Tetrazolium dyes as tools in cell biology: New insights into their cellular reduction

Biotechnology Annual Review

Volumn 11, Issue SUPPL., 2005, Pages 127-152

  Berridge, Michael V ^a   Herst, Patries M ^a   Tan, An S ^a  

^a MALAGHAN INSTITUTE OF MEDICAL RESEARCH   (New Zealand)

Author keywords

Cell reduction; Microorganism; Mitochondria; MTS; MTT; NADH; NBT; Plasma membrane electron transport; Superoxide; Tetrazolium salts; WST 1; XTT

Indexed keywords

CYANIDE; DICOUMAROL; DRUG RECEPTOR; FORMAZAN; NITROBLUE TETRAZOLIUM; OXYGEN; PYRIDINE NUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; ROTENONE; TETRAZOLIUM;

CELL FRACTIONATION; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL MEMBRANE POTENTIAL; CELL METABOLISM; CELL SURFACE; CYTOLOGY; CYTOPLASM; DRUG DETERMINATION; DRUG SCREENING; ELECTRON TRANSPORT; ENDOSOME; LYSOSOME; MAMMAL CELL; MITOCHONDRION; REVIEW;

ANIMALS; CELL DIVISION; CELL SURVIVAL; COLORING AGENTS; CYTOLOGICAL TECHNIQUES; HUMANS; MOLECULAR STRUCTURE; OXIDATION-REDUCTION; TETRAZOLIUM SALTS;

MAMMALIA;

EID: 27144488205     PISSN: 13872656     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S1387-2656(05)11004-7     Document Type: Review

References (108)

1. Mattson AM Jenson CO Dutcher RA. Triphenyltetrazolium as a dye for vital tissues Science 106 1947 294-295 295
2. Pagliacci MC Spinozzi F Migliorati G Fumi G Smacchia M Grignani F Riccardi C and Nicoletti I. Genistein inhibits tumour cell growth in vitro but enhances mitochondrial reduction of tetrazolium salts - A further pitfall in the use of the MTT assay for evaluating cell growth and survival Eur J Cancer 29A 1993 1573-1577
3. Pearse AGE. Histochemistry, Theoretical and Applied, Vol. 2, Churchill Livingstone, 1972
4. Stoward PJ and Pearse AGE. Histochemistry, Theoretical and Applied, Vol. 2, Edinburgh, Churchill Livingstone, 1991
5. Marshall NJ Goodwin CJ and Holt SJ. A critical assessment of the use of microculture tetrazolium assays to measure cell growth and function Growth Regulation 5 1995 69-84
6. Peckman H von and Runge P. Oxydation der formazylverbindungen I Ber Dtsch Chem Gas 27 1894 323-324
7. Peckman H von and Runge P. Oxydation der formazylverbindungen II Ber Dtsch Chem Gas 27 1894 2920-2930
8. Hoyer PE Andersen H. Specificity in steroid histochemistry, with special reference to the use of steroid solvents. Distribution of 11-beta-hydroxysteroiddehydrogenase in kidney and thymus from the mouse Histochemie 24 1970 292-306
9. Anderson GL and Deinard AS. The nitrobule tetrazolium (NBT) test: A review Am J Med Technol 40 1974 345-353
10. Hayhoe FGJ, Quaglino D and de Pasquale A. Haematological Cytochemistry, Edinburgh, Churchill Livingstone, 1988
11. Patterson C Ruef J Madamanchi NR Barry-Lane P Hu Z Horaist C Ballinger CA Brasier AR Bode C and Runge MS. Stimulation of a vascular smooth muscle cell NAD(P)H oxidase by thrombin. Evidence that p47(phox) may participate in forming this oxidase in vitro and in vivo J Biol Chem 274 1999 19814-19822
12. Baehner RL and Nathan DG. Quantitative nitroblue tetrazolium test in chronic granulomatous disease N Engl J Med 278 1968 971-976
13. Pick E Charon J and Mizel D. A rapid densitometric microassay for nitroblue tetrazolium reduction and application of the microassay to macrophages J Reticuloendothel Soc 30 1981 581-593
14. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxic assays J Immunol Meth 65 1983 55-63
15. Prochazkova J Marecek D and Zaydlar K. A microassay for tetrazolium-reductase activity of polymorphonuclear leukocytes - comparison with a test-tube technique J Hyg Epidemiol Microbiol Immunol 29 1985 447-455
16. Stellmach J. Fluorescent redox dyes. 1. Production of fluorescent formazan by unstimulated and phorbol ester- or digitonin-stimulated Ehrlich ascites tumor cells Histochemistry 80 1984 137-143
17. Stellmach J Severin E. A fluorescent redox dye. Influence of several substrates and electron carriers on the tetrazolium salt-formazan reaction of Ehrlich ascites tumour cells Histochem J 19 1987 21-26
18. Paull KD Shoemaker RH Boyd MR Parsons JL Risbood PA Barbera WA Sharma MN Baker DC Hand E Scudiero DA Monks A Alley MC and Grote M. The synthesis of XTT - a new tetrazolium reagent that is bioreducible to a water-soluble formazan J Heter Chem 25 1988 911-914
19. Scudiero DA Shoemaker RH Paull KD Monks A Tierney S Nofziger TH Currens MJ Seniff D. and Boyd MR. Evaluation of a soluble tetrazolium/formazan assay for cell growth and drug sensitivity in culture using human and other tumor cell lines Cancer Res 48 1988 4827-4833
20. Barltrop JA Owen TC Cory AH and Cory JG. 5-(3-Carboxylmethoxyohenyl)-2(4-5-Dimethylthiazolyl)-3-(4-sulfophenyl) tetrazolium, inner salt (MTS) and related analogues of MTT reducing to purple water-soluble formazans as cell-viability indicators Bioorg Med Chem Lett 1 1991 611-614
21. Cory AH Owen TC Barltrop JA and Cory JG. Use of an aqueous soluble tetrazolium/formazan assay for cell growth assays in culture Cancer Commun 3 1991 207-212
22. Morre DJ Brightman AO. NADH oxidase of plasma membranes J Bioenerg Biomem 23 1991 469-489
23. Ly JD and Lawen A. Transplasma membrane electron transport: Enzymes involved and biological function Redox Rep 8 2003 3-21
24. Ishiyama M Shiga M Sasamoto K Mizoguchi M and He P. A new sulfonated tetrazolium salt that produces a highly water-soluble formazan dye Chem Pharm Bull 41 1993 1118-1122
25. Ishiyama M Sasamoto K Shiga M Ohkura Y Ueno K Nishiyama K and Taniguchi I. Novel disulfonated tetrazolium salt that can be reduced to a water-soluble formazan and its application to the assay of lactate dehydrogenase Analyst 120 1995 113-116
26. Berridge MV Tan AS McCoy KD and Wang R. The biochemical and cellular basis of cell proliferation assays that use tetrazolium salts Biochemica 4 1996 15-20
27. Berridge MV and Tan AS. Trans-plasma membrane electron transport: A cellular assay for NADH- and NADPH-oxidase based on extracellular, superoxide - mediated reduction of the sulfonated tetrazolium salt WST-1 Protoplasma 205 1998 74-82
28. Berridge MV and Tan AS. High-capacity redox control at the plasma membrane of mammalian cells: Trans-membrane, cell surface, and serum NADH-oxidases Antiox Redox Signal 2 2000 231-242
29. Tan AS and Berridge MV. Superoxide produced by activated neutrophils efficiently reduces the tetrazolium salt, WST-1 to produce a soluble formazan: A simple colorimetric assay for measuring respiratory burst activation and for screening anti-inflammatory agents J Immunol Meth 238 2000 59-68
30. Tominaga H Ishiyama M Ohseto F Sasamoto K Hamamoto T Suzuki K and Watanabe M. A water-soluble tetrazolium salt useful for colorimetric cell viability assay Anal Commun 36 1999 47-50
31. Reungpatthanaphong P Dechsupa S Meesungnoen J Loetchutinat C and Mankhetkorn S. Rhodamine B as a mitochondrial probe for measurement and monitoring of mitochondrial membrane potential in drug-sensitive and -resistant cells J Biochem Biophys Methods 57 2003 1-16
32. Smith RA Porteous CM Gane AM and Murphy MP. Delivery of bioactive molecules to mitochondria in vivo Proc Natl Acad Sci USA 100 2003 5407-5412
33. Halliwell B and Gutteridge JMC. Free Radicals in Biology and Medicine, University Press, Oxford, 1999
34. Herst PM Tan AS Scarlett DJ and Berridge MV. Cell surface oxygen consumption by mitochondrial gene knockout cells Biochim. Biophys Acta 1656 2004 79-87
35. Winterbourn CC. Cytochrome c reduction by semiquinone radicals can be indirectly inhibited by superoxide dismutase Arch Biochem Biophys 209 1981 159-167
36. Liochev SI Batinic-Haberle I and Fridovich I. The effect of detergents on the reduction of tetrazolium salts Archiv Biochem Biophys 324 1995 48-52
37. Liu YB and Peterson DA Kimura H Schubert D. Mechanism of cellular 3-(4,5-dimethylthiazol-2-yl)-2,5- diphenyltetrazolium bromide (MTT) reduction J Neurochem 69 1997 581-593
38. Bernas T and Dobrucki J. Mitochondrial and nonmitochondrial reduction of MTT: Interaction of MTT with TMRE, JC-1, and NAO mitochondrial fluorescent probes Cytometry 47 2002 236-242
39. Bernas T and Dobrucki JW. The role of plasma membrane in bioreduction of two tetrazolium salts, MTT, and CTC Arch Biochem Biophys 380 2000 108-116
40. Farber E and Bueding E. Histochemical localization of specific oxidative enzymes. V. The dissociation of succinic dehydrogenase from carriers by lipase and the specific histochemical localization of the dehydrogenase with phenazine methosulfate and tetrazolium salts J Histochem Cytochem 4 1956 357-362
41. Hisada R and Yagi T. 1-Methoxy-5-methylphenazinium methyl sulfate. A photochemically stable electron mediator between NADH and various electron acceptors J Biochem (Tokyo) 82 1977 1469-1473
42. Kugler P. Quantitative dehydrogenase histochemistry with exogenous electron carriers (PMS, MPMS, MB) Histochemistry 75 1982 99-112
43. Burdon RH Gill V and Rice-Evans C. Reduction of a tetrazolium salt and superoxide generation in human tumor cells (HeLa) Free Radic Res Commun 18 1993 369-380
44. Tan AS and Berridge MV. (2004) Tetrazolium dye reduction discriminates between mitochondrial and glycolytic metabolism. Redox Report 2004;9:302-307
45. Bernas T and Dobrucki J. Reduction of a tetrazolium salt, CTC, by intact HepG2 human hepatoma cells: Subcellular localisation of reducing systems Biochim Biophys Acta 1451 1999 73-81
46. Goodwin CJ Holt SJ Riley PA Downes S and Marshall NJ. Growth hormone-responsive DT-diaphorase-mediated bioreduction of tetrazolium salts Biochem Biophys Resl Comml 226 1996 935-941
47. Slater TF Sawyer B and Straeuli U. Studies on succinate-tetrazolium reductase systems. III. Points of coupling of four different tetrazolium salts Biochim Biophys Acta 77 1963 383-393
48. Vistica DT Skehan P Skudiero D Monks A Pittman A and Boyd MR. Tetrazolium-based assays for cellular viability: A critical examination of selected parameters affecting formazan production Cancer Res 51 1991 2515-2520
49. Berridge MV and Tan AS. Characterization of the cellular reduction of 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT): subcellular localization, substrate dependence, and involvement of mitochondrial electron transport in MTT reduction Archiv Biochem Biophys 303 1993 474-482
50. Berridge MV Horsfield JA Tan AS. Evidence that cell survival is controlled by interleukin-3 independently of cell proliferation J Cellular Physiology 163 1995 466-476
51. Picker SD and Fridovich I. On the mechanism of production of superoxide radical by reaction mixtures containing NADH, phenazine methosulfate, and nitroblue tetrazolium Archiv Biochem Biophys 228 1984 155-158
52. van Noorden CJ and Butcher RG. The involvement of superoxide anions in the nitro blue tetrazolium chloride reduction mediated by NADH and phenazine methosulfate. Histochemical localization of NADP-dependent dehydrogenase activity with four different tetrazolium salts Anal Biochem 176 1989 170-174
53. Dunigan DD Waters SB and Owen TC. Aqueous soluble tetrazolium/formazan MTS as an indicator of NADH- and NADPH-dependent dehydrogenase activity Biotechniques 19 1995 640-649
54. Goodwin CJ Holt SJ Downes S and Marshall NJ. Microculture tetrazolium assays: A comparison between two new tetrazolium salts, XTT and MTS J Immun Meth 179 1995 95-103
55. Yamaue H Tanimura H Tsunoda T Tani M Iwahashi M Noguchi K Tamai M Hotta T and Arii K. Chemosensitivity testing with highly purified fresh human tumour cells with the MTT colorimetric assay Eur J Cancer 27 1991 1258-1263
56. Goodwin CJ Holt SJ Downes S and Marshall NJ. The use of intermediate electron acceptors to enhance MTT bioreduction in a microculture tetrazolium assay for human growth hormone Life Sciences 59 1996 1745-1753
57. Rich PR Mischis LA Purton S and Wiskich JT. The sites of interaction of triphenyltetrazolium chloride with mitochondrial respiratory chains FEMS Microbiol Lett 202 2001 181-187
58. Berridge MV Tan AS. Cell-surface NAD(P)H-oxidase: Relationship to trans-plasma membrane NADH-oxidoreductase and a potential source of circulating NADH-oxidase Antiox Redox Signal 2 2000 277-288
59. Berridge MV Tan AS and Hilton CJ. Cyclic adenosine monophosphate promotes cell survival and retards apoptosis in a factor-dependent bone marrow-derived cell line Exp Hematol 21 1993 269-276
60. Vaillant F Larm JA McMullen GL Wolvetang EJ and Lawen A. Effectors of the mammalian plasma membrane NADH-oxidoreductase system. Short-chain ubiquinone analogues as potent stimulators J Bioenerg Biomem 28 1996 531-540
61. Baker MA Krutskikh A Curry BJ McLaughlin EA and Aitken RJ. Identification of cytochrome P450-reductase as the enzyme responsible for NADPH-dependent lucigenin and tetrazolium salt reduction in rat epididymal sperm preparations Biol Reprod 71 2004 307-318
62. Rubinstein LV Shoemaker RH Paull KD Simon RM Tosini S Skehan P Scudiero DA Monks A and Boyd MR. Comparison of in vitro anticancer-drug-screening data generated with a tetrazolium assay versus a protein assay against a diverse panel of human tumor cell lines J Natl Cancer Inst 82 1990 1113-1118
63. Bellamy WT. Prediction of response to drug therapy of cancer. A review of in vitro assays Drugs 44 1992 690-708
64. Hayon T Dvilansky A Shpilberg O and Nathan I. Appraisal of the MTT-based assay as a useful tool for predicting drug chemosensitivity in leukemia Leuk Lymphoma 44 2003 1957-1962
65. Sargent JM. The use of the MTT assay to study drug resistance in fresh tumour samples Recent Results Cancer Res 161 2003 3-25
66. Serrano M Morales C and Radua P. Limitations of the triphenyl tetrazol method in the assay of the viability of seeds with a high carbohydrate content Farmacognosia 27 1967 1-8
67. Larney FJ and Blackshaw RE. Weed seed viability in composted beef cattle feedlot manure J Environ Qual 32 2003 1105-1113
68. Comley JC Townson S Rees MJ and Dobinson A. The further application of MTT-formazan colorimetry to studies on filarial worm viability Trop Med Parasitol 40 1989 311-316
69. Mukherjee M Misra S Chatterjee RK Comley JC Townson S Rees MJ and Dobinson A. Optimization of test conditions for development of MTT as in vitro screen. The further application of MTT-formazan colorimetry to studies on filarial worm viability Indian J Exp Biol 35 1997 73-76
70. Mukherjee M Misra S and Chatterjee RK. Development of in vitro screening system for assessment of antifilarial activity of compounds Acta Trop 70 1998 251-255
71. Lester RL and Smith AL. Studies on the electron transport system. 28. The mode of reduction of tetrazolium salts by beef heart mitochondria; role of coenzyme Q and other lipids Biochim Biophys Acta 47 1961 475-496
72. Baehner RL Boxer LA and Davis J. The biochemical basis of nitroblue tetrazolium reduction in normal human and chronic granulomatous disease polymorphonuclear leukocytes Blood 48 1976 309-313
73. Chanock SJ el Benna J Smith RM and Babior BM. The respiratory burst oxidase J Biol Chem 269 1994 24519-24522
74. Nisimoto Y and Otsuka-Murakami H. NADPH: Nitroblue tetrazolium reductase found in plasma membrane of human neutrophil Biochim Biophys Acta 1040 1990 260-266
75. Pruett SB and Loftis AY. Characteristics of MTT as an indicator of viability and respiratory burst activity of human neutrophils Int Arch Allergy Appl Immunol 92 1990 189-192
76. Able AJ Guest DI and Sutherland MW. Use of a new tetrazolium-based assay to study the production of superoxide radicals by tobacco cell cultures challenged with avirulent zoospores of phytophthora parasitica var nicotianae Plant Physiol 117 1998 491-499
77. Mackenzie CD Jungery M Taylor PM and Ogilvie BM. The in-vitro interaction of eosinophils, neutrophils, macrophages and mast cells with nematode surfaces in the presence of complement or antibodies J Pathol 133 1981 161-175
78. Fatima M Ahmad II Sayeed II Athar M and Raisuddin S. Pollutant-induced over-activation of phagocytes is concomitantly associated with peroxidative damage in fish tissues Aquatic Toxicol. 49 2000 243-250
79. Ahmad I Pacheco M and Santos MA. Naphthalene-induced differential tissue damage association with circulating fish phagocyte induction Ecotoxicol Environ Safety 54 2003 7-15
80. Genova ML Pich MM Bernacchia A Bianchi C Biondi A Bovina C Falasca AI Formiggini G Castelli GP and Lenaz G. The mitochondrial production of reactive oxygen species in relation to aging and pathology Ann N Y Acad Sci 1011 2004 86-100
81. Lambeth JD. NOX enzymes and the biology of reactive oxygen Nat Rev Immunol 4 2004 181-189
82. Ago T Kitazono T Ooboshi H Iyama T Han YH Takada J Wakisaka M Ibayashi S Utsumi H and Iida M. Nox4 as the major catalytic component of an endothelial NAD(P)H oxidase Circulation 109 2004 227-233
83. Aitken RJ Ryan AL Curry BJ and Baker MA. Multiple forms of redox activity in populations of human spermatozoa Mol Hum Reprod 9 2003 645-661
84. Beauchamp C and Fridovich I. Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels Anal Biochem 44 1971 276-287
85. Peskin AV and Winterbourn CC. A microtiter plate assay for superoxide dismutase using a water-soluble tetrazolium salt (WST-1) Clin Chim Acta 293 2000 157-166
86. Kepner RL Jr. and Pratt JR. Use of fluorochromes for direct enumeration of total bacteria in environmental samples: Past and present Microbiol Rev 58 1994 603-615
87. Bernard L Courties C Duperray C Schafer H Muyzer G and Lebaron P. A new approach to determine the genetic diversity of viable and active bacteria in aquatic ecosystems Cytometry 43 2001 314-321
88. Corrado M and Rodrigues KF. Antimicrobial evaluation of fungal extracts produced by endophytic strains of Phomopsis sp J Basic Microbiol 44 2004 157-160
89. Lee DG Park Y Kim HN Kim HK Kim PI Choi BH and Hahm KS. Antifungal mechanism of an antimicrobial peptide, HP (2-20), derived from N-terminus of Helicobacter pylori ribosomal protein L1 against Candida albicans Biochem Biophys Res Commun 291 2002 1006-1013
90. R Iturriaga R and Becker-Birck J. Simultaneous determination of the total number of aquatic bacteria and the number thereof involved in respiration Appl Environ Microbiol 36 1978 926-935
91. Savenkoff C Packard TT Rodier M Gerino M Lefevre D and Denis M. Relative contribution of dehydrogenases to overall respiratory ETS activity in some marine organisms J Plankton Res 17 1995 1593-1604
92. Hatzinger PB Palmer P Smith RL Penarrieta CT and Yoshinari T. Applicability of tetrazolium salts for the measurement of respiratory activity and viability of groundwater bacteria J Microbiol Methods 52 2003 47-58
93. Tunney MM Ramage G Field TR Moriarty TF and Storey DG. Rapid colorimetric assay for antimicrobial susceptibility testing of Pseudomonas aeruginosa Antimicrob Agents Chemother 48 2004 1879-1881
94. Hurwitz SJ and McCarthy TJ. 2,3,5-Triphenyltetrazolium chloride as a novel tool in germicide dynamics J Pharm Sci 75 1986 912-916
95. Gabrielson G Kuhn I Colque-Navarro P Hart M Iversen A McKenzie D and Mollby R. Microplate-based microbial assay for risk assessment and (eco)toxic fingerprinting of chemicals Anal Chimica Acta 485 2003 121-130
96. Suller MT and Lloyd D. Fluorescence monitoring of antibiotic-induced bacterial damage using flow cytometry Cytometry 35 1999 235-241
97. Yamaguchi N Sasada M Yamanaka M and Nasu M. Rapid detection of respiring Escherichia coli O157:H7 in apple juice, milk, and ground beef by flow cytometry Cytometry 54A 2003 27-35
98. Rodriguez GG Phipps D Ishiguro K and Ridgway HF. Use of a fluorescent redox probe for direct visualization of actively respiring bacteria Appl Environ Microbiol 58 1992 1801-1808
99. Schaule G Flemming HC and Ridgway HF. Use of 5-cyano-2,3-ditolyl tetrazolium chloride for quantifying planktonic and sessile respiring bacteria in drinking water Appl Environ Microbiol 59 1993 3850-3857
100. Winding A Binnerup SJ and Sorensen J. Variability of indigenous soil bacteria assayed by respiratory activity and growth Appl Environ Microbiol 60 1994 2869-2875
101. Bartosch A Manesh R Knotzsch K and Bock E. CTC staining and counting of actively respiring bacteria in natural stone using confocal laser scanning microscopy J Microbiol Methods 52 2003 75-84
102. Bakker BM Overkamp KM van Maris AJ Kotter P Luttik MA van Dijken JP and Pronk JT. Stoichiometry and compartmentation of NADH metabolism in Saccharomyces cerevisiae FEMS Microbiol Rev 25 2001 15-37
103. Friedrich T Bottcher B. The gross structure of the respiratory complex I: A Lego System Biochim Biophys Acta 1608 2004 1-9
104. Kita K Konishi K and Anraku Y. Terminal oxidases of Escherichia coli aerobic respiratory chain. II. Purification and properties of cytochrome b558-d complex from cells grown with limited oxygen and evidence of branched electron-carrying systems J Biol Chem 259 1984 3375-3381
105. Lopez-Amoros R Castel S Comas-Riu J and Vives-Rego J. Assessment of E. coli and Salmonella viability and starvation by confocal laser microscopy and flow cytometry using rhodamine 123, DiBAC4(3), propidium iodide, and CTC Cytometry 29 1997 298-305
106. Servais P Agogue H Courties C Joux F and Lebaron P. Are the actively respiring cells (CTC+) those responsible for bacterial production in aquatic environments? FEMS Microbiol Ecol 35 2001 171-179
107. Kuhn DM Balkis M Chandra J Mukherjee PK and Ghannoum MA. Uses and limitations of the XTT assay in studies of Candida growth and metabolism J Clin Microbiol 41 2003 506-508
108. Creach V Baudoux AC Bertru G and Rouzic BL. Direct estimate of active bacteria: CTC use and limitations J Microbiol Methods 52 2003 19-28