high conductivity media. J Microb Methods 50 (2002) 55-62
57. Guliy O.I., Ignatov O.V., Markina L.N., Bunin V.D., and Ignatov V.V. Action of ampicillin and kanamicin on the electrophysical characteristics of Escherichia coli cells. Int J Environ Anal Chem 85 (2005) 981-992
58. Fink S.L., and Cookson B.T. Apoptosis, pyroptosis, and necrosis: Mechanistic description of dead and dying eukaryotic cells. Infect Immun 73 (2005) 1907-1916
59. Schwartz S.M., and Bennett M.R. Death by any other name. Am J Pathol 147 (1995) 229-234
60. Kell D.B., Kaprelyants A.S., Weichart D.H., Harwood C.R., and Barer M.R. Viability and activity in readily culturable bacteria: a review and discussion of the practical issues. Antonie van Leeuwenhoek 73 (1998) 169-187
61. Kaprelyants A.S., Gottschal J.C., and Kell D.B. Dormancy in non-sporulating bacteria. FEMS Microb Rev 104 (1993) 271-286
62. McNeil P.L., and Terasaki M. Coping with the inevitable: how cells repair a torn surface membrane. Nature Cell Biol 3 (2001) E124-E129
63. Wang X.J., Becker F.F., and Gascoyne P.R.C. Membrane dielectric changes indicate induced apoptosis in HL-60 cells more sensitively than surface phosphatidylserine expression or DNA fragmentation. Biochim Biophys Acta: Biomembr 1564 (2002) 412-420
64. Huang C.J., Chen A.L., Wang L., Guo M., and Yu J. Electrokinetic measurements of dielectric properties of membrane for apoptotic HL-60 cells on chip-based device. Biomed Microdev 9 (2007) 335-343
65. Zhou X.F., Burt J.P.H., and Pethig R. Automatic cell electrorotation measurements: studies of the biological effects of low-frequency magnetic fields and of heat shock. Phys Med Biol 43 (1998) 1075-1090
66. Sudsiri J., Wachner D., and Gimsa J. On the temperature dependence of the dielectric membrane properties of human red blood cells. Bioelectrochemistry 70 (2007) 134-140
67. Ferris L.E., Davey C.L., and Kell D.B. Evidence from its temperature-dependence that the beta-dielectric dispersion of cell-suspensions is not due solely to the charging of a static membrane capacitance. Eur Biophys J 18 (1990) 267-276
68. Morita S., Shimanouchi T., Sasaki M., Umakoshi H., and Kuboi R.J. Detection of a heat stress-mediated interaction between protein and phospholipid membrane using dielectric measurement. Bioscience Bioeng 95 (2003) 252-256
69. Stoneman M., Chturvedi A., Jansma D.B., Kosepma M., Zeng C., and Raicu V. Protein influence on the plasma membrane dielectric properties: In vivo study utilizing dielectric spectroscopy and fluorescence microscopy. Bioelectrochemistry 70 (2007) 542-550
70. Kent M., Knochel R., Daschner F., Schimmer O., Oehlenschlager J., Mierke-Klemeyer S., et al. Intangible but not intractable: the prediction of fish 'quality' variables using dielectric spectroscopy. Meas Sci Technol 18 (2007) 1029-1037
71. Querido D. Temperature-correction of abdominal impedance: improved relationship between impedance and postmortem interval. Forensic Sci Int 109 (2000) 39-50
72. McRae D.A., Esrick M.A., and Mueller S.C. Changes in the noninvasive, in vivo electrical impedance of three xenografts during the necrotic cell-response sequence. Int J Radiat Oncol Biol Phys 43 (1999) 849-857
73. Raicu V., Saibara T., and Irimajiri A. Multifrequency method for dielectric monitoring of cold-preserved organs. Phys Med Biol 45 (2000) 1397-1407
74. Freitag R., Schügerl K., Arnold W.M., and Zimmermann U. The effect of osmotic and mechanical stresses and enzymatic digestion on the electro-rotation of insect cells (Spodoptera frugiperda). J Biotechnol 11 (1989) 325-336
75. Sukhorukov V.L., Arnold W.M., and Zimmermann U. Hypotonically induced changes in the plasma-membrane of cultured mammalian cells. J Membr Biol 132 (1993) 27-40
76. Davey C.L., Kell D.B., Kemp R.B., and Meredith R.W.J. On the audio- and radio-frequency dielectric behaviour of anchorage-independent, mouse L929-derived LS fibroblasts. Bioelectrochem Bioenerg 20 (1988) 83-98
77. Davey C.L., Markx G.H., and Kell D.B. On the dielectric method of monitoring cellular viability. Pure Appl Chem 65 (1993) 1921-1926
78. Seeman P. Membrane actions of anesthetics and tranquillizers. Pharmacol Rev 24 (1972) 583-655
79. Asami K. Dielectric dispersion of erythrocyte ghosts. Phys Rev E 73 (2006) 052903
80. Asami K. Effects of membrane disruption on dielectric properties of biological cells. J Phys D: Appl Phys 39 (2006) 4656-4663
81. Zhou X.F., Markx G.H., and Pethig R. Effect of biocide concentration on electrorotation spectra of yeast cells. Biochim Biophys Acta 1281 (1996) 60-64
82. Salter G.J., and Kell D.B. Solvent selection for whole-cell biotransformations in organic media. Crit Rev Biotechnol 15 (1995) 139-177
83. Laane C., Boeren S., and Vos K. On optimizing organic solvents in multi-liquid-phase biocatalysis. Trends Biotechnol 3 (1985) 251-252
84. Pauli W., Berger S., Kohler M., and Gies A. Detecting membrane impairment caused by xenobiotics. Environ Toxicol Water Qual 8 (1993) 173-189
85. Raicu V., Gusbeth C., Anghel D.F., and Turcu G. Effects of cetyltrimethylammonium bromide (CTAB) surfactant upon the dielectric properties of yeast cells. Biochim Biophys Acta: Gen Subj 1379 (1998) 7-15
86. Johari J., Hubner Y., Hull J.C., Dale J.W., and Hughes M.P. Dielectrophoretic assay of bacterial resistance to antibiotics. Phys Med Biol 48 (2003) N193-N198
87. Hoettges K.F., Dale J.W., and Hughes M.P. Rapid determination of antibiotic resistance in E. coli using dielectrophoresis. Phys Med Biol 52 (2007) 6001-6009
88. Hölzel R. Nystatin-induced changes in yeast monitored by time-resolved automated single cell electrorotation. Biochim Biophys Acta 1425 (1998) 311-318
89. Bai W., Zhao K.S., and Asami K. Effects of copper on dielectric properties of E. coli cells. Colloid Surf B: Biointerfaces 58 (2007) 105-115
90. Arnold W.M., Geier B.M., Wendt B., and Zimmermann U. The change in the electro-rotation of yeast cells effected by silver ions. Biochim Biophys Acta 889 (1986) 35-48
91. Geier B.M., Wendt B., Arnold W.M., and Zimmermann U. The effect of mercuric salts on the electro-rotation of yeast cells and comparison with a theoretical model. Biochim Biophys Acta 900 (1987) 45-55
92. Archer S., Morgan H., and Rixon F.J. Electrorotation studies of baby hamster kidney fibroblasts infected with herpes simplex virus type 1. Biophys J 76 (1999) 2833-2842
93. Gimsa J., Pritzen C., and Donath E. Characterization of virus-red-cell interaction by electrorotation. Stud Biophys 130 (1989) 123-131
94. Zeiser A., Elias C.B., Voyer R., Jardin B., and Kamen A.A. On-line monitoring of physiological parameters of insect cell cultures during the growth and infection process. Biotechnol Prog 16 (2000) 803-808
95. Zeiser A., Bedard C., Voyer R., Jardin B., Tom R., and Kamen A.A. On-line monitoring of the progress of infection in Sf-9 insect cell cultures using relative permittivity measurements. Biotechnol Bioeng 63 (1999) 122-126
96. Ansorge S., Esteban G., and Schmid G. On-line monitoring of infected Sf-9 insect cell cultures by scanning permittivity measurements and comparison with off-line biovolume measurements. Cytotechnology 55 (2007) 115-124
97. Carvell J., Bhat A., Patel P.M., and Markx G.H. Recent developments in using scanning radio-frequency impedance measurements on cell culture processes. Bioprocess J 4 (2007) 24-27
98. Bonincontro A., Di Ilio V., Pedata O., and Risuleo G. Dielectric properties of the plasma membrane of cultured murine fibroblasts treated with a nonterpenoid extract of Azadirachta indica seeds. J Membr Biol 215 (2007) 75-79
99. Cannizzaro C., Gugerli R., Marison I., and von Stockar U. On-line biomass monitoring of CHO perfusion culture with scanning dielectric spectroscopy. Biotechnol Bioeng 84 (2003) 597-610
100. Maskow T., Röllich A., Fetzer I., Ackemann J.U., and Harms H. On-line monitoring of lipid storage in yeast using impedance spectroscopy. J Biotechnol 135 (2008) 64-70
101. Green N.G., and Jones T.B. Numerical determination of the effective moments of non-spherical particles. J Phys D: Appl Phys 40 (2007) 78-85
102. Gimsa J. A comprehensive approach to electro-orientation, electrodeformation, dielectrophoresis, and electrorotation of ellipsoidal particles and biological cells. Bioelectrochem 54 (2001) 23-31
103. Asami K. Characterization of biological cells by dielectric spectroscopy. J Non Cryst Solids 305 (2002) 268-277
104. Pavlin M., and Miklavcic D. Effective conductivity of a suspension of permeabilised cells: a theoretical analysis. Biophys J 85 (2003) 719-729
105. Morgan H., Tao S., Holmes D., Gawad S., and Green N.G. Single cell dielectric spectroscopy. J Phys D: Appl Phys 40 (2007) 61-70
106. Gawad S., Cheung K., Seger U., Bertsch A., and Renaud P. Dielectric spectroscopy in a micromachined flow cytometer: theoretical and practical considerations. Lab Chip 4 (2004) 241-251
107. Lapizco-Encinas B.H., Simmons B.A., Cummings E.B., and Fintschenko Y. Dielectrophoretic concentration and separation of live and dead bacteria in an array of insulators. Anal Chem 76 (2004) 1571-1579
108. Demierre N., Braschler T., Muller R., and Renaud P. Focusing and continuous separation of cells in a microfluidic device using lateral dielectrophoresis. Sens Actuators B: Chem 132 (2008) 388-396
109. Hawkins B.G., Smith A.E., Syed Y.A., and Kirby B.J. Continuous-flow particle separation by 3D insulative dielectrophoresis using coherently shaped, dc-biased, ac electric fields. Anal Chem 79 (2007) 7291-7300
110. Urdaneta M., and Smela E. Multiple frequency dielectrophoresis. Electrophoresis 28 (2007) 3145-3155
111. Chin S., Hughes M.P., Coley H.M., and Labeed F.H. Rapid assessment of early biophysical changes in K562 cells during apoptosis determined using dielectrophoresis. Int J Nanomed 1 (2006) 333-337
112. Pethig R., Bressler V., Carswell-Crumpton C., Chen Y., Foster-Haje L., Garcia-Ojeda M.E., et al. Dielectrophoretic studies of the activation of human T lymphocytes using a newly developed cell profiling system. Electrophoresis 23 (2002) 2057-2063
113. Burt J.P.H., Goater A.D., Menachery A., Pethig R., and Rizvi N.H. Development of microtitre plates for electrokinetic assays. J Micromech Microeng 17 (2007) 250-257
114. Hoettges K.F., Hubner Y., Broche L.M., Ogin S.L., Kass G.E.N., and Hughes M.P. Dielectrophoresis-activated multiwell plate for label-free high-throughput drug assessment. Anal Chem 80 (2008) 2063-2068
115. Talary M.S., Burt J.P.H., and Pethig R. Future trends in diagnosis using laboratory-on-a-chip technologies. Parasitology 117 (1998) S191-S203