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Oxygen Radicals, Nitric Oxide and Human Inflammatory Joint Disease

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Oxygen Radicals, Nitric Oxide and Human Inflammatory Joint Disease Annals ofthe Rheumatic Diseases 1995; 54: 505-5 10 505 Oxygen radicals, nitric oxide and human Ann Rheum Dis: first published as 10.1136/ard.54.6.505 on 1 June 1995. Downloaded from inflammatory joint disease Barry Halliwell Interest in the role of free radicals in OH") and important non-radical derivatives of rheumatoid arthritis (RA) stems from the oxygen such as H202 and hypochlorous acid seminal work of McCord,' who noted the (HOCI). decreased viscosity of synovial fluid in RA patients and showed that a similar decrease could be produced by exposing synovial fluid, Reactive oxygen species in vivo or solutions of hyaluronic acid, to a system The chemical reactivity of oxygen radicals generating superoxide radical, 02-. McCord's varies (table 1). The most reactive is hydroxyl observations led to interest in the use of intra- radical (OH"), which reacts very fast with articular injections of the antioxidant enzyme almost all molecules in vivo. When OH" is superoxide dismutase as a treatment in RA. formed, it damages whatever it is generated However, the clinical data presented did not next to; it cannot migrate within the cell.4 convince many rheumatologists2 3 and over- enthusiastic interpretations of the data may have led to unwarranted scepticism about the NITRIC OXIDE real role of free radicals in RA. Let us review Whereas OH is probably always harmful, our current knowledge. other (less reactive) free radicals may be useful in vivo. For example, NO is synthesised from L-arginine by many cell types, including Basic definitions chondrocytes.8 However, although human Electrons in atoms and molecules occupy phagocytes can make NO,9 it is not yet clear regions of space termed orbitals, each of which how often they do so in vivo; much of the work holds a maximum of two electrons. A free with NO has investigated rats and mice, both radical is any species capable of independent of which species have phagocytes that make existence that contains one or more unpaired NO much more readily. electrons-that is, electrons alone in an orbital. http://ard.bmj.com/ Table 1 gives examples. Radicals react with other molecules in a SUPEROXIDE number of ways.4 If two radicals meet, they Superoxide is produced by phagocytes as a can combine their unpaired electrons and killing mechanism.6 Lesser amounts of extra- join to form a covalent bond (a shared pair cellular O2* may be generated, perhaps as an of electrons). An important example is the intercellular signal molecule, by several other fast reaction of 02- with nitric oxide (also a cell types, including vascular endothelial cells, on September 28, 2021 by guest. Protected copyright. free radical, NO') to form the non-radical osteoclasts, chondrocytes, lymphocytes, and peroxynitrite:5 fibroblasts.""'3 For example, treatment of human fibroblasts with RA synovial fluid O2-- + NO- ONOO- (1) causes 02- secretion. 3 A free radical might donate its unpaired In addition to this 'deliberate' 02 -genera- electron to another molecule. Thus °2- reduces tion, some 02-- iS produced within cells by ferric (Fe3") cytochrome c to ferrous (Fe2+) mitochondria and endoplasmic reticulum, cytochrome c, a reaction often used to assay apparently by the unavoidable 'leakage' of 02- production by activated phagocytes:6 electrons onto oxygen from their correct paths in electron transfer chains and by chemical cyt c (Fe3+) + 02-- ' cyt c (Fe2+) + 02 (2) 'autoxidation' reactions.4 A free radical might take an electron from another molecule, thus oxidising it. For example, 02 oxidises ascorbic acid, a process HYPOCHLOROUS ACID believed to occur in RA:7 Another killing mechanism used by neutro- + - phils (but not macrophages) is the enzyme ascorbate + 02 H+ ascorbate radical myeloperoxidase,14 which uses H202 to oxidise + H202 (3) chloride ions into hypochlorous acid (HOCI), a Left to itself, 02- undergoes the dismutation powerful oxidising and chlorinating agent: reaction: H202 +Cl- - HOCI + OH- (5) 02*- + 02-- +2H+ - H202 + 02 (4) Pharmacology Group, King's College, Hydrogen peroxide, H2 02, is not a free University ofLondon, electrons are present). oxide interactions London SW3 6LX, radical (no unpaired Superoxide-nitric United Kingdom The global term reactive oxygen species is often What happens if both 02- and NO are B Halliwell used to include the oxygen radicals (02- and produced at the same site, for example by 506 Halliwell Table 1 Examples offree radicals Transition metals and hydrogen peroxide Many transition metals have variable oxidation Name Formula Comments numbers: for example iron as Fe2+ or Fe3+, and Ann Rheum Dis: first published as 10.1136/ard.54.6.505 on 1 June 1995. Downloaded from Hydrogen atom *H. The simplest free radical known. copper as Cu+ or Cu24. Changing between Trichloromethyl CC13 A carbon centred radical (the unpaired electron resides on carbon). CC3l is formed during metabolism of these oxidation states transfers single electrons, carbon tetrachloride (CC14) in the liver and for example: contributes to the toxic effects of this solvent. Superoxide 02- An oxygen centred radical. Reacts quickly with a few molecules (such as nitric oxide) but generally not very Fe3+ + e- = Fe2+ (6) reactive. Hydroxyl OH An oxygen centred radical. The most highly reactive Also, for titanium salts: oxygen radical known. When generated in vivo, reacts at its site offormation. Ti4+ + e- = Ti3+ (7) Thiyl RS' General name for a group of radicals with an unpaired electron residing on sulphur. Reactivity varies; often Thus transition metal ions are good react with oxygen to give damaging oxysulphur radicals. promoters of free radical reactions. For Peroxyl, alkoxyl RO2., RO Oxygen centred radicals formed during the breakdown of example, copper, iron and titanium ions react organic peroxides. Oxides ofnitrogen NO, NO2. Both are free radicals. NO is formed in vivo from the with H202 to form OH" radicals:4 amino acid L-arginine. N02 is made when NO reacts with oxygen, and is found in polluted air and smoke from burning organic materials, such as cigarette Cu4+ H202- Cu2+ +OH' + OH- (8) smoke. Ti3+ + H202 -_ Ti4+ + OH + OH- (9) *A superscript dot is used to denote free radical species. H202 is produced in vivo by dismutation of O2- and by several oxidase enzymes, including xanthine oxidase.4 Like 02', H202 can be activated macrophages, or when neutrophils useful in vivo; for example, it is a substrate for adhering to endothelium (a source of NO0) a thyroid peroxidase enzyme that helps make generate 02"-? One possibility is that 02- thyroid hormones."8 It can also regulate gene and NO antagonise each other's bio- expression, for example by activating the logical actions. Inappropriate antagonism of cytoplasmic gene transcription factor NF-KB.'9 NO, by excess 02-, has been suggested H202 is very diffusible within and between to contribute to impaired endothelium cells,4 but if it comes into contact with mediated vasodilatation, for example in transition metal ions, OH will be generated at hypertension. 15 that site and cause immediate damage. The interaction of 02- and NO can also be dangerous.5 The product, peroxynitrite (equation (2)) is not only directly toxic, for Antioxidant defences example by oxidising methionine and protein ENZYMES -SH groups, but also it breaks down to Living organisms have evolved multiple generate multiple toxic products (figure), in- antioxidant defence systems. Superoxide http://ard.bmj.com/ cluding nitrogen dioxide gas (NO2'), OH' and dismutase (SOD) enzymes remove 02'- by nitronium ion (NO24).5 16 Some of these accelerating its dismutation by about four species will nitrate aromatic amino acids, so orders of magnitude. Human cells have an that formation of nitroaromatics (especially SOD enzyme containing active site manganese nitrotyrosine) is thought to be a 'marker' of (MnSOD) in mitochondria, whereas cytosol peroxynitrite generation.5 17 contains a copper and zinc containing SOD (CuZnSOD).4 H202 can be destroyed by on September 28, 2021 by guest. Protected copyright. catalases, but the most important H2 02 0; + NO removing enzymes in human cells are gluta- thione peroxidases, which remove H202 by using it to oxidise reduced glutathione (GSH) to oxidised glutathione (GSSG): 2GSH + H202- GSSG + 2H20 (10) ONOO- Peroxynitrite METAL ION SEQUESTRATION H+ Another important antioxidant defence is that iron and copper ions are kept safely protein bound whenever possible, so that OH ONOOH Peroxynitrous acid formation is largely prevented. This is particularly important in extracellular fluids, including synovial fluid, because their levels of antioxidant defence enzymes are low.7 20 21 The value of this sequestration of metal ions is illustrated by an inspection of the severe NO- NO+ NO. Nitrogen dioxide pathology suffered by patients with metal 2 radical overload diseases. For example, in patients Nitrate ion Nitronium with iron overload secondary to idiopathic ion haemochromatosis, transferrin is iron satu- rated and iron ions 'catalytic' for free radical OH- 'OH Hydroxyl radical reactions circulate in the blood.22 Among many Formation and decomposition ofperoxynitrite. other problems, these patients can suffer joint Oxygen radicals, nitric oxide and human inflammatoryjoint disease 507 inflammation,23 illustrating the well known produce 02'-, H202, HOCI, and possibly NO'; relationship between chronic inflammation in excess, these cause damage. Tissue injury and disordered iron metabolism.24 releases iron and copper ions and haem Ann Rheum Dis: first published as 10.1136/ard.54.6.505 on
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