Hydrogen Peroxide
2006; Lippincott Williams & Wilkins; Volume: 26; Issue: 9 Linguagem: Inglês
10.1161/01.atv.0000238355.56172.b3
ISSN1524-4636
Autores Tópico(s)Analytical Chemistry and Sensors
ResumoHomeArteriosclerosis, Thrombosis, and Vascular BiologyVol. 26, No. 9Hydrogen Peroxide Free AccessEditorialPDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissions ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toFree AccessEditorialPDF/EPUBHydrogen PeroxideWatery Fuel for Change in Vascular Biology Frank M. Faraci Frank M. FaraciFrank M. Faraci From the Departments of Internal Medicine and Pharmacology, Cardiovascular Center, University of Iowa Carver College of Medicine, Iowa City. Originally published1 Sep 2006https://doi.org/10.1161/01.ATV.0000238355.56172.b3Arteriosclerosis, Thrombosis, and Vascular Biology. 2006;26:1931–1933Cells within the vessel wall have the capacity to produce a variety of reactive oxygen species (ROS: superoxide anion, hydrogen peroxide [H2O2], hydroxyl radical, etc).1–3 In diverse experimental models and in patients with disease, levels of ROS in blood vessels increase and contribute to vascular pathophysiology.1–3 Although not widely appreciated initially, it has become increasing apparent that relatively low concentrations of ROS can function as signaling molecules,4–7 and thus may be involved with normal regulation of vascular structure and function.See page 2035Superoxide can be produced by multiple enzymatic and non-enzymatic sources and is the precursor for many ROS including the highly reactive hydroxyl radical (Figure). In addition to the rate of production, steady state levels of ROS are also determined by the activity of an array of antioxidant enzymes including superoxide dismutases (SOD) which convert superoxide to H2O2 (Figure).8,9 H2O2 levels are regulated by catalase and a group of glutathione peroxidases which metabolize H2O2 to water (Figure).7–10Download figureDownload PowerPointSchematic summary of selected changes within the vessel wall in relation to H2O2. Superoxide (O2−) is produced from molecular oxygen by a variety of sources including NAD(P)H oxidase (Nox). Superoxide can react with nitric oxide (NO) to form peroxynitrite (ONOO−). H2O2 is formed from the activity of superoxide dismutases (SOD) or possibly directly by NAD(P)H oxidase containing Nox4. H2O2 can be degraded to water by glutathione peroxidases (GPx) or catalase (Cat). H2O2 can exert multiple effects in blood vessels including: (1) amplify oxidative stress by further increasing expression and activity of NAD(P)H oxidase, (2) form hydroxyl radical (via an iron dependent process), a highly reactive free radical species, (3) increase expression of arginase, thus reducing levels of L-arginine available to NO synthases, (4) increase or decrease vascular tone, (5) alter expression of clusters of genes, and (6) increase vascular growth (hypertrophy). See text for details.Discovered in 1818 by the French chemist Louis-Jacques Thenard,11 H2O2 has a wide array of uses including as an antiseptic, a bleaching agent, in food processing, and as a fuel for rockets.12 Much more recently, the role of H2O2 in vascular biology has begun to be appreciated and better defined. In both disease models and in normal aging, local concentrations of H2O2 increase in blood vessels and in vascular cells in culture.13–19 Although SOD activity is a major source of H2O2 (Figure), there may be other sources as well. For example, ROS in vascular cells can be produced by NAD(P)H oxidases (Figure)20–22 and the NAD(P)H oxidase containing Nox4 [NAD(P)H oxidase 4] may predominantly produce H2O2, rather than superoxide (Figure).23Increasing evidence suggests that H2O2 may play diverse and important roles in vascular biology. Water and H2O2 share many physical features.6 The addition of a second oxygen atom to water (described as "oxygenated water" by Thenard), however, results in a molecule with many distinct chemical and biological properties. Similar to nitric oxide (NO), H2O2 is chemically more stable than superoxide and other ROS.5,6 H2O2 is also relatively cell permeable, although some movement through cell membranes may occur via aquaporins.6 Both short- and long-term effects of H2O2 on vascular cells continue to be explored. For example, H2O2 produces relaxation of many blood vessels, but can produce vasoconstriction depending on the species, the segment of the vasculature, and the concentration of H2O2 (Figure).7,24–31 Vasodilation in response to H2O2 can occur indirectly through endothelium-dependent relaxation or via direct effects on vascular muscle, possibly including formation of calcium sparks.24,25,27–29 H2O2 can mediate vascular responses to varied stimuli including endothelium-dependent agonists, increases in blood flow,25,30,32 and arachidonic acid.33 H2O2 may contribute to increases in myogenic tone with increases in blood pressure.34 In addition to promoting the formation of other vasodilators, H2O2 may function as one of a family of endothelium-derived hyperpolarizing factors.35,36 Along with effects on vascular tone, H2O2 can increase permeability of endothelium.21,37Regarding more long-term effects, H2O2 has the potential to alter expression of many genes,38 including some thought to play a major role in vascular biology (Figure). For example, H2O2 activates transcription factors including NF-κB,17 stimulates expression of endothelial and inducible isoforms of NO synthase (eNOS and iNOS, respectively)39–41 and components of NAD(P)H oxidase.42 Substantial evidence suggests that H2O2 functions as a mediator of vascular growth contributing to vascular hypertrophy during hypertension (Figure).19,21 Whether H2O2 plays a role in other structural changes such as inward vascular remodeling is unclear. H2O2 may play a larger role in the development and progression of atherosclerosis than does superoxide43 and may contribute to vascular injury and cell death, particularly after conversion to hydroxyl radical (Figure).44 Interestingly, the rate of cardiovascular events in patients with atherosclerosis is inversely related to activity of glutathione peroxidase in erythrocytes,45 which is consistent with a role for H2O2 in vascular disease.Although ROS can themselves alter vascular tone, these molecules can also impair vasomotor responses to other stimuli. The impact of superoxide on endothelial function continues to be a major area of research focus. Wei and Kontos provided the first evidence that ROS can impair endothelium-dependent relaxation.46 Superoxide reacts highly efficiently with NO (Figure), reducing its bioavailability for further signaling.2,3 Studies using exogenous application of H2O2 or mice deficient in expression of glutathione peroxidase suggest that H2O2 can also impair NO-mediated signaling in blood vessels.47–50 Nevertheless, the mechanism(s) by which H2O2 impairs endothelial function are likely to be more complex. For example, H2O2 may impair endothelium-dependent relaxation after conversion to hydroxyl radical.47,48 H2O2 can stimulate NAD(P)H oxidase in vascular cells (Figure),21,51,52 reduce levels of tetrahydrobiopterin,53 and thus may promote uncoupling of eNOS, further increasing the levels of superoxide.52,53 This increase in superoxide presumably results in a feed-forward mechanism that further amplifies oxidative stress (Figure).The recent study by Thengchaisi et al in this issue of Arteriosclerosis, Thrombosis, and Vascular Biology suggests an additional mechanism by which H2O2 may impair endothelial function.54 In this study, exogenous application of H2O2 both increased expression of arginase I and selectively decreased endothelium-dependent (NO-mediated) responses in coronary arterioles. Arginases metabolize L-arginine to urea and L-ornithine,55 so increased activity of the enzyme may reduce availability of L-arginine needed for production of NO (L-arginine is the substrate for NO production). Pharmacological inhibitors of arginase or exogenous L-arginine restored endothelial function in arterioles treated with H2O2. Additional experiments with deferoxamine suggested that hydroxyl radical may actually be the mediator of the H2O2-induced vascular dysfunction.Several question arise from this work. The concentration of H2O2 needed to produce these effects (100 μmol/L) was relatively high and may be supraphysiological.5 Studies of ROS are sometimes criticized for the use of high levels of H2O2. In addition, the extracellular application of exogenous H2O2 may not completely mimic effects of endogenously produced H2O2 because of the compartmentalization of ROS effects.8,56 Thus, a key unanswered question is whether levels of endogenously formed H2O2 are sufficient to produce similar effects on the vasculature. Considering the array of mechanisms that have been implicated in previous studies (see above), can endothelial dysfunction in response to H2O2 be fully explained by changes in activity of arginase? Through what mechanism does H2O2 or oxidative stress increase expression and activity of arginase? There are two isoforms of arginase, and RT-PCR data suggested that only arginase I is expressed in coronary arterioles. Other studies indicate, however, that both arginase I and II are expressed in vascular cells, and this expression can change in disease.57–59 Thus, the question of the relative importance of different arginase isoforms under physiological and pathophysiological conditions remains unanswered. Most studies, including the study be Thengchaisi,54 used pharmacological inhibitors that do not discriminate between arginase isoforms.In summary, oxidative stress in the vasculature is common in diverse experimental models and occurs in diseased blood vessels in humans. Because of their complex interrelationships, it has been difficult to fully define the role of specific ROS in blood vessels. There is increasing interest into the role of H2O2 in vascular biology, both as a signaling molecule and a mediator of vascular disease and altered growth. The wide variety of effects that H2O2 has in vascular cells is already impressive in scope but continues to grow.The author thanks Dr Jon Andresen for critical evaluation of this manuscript.Sources of FundingWork reviewed in this manuscript from this laboratory was supported by National Institutes of Health grants HL-38901, NS-24621, HL-62984, and by a Bugher Foundation Award in Stroke from the American Heart Association (0575092N).DisclosuresNone.FootnotesCorrespondence to Frank M. Faraci, PhD, Department of Internal Medicine, E315-GH, University of Iowa, Carver College of Medicine, Iowa City, Iowa 52242-1081. E-mail [email protected] References 1 Madamanchi NR, Vendrov A, Runge MS. Oxidative stress and vascular disease. Arterioscler Thromb Vasc Biol. 2005; 25: 29–38.LinkGoogle Scholar2 Mueller CF, Laude K, McNally JS, Harrison DG. Redox mechanisms in blood vessels. Arterioscler Thromb Vasc Biol. 2005; 25: 274–278.LinkGoogle Scholar3 Faraci FM. 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