RNA hydrolysis by cobalt(III) complexes ¹

Abstract

Adenylyl(3′-5′)adenosine (ApA) and uridylyl(3′-5′)uridine (UpU) are hydrolyzed at pH 7.0 and 50 °C by [Co(N)₄(OH₂)₂]³⁺ complexes (N: coordinated nitrogen atom). The pseudo-first-order rate constants for ApA hydrolysis by the triethylenetetramine and the tris(2-aminoethyl)amine complexes (0.1 mol dm^–3) are 1.5 × 10^–2 h^–1, corresponding to 10⁵-fold acceleration. The Co^III complexes are also active for the hydrolysis of 2′,3′-cyclic monophosphates of ribonucleotides. The pH–rate constant profile for ApA hydrolysis is bell-shaped with a maximum around pH 7, and a notable D₂O solvent isotope effect (2.0) is observed. It is proposed that the coordination water molecules on the Co^III ions promote (as general acid catalysts) the departure of the alkoxide ion of 5′-OH from the phosphorus atom.

References

1. Preliminary communication: Y. Matsumoto and M. Komiyama, J. Chem. Soc., Chem. Commun., 1990, 1050.
2. Reviews: (a) T. R. Cech, Science, 1987, 236, 1532; (b) M. Komiyama, J. Biochem., 1995, 118, 665; (c) R. Breslow, Acc. Chem. Res., 1991, 24, 317; (d) D. M. Perreault and E. V. Anslyn, Angew. Chem., Int. Ed. Engl., 1997, 36, 432.
3. G. L. Eichhorn, in Inorganic Biochemistry, ed. G. L. Eichhorn, Elsevier, Amsterdam, 1973, vol. 2, ch. 32.
4. B. Barbier and A. Brack, J. Am. Chem. Soc., 1988, 110, 6880.
5. J. Ciesiolka, T. Marciniec and W. Krzyzosiak, Eur. J. Biochem., 1989, 182, 445.
6. M. K. Stern, J. K. Bashkin and E. D. Sall, J. Am. Chem. Soc., 1990, 112, 5357.
7. K. Yoshinari, K. Yamazaki and M. Komiyama, J. Am. Chem. Soc., 1991, 113, 5899.
8. R. Breslow and D.-L. Huang, Proc. Natl. Acad. Sci. USA, 1991, 88, 4080.
9. M. Komiyama, K. Matsumura and Y. Matsumoto, J. Chem. Soc., Chem. Commun., 1992, 640.
10. J. R. Morrow, L. A. Buttrey, V. M. Shelton and K. A. Berback, J. Am. Chem. Soc., 1992, 114, 1903.
11. (a) D. R. Jones, L. F. Lindoy and A. M. Sargeson, J. Am. Chem. Soc., 1983, 105, 7327; (b) D. R. Jones, L. F. Lindoy and A. M. Sargeson, J. Am. Chem. Soc., 1984, 106, 7807; (c) R. Wijesekera, P. Hendry and A. M. Sargeson, Aust. J. Chem., 1992, 45, 1187.
12. (a) G. Rawji, M. Hediger and R. M. Milburn, Inorg. Chim. Acta, 1983, 79, 247; (b) R. M. Milburn, M. Gautem-Basak, R. Tribolet and H. Sigel, J. Am. Chem. Soc., 1985, 107, 3315.
13. (a) J. Chin and X. Zou, Can. J. Chem., 1987, 65, 1882; (b) J. Chin, M. B. Banaszczyk, V. Jubian and X. Zou, J. Am. Chem. Soc., 1989, 111, 186; (c) J. Chin and M. Banaszczyk, J. Am. Chem. Soc., 1989, 111, 4103; (d) J. H. Kim and J. Chin, J. Am. Chem. Soc., 1992, 114, 9792 and references therein.
14. (a) Y. Matsumoto, M. Komiyama and K. Takeuchi, Chem. Lett., 1990, 427; (b) Y. Matsumoto and M. Komiyama, Nucleic Acids, Symp. Ser., 1991, 25, 105; (c) K. Yonezawa, Y. Matsumoto and M. Komiyama, Nucleic Acids, Symp. Ser., 1991, 25, 145; (d) K. Yonezawa, Y. Matsumoto and M. Komiyama, Chem. Express, 1991, 6, 965.
15. P. R. Norman and R. D. Cornelius, J. Am. Chem. Soc., 1982, 104, 2356.
16. R. A. Kenley, R. H. Fleming, R. M. Laine, D. S. Tse and J. S. Winterle, Inorg. Chem., 1984, 23, 1870.
17. R. Hettich and H.-J. Schneider, J. Am. Chem. Soc., 1997, 119, 5638.
18. N. E. Dixon, R. J. Geue, J. N. Lambert, S. Moghaddas, D. A. Pearce and A. M. Sargeson, Chem. Commun., 1996, 1287.
19. C. K. Poon and M. L. Tobe, J. Chem. Soc. A, 1968, 1549.
20. The Co^III complexes of diethylenetriamine and 1,10-phenanthroline were inactive, probably due to insufficient stability in the reaction mixtures.
21. (a) R. G. Kuimelis and L. W. McLaughlin, Nucleic Acids Res., 1995, 23, 4753; (b) D.-M. Zhou, N. Usman, F. E. Wincott, J. M. Adamic, M. Orita, L.-H. Zhang, M. Komiyama, P. K. R. Kumar and K. Taira, J. Am. Chem. Soc., 1996, 118, 5862.
22. The present argument also holds even if the formation of the pentacoordinated intermediate and its breakdown proceed as a concerted process (see ref. 2d). There, the proposal should be read as ‘the scission of the P-O(5′) bond takes place only near the top of the reaction coordinate’.
23. (a) T. C. Bruice, T. H. Fife, J. J. Bruno and N. E. Brandon, Biochemistry, 1962, 1, 7; (b) Z. Shaked, R. P. Szajewski and G. M. Whitesides, Biochemistry, 1980, 19, 4156.
24. M. Oivanen, M. Ora, H. Almer, R. Stromberg and H. Lönnberg, J. Org. Chem., 1995, 60, 5620.
25. The substitution of 3′O for sulfur accelerated the alkaline hydrolysis; L. B. Weinstein, D. J. Earnshaw, R. Cosstick and T. R. Cech, J. Am. Chem. Soc., 1996, 118, 10 341 The effect was primarily attributed to the relief of strain in the five-membered ring (formed by the nucleophilic attack by 2′-OH), although some contribution of the increased polarizability was also indicated. Since no ‘strain effect’ is expected for the 5′O→S substitution and the acceleration is greater than that for the 3′O→S substitution, it is reasonable to ascribe the remarkable acceleration mostly to the difference in pK_a. The argument is further supported by the fact that the S-substitution of non-bridging oxygen atoms causes no notable acceleration (ref. 24).
26. The equilibrium constant for the complex formation between ApA and [Co(trien)(OH₂)₂]³⁺ at pH 7 and 50 °C has been determined to be 0.1 mol^–1 dm³ by ³¹P NMR. Thus the rate of ApA hydrolysis linearly increases with [Co^III complex]₀ under the conditions employed.
27. Previous proposal of general base catalysis by the Co^III-bound hydroxide (ref. 1), which was based on the assumption that formation of the pentacoordinated intermediate is rate-limiting, should be withdrawn.
28. Experimental error in these parameters is estimated to be around 10%. The smaller value of k₃ than k₄ is ascribed to electrostatic repulsion between the metal-bound hydroxide in [Co(trien)(OH₂)(OH)]²⁺ and hydroxide ion. The equilibrium constants (K) for the formation of the substrate–Co^III complex are not taken into consideration in the calculation, since they do not affect the relative ratios of the parameters.
29. Here the reactivities of [Co(trien)(OH₂)(OH)]²⁺ and [Co(trien)(OH₂)₂]³⁺ are taken as equal to each other, although it is not necessarily the case. The context is unchanged, whether this assumption is strictly correct or not.
30. According to an estimation using the results by P. Hendry and A. M. Sargeson(Inorg. Chem., 1990, 29, 92), the coordination of phosphate to Co^III complexes increases the electrophilicity of the phosphate around 50-fold, due to electrostatic effect: N. H. Williams and J. Chin, J. Chem. Soc., Chem. Commun., 1996, 131.
31. (a) M. Yashiro, A. Ishikubo and M. Komiyama, J. Chem. Soc. Chem. Commun., 1995, 1793; (b) A. Tsubouchi and T. C. Bruice, J. Am. Chem. Soc., 1995, 117, 7399; (c) K. G. Ragunathan and H.-J. Schneider, Angew. Chem., Int. Ed. Engl., 1996, 35, 1219; (d) M. Yashiro, A. Ishikubo and M. Komiyama, Chem. Commun., 1997, 83.
32. T. Shiiba and M. Komiyama, Tetrahedron Lett., 1992, 33, 5571.
33. J. L. Van Winkle, J. D. McClure and P. H. Williams, J. Org. Chem., 1966, 31, 3300.
34. R. Sayre, J. Am. Chem. Soc., 1955, 77, 6689.
35. A. M. Sargeson and G. H. Searle, Inorg. Chem., 1967, 6, 787.
36. F. Tafesse and R. M. Milburn, Inorg. Chim. Acta, 1987, 135, 119.
37. P. K. Glasoe and F. A. Long, J. Phys. Chem., 1960, 64, 188.