Reactions of Hydroxyl Radicals with Nucleic Acid Bases and. the Related Compounds in Gamma-irradiated Aqueous Solution
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1 Reactions of Hydroxyl Radicals with Nucleic Acid Bases and the Related Compounds in Gamma-irradiated Aqueous Solution MASUDA, T.,* SHINOHARA, H.* and KONDO, M.* Department of Chemistry, Faculty of Science, Tokyo Metropolitan University, Tokyo 158, Japan (Received March 14, 1975; Revised version received April 11, 1975) Rate constants for reactions of hydroxyl radicals with nucleic acid bases and the related compounds were determined by the p-nitrosodimethylaniline method. For addition reaction of hydroxyl radical to the compounds, reactivity indices, namely free valence, localization energy, frontier-electron-density and superdelocalizability, were calculated by Hiickel MO method. Among the examined reactivity indices, superdelocalizability was found to have a linear cor relation with logarithms of relative rate constants of pyrimidine bases, while the correlation was not observed for purine bases. INTRODUCTION Numerous studies have been published on radiation chemistry of nucleic acid constituents and the related compounds, because of their significance in radiation induced damage to biological systems. For radiation susceptibility of nucleic acid bases in aqueous solution, Pullman and Pullman' made an interesting suggestion from the argument based on G-value for destruction of bases that reaction site and reactivity of a nucleic acid base toward free radicals can be interpreted by mobile bond order and free valence of the base ring. Since G-value reflects net reactivity for destruction process that include generally more than one step and does not correspond to necessarily an elementary reaction, the suggestion is not satisfactory. On the other hand, rate constants for reactions of nucleic acid bases with hydroxyl radicals can be expec ted to give more exact basis for the argument on a structural feature responsible for the relative ease of reaction in different compounds. Although the rate con stants for the reactions of nucleic acid constituents with hydroxyl radicals have been already determined in several laboratories2 4>, the reported values differ from each other depending on the method of determination and the difference is serious at least for the quantitative discussion on reactivity and structural feature. Fur thermore, rate constants are not available in literature for a series of the related compounds required for the present study.
2 In the present investigation, we determined the rate constants for reactions of nucleic acid bases and the related compounds with hydroxyl radicals by the p nitrosodimethylaniline method"'), which was found in the previous work 7,8) to give relaiable values for rate constants of amino acids and enzyme proteins by com paring with pulse radiolysis data. In order to examine an applicability of Pull man's explanation and also to find more adequate reactivity index, the following reactivity indices were calculated by Huckel MO method ; free valence9), localiza tion energy1 ), frontier-electron-density"), and superdelocalizability12). Consequently superdelocalizability was found to have a linear relationship with the logarithms of relative rate constants. MATERIALS AND METHOD Uracil, cytosine, uric acid, guanine and hypoxanthine were obtained from Wako Pure Chemical Industries, Ltd. Pyrimidine, 2-aminopyrimidine, dihydrouracil, orotic acid, isoorotic acid, purine, 2-hydroxypurine, 2-aminopurine and isoguanine were obtained from Sigma Chemical Corp. Thymine was obtained from Daiichi Pure Chemical Ltd. and xanthine from Nutritional Biochemical Corp. All compounds were purchased as the purest grade preparation. Solutions for irradiation were prepared with triply distilled water and adjusted to neutral ph with sodium hydroxide, except for solutions of guanine, isoguanine and xanthine which were adjusted to alkaline ph. Irradiation was carried out with gamma rays from 137Cs source at about 1TC. Dose rate was determined to be 1.92x 1016 ev g-1 min-1 by Fricke dosimeter tak ing G (Fe 31) =15.5 Rate constants for reactions of nucleic acid bases and the related compounds with hydroxyl radicals were determined by competition kinetics using p-nitrosodi methylaniline as a reference compound 5'6). Rate constant for the reaction of p-nitrosodimethylaniline with hydroxyl radicals was taken to be 1.25X10" M-1 sec-1 13) Reactivity indices were calculated by Huckel approximation, using the parame ters of Hoffman and Ladik14) with the aid of a FACOM S computer. Cou lomb integrals of C* in N-C*-CH3 and 12N-C*=N were estimated to be and N 0.21 respectively, assuming the additivity of Coulomb integrals. Since rate con stants were determined mainly at neutral ph, calculation was carried out for the keto and amino-forms of bases. RESULTS AND DISCUSSION Second order rate constants for reactions of hydroxyl radicals with nucleic acid bases and the related compounds determined by the p-nitrosodimethylaniline method are shown in Table 1. Values cited as reference were corrected for the recent rate constant of thiocyanate ion of 1.1 x 1010 M-1 sec-1 when thiocyanate ion
3 Table 1 Rate constants for reactions of hydroxyl radicals with nucleic acid bases and the related compounds a. Reference 2. b. Reference 3 and 4. c. Reference 13. was used as a reference compound in pulse radiolysisz-4.13> Although the values obtained in the present study are slightly lower than the reported ones except adenine, the difference is not serious. While most measurements were made at ph 6-7, rate constants of guanine, isoguanine, and xanthine were determined at ph 10.0, 11.0, and 8.0, respectively, because of their poor solubility at neutral ph. The present study indicates that the reactivity of nucleic acid base is put in the following order. guanine > xanthine > adenine > thymine > uracil > cytosine purine pyrimidine. Pullman and Pullman represented the following order of the reactivity de duced from consideration of mobile bond order and free valence of base molecule. uracil > thymine > cytosine > purines. They also predicted that guanine is more sensitive than adenine. The present result accords with their prediction except for orders of purines. The reaction of hydroxyl radical with nucleic acid base is recognized as an addition reaction and the reaction product, OH adduct, was verified by ESR evidence for pyrimidine bases"-17). In the case of dihydrouracil, the reaction with hydroxyl radicals seems to be abstraction with the radical and the rate constant shown in Table 1 may
4 indicate the difference in reactivity between addition and abstraction. As Pullman and Pullman pointed out, behavior of it electrons of a molecule is concerned sig nificantly with relative ease of addition reaction. This is also supported by the present result consistent with the prediction based on mobile bond order and free valence. However, no simple and quantitative correlation was found between rate constants and free valences of the atoms which form the bond having the highest mobile bond order in the base molecule. Table 2 shows several reactivity indices calculated by Mickel MO method for pyrimidine bases. The numbers in paren theses in the column "Fr (R) " indicate the position of the carbon atom in the pyrimidine ring. As concerns localization energy, no tendency was found to corre late the rate constants. Fukui and his coworkers") indicated that superdelocali zability (Sr), a theoretical reactivity index derived by application of perturbation theory to a model in which the incoming group forms a weak it-bond to atom r of an otherwise unmodified 2r-system, predicts finely a reaction site and relative ease for addition reaction of aromatic hydrocarbons. In Table 2, are tabulated the val ues of Sr calculated for addition reaction of free radicals according to the follow ing equation. occ unocc Sr (R)= (Cri)2/2i+ (Crj)2/-2j 11) where Cri and Cr; are the coefficients of the r-th atomic orbital of the i-th and the Table 2 Reactivity indices of pyrimidine bases and the related compounds for addition reaction a. Frontier electron density. b. Superdelocalizability. c. Free valence. d. Localization energy.
5 j-th molecular orbitals, respectively. A; and A; are the energies of the i-th and the occ j-th molecular orbitals, respectively. or represents the summation for the occupied or the unoccupied molecular orbital. Frontier-electron-density, Fr (R), which was proposed also by Fukui and his coworkers") as an effective reactivity index indicating an intramolecular reaction site, was calculated for OH addition reaction by the following equation. Fr (R)_ (C,.HOMO)2+ (C,LUMO)2 (2) where HOMO or LUMO represents the highest occupied molecular orbital or the lowest unoccupied one. In the cases of cytosine, 5-methylcytosine and isoorotic acid, different site is indicated by Fr (R) and Sr (R). It is predicted from Sr (R) that the 5 position is more reactive than the 6 position. This is consistent with the experimental result, since OH adduct of isoorotic acid or cytosine at the 5 position was identified by electron spin resonance spectrometry 15' 16) For uracil and orotic acid, OH adduct at the 5 position was also confirmed by ESR experi mentsls.l') unocc
6 Fig. 1 Logarithms of relative rate constants for reactions of hydroxyl radi cals with pyrimidine bases plotted against the difference in super delocalizability. The rate constant of pyrimidine is taken as k0. Sr, is superdelocalizability of pyrimidine. Symbols are as follows ; T, thymine ; 0, orotic acid; U, uracil ; 5, 5-methylcytosine ; C, cytosine ; I, isoorotic acid; 2, 2-aminopyrimidine ; P, pyrimidine. To calculate the difference in Sr, the largest value of superdelocali zability was taken for each base. pyrimidine, respectively. Low activation energy for 5-methylcytosine or thymine suggests that the reaction proceeds at the encounter-controlled rate. (6). From a linear portion of the straight line in Fig. 1, one can derive equation ln(k/ko)=22.1 (Sr-Sro) (6) Combining equation (6) with (4), equation (7) is obtained. (Eo-E)/RT=22.1 (Sr-Sro) (7) Using the linear portion of the straight line in Fig. 1 and equations (6) and (7), about 11 Kcal mole-' is calculated as the difference in activation energy cor
7 responding to unity of Sr(R). From the value, the difference in activation energy between thymine and 5-methylcytosine is obtained to be 2.2 Kcal mole-'. Since activation energy of diffusion in aqueous medium is generally around a few Kcal mole-', it is apparent that thymine, orotic acid, uracil and 5-methylcytosine react with hydroxyl radicals at encounter-controlled rate. The difference in Sr (R) among the above compounds which belong to the plateau portion in Fig. 1 may correspond to a probability of effective collision at every encounter. Superdelocalizability can be correlated to reactivity constant, Qr, by the following equation" ur=23.1 Sr-22.5 (8) Urp* is defined to be equal to logarithm of relative rate constant in the same manner with Hammett's up treatment, when p* is reaction constant. For addition reaction of hydroxyl radical, the relation has not been confirmed and p* is not Table 3 Reactivity indices of purine bases and the related compounds for addition reaction a. Frontier electron density. b. Superdelocalizability. c. Free valence. d. Localization energy.
8 available. If p* is, however, assumed to be unity, the difference in the activation energy is estimated as about 14 Kcal mole-1 for unity change in Sr, since a dif ference in the activation energy equals to RTar p*. The value accords fairly with the present estimation of 11 Kcal mole-'. For purine bases, the above simple correlation between logarithms of relative rate constants and Sr(R) could not be found. The reaction site indicated by the reactivity indices shown in Table 3 varies according to purine base and among the reactivity indices for the same base is there a disagreement of indication of the reaction site. Since ESR data which identify the radical structure of OH ad duct of purine base are not available at present, it is difficult to determine the reaction site on purine bases. In the present estimation of Sr(R), an assumption was made that an energy of pseudo-2r-orbital is equal to a, which is the coulomb integral of a carbon atom of benzene. If the assumption is not relevant, Sr (R) should be calculated by the following equation. -re un ~o-tcc Sr(R) = (Cri) 2/(2i x) + 7 (Crj)2/(2j + x) (9) When 0.3 is taken as x, the correlation between logarithms of relative rate constants and Sr(R) is slightly improved. The situation, however, is not the same with pyrimidine bases. An irregularity observed in reactivities of purines may be interpreted as due to neglection of steric factor which is possibly significant for a size of purine or to rate constants determined at alkaline ph. Although there remains a discrepancy for purine bases, a kind of linear free energy relation would be observed between reactivity of pyrimidine base toward hydroxyl radicals and superdelocalizability. A similar relation was reported by Rao and Hayon between the rate of electron transfer and redox potential of ac ceptor dye20>. ACKNOWLEDGMENTS The authors thank Dr. Akira Imamura of National Cancer Center Research Institute for his helpful discussion on theoretical treatment and also acknowledge the financial support of the Department of Education of Japan. REFERENCES 1. Pullman, B. and Pullman, A. (1963) Quantum Biochemistry. Interscience Publishers, New York and London. pp Scholes, G., Shaw, P., Willson, R. L. and Ebert, M. (1965) Pulse radiolysis studies of aqueous solutions of nucleic acid and related substances. Pulse Radiolysis (eds. M. Ebert, J. P. Keene, A. J. Swallow and J. H. Baxendale). Academic Press, London and New York. pp Greenstock, C. L., Hunt, J. W. and Ng, M. (1969) Pulse radiolysis studies of uracil and its derivatives. Trans. Faraday Soc. 65: Greenstock, C. L., Ng, M. and Hunt, J. W. (1968) Pulse radiolysis studies of reactions of primary species in water with nucleic acid derivatives. Adv. Chem. Ser. 81: (Radi ation Chemistry) :
9 5. Kraljic, I. and Trumbore, C. N. (1965) p-nitrosodimethylaniline as an OH radical scavenger in radiation chemistry. J. Am. Chem. Soc. 87: Shah, S., Trumbore, C. N., Giessner, B. and Park, W. (1968) Studies in the radiation and photochemistry of aqueous p-nitrosodimethylaniline. Adv. Chem. Ser. 81, (Radi ation Chemistry) : Masuda, T., Nakano, S. and Kondo, M. (1973) Rate constants for the reactions of OH radicals with the enzyme proteins as determined by the p-nitrosodimethylaniline meth od. J. Radiat. Res. 14: Masuda, T., Nakano, S. and Kondo, M. (1974) Reactivities of enzymes toward hydroxyl radicals. J. Radiat. Res. 15: Burkitt, F. H., Coulson, C. A. and Longuet-Higgins, H. C. (1951) Free valence in un saturated hydrocarbons. Trans. Faraday Soc. 47: Wheland, G. W. (1942) A quantum mechanical investigation of the orientation of sub stituents in aromatic molecules. J. Amer. Chem. Soc. 64: Fukui, K., Yonezawa, T. and Shingu, H. (1952) A molecular orbital theory of reactivity in aromatic hydrocarobons. J. Chem. Phys. 20: Fukui, K., Nagata, C., Yonezawa, T. and Morokuma, K. (1961) Theoretical reactivity index of addition in the " Frontier Electron Theory ". Bull Chem. Soc. Japan 34, Willson, R. L., Greenstock, C. L., Adams, G. E., Wageman, R. and Dorfman, L. M. (1971) The standardization of hydroxyl radical rate data from radiation chemistry. Int. J. Radiat. Phys. Chem. 3: Hoffman, T. A. and Ladik, J. (1964) Quantum mechanical considerations on some properties of DNA. Adv. Chem. Phys. 7: Ormerod, M. G. and Singh, B. B. (1966) Reaction of OH radicals with nucleic acid bases an ESR study. Int. J. Radiat. Biol. 10: Nicolau, C., McMillan, M. and Norman, R. O. C. (1969) An ESR study of short-lived radicals derived from pyrimidines in aqueous solution. Biochirn. Biophys. Acta 174: Hutterman, J., Ward, J. F. and Meyers, Jr., L. S. (1970) Electron spin resonance studies of free radicals formed from orotic acid. J. Phys. Chem. 74: Moelwyn-Hughes, E. A. (1971) Chemical Statics and Kinetics of Solution. Academic Press, London and New York. pp Streitwieser, J. R. A. (1961) Molecular Orbital Theory for organic chemists. John Wiley and Sons, Inc., New York and London. pp Rao, P. S. and Hayon, E. (1973) Reduction of dyes by free radicals in solution. Cor relation between reaction rate constants and redox potentials. J. Phys. Chem. 77:
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