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Oxygen-Derived Species: Their Relation to Human Disease and Environmental Stress Barry Halliwell'2 and Carroll E

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Oxygen-Derived Species: Their Relation to Human Disease and Environmental Stress Barry Halliwell'2 and Carroll E Oxygen-derived Species: Their Relation to Human Disease and Environmental Stress Barry Halliwell'2 and Carroll E. Cross1 1Pulmonary-Critical Care Medicine, University of California-Davis Medical Center, Sacramento, California; 2Pharmacology Group, University of London Kings College, London, England Free radicals and other reactive oxygen species (ROS) are constantly formed in the human body, often for useful metabolic purposes. Antioxidant defenses protect against them, but these defenses are not completely adequate, and systems that repair damage by ROS are also necessary. Mild oxidative stress often induces antioxidant defense enzymes, but severe stress can cause oxidative damage to lipids, proteins, and DNA within cells, leading to such events as DNA strand breakage and disruption of calcium ion metabolism. Oxidative stress can result from exposure to toxic agents, and by the process of tissue injury itself. Ozone, oxides of nitrogen, and cigarette smoke can cause oxidative damage; but the molecular targets that they damage may not be the same. - Environ Health Perspect 1 02(Suppl 1 0):5-12 (1994) Key words: free radical, oxygen radical, superoxide, hydroxyl, hydrogen peroxide, oxidative stress, transition metals, ozone, nitrogen dioxide, cigarette smoke Introduction technique of electron spin resonance is mental air pollutant to appear in large There is considerable current interest in the often used to measure free radicals; it quantities on the planet. role of free radicals, oxygen radicals, and records the energy changes that occur as However, even present-day aerobes suf- oxidative stress as mediators of tissue injury unpaired electrons align in response to a fer oxidative damage if they are exposed to in human disease and of the effects of air magnetic field. A superscript dot ( ) is used 02 at concentrations greater than 21% (2). pollutants, such as ozone (03), nitrogen to denote free radical species. Oxygen toxicity has been demonstrated in dioxide (NO2), and tobacco smoke. This plants, animals and microorganisms. For article explains the meaning of these terms Oxygen-A Free Radical and example, exposure of adult humans to pure and summarizes current knowledge of the Environmental Toxin 02 at 1 atm pressure for as little as 6 hr roles they play in these various situations. When living organisms first appeared on causes chest soreness, cough, and sore the earth, they did so under an atmosphere throat in some subjects; and longer periods What Is a Radical? containing very little 02, i.e., they were of exposure lead to lung damage. The inci- In the structure of atoms and molecules, essentially anaerobes. Anaerobic microor- dence of ocular damage in babies known as electrons usually associate in pairs, each ganisms still survive to this day, but their retrolental fibroplasia ("formation of pair moving within a defined region of growth is inhibited and they can often be fibrous tissue behind the lens") increased space (an atomic or molecular orbital). killed by exposure to 21% 02, the current abruptly in the early 1940s among babies One electron in each pair has a spin quan- atmospheric level. As the 02 content of born prematurely and led to many cases of tum number of +1/2, the other -1/2. A the atmosphere rose (due to the evolution blindness. Not until 1954 was it realized free radical is any species capable of inde- of organisms with photosynthetic water- that retrolental fibroplasia is associated with pendent existence (hence the term "free") splitting capacity) many primitive organ- the use of high 02 concentrations in incu- that contains one or more unpaired elec- isms probably died. Present-day anaerobes bators for premature babies. More careful trons, an unpaired electron being one that are presumably the descendants of those control of 02 concentrations (continuous is alone in an orbital (1). The simplest free primitive organisms that followed the evo- transcutaneous 02 monitoring, with sup- radical is a hydrogen atom, with one pro- lutionary path of "adapting" to rising plementary 02 given only where necessary) ton and a single electron. Table 1 gives atmospheric 02 levels by restricting them- and administration of x-tocopherol have some examples of other free radicals. Note selves to environments that 02 did not decreased its incidence, but the problem has that the gases nitric oxide (NO0) and nitro- penetrate. However, other organisms not disappeared, since many premature gen dioxide (NO;) are free radicals, began the evolutionary process of evolving infants need continuous high 02 to survive whereas ozone (03) is not-no unpaired antioxidant defense systems to protect at all (3). electrons are present. The spectroscopic against 02 toxicity. In retrospect, this was The damaging effects of elevated 02 on a fruitful path to follow since organisms aerobes vary considerably with the organism that tolerated the presence of 02 could studied, age, physiologic state, and diet; and This paper was presented at the Conference on also evolve to use it for metabolic transfor- different tissues are affected in different Oxygen Radicals and Lung Injury held 30 August-2 mations (involving enzymes such as oxi- ways. Thus, cold-blooded animals such as September 1993 in Morgantown, West Virginia. The authors are grateful to National Institutes of dases and oxygenases) and for efficient turtles and crocodiles are relatively resistant Health (grants HL47628, RR-00169, and ES-00628) energy production (by using electron to 02 at low environmental temperatures, and to MAFF (UK) for research support. transport chains with as the terminal but become more sensitive at higher tem- Address correspondence to Barry Halliwell, 02 Pharmacology Group, Kings College, Manresa Road, electron acceptor, such as the mitochon- peratures. Neonatal rats resist lung damage London SW3 6LX, England. Telephone 44 71 333 drial oxidative phosphorylation system). in an atmosphere of 100% 02 far more 4860. Fax 44 71 333 4949. Hence, 02 was probably the first environ- effectively than do adult rats (2). Environmental Health Perspectives 5 HALLIWELL AND CROSS Table 1. Examples of free radicals. although the precise amounts generated Name Formula Comments and the steady-state concentrations Hydrogen atom H The simplest free radical known. achieved are still uncertain. Generation of Trichloromethyl CCI5 A carbon-centered radical (i.e., the unpaired electron resides on these species occurs by two types of carbon). CClI is formed during metabolism of CCI4 in the liver processes described below. and contributes to the toxic effects of this solvent (7). "Accidental" Generation. This Superoxide O° An oxygen-centered radical. Hydroxyl OH An oxygen-centered radical. The most highly reactive oxygen radi- encompasses such mechanisms as "leakage" cal known. of electrons onto 02 from mitochondrial Thiyl RS- General name for a group of radicals with an unpaired electron electron transport chains, microsomal residing on sulfur. cytochromes P450 and their electron Peroxyl, alkoxyl RO1, RO- Oxygen-centered radicals formed during the breakdown of organic donating enzymes, and other systems peroxides. (1,5,20). It also includes so-called autoxi- Oxides of nitrogen NO,, NO2 Both are free radicals. NO is formed in vivo from the amino acid in which compounds such L-arginine (8). NOi is made when NO reacts with 02 and is dation reactions found in polluted air and smoke from burning organic materials, as catecholamines, ascorbic acid, and e.g., cigarette smoke. reduced flavins are alleged to react directly with °2 to form O-- (5). In fact, such autoxidations are usually catalyzed by tran- sition metal ions (1). The earliest suggestion made to explain All organisms suffer some exposure to Deliberate Synthesis. The classic 02 toxicity was that 02 is a direct inhibitor OH-, because it is generated in vivo by example of deliberate metabolic generation of enzymes, thereby interfering with metab- homolytic fission of 0-H bonds in water, of ROS for useful purposes is the produc- olism. However, very few targets of direct driven by our continuous exposure to back- tion of O2, HOCI, and H202 by activated damage by 02 have been identified in aer- ground ionizing radiation (6). Hydroxyl phagocytes (21). Hydrogen peroxide is obes. In 1954, Gerschman et al. (4) pro- radical is so reactive with all biological mol- additionally generated in vivo by several posed that the damaging effects of 02 could ecules that it is impossible to evolve a oxidase enzymes, such as glycolate oxidase, be attributed to the formation of oxygen specific scavenger of it-almost everything xanthine oxidase, and D-amino acid oxi- radicals. This hypothesis was popularized in living organisms reacts with OH with dase (18,22). Evidence is accumulating and converted into the superoxide theory of second-order rate constants of 109 to 1010 that 0 - is also produced by several cell 02 toxicity following the discovery of super- M - 1sec l (essentially, if OH- contacts the types other than phagocytes, including oxide dismutase (SOD) enzymes by compound, reaction occurs). Damage lymphocytes (23), fibroblasts (24,25), and McCord and Fridovich (5). In its simplest caused by OH-, once this radical has been vascular endothelial cells (26-28). Such form, this theory states that 02 toxicity is formed, is probably unavoidable and is Op might be involved in intercellular sig- due to excess formation of superoxide radi- dealt with by repair processes (Table 2). nalling and could serve important biologic cal (O2-)' the one electron reduction
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