Abstract
Here we report the structural characterization of the product formed from the reaction between hydroethidine (HE) and superoxide (O(2)(.-)). By using mass spectral and NMR techniques, the chemical structure of this product was determined as 2-hydroxyethidium (2-OH-E(+)). By using an authentic standard, we developed an HPLC approach to detect and quantitate the reaction product of HE and O(2)(.-) formed in bovine aortic endothelial cells after treatment with menadione or antimycin A to induce intracellular reactive oxygen species. Concomitantly, we used a spin trap, 5-tert-butoxycarbonyl-5-methyl-1-pyrroline N-oxide (BMPO), to detect and identify the structure of reactive oxygen species formed. BMPO trapped the O(2)(.-) that formed extracellularly and was detected as the BMPO-OH adduct during use of the EPR technique. BMPO, being cell-permeable, inhibited the intracellular formation of 2-OH-E(+). However, the intracellular BMPO spin adduct was not detected. The definitive characterization of the reaction product of O(2)(.-) with HE described here forms the basis of an unambiguous assay for intracellular detection and quantitation of O(2)(.-). Analysis of the fluorescence characteristics of ethidium (E(+)) and 2-OH-E(+) strongly suggests that the currently available fluorescence methodology is not suitable for quantitating intracellular O(2)(.-). We conclude that the HPLC/fluorescence assay using HE as a probe is more suitable [corrected] for detecting intracellular O(2)(.-).
MeSH Terms
Animals
Aorta/cytology
Biological Assay/methods
Cattle
Ceramides/pharmacology
Chromatography, High Pressure Liquid/methods
Cyclic N-Oxides/chemistry
Endothelial Cells/chemistry,drug effects
Fluorescent Dyes/chemistry
Molecular Structure
Oxidation-Reduction
Phenanthridines/chemistry
Reactive Oxygen Species/chemistry
Spin Trapping
Superoxides/chemistry
Vitamin K 3/chemistry
Chemicals
5-tert-butoxycarbonyl 5-methyl-1-pyrroline N-oxide
Ceramides
Cyclic N-Oxides
Fluorescent Dyes
Phenanthridines
Reactive Oxygen Species
Superoxides
hydroethidine
Vitamin K 3
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Zhao Hongtao
Department of Biophysics and Free Radical Research Center, Medical College of Wisconsin, Milwaukee, WI 53226, USA.
Joseph Joy
Fales Henry M
Sokoloski Edward A
Levine Rodney L
Vasquez-Vivar Jeannette
Kalyanaraman B
References (24)
24 references, click to expand
-
Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: potential implications in intracellular fluorescence detection of superoxide.
Free Radic Biol Med. 2003 Jun 1;34(11):1359-68
PMID: 12757846
-
Oxidative stress-induced iron signaling is responsible for peroxide-dependent oxidation of dichlorodihydrofluorescein in endothelial cells: role of transferrin receptor-dependent iron uptake in apoptosis.
Circ Res. 2003 Jan 10;92(1):56-63
PMID: 12522121
-
Ceramide-induced intracellular oxidant formation, iron signaling, and apoptosis in endothelial cells: protective role of endogenous nitric oxide.
J Biol Chem. 2004 Jul 2;279(27):28614-24
PMID: 15102832
-
Detection of intracellular superoxide formation in endothelial cells and intact tissues using dihydroethidium and an HPLC-based assay.
Am J Physiol Cell Physiol. 2004 Oct;287(4):C895-902
PMID: 15306539
-
Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine and 2',7'-dichlorofluorescin.
J Leukoc Biol. 1990 May;47(5):440-8
PMID: 2159514
-
Hypercholesterolemia increases endothelial superoxide anion production.
J Clin Invest. 1993 Jun;91(6):2546-51
PMID: 8390482
-
Intracellular hydrogen peroxide and superoxide anion detection in endothelial cells.
J Leukoc Biol. 1994 Feb;55(2):253-8
PMID: 8301222
-
In vivo evidence for microvascular oxidative stress in spontaneously hypertensive rats. Hydroethidine microfluorography.
Hypertension. 1995 May;25(5):1083-9
PMID: 7737720
-
A metalloporphyrin superoxide dismutase mimetic protects against paraquat-induced endothelial cell injury, in vitro.
J Pharmacol Exp Ther. 1995 Dec;275(3):1227-32
PMID: 8531085
-
Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine.
J Neurosci. 1996 Feb 15;16(4):1324-36
PMID: 8778284
-
Mitochondrial membrane potential and hydroethidine-monitored superoxide generation in cultured cerebellar granule cells.
FEBS Lett. 1997 Sep 22;415(1):21-4
PMID: 9326361
-
Superoxide production in vascular smooth muscle contributes to oxidative stress and impaired relaxation in atherosclerosis.
Circ Res. 1998 Jun 29;82(12):1298-305
PMID: 9648726
-
Critical evaluation of the use of hydroethidine as a measure of superoxide anion radical.
Free Radic Biol Med. 1998 Nov 1;25(7):826-31
PMID: 9823548
-
Exacerbation of delayed cell injury after transient global ischemia in mutant mice with CuZn superoxide dismutase deficiency.
Stroke. 1999 Sep;30(9):1962-8
PMID: 10471451
-
Spin traps: in vitro toxicity and stability of radical adducts.
Free Radic Biol Med. 2003 Jun 1;34(11):1473-81
PMID: 12757857
-
Production and actions of superoxide in the renal medulla.
Hypertension. 2001 Feb;37(2 Pt 2):547-53
PMID: 11230333
-
Increased mitochondrial superoxide generation in neurons from trisomy 16 mice: a model of Down's syndrome.
Free Radic Biol Med. 2000 Jan 15;28(2):235-50
PMID: 11281291
-
Synthesis and biochemical applications of a solid cyclic nitrone spin trap: a relatively superior trap for detecting superoxide anions and glutathiyl radicals.
Free Radic Biol Med. 2001 Sep 1;31(5):599-606
PMID: 11522444
-
Manganese superoxide dismutase deficiency exacerbates cerebral infarction after focal cerebral ischemia/reperfusion in mice: implications for the production and role of superoxide radicals.
Stroke. 2002 Mar;33(3):809-15
PMID: 11872908
-
In vivo evidence for antioxidant potential of estrogen in microvessels of female spontaneously hypertensive rats.
Hypertension. 2002 Feb;39(2 Pt 2):405-11
PMID: 11882581
-
Superoxide production and expression of nox family proteins in human atherosclerosis.
Circulation. 2002 Mar 26;105(12):1429-35
PMID: 11914250
-
Increased NADPH oxidase activity, gp91phox expression, and endothelium-dependent vasorelaxation during neointima formation in rabbits.
Circ Res. 2002 Jul 12;91(1):54-61
PMID: 12114322
-
Evidence that accumulation of ceramides and cholesterol esters mediates oxidative stress-induced death of motor neurons in amyotrophic lateral sclerosis.
Ann Neurol. 2002 Oct;52(4):448-57
PMID: 12325074
-
Detection of reactive oxygen species by flow cytometry after spinal cord injury.
J Neurosci Methods. 2002 Oct 15;120(1):105-12
PMID: 12351211