Methodological aspects of measuring absolute values of membrane potential in human cells by flow cytometry

Cytometry Part A

Volumn 75, Issue 7, 2009, Pages 593-608

  Klapperstück, Thomas ^a   Glanz, Dagobert ^a   Klapperstück, Manuela ^a   Wohlrab, Johannes ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

Bis barbituric acid oxonol; Flow cytometry; Membrane potential; mV scale calibration

Indexed keywords

BARBITURIC ACID DERIVATIVE; CELL PROTEIN; FLUORESCENT DYE; POTASSIUM;

ARTICLE; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE POTENTIAL; CELL SIZE; CELL VOLUME; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EXTRACELLULAR SPACE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MELANOMA CELL; PHOTOCHEMICAL QUENCHING; PRIORITY JOURNAL; PROTEIN CONTENT; SPECTROFLUOROMETRY;

ANIMALS; BARBITURATES; CELL LINE; CELL LINE, TUMOR; CHO CELLS; CRICETINAE; CRICETULUS; FLOW CYTOMETRY; FLUORESCENT DYES; HUMANS; ISOXAZOLES; MEMBRANE POTENTIALS; MICROSCOPY, CONFOCAL;

EID: 67649518193     PISSN: 15524922     EISSN: 15524930     Source Type: Journal    
DOI: 10.1002/cyto.a.20735     Document Type: Article

References (84)

1. Zhang J, Davidson RM, Wei M-D, Loew LM. Membrane electric properties by combined patch clamp and fluorescence ratio imaging in single neurons. Biophys J 1998;74:48-53. (Pubitemid 28041735)
2. Baxter DF, Kirk M, Garcia AF, Raimondi A, Holmqvist MH, Flint KK, Bojanic D, di Stefano PS, Curtis R, Xie Y. A novel membrane-potential-sensitive fluorescent dye improves cell-based assays for ion channels. J Biomol Screen 2002;7:79-85. (Pubitemid 34208865)
3. Shapiro HM, Natale PJ, Kamentsky LA. Estimation of membrane potentials of individual lymphocytes by flow cytometry. Proc Natl Acad Sci USA 1979;76:5728-5730.
4. Brauner T, Holser DF, Strasser RJ. Comparative measurements of membrane potentials with microelectrodes and voltage-sensitive dyes. Biochim Biophys Acta 1984;771:208-216.
5. Wilson HA, Seligmann BE, Chused TM. Voltage-sensitive cyanine dye fluorescence signals in lymphocytes: Plasma membrane and mitochondrial components. J Cell Physiol 1985;125:61-71. (Pubitemid 15012070)
6. 2+ sensitive potassium channels described by oxonol dye fluorescence measurement. J Cell Physiol 1985;125:72-81.
7. Civitelli R, Reid IR, Halstead LR, Avioli V, Hruska KA. Membrane potential and cation content of osteoblast-like cells (UMR 106) assessed by fluorescent dyes. J Cell Physiol 1987;131:434-441. (Pubitemid 17113059)
8. Krasznai Z, Marian T, Balkay L, Emri M, Tron L. Flow cytometric determination of absolute membrane potential of cells. J Photochem Photobiol B 1995;28:93-99.
9. Dall'Asta V, Gatti R, Orlandini G, Rossi PA, Rotoli BM, Sala R, Bussolati O, Gazzola GC. Membrane potential changes visualized in complete growth media through confocal laser scanning microscopy of bis-oxonol-loaded cells. Exp Cell Res 1997;231:260-268. (Pubitemid 27187977)
10. Mandala M, Serck-Hanssen G, Martino G, Helle KB. The fluorescent cationic dye rhodamine 6G as a probe for membrane potential in bovine aortic endothelial cells. Anal Biochem 1999;274:1-6. (Pubitemid 29466348)
11. Wolff C, Fuks B, Chatelain P. Comparative study of membrane potential-sensitive fluorescent probes and their use in ion channel screening assays. J Biomol Screen 2003;8:533-543. (Pubitemid 40503585)
12. - currents regulate steady-state and dynamic membrane potentials in cultured rat microglia. J Physiol 2005;567:869-890.
13. Bunting JR, Phan TV, Kamali E, Dowben RM. Fluorescent cationic probes of mitochondria metrics and mechanism of interaction. Biophys J 1989;56:979-993.
14. Plasek J, Vojtiskova A, Houstek J. Flow-cytometric monitoring of mitochondrial depolarisation: From fluorescence intensities to millivolts. J Photochem Photobiol B 2005;78:99-108. (Pubitemid 40123685)
15. Brewis IA, Morton IE, Mohammad SN, Browes CE, Moore HD. Measurement of intracellular calcium concentration and plasma membrane potential in human spermatozoa using flow cytometry. J Androl 2000;21:238-249. (Pubitemid 30123705)
16. Marian T, Balkay L, Krasznai Z, Tron L. Membrane permeability changes induce hyperpolarization in transformed lymphoid cells under high-density culture conditions. Cytometry 2000;41:186-192. (Pubitemid 30813095)
17. Patrat C, Serres C, Jouannet P. Progesterone induces hyperpolarization after a transient depolarization phase in human spermatozoa. Biol Reprod 2002;66:1775-1780. (Pubitemid 34547276)
18. Hladky SB, Rink TJ. Potential difference and the distribution of ions across the human red blood cell membrane; a study of the mechanism by which the fluorescent cation, diS-C3-(5) reports membrane potential. J Physiol 1976;263:287-319.
19. Tsien RY, Hladky SB. A quantitative resolution of the spectra of a membrane potential indicator, diS-C3-(5), bound to cell components and to red blood cells. J Membr Biol 1978;38:73-97.
20. Chowdhury A, Wachsmann-Hogiu S, Bangal PR, Raheem I, Peteanu LA. Characterization of chiral H and J aggregates of cyanine dyes formed by DNA templating using Stark and fluorescence spectroscopies. J Phys Chem B 2001;105:12196-12201. (Pubitemid 35338379)
21. Zhang Y, Xiang J, Tang Y, Xu G, Yan W. Transition of H- and J-aggregate of a cyanine dye based on cation embedded in aggregation. Chem Lett 2006;35:1316-1317.
22. Novo D, Perlmutter NG, Hunt RH, Shapiro HM. Accurate flow cytometric membrane potential measurement in bacteria using diethyloxacarbocyanine and a ratiometric technique. Cytometry 1999;35:55-63. (Pubitemid 29031192)
23. Zeng Y, Clark EN, Florman HM. Sperm membrane potential: Hyperpolarization during capacitation regulates zona pellucida-dependent acrosomal secretion. Dev Biol 1995;171:554-563.
24. Shapiro HM. Membrane potential estimation by flow cytometry. Methods 2000;21:271-279. (Pubitemid 32896751)
25. Lloyd D, Harris JC, Biagini GA, Hughes MR, Maroulis S, Bernard C, Wadley RB, Edwards MR. The plasma membrane of microaerophilic protists: Oxidative and nitrosative stress. Microbiology 2004;150:1183-1190. (Pubitemid 38744719)
26. Sguilla FS, Tedesco AC, Bendhack LM. A membrane potential-sensitive dye for vascular smooth muscle cells assays. Biochem Biophys Res Commun 2003;301:113-118. (Pubitemid 36268856)
27. + ATPase as a signaling molecule during bovine sperm capacitation. Biol Reprod 2006;75:308-317.
28. Mohr FC, Fewtrell C. IgE receptor-mediated depolarisation of rat basophilic leukaemia cells measured with the fluorescent probe bis-oxonol. J Immunol 1987;138:1564-1570. (Pubitemid 17029458)
29. Bortner CD, Gomez-Angelats M, Cidlowski JA. Plasma membrane depolarization without repolarization is an early molecular event in anti-Fas-induced apoptosis. J Biol Chem 2001;276:4304-4314. (Pubitemid 37371520)
30. Plasek J, Sigler K. Slow fluorescent indicators of membrane potential: A survey of different approaches to probe response analysis. J Photochem Photobiol B: Biol 1996;33:101-124. (Pubitemid 26193794)
31. 4(3)) in model systems and cells. Chem Phys Lipids 1994;69:137-150.
32. Varga Z, Bene L, Pieri C, Damjanovich S, Gáspár R Jr. The effect of juglone on the membrane potential and whole-cell K1 currents of human lymphocytes. Biochem Biophys Res Commun 1996;218:828-832. (Pubitemid 26050748)
33. Louzao MC, Cagide E, Vieytes MR, Sasaki M, Fuwa H, Yasumoto T, Botana LM. The sodium channel of human excitable cells is a target for gambierol. Cell Physiol Biochem 2006;17:257-268. (Pubitemid 43948348)
34. Piacenza L, Irigoin F, Alvarez MN, Peluffo G, Taylor MC, Kelly JM, Wilkinson SR, Radi R. Mitochondrial superoxide radicals mediate programmed cell death in Trypanosoma cruzi: Cytoprotective action of mitochondrial iron superoxide dismutase overexpression. Biochem J 2007;403:323-334. (Pubitemid 46596589)
35. Szaszi K, Sirokmany G, Di Ciano-Oliveira C, Rotstein OD, Kapus A. Depolarization induces Rho-Rho kinase-mediated myosin light chain phosphorylation in kidney tubular cells. Am J Physiol Cell Physiol 2005;289:C673-C685. (Pubitemid 41192677)
36. Becherer U, Rodeau J-L, Feltz A. Resting potential of rat cerebellar granule cells during early maturation in vitro. J Neurobiol 1998;32:11-21.
37. (2+) overload in cardiac myocytes via modulation of the diastolic membrane potential. Br J Pharmacol 2004;141:1059-1067.
38. Defrise-Quertain F, Fraser-l'Hostis C, Coral D, Deshusses J. Kinetic study of the plasma-membrane potential in procyclic and bloodstream forms of Trypanosoma brucei using the fluorescent probe bisoxonol. Biochem J 1996;314:595-601. (Pubitemid 26074775)
39. + channel openers and glucose deprivation. J Physiol 1997;502 (Part 2):397-408.
40. + channel excitability in embryonic rat cortical cells. Eur J Neurosci 1998;10:2532-2546.
41. (2+) exchange. Am J Physiol Cell Physiol 2002;282:C1000-C1008.
42. Bancila V, Nikonenko I, Dunant Y, Bloc A. Zinc inhibits glutamate release via activation of pre-synaptic KATP channels and reduces ischaemic damage in rat hippocampus. J Neurochem 2004;90:1243-1250. (Pubitemid 39167357)
43. Konig S, Hinard V, Arnaudeau S, Holzer N, Potter G, Bader CR, Bernheim L. Membrane hyperpolarization triggers myogenin and myocyte enhancer factor-2 expression during human myoblast differentiation. J Biol Chem 2004;279:28187-28196. (Pubitemid 38900094)
44. Chifflet S, Hernandez JA, Silvina Grasso S. A possible role for membrane depolarization in epithelial wound healing. Am J Physiol Cell Physiol 2005;288:C1420-C1430. (Pubitemid 40991079)
45. Kremer SC, Breuer WV, Skorecki K. Vasoconstrictor hormones depolarize renal glomerular mesangial cells by activating chloride channels. J Cell Physiol 1989;138:97-105. (Pubitemid 19038676)
46. ++ exchange in the neuroblastoma cell line SK-N-SH. J Pharmacol Exp Ther 1997;280:795-801.
47. Bankers-Fulbright JL, Gleich GJ, Kephart GM, Kita H, O'Grady SM. Regulation of eosinophil membrane depolarization during NADPH oxidase. J Cell Sci 2003;116:3221-3226. (Pubitemid 37038970)
48. Seidl J, Knuechel R, Kunz-Schughart LA. Evaluation of membrane physiology following fluorescence activated or magnetic cell separation. Cytometry 1999;36:102-111.
49. Dryselius S, Lund P-E, Hellman B. Local changes of medium in studies of individual cells. Cell Struct Funct 1994;19:385-390.
50. Chifflet S, Hernandez JA, Grasso S, Cirillo A. Nonspecific depolarization of the plasma membrane potential induces cytoskeletal modifications of bovine corneal endothelial cells in culture. Exp Cell Res 2003;282:1-13. (Pubitemid 36062607)
51. Tarnok A. Rare-event sorting by fixed-time flow cytometry based on changes in intracellular free calcium. Cytometry 1997;27:65-70. (Pubitemid 27059783)
52. Seamer LC, Mandler RN. Method to improve the sensitivity of flow cytometric membrane potential measurements in mouse spinal cord cells. Cytometry 1992;13:545-552.
53. Radosevic K, Schut TCB, van Graft M, de Grooth BG, Greve J. A flow cytometric study of the membrane potential of natural killer and K562 cells during the cytotoxic process. J Immunol Methods 1993;161:119-128. (Pubitemid 23142136)
54. Shapiro HM. Estimation of membrane potential by flow cytometry. In: Robinson JP, Darzynkiewicz Z, Hoffman R, Nolan J, Orfao A, Rabinovitch P, Watkins S, editors. Current Protocols in Cytometry. New York: Wiley; 2004. pp 9.6.1-9.6.12.
55. Rink TJ, Montecucco C, Hesketh TR, Tsien RY. Lymphocyte membrane potential assessed with fluorescent probes. Biochim Biophys Acta 1980;595:15-30. (Pubitemid 10174464)
56. Burry RW, Wood JG. Contributions of lipids and proteins to the surface charge of membranes. J Cell Biol 1979;82:726-741.
57. Chan JW, Taylor DS, Thompson DL. The effect of cell fixation on the discrimination of normal and leukemia cells with laser tweezers Raman spectroscopy. Biopolymers 2009;91:132-139.
58. Nelson R, Bender AM, Connaughton VP. Stimulation of sodium pump restores membrane potential to neurons excited by glutamate in zebrafish distal retina. J Physiol 2003;549:787-800. (Pubitemid 36889769)
59. Haslberger A, Romanin C, Koerber R. Membrane potential modulates release of tumor necrosis factor in lypopolysaccharide-stimulated mouse macrophages. Mol Biol Cell 1992;3:451-460. (Pubitemid 23079747)
60. 4(3), a voltage-sensitive fluorescent dye, for the measurement of membrane potentials regulated by recombinant large conductance Ca2+-activated K1 channels in HEK293 cells. Jpn J Pharmacol 2001;86:342-350.
61. Emri M, Balkay L, Krasznai Z, Tron L, Marian T. Wide applicability of a flow cytometric assay to measure absolute membrane potentials on the millivolt scale. Eur Biophys J 1998;28:78-83. (Pubitemid 29222686)
62. Wonderlin WF, Woodfork KA, Strobl JS. Changes in membrane potential during the progression of MCF-7 human mammary tumor cells through the cell cycle. J Cell Physiol 1995;165:177-185.
63. Gavrilova-Ruch O, Schönherr K, Gessner G, Schönherr R, Klapperstück T, Wohlrab W, Heinemann SH. Effects of imipramine on ion channels and proliferation of IGR1 melanoma cells. J Membr Biol 2002;188:137-149. (Pubitemid 34804258)
64. Panner A, Wurster RD. T-type calcium channels and tumor proliferation. Cell Calcium 2006;40:253-259. (Pubitemid 43942305)
65. Valic B, Golzio M, Pavlin M, Schatz A, Faurie C, Gabriel B, Teissie J, Rols M-P, Miklavcic D. Effect of electric field induced transmembrane potential on spheroidal cells: Theory and experiment. Eur Biophys J 2003;32:519-528. (Pubitemid 37408656)
66. Zhang Z, Huang JMC, Turner MR, Rhinehart KL, Pallone TL. Role of chloride in constriction of descending vasa recta by angiotensin II. Am J Physiol Regul Integr Comp Physiol 2001;280:R1878-R1886. (Pubitemid 32552478)
67. 3(3) assay for relative potentials as an indicator of real changes. Biochim Biophys Acta 1994;1196:181-190.
68. 3 cotransporter in mouse sperm capacitation. J Biol Chem 2003;278:7001-7009.
69. Aleman C, Annereau J-P, Liang X-J, Cardarelli CO, Taylor B, Yin JJ, Aszalos A, Gottesman MM. P-glycoprotein, expressed in multidrug resistant cells, is not responsible for alterations in membrane fluidity or membrane potential. Cancer Res 2003;63:3084-3091. (Pubitemid 36735857)
70. 2+ influx and subsequent initiation of sperm motility in the common carp. Proc Natl Acad Sci USA 2000;97:2052-2057.
71. + uptake. Am J Physiol Cell Physiol 2007;292:C935-C944.
72. Breittmayer JP, Pelassy C, Aussel C. Effect of membrane potential on phosphatidylserine synthesis and calcium movements in control and CD3-activated Jurkat T cells. J Lipid Mediat Cell Signal 1996;13:151-161. (Pubitemid 26080622)
73. Berney M, Weilenmann H-U, Egli T. Flow-cytometric study of vital cellular functions in Escherichia coli during solar disinfection (SODIS). Microbiology 2006;152:1719-1729. (Pubitemid 43919257)
74. Alper SL, Chernova MN, Williams J, Zasloff M, Law FY, Knauf PA. Differential inhibition of AE1 and AE2 anion exchangers by oxonol dyes and by novel polyaminosterol analogs of the shark antibiotic squalamine. Biochem Cell Biol 1998;76:799-806. (Pubitemid 29318177)
75. Schmieder S, Soriani O, Brochiero E, Raschi C, Bogliolo S, Lindenthal S, Ehrenfeld J. Characterization of the taurine transport pathway in A6 kidney cells. J Membr Biol 2002;190:145-158. (Pubitemid 36930429)
76. Liu X, Williams JB, Sumpter BR, Bevensee MO. Inhibition of the Na/bicarbonate cotransporter NBCe1-A by diBAC oxonol dyes relative to niflumic acid and a stilbene. J Membr Biol 2007;215:195-204. (Pubitemid 47282685)
77. + channels in the control of membrane potential in rabbit renal arcuate artery. J Physiol 1998;511:159-169.
78. + channel a-subunit. Mol Pharmacol 2002;62:836-846.
79. Liu X, Chang Y, Reinhart PH, Sontheimer H. Cloning and characterization of glioma BK, a novel BK channel isoform highly expressed in human glioma cells. J Neurosci 2002;22:1840-1849. (Pubitemid 35386302)
80. Ca channel in cultured smooth muscle cells of human trachea by magnolol. Thorax 2002;57:67-74.
81. Friis UG, Jorgensen F, Andreasen D, Jensen BL, Skott O. Membrane potential and cation channels in rat juxtaglomerular cells. Acta Physiol Scand 2004;181:391-396. (Pubitemid 39078834)
82. + channels in breast cancer cells. Biochem Biophys Res Commun 2004;316:244-251.
83. 2+-activated big conductance K channels in cultured human endothelial cells. Hypertension 2007;50:643-651.
84. + channel activators selective for beta1 and beta4 but not for beta2 subunits. Mol Pharmacol 2007;71:1075-1088.