Environmental Health PerspectivesVol. 64, pp. 209-217, 1985

Free-Radical Chemistry of Sulfiteby P. Neta* and Robert E. Huie*

The free-radical chemistry of sulfite oxidation is reviewed. Chemical transformations of organic andbiological molecules induced by sulfite oxidation are summarized. The kinetics of the free-radical oxidationsof sulfite are discussed, as are the kinetics of the reactions of the sulfite-derived radicals A03 and the peroxyderivative S(6 with organic compounds.

Sulfur dioxide is a major air pollutant, formed pri-marily during the combustion of fossil fuels. Othersources include natural gas scrubbing, the oxidation ofnaturally emitted reduced sulfur compounds, and smelt-ing of sulfide ores (1). Sulfur dioxide is water-soluble,forming bisulfite and sulfite

S02*aq ±H + +HSO-HSO- zt H+ + SO23-

PKa = 1.86 (2)PKa = 7.2 (3)

and at very high concentration, disulfite.

HSO- + S02eaq -t HS20O PKa = 1.5 (4) (3)

At any physiological pH, sulfite and bisulfite will bothbe important forms of S(IV). We will use primarily theterm sulfite to refer to the equilibrium mixture, exceptwhen referring specifically to bisulfite. The term S(IV)will be used to include other compounds containing sul-fur in the + 4 oxidation state.

Sulfur dioxide can produce bronchoconstriction uponinhalation, particularly in asthmatics and during exer-cise (5,6). In addition to inhalation of SO2, sulfite canenter the body due to its use as a preservative in food,wine, and medications. Finally, sulfite is a likely inter-mediate in the metabolism of sulfur containing aminoacids such as methionine and cysteine.Both liver and lung tissues contain the enzyme sulfite

oxidase which catalyzes the oxidation of sulfite to sul-fate. This has led to two contrary views of the possiblephysiological consequences ofingested sulfite. One pointofview is that the body contains sufficient sulfite oxidaseto detoxify any reasonably likely dose of sulfite fromeither inhaled atmospheric SO2 or from food additives(7). The other view is that sulfite reaches the blood andforms S-sulfocysteine, RSS03 and, therefore, the sub-

*Chemical Kinetics Division, National Bureau of Standards, Gaith-ersburg, MD 20899.

sequent chemistry of S(IV), at least as the S-sulfocy-steine, must be considered (8). Further, epidemiologicalevidence suggests a relation between SO2 and lung can-cer in workers exposed to arsenic and animal studieson benz(a)pyrene correlate cancer development withSO2 exposure (8).

Sulfite is a strong nucleophile and reacts with manybiomolecules by substitution at electrophilic positions.These reactions have been reviewed by Petering (8) andwill not be discussed here, other than the reaction ofbisulfite with cystine [Eq. (4)].

RSSR + HSO- z± RSSO- + RSH (4)

This reaction has an equilibrium constant of 0.089 at pH7.75 and 37°C (9). The large concentration of RSSRcauses most sulfite in the blood to be bound as S-sul-focysteine, RSS03-. As Petering points out, the bio-chemistry of HS03- becomes the biochemistry ofRSS03 beyond the lung.Because of the above equilibrium, however, S-sulfo-

cysteine may act as a reservoir for sulfite; when itreaches cells in which RSH is in greater abundance thanRSSR, e.g., liver cells, where RSH:RSSR = 102_103(10), the equilibrium may shift to the left to producesulfite.The present review deals exclusively with elements

of the radical chemistry of sulfite. In light of the dis-cussion above, it might appear that radical reactionsinitiated by sulfite are likely to be unimportant. Thereare, however, two possible sources of radicals from sul-fite that can be considered.

First, the lung and the rest ofthe respiratory system,being rich in oxygen, provide an environment for theautoxidation of sulfite before it can either be removedby sulfite oxidase or converted to S-sulfocysteine. Theautoxidation of sulfite may be initiated by trace metalions or certain enzymes and clearly involves free radi-cals (11,12). The second possible source of radicals is

NETA AND HUIE

from S-sulfocysteine. The one-electron reduction ofRSSO3 can be written as either

RSSO- + e- RS- + SO§ (5a)or

RSSO- + e- - RS + SO2- (5b)

Pulse radiolysis experiments in which cysteine radicalswere produced in the presence of So32, or in whichSO3- radicals were R2roduced in the presence of cys-teine, showed that RS oxidizes sulfite and that, there-fore, the first path is more likely.

Chemical Transformations Inducedby Sulfite OxidationMuch of the interest in the chemistry of radicals de-

rived from sulfite arises from the observations that thereaction of sulfite with several organic compounds re-quires the presence of an oxidizing agent, usually mo-lecular oxygen. Complementary to these observationsare the many studies that show that certain organiccompounds inhibit the oxidation of sulfite by oxygen.The investigation of the effects of organic substances

on the rate of oxidation of sulfite solutions by oxygenwas initiated by Bigelow (13) and carried on actively forseveral years (14,15). In the work involving the oxi-dation of sulfite catalyzed by trace metal ions, the in-hibition could have been caused by the complexation ofthe metal ion. Therefore, studies were carried out inwhich sulfite oxidation was inititated by ultraviolet light(16). Again, organic substances were found to inhibitthe reaction. The photochemical reaction was shownsubsequently to be a chain reaction and the inhibitionby organic compounds due to breaking the free-radicalchains.

Since the inhibition of sulfite oxidation involves, ingeneral, only small total amounts of reaction, productsof the chain brealdng reaction usually have not beendiscussed. Also, in some cases the initial reactant mightbe regenerated in a secondary process. In other cases,however, the chemical transformation of the inhibitorwas evident. This was observed initially for quinine sul-fate and pyridine, which turned green, and hydroqui-none, which became opalescent (16). Other work showedthat the inhibition of sulfite oxidation by alcohols wasaccompanied by their oxidation (17). In subsequentwork, the oxidation of sulfite in the presence of unsat-urated compounds was found to result in the additionof sulfite to double bonds (18). With pyridine this leadsto formation of N-pyridinium sulfonate (19). The reac-tion of hydroquinone with sulfite in the presence of oxy-gen is perhaps the most studied (20,21), since sulfitewas used as a preservative in hydroquinone-based pho-tographic developers (22). In this system two types ofreaction appear to take place: (a) oxidation of the hy-droquinone by sulfite radicals and by molecular oxygen,and (b) sulfonation of the quinone to form hydroquinone

sulfonates (followed by oxidation ofthe latter to quinonesulfonates) (21).From the point of view of this review, the most im-

portant observations have been on the transformationof biological molecules by sulfite in the presence of oxy-gen. Fridovich and Handler (23) have shown that a mix-ture of horseradish peroxidase, hydrogen peroxide, anda peroxidizible substance initiate sulfite oxidation. In-deed, they used the oxidation of sulfite as a sensitivetest for the production of radicals in biological systems(24). Klebanoff (25) confirmed this finding and furtherreported that the oxidation of NADH by Mn2+, per-oxidase, and 02 was stimulated by sulfite. Therefore, abiological system can initiate the oxidation of sulfite andthe subsequent chain reaction can provide reactive in-termediates capable of reacting with biological mole-cules.

Since this early work, there have been several paperson the oxygen induced reactions of biological moleculeswith sulfite. It has been found that oxygen is requiredfor the complete sulfonation of protein S-H groups bysulfite (26). Sulfite was found to form sulfonates with 4-thiouracil derivatives in the presence of oxygen and thisreaction was observed to be inhibited by hydroquinone(27,28). Methionine has been shown to be oxidized tothe sulfoxide in the presence of sulfite, 02, and Mn2+(29). This reaction appears to be inhibited by superoxidedismutase. Sulfite cleaves DNA in the presence of 02and Mn2+ (30), this reaction is inhibited by hydroquin-one. The autoxidation of sulfite can destroy indole-3-acetic acid (31) or tryptophan (32) and several nucleo-tides and nucleic acids have been shown to react withsulfite in the presence of oxygen (33).

Lipid peroxidation has been induced by sulfite (34).This reaction is not only quenched by an antioxidant,2,6-di-tert-butyl-4-hydroxymethylphenol, but also byMn2+. This supression of lipid peroxidation by Mn2+has also been observed in rat liver homogenate (35).Both n-carotene (36) and vitamin Bi (37) are destroyedduring the autoxidation of sulfite. Finally, papain is in-activated during sulfite autoxidation in a reaction whichleads to the incorporation of sulfite into the protein (38).

In this review, we will discuss the chemistry of thefree radicals S03- and S05-, key intermediates formedin the autoxidation of sulfite. In addition, we will discussbriefly the radicals S02 and S04- and the ion HS05,due to their possible relationship to the behavior of sul-fite in the body.

Formation and Detection of S03-RadicalsThe sulfite radical is generally produced by the one-

electron oxidation of sulfite or bisulfite ions, eitherchemically or photolytically. The radical is detectedeither by ESR or by optical absorption spectroscopy.Although the ESR detection is more definitive, kineticstudies on the sulfite radical are more often carried outby absorption spectroscopy, by monitoring either the

210

FREE-RADICAL CHEMISTRY OF SULFITE

absorption of S03- itself or more frequently by folloing the formation of other more strongly absorbing sjcies arising from S03- reactions with substrates.The S03 radical has been produced by oxidation

sulfite with Ce4+ in acid solution (39-41), by reactiof sulfite with rad.icals produced by Fenton-type iagents, e.g., OH, NH2, and S4- (from the reactionTi + with H202, NH2OH, S2082, respeetively) (42),reaction with radiolytically produced OH radicalsother oxidizing radicals (43-47)

OH + S02 - R OH- + SOg-

by photoionization of sulfite directly (3,48,49) or throuphotosensitizers (49)

S032- + hv-SO- + e-

or by photolysis of dithionate (50) or thiosulfate (5The S03- single-line ESR spectrum has been detectby using all ofthe above techniques (39-42,46,47,49,5as well as in biochemical systems such as horseradiperoxidase-hydrogen peroxide (52) or prostaglan(hydroperoxidase (53). Most of these studies reporta g factor for S03 around 2.0030, except experimerwith Ce4+ in acid solutions, where g = 2.0022 has bemeasured (39-41). This difference may suggest a psible complexation of S03- with Ce

Ce4+ + S082- [Ce3'...SO ] ± Ce3+ + S8o-

The alternative explanation that the g-factor shift is dto protonation of the radical

S§O- + H+¢ HSO3

appears unlikely, since the Ce4+ experiments were cried out at pH - 2, while radiolytic and photolytic (periments showed no g-factor shift between pH 0 apH 12 (49,54). The unpaired spin on S03 has been cculated to be 62% on the sulfur and 13% on each of toxygens (55,56). SO3- can be considered, therefore,a sulfur-centered radical.The optical absorption of S03- exhibits Xma,, = 2

nm with e_m = 1000 M-1 cm-' (48). This relativ4weak UV absorption has been used to determine tsecond-order decay rate constant for this radical

2S03- - S2026 or SO + SO32-

(2k=1.1x109 M-1sec-1) (3,44,49) but is not conveently used for following the kinetics of S03 reacticwith substrates since manx of these substrates or thradical products mask the SO3 UV absorption. The:fore, in pulse radiolysis experiments often the absoition of the other substrate radical was monitored.

,w- Kinetics of One-Electron Oxidationpe- of Sulfite

of As mentioned above, sulfite or bisulfite ions undergoion 9ne-electron oxidation by several radicals to producere- S03-. Rate constants for a number of reactions of thisof type have been determined by pulse radiolysis and are

by summarized in Table 1. The hydroxyl radical reacts withor both sulfite and bisulfite with very high rate constants,

near the diffusion-controlled limit. The rate of oxidationby other radicals decreases in an order that appears toreflect the order of expected oxidation potentials of

(6) these radicals. Measurements of rate constants over awide range of pH allows the separate determination of

igh rate constants for the oxidation of sulfite and bisulfite.Whereas the hydroxyl and sulfate radicals react withbisulfite about twice as fast as with sulfite, for everyother radical the reaction with sulfite is the faster by

(7) far. For Br2 the ratio is about 4; for the weaker oxidantI2 , the ratio is about 200. For the dimethylaniline rad-

1). ical cation, the reaction with sulfite is very fast (9.9 x 10"ed M-Wsec-1) while the reaction with bisulfite is too slow1), to measure, (<8 x i05 M-1 sec-1). Similarly, the anilineish radical cation C6H5NH%+ oxidizes SO 2- with k = 4 xdun 109 M-1sec' and HS03- much more slowly, k = 4.8ted x 106M-1 sec-1.

C6H514H+ + S032- - C6H5NH2 + S03- (11)

C6H5f4H+ + HS03- - C6H5NH2 + H+ + S03- (12)

(8) C6H5I4H + SO32(HSO-) -- no reaction (13)

lue The neutral aniline radical, C6H5NH, on the other hand,does not oxidize sulfite. The cation radicals from pro-methazine, tryptophan, and tryptamine also oxidizeHS03 with moderate rate constants (Table 1) and in

(9) these cases the reactions were found to lead to equilib-rium. The reverse reactions and equilibrium constants

ar- will be discussed below.ex- Since the autoxidation of sulfite solutions was foundnd to be catalyzed strongly by trace amounts of transitional- metal ions, the reactions of sulfite with metal ions inthe their higher oxidation states has been the subject ofas many studies (11). Frequently, these studies are com-

plicated by the ability of sulfite to complex these metal)55 ions. These complexes are often quite stable; mercuricely ion ( in the presence of chloride) is used to protect sulfitethe from air oxidation (67). Other metal ion-sulfite com-

plexes are more labile, decomposing presumably to thereduced metal ion and the sulfite free radical. For strongoxidants like Mn(III), the reaction is fast and apparently

(10) irreversible (68). For weaker oxidants like Fe(III), thereaction is much slower and reversible, making the de-

ni- rivation of an elementary rate constant for the oxidationrns of sulfite difficult.Leir For substitution-inert metal ion complexes, the sit-re- uation is somewhat simpler since complex formation byrp- sulfite is not important. Rates have been measured for

the reactions of several metal ion complexes and rate

211

NETA AND HUIE

Table 1. Rate constants for reactions of sulfite with radicals.

Reaction pH k, M1 sec-' ReferenceOH + HS03- 9.5 x 109 (57)OH+So32- 5.5x 109 (57)0 +So32- 14 3 x 108 (43)02 + SO32 9.8 82 (45)S04- + HS03 - 3-1 x 109 (3)S04- + So32- - 5 x 108 (3)S04- + HS03-/So32- 7.8 2.6 x 108 (58)SOr- + HS03 6.8 3 x 106 (59)H2PO4 + HS03 4 2.7 x 108 (59)HP04- + So32 9 2.7 x 107 (60)po42- + SO32- 12 4.1 x 107 (60)C03 +So32- 11 1 x 107 (61)C12- +SO32-/HSO3- 7 3.3 x 107 (62)Br2- + HS03- 4.2 6.9 x 107 (63)Br2- +so32- 10 2.6 x 108 (63)I2- + HS03- 3 1.1 x 106 (63)I2- + HSO37/SO32- 6.7 1 x 107 (63)I2- + So32- 11 1.9 x 108 (63)NH2 + So32- 11 a (63)C6H60 + SO 2- 11 1 X 107 (63)1,3-HOC6H4O + -nSO32SO- 7 2.3 x 106 (64)1,3,5-(HO)2C6H30 + HS032-/ 7 3.2 x 106 (64)So32-C6H5NH2 + HS03 2.5 4.8 x 106 (63)C6H6NH2 + S03O2- b 4 x 109 (63)C6H51H +SO32- 13 <3 x 104 (63)C6H5N(CH3)3 + 2-

3.6 <8 x 105 (63)C6H5N(CH3)2+ +so3 10.9 9.9 x 108 (63)(chlorpromazine) + + HS03 3.6 -5 x 108 (59)(promethazine)Y+ + HS03- 3.6 6 x 108 (59)(promethazine)Y + HSO3-iSO32- 6.6 1.2 x 108 (59)(tryptophan)Y+ + HS03- 3.2 4.2 x 106 (65)(tryptamine)Y + HS03- 3 7.8 x 106 (65)(tryptophanamide)Y+ + HS03- 3 2.2 x 10W (65)(iodole)Y+ + HS03- 3 4 x 10W (65)(cystine)W- + HSO3-,SO32- 7.4 5.4 x 107 (66)aNo reaction detected (k<108M-lsec-1). The redox potentials for

NH2 and S03 radicals appear to be very similar, judging from rateconstants for their reactions with several reactants.

b Calculated from the pH dependence of the rate constant.

constants derived for the primary step, the one electronoxidation of sulfite. Bisulfite and S02 aq are assumedto be unreactive and the reported values depend uponthe acid dissociation constants chosen. Some values re-ported are given in Table 2.There is no information on the oxidation by free rad-

icals of S02 aq, the form of sulfite present in strongacid. Mn(III), a strong oxidant (E=1.4 V), does reactwith S(IV) in 2-6 M HC104. The very strong inversedependence of the rate constant on the acid concentra-tion was interpreted as showing that bisulfite was theimportant reactant, not SO2 * aq (68).

One-Electron Reduction of S(IV)Although not of importance in autoxidation, the re-

duction of S(IV) could be important in some biologicalsystems. The hydrated electron is unreactive towardSo32-(k < 106 M-1sec-I) and reacts very slowly withHS03- to produce hydrogen atoms (k = 2 x107WM-1sec-1) (3). On the other hand, SO2 is reported

Table 2. Rate constants for the oxidation of SO32- by complexedmetal ions.

Oxidant k M-1sec-' Reference

Fe(CN)6 - 0.96 (69)Fe(phen)3+ 4.6 x 106 (70)Fe(bpy)" 2.1 x 108 (71)IrCl62 5.6 x 104 (71)IrBr 2- 3.2 x 105 (71)*Ru(bpy)32+ 3 x 105 (72)Ru(bpy)33+ 2.2 x 109 (72)Os(bpy)33' 9 x 103 (72)Cu(tetraglycine)- 3.7 x 104 (73)Mo(CN)83- 6.2 x 103 (74)W(CN)83- 22.3 (74)

to be reduced rapidly by C02 to produce S02-, whileHS03- and So3 were unreactive (75). S02- also isproduced by the reduction of bisulfite using methyl viol-ogen radical, flavodoxins, and in a H2/hydrogenase sys-tem (76, Z7). More recently, enzymatic reduction of bis-ulfite to S02 was demonstrated in hepatic microsomalprotein and ascribed to reaction of cytochrome P-450(78). Also Ti3+ was found to react with sulfite in acidsolutions (pH 2-6) to produce S02 (42). All the abovereactions probably occur by electron transfer to S02rather then bisulfite. The radical S02- produced inthese processes is in equilibrium with dithionite(S2042-) and is known to be a highly reactive one-elec-tron reductant. It reduces metalloporphyrins containingFe(III), Co(III), and Mn(III) (79-81) and a wide varietyof electron-transfer proteins (82). The reactivity of S02-appears to follow the same pattern as 02, with rateconstants about 103 times higher (83). The potential forthe process

S02(aq) + e - 802 (14)

has been estimated as -0.26 V (84).

Reactions of Sulfite RadicalsThe S03- radical is for the most part a sulfur-centered

radical which can act as an oxidant or reductant andlike most other radicals may engage in hydrogen ab-straction or addition to double bonds. Hydrogen ab-straction, e.g., from isopropanol, was found to be un-important (k 103 M1 sec) (3). This finding is notsurprising, since the S-H bond expected to be formedin this process is much weaker than the C-H bond. (For-mation of an 0-H bond on sulfite is not likely due to thelow spin density on the oxygens of this radical) (56).

Addition of sulfite radicals to unsaturated bonds(C = C, C = N, and C-C) has been demonstrated byESR (39-42,49,55). These reactions were found to bevery sensitive to steric effects by substituents on theunsaturated bond. Because of the steady-state natureof these ESR experiments no kinetic data are available.Attempts to measure addition rate constants by pulseradiolysis using allyl alcohol as an example gave only

212

FREE-RADICAL CHEMISTRY OF SULFITE

an upper limit of 106 M-1 sec-' (66). The ESR resultsdemonstrate, however, the feasibility of sulfite radicaladdition to unsaturated biological targets.Extensive kinetic studies were carried out by pulse

radiolysis on the oxidation of organic substrates by503 . The results are summarized in Table 3. The sulfiteradical is found to oxidize ascorbate, trolox ( a water-soluble tocopherol derivative), methoxyphenol, hydro-quinone, phenylenediamines, and chlorpromazine withmoderate rate constants varying in the range of 106 to109 M-1sec- 1, depending on the redox potential of thesubstrate and on the pH, for example with ascorbate

S§0 + H2A - HSO + A- + H+ k<106 M-lsec'- (15)

S03 + HA- SO2- + A- + H+ k=9x106M-1sec-1 (16)

SO- + A2- S02- + A- k=3x108 M-'sec- (17)

For hydroquinone, catechol, and several other di- andtrihydroxybenzenes, the effect ofpH on their reactivitywith S03 was demonstrated in detail (64). All of thesecompounds were unreactive in neutral solutions but be-came highly reactive as they deprotonated in basic so-lutions. Compared to other oxidizing radicals such asBr2 , I2- (86), and phenoxyl (87), S03 reacts moreslowly and appears to be a milder oxidant. From a redoxequilibrium established between bisulfite and chlor-promazine at pH 3.6 [Eq.(18)],

S03 + ClPz + H+ a HSO + ClPz+ (18)

the redox potential for the couple S03-/HS03- wasmeasured to be 0.84V vs. NHE (59). The redox poten-tial for the S032 /SO32 couple in basic solutions is cal-culated (from the pKa of HS03- 3SO + H+) to be0.63 V vs. NHE. This change in potential explains whySo32- is oxidized by the same oxidant more readily thanHS03 , as discussed above (Table 1).

Since the SO3-/SO3 - potential is now known, reac-tions of S03- can be used to determine the potential forthe one-electron oxidation of other species, in thosecases where the electron transfer reaction is fast enoughso that the decay of 503 due to self-reaction is notimportant. This was initially carried out for phenol (59),leading to a new value of its one-electron redox poten-tial. More recently, equilibrium constants also havebeen measured for the reactions of 03- with trypto-phan, tryptamine, and tryptophanamide (65), and di-methylaniline (63).Knowing the redox potential for the reduction of S03-

allows us to calculate its oxidation potential from theknown two-electron redox potential for So32- in basicsolution:

S04 + H20 + 2e- - S032 + 20H- E = -0.92 V (19)

Table 3. Rate constants for reactions of SO3- radicals with var-ious reactants.

ReactantAscorbic acidAscorbate ionAscorbate dianionTroloxPhenolp-Methoxyphenolp-MethoxyphenolHydroquinoneHydroquinoneHydroquinoneHydroquinoneResorcinolp-Phenylenediaminep-Phenylenediaminep-PhenylenediamineN,N,N, 'N'-Tetramethyl-p-phenylenediamineN,N,N, 'N'-Tetramethyl-p-phenylenediamine

TryptophanTryptamineTryptophanamideChlorpromazine02Lipoic acidN-Methylisonicotinic acidAnthraquinone-2-sulfonateHistidineAllyl alcohol

pH<35-10

>129

11.19.2

12.478.9

10.512.912.53.45.39.34.5

9.5

3.2333.66.87,127777

k, M-'sec-<1069 x 1063 x 108_ 1066 x 10i54 x 1071.2 x 108<1064.5x 1065.4x 1073.2x 1081.5 x 108<5 x 1084.2 x 1065.0x 1078.2x 106

5.2 x 108

-8 x 10k5 x 1044 x 108a-5 x 101.5 x 109NRbNRNRNRNR

Reference(85)(85)(85)(85)(59)(59)(59)(64)(64)(64)(64)(64)(63)(63)(63)(63)

(63)

(65)(65)(65)(59)(59)(64)(64)(64)(64)(64)

a Reaction leads to equilibrium; see back reaction in Table 1.b No reaction detected by pulse radiolysis, indicating usually k<105

M'1sec1.

Subtracting E(SO3-) = 0.63 V from twice the formervalue (-0.92 V) leads to

S042 + H20 + e e~S03 + 20H E = -2.47 V (21)

This suggests that 03- can act as both a mild oxidantor a strong reductant. It may be difficult to demonstratethe reducing power of S03- since many oxidants willreact with sulfite ions before the 503- radicals are pro-duced in the radiolysis. Moreover, the above calculationof redox potential may not reflect the actual reducingpower of S03- since the initialTproduct is SO3, which issubsequently hydrated to S04 , possibly much moreslowly than the electron transfer (as argued for the caseof S02-) (84). In addition, it has been argued on thebasis of spin density on the sulfur, that SO3 is a muchweaker reductant than 0O2 (55).

Biological damage by S03 may be partly due to ox-idation reactions similar to those in Table 3. But themain harmful effects of this radical may lie in the factthat it reacts very rapidly with 02, k = 1.5 x 109M- 1sec- 1, to form a peroxyl radical which is much morereactive.

* + 0- s°3- + 2 > ° (22)

E = 0.63 V (20) The alternative reaction path forming SO3 + O2- was

213

.0- + e- --* S03'-

NETA AND HUIE

found (85) to be unimportant, at least under the exper-imental conditions of pH 3-12.

Reactions of Peroxysulfate RadicalThe S65 radical is a stronger oxidant than S03-; its

one-electron redox potential is estimated to be about1.1 V at pH 7 (59). Table 4 indeed shows that SO-oxidizes several substrates considerably more rapidlythan S03-, e.g., with ascorbate

SO6 + HA--- HSOg + A- k = 1.4 x 108 M-sec-1 (23)

Moreover, it can oxidize certain substrates (aniline anddimethylaniline, for example) which are not attacked byS03 at all and which, in fact, can form radicals thatoxidize sulfite ions. In such cases, when the redox po-sterqtial of the substrate is intermediate between thoseof S03- and S05-, a chain reaction is likely to developin the presence of 02 following the general patternshown in eqs. (24)-(26).

S03 + 02 -*s565 (24)

S06- + X SO52- + X+ (25)

X+ + SO3- X + SO (26)

Although SO6- can oxidize directly sulfite or bisulfiteions, the intermediacy of a substrate X may enhancethe chain process of sulfite oxidation (or peroxidation)by oxygen.The one-electron reduction of S05- yields HS05-,

peroxymonosulfate (Caro's acid). This is a strong oxi-dant, with a standard two-electron reduction potentialof 1.82 V (88).

HSO- + 2H+ + 2e- - HS04 + H20 (27)

Peroxymonosulfate is known to oxidize many organiccompounds (89). Of considerable interest is its abilityto oxidize sulfides to sulfones (90) and primary arylamines to nitroso compounds (91). In addition to thesereactions with organic compounds, which might involveoxygen atom transfer, peroxymonosulfate can be re-duced by metal ions, ppssibly producing the highly re-active free radicals, S04 or OH, as it does upon re-action with e,q- (92), e.g.

Fe2+ + HSO - Fe3+ + OH + S042- (28)

Fe2+ + HS05- Fel+ + OH- + SO4- (29)

These radicals, in turn, are capable of rather indiscrim-inate attack on biological molecules.The S65- radical possibly can also react by atom

transfer. This mechanism has been proposed for its re-action with bisulfite (30).

SO6 + HSO- -- + HSO,

Table 4. Comparison of some rate constants for reactions ofS03, S65 and S04 with organic compounds.

Rate constants, M-1 sec-1

Compound S03- S05- S04-

Ascorbic <106 2 x 106a bAscorbate 9x 106 1.4 x 10" bTrolox _106 1.2 x 07a bHydroquinone <106 2.7 x 106f bHydroquinone-monoanion 5 x 10 bCatechol <106 2.7 x 106 bResorcinol (reverse) <1 x 106 bAniline (reverse) 3 x lek bN,N-Dimethylaniline (reverse) 1 x i07c bTyrosine <106 -3 x 106dTryptophan 8 x 104 -2 x 106dHistidine NR -2.5 x lopdi-PrOH <103 -8 x l07dEthanol <103 -3 x 107dFumurate <106 -2 x 107dAllyl alcohol NR 1.5 x 106dGlycine <106 -9 x lO6dHSO3- 3 x 106f -lod

a Data of Huie and Neta (85).bWas not measured because of thermal reaction of the substrate

with S20 the precursor of S04-. The reaction, however, is ex-pected to be very fast (k109 M'sec').

c Data of Neta and Huie (63).d From Ross and Neta (86).e Data of Hayon et al. (3).'Data of Hlie and Neta (59).

Other reactions of bisulfite are known to involve oxygenatom transfer (93-97).

If SO5- is capable of transferring an oyxgen atom,the direct oxygenation of qrganic compounds is feasible,possibly producing the S04- radical as a by product.The existence of this type of reaction has not beenconfirmed.The mechanism of the self-reaction of SO65- is not

known. It has been proposed that the reaction leads tostable products and serves to terminate the autoxida-tion of sulfite (11). On the other hand the reaction hasbeen proposed to go to S04- or S208 (98).

2SO6 -* 2SO4 + 02

2SO6 -* S2o° + 02

(31)

(32)

with the ratio k(SO2-)/k(S20 2-) = 9. Although thisreaction is not likely to be important in the physiologicalrole of sulfite, it could be important in some of the lab-oratory studies of the effects of sulfite oxidation on bi-ological systems. The mechanism of this reaction cer-tainly deserves more study.

Reactions of Sulfate RadicalThe S04- radical, possibly produced by the reactions

discussed above, is very reactive toward organic com-pounds. It can abstract H atoms, add to double bonds,

214

FREE-RADICAL CHEMISTRY OF SULFITE 215

and oxidize by electron transfer quite rapidly. The rateconstants for such reactions with many organic com-pounds are summarized in a recent compilation (86) (seeexamples in Table 4) and will not be discussed here. Itis clear, however, that S04 attacks biological targetsindiscriminately.

ConclusionsIt has been apparent for some time that the effects

of SO2 autoxidation on organic and biological systemsare due to reactive internediates. Since the reactivitiesof many of these intermediates are now known, themechanism of these effects can be better understood.For several of the organic compounds, like hydroqui-none and other phenolic species, reaction with S03- andS65- is possible. Indeed, they prove to be the mostefficient inhibitors of SO2 autoxidation. For other or-ganic compounds, like mannitol and methionine, onlyreactions with S04 are, likely. Production of HS05from the reduction of S05 opens up additional possi-bilities, including direct reaction of HS05 and its de-composition to produce S04 or OH.Within the body, it is apparent that if SO2 is allowed

to undergo autoxidation, cellular damage is inevitable.Whether the presence of S(IV) beyond the region of thelungs can lead to similar damage is not apparent. To alarge extent this damage will depend on the equilibrium

RSSR + HSO- a± RSSO- + RSH

and the probability of forming radicals from RSS03-.One-electron reduction of this compound is expected toyield SO3- radicals. This was recently supported bypulse radiolysis experiments, whereby reduction ofRSS03 by eaq- and (CH3)2COH was found to form aradical which oxidized ascorbate with the same rateconstant as does S03- (66). If reduction of RSS03- toSO3- radical occurs with biological reductants, thiscould lead to oxidative damage by the S03- and theother radicals produced from it. Thus the RS groupserves not only as a carrier of sulfite but it also changesthe requirements for S03- radical formation from oxi-dation to reduction.

This work was supported in part by the Office of Basic EnergySciences of the U. S. Department of Energy.

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