The energetics of hydrogen bonds in model systems: Implications for enzymatic catalysis

Science

Volumn 272, Issue 5258, 1996, Pages 97-101

  Shan, Shu Ou ^a   Loh, Stewart ^a   Herschlag, Daniel ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CATALYSIS; ENERGY TRANSFER; ENZYME MECHANISM; HYDROGEN BOND; MOLECULAR MODEL; PRIORITY JOURNAL;

EID: 0029926948     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.272.5258.97     Document Type: Article

References (79)

1. a = 0 to catalysis, not to the bond length or nature of the H-bond potential
2. W W Cleland, Biochemistry 31, 317 (1992), _ and M. M Kreevoy, Science 264, 1887 (1994)
3. W W Cleland, Biochemistry 31, 317 (1992), _ and M. M Kreevoy, Science 264, 1887 (1994)
4. J. A. Gerlt and P. G. Gassman, Biochemistry 32, 11943 (1993); J Am. Chem Soc. 115, 11552 (1993).
5. J. A. Gerlt and P. G. Gassman, Biochemistry 32, 11943 (1993); J Am. Chem Soc. 115, 11552 (1993).
6. P. A. Frey, S A. Whitt, J B. Tobin, Science 264, 1927 (1994).
7. J W Larson and T. B. McMahon, J Am Chem. Soc 105, 2944 (1983), J. E. Mihalick, G G. Gatev J. Brauman, in preparation.
8. R. Yamdagni and P. Kebarle, J. Am. Chem. Soc. 93, 7139 (1971); H. P. Dixon, H. D. B. Jenkins, T. C. Waddington, J. Chem Phys. 57, 4388 (1972).
9. R. Yamdagni and P. Kebarle, J. Am. Chem. Soc. 93, 7139 (1971); H. P. Dixon, H. D. B. Jenkins, T. C. Waddington, J. Chem Phys. 57, 4388 (1972).
10. F. Hibbert and J. Emsley, Adv Phys. Org. Chem. 26, 255 (1990).
11. W. P. Jencks, Catalysis in Chemistry and Enzymology (Dover, New York, ed. 2, 1987), chap. 6
12. P. Gilli, V. Bertlasi, V. Ferretti, G. Gilli, J. Am. Chem. Soc. 116, 909 (1994).
13. C. L. Perrin and J. D. Thorbum, ibid. 111, 8010 (1989); ibid. 114, 8559 (1992), C. L Perrin, Science 266, 1665 (1994).
14. C. L. Perrin and J. D. Thorbum, ibid. 111, 8010 (1989); ibid. 114, 8559 (1992), C. L Perrin, Science 266, 1665 (1994).
15. C. L. Perrin and J. D. Thorbum, ibid. 111, 8010 (1989); ibid. 114, 8559 (1992), C. L Perrin, Science 266, 1665 (1994).
16. J. Hine, Physical Organic Chemistry (McGraw-Hill, New York, ed. 2, 1962), chap 4; J Am. Chem. Soc 94, 5766 (1972).
17. J. Hine, Physical Organic Chemistry (McGraw-Hill, New York, ed. 2, 1962), chap 4; J Am. Chem. Soc 94, 5766 (1972).
18. L. H Funderburk and W, P. Jencks, J. Am. Chem Soc. 100, 6708 (1978); N. Stahl and W. P. Jencks, ibid 108, 4196 (1986); M E. Rothenberg, J. P. Richard, W P. Jencks, ibid. 107, 1340 (1985)
19. L. H Funderburk and W, P. Jencks, J. Am. Chem Soc. 100, 6708 (1978); N. Stahl and W. P. Jencks, ibid 108, 4196 (1986); M E. Rothenberg, J. P. Richard, W P. Jencks, ibid. 107, 1340 (1985)
20. L. H Funderburk and W, P. Jencks, J. Am. Chem Soc. 100, 6708 (1978); N. Stahl and W. P. Jencks, ibid 108, 4196 (1986); M E. Rothenberg, J. P. Richard, W P. Jencks, ibid. 107, 1340 (1985)
21. M. Meot-ner and L W Sieck, J. Phys. Chem. 90, 6687 (1986); J. Am. Chem. Soc. 108, 7525 (1986); M Meot-ner, ibid. 106, 1257 (1984), G. Caldwell, M. D. Rozeboom, J. P. Kiplinger, J. E. Bartness, ibid, p. 4660.
22. M. Meot-ner and L W Sieck, J. Phys. Chem. 90, 6687 (1986); J. Am. Chem. Soc. 108, 7525 (1986); M Meot-ner, ibid. 106, 1257 (1984), G. Caldwell, M. D. Rozeboom, J. P. Kiplinger, J. E. Bartness, ibid, p. 4660.
23. M. Meot-ner and L W Sieck, J. Phys. Chem. 90, 6687 (1986); J. Am. Chem. Soc. 108, 7525 (1986); M Meot-ner, ibid. 106, 1257 (1984), G. Caldwell, M. D. Rozeboom, J. P. Kiplinger, J. E. Bartness, ibid, p. 4660.
24. M. Meot-ner and L W Sieck, J. Phys. Chem. 90, 6687 (1986); J. Am. Chem. Soc. 108, 7525 (1986); M Meot-ner, ibid. 106, 1257 (1984), G. Caldwell, M. D. Rozeboom, J. P. Kiplinger, J. E. Bartness, ibid, p. 4660.
25. Z Pawlak, G Zundel, J. Fritsch, Z Naturforsch. Teil A Electrochim. Acta 29, 391 (1984); G. Albrecht and G. Zundel, Z Naturforsch. 39A, 986 (1984); J. Chem. Soc. Faraday Trans. 1 80, 553 (1983); H. Schmiderer et al., J Mol Struct 161, 87 (1987).
26. Z Pawlak, G Zundel, J. Fritsch, Z Naturforsch. Teil A Electrochim. Acta 29, 391 (1984); G. Albrecht and G. Zundel, Z Naturforsch. 39A, 986 (1984); J. Chem. Soc. Faraday Trans. 1 80, 553 (1983); H. Schmiderer et al., J Mol Struct 161, 87 (1987).
27. Z Pawlak, G Zundel, J. Fritsch, Z Naturforsch. Teil A Electrochim. Acta 29, 391 (1984); G. Albrecht and G. Zundel, Z Naturforsch. 39A, 986 (1984); J. Chem. Soc. Faraday Trans. 1 80, 553 (1983); H. Schmiderer et al., J Mol Struct 161, 87 (1987).
28. Z Pawlak, G Zundel, J. Fritsch, Z Naturforsch. Teil A Electrochim. Acta 29, 391 (1984); G. Albrecht and G. Zundel, Z Naturforsch. 39A, 986 (1984); J. Chem. Soc. Faraday Trans. 1 80, 553 (1983); H. Schmiderer et al., J Mol Struct 161, 87 (1987).
29. L J. Altman, D. Laungani, G Gunnarson, H Wennerstrom, S. Forsen, J. Am Chem. Soc. 100, 8264 (1978); G Gunnarson, H. Wennerstrom, W. Egan, S Forsen, Chem. Phys Lett 38, 96 (1976).
30. L J. Altman, D. Laungani, G Gunnarson, H Wennerstrom, S. Forsen, J. Am Chem. Soc. 100, 8264 (1978); G Gunnarson, H. Wennerstrom, W. Egan, S Forsen, Chem. Phys Lett 38, 96 (1976).
31. H. Bartl and H. Kuppers, Z Kristallogr. 152, 161 (1980); M. Biagini-Cingi, A. M. Manotti-Lanfredi, A. Tiripicchio, M. Tiripicchio-Camelini, Acta Crystallogr. Sect B 33, 3772 (1977)
32. H. Bartl and H. Kuppers, Z Kristallogr. 152, 161 (1980); M. Biagini-Cingi, A. M. Manotti-Lanfredi, A. Tiripicchio, M. Tiripicchio-Camelini, Acta Crystallogr. Sect B 33, 3772 (1977)
33. a's below 6 were also confirmed by measurement of self-dissociation of the acid (40). Values are reported as mean ± 2 SD.
34. a on the σ values of the substituents for a homologous series of compounds, and "X, meta or para" refers to the substituent in either meta or para position (the lower of the two calculated values reflects the group that will be deprotonated first) Values of σ are from O. Exner, Correlation Analysis of Chemical Data (Plenum, New York, 1988), pp 439-540. A p value of 2 4 in DMSO (40) was used.
35. a's are matched.
36. S. Shan and D. I lerschlag, in preparation.
37. a's of the donor and acceptor are varied independently in the intermolecular system
38. M. M. Kreevoy and T. M. bang, J. Am. Chem. Soc 102, 3315 (1980).
39. a = O, nor does it change the slopes in Fig. 3 significantly (41).
40. a (that is, the slope). Analogous considerations hold for the intramolecular H bonds in substituted PAs.
41. S. Schemer and T. Kar, J. Am. Chem Soc. 117, 6970 (1995).
42. For examples, see J. Rubin and G. S Panson, J. Phys Chem. 69, 3089 (1965); O. Kasende and Th. Zeegers-Huyskens, ibid. 88, 2636 (1984); A. D. Sherry and K. F Purcell, ibid. 74, 3535 (1970); J. E. Gordon, J. Org Chem. 26, 738 (1961); R. W. Taft, D Gurka, L Joris, P. v. R. Schleyer, J. W. Rakshys, J Am Chem. Soc. 91, 4801 (1969); C. Wilcox et al, Tetrahedron 51, 621 (1995)
43. For examples, see J. Rubin and G. S Panson, J. Phys Chem. 69, 3089 (1965); O. Kasende and Th. Zeegers-Huyskens, ibid. 88, 2636 (1984); A. D. Sherry and K. F Purcell, ibid. 74, 3535 (1970); J. E. Gordon, J. Org Chem. 26, 738 (1961); R. W. Taft, D Gurka, L Joris, P. v. R. Schleyer, J. W. Rakshys, J Am Chem. Soc. 91, 4801 (1969); C. Wilcox et al, Tetrahedron 51, 621 (1995)
44. For examples, see J. Rubin and G. S Panson, J. Phys Chem. 69, 3089 (1965); O. Kasende and Th. Zeegers-Huyskens, ibid. 88, 2636 (1984); A. D. Sherry and K. F Purcell, ibid. 74, 3535 (1970); J. E. Gordon, J. Org Chem. 26, 738 (1961); R. W. Taft, D Gurka, L Joris, P. v. R. Schleyer, J. W. Rakshys, J Am Chem. Soc. 91, 4801 (1969); C. Wilcox et al, Tetrahedron 51, 621 (1995)
45. For examples, see J. Rubin and G. S Panson, J. Phys Chem. 69, 3089 (1965); O. Kasende and Th. Zeegers-Huyskens, ibid. 88, 2636 (1984); A. D. Sherry and K. F Purcell, ibid. 74, 3535 (1970); J. E. Gordon, J. Org Chem. 26, 738 (1961); R. W. Taft, D Gurka, L Joris, P. v. R. Schleyer, J. W. Rakshys, J Am Chem. Soc. 91, 4801 (1969); C. Wilcox et al, Tetrahedron 51, 621 (1995)
46. For examples, see J. Rubin and G. S Panson, J. Phys Chem. 69, 3089 (1965); O. Kasende and Th. Zeegers-Huyskens, ibid. 88, 2636 (1984); A. D. Sherry and K. F Purcell, ibid. 74, 3535 (1970); J. E. Gordon, J. Org Chem. 26, 738 (1961); R. W. Taft, D Gurka, L Joris, P. v. R. Schleyer, J. W. Rakshys, J Am Chem. Soc. 91, 4801 (1969); C. Wilcox et al, Tetrahedron 51, 621 (1995)
47. For examples, see J. Rubin and G. S Panson, J. Phys Chem. 69, 3089 (1965); O. Kasende and Th. Zeegers-Huyskens, ibid. 88, 2636 (1984); A. D. Sherry and K. F Purcell, ibid. 74, 3535 (1970); J. E. Gordon, J. Org Chem. 26, 738 (1961); R. W. Taft, D Gurka, L Joris, P. v. R. Schleyer, J. W. Rakshys, J Am Chem. Soc. 91, 4801 (1969); C. Wilcox et al, Tetrahedron 51, 621 (1995)
48. We do not mean to imply that H bonds have no covalent character. Indeed, the unusual spectroscopic behavior cited in the text is most simply accounted for by some degree of covalent character of certain H bonds (7, 8). Rather, our discussion deals solely with the energetic behavior of H bonds The results suggest that the energetics can be under stood from simple electrostatic considerations, and that covalent bonding character does not lead to unusual energetic behavior of these H bonds Further, the near additivity of the energy of the two H bonds in 2,6-dihydroxybenzoate in DMSO suggests that these H bonds are not predominantly covalent in nature (37).
49. a = 0 is traversed This is not accounted for in Eq. 2
50. The use of the bulk dielectric constant ε in Eq 2 is a simplification included to illustrate the effect of solvent properties on H bonding Local solvation effects are important determinants of the stability of H-bonded species [for examples, see C Beeson and T. A. Dix, J. Am. Chem. Soc. 115, 10275 (1993); T. M Krygowsk and W. R. Fawcett, ibid 97 2143 (1975); A Allerhand and P. R. Schleyer, ibid 85 371 (1963), E. B. Nadler and Z. Rappoport, ibid 111, 213 (1989)]
51. The use of the bulk dielectric constant ε in Eq 2 is a simplification included to illustrate the effect of solvent properties on H bonding Local solvation effects are important determinants of the stability of H-bonded species [for examples, see C Beeson and T. A. Dix, J. Am. Chem. Soc. 115, 10275 (1993); T. M Krygowsk and W. R. Fawcett, ibid 97 2143 (1975); A Allerhand and P. R. Schleyer, ibid 85 371 (1963), E. B. Nadler and Z. Rappoport, ibid 111, 213 (1989)]
52. The use of the bulk dielectric constant ε in Eq 2 is a simplification included to illustrate the effect of solvent properties on H bonding Local solvation effects are important determinants of the stability of H-bonded species [for examples, see C Beeson and T. A. Dix, J. Am. Chem. Soc. 115, 10275 (1993); T. M Krygowsk and W. R. Fawcett, ibid 97 2143 (1975); A Allerhand and P. R. Schleyer, ibid 85 371 (1963), E. B. Nadler and Z. Rappoport, ibid 111, 213 (1989)]
53. The use of the bulk dielectric constant ε in Eq 2 is a simplification included to illustrate the effect of solvent properties on H bonding Local solvation effects are important determinants of the stability of H-bonded species [for examples, see C Beeson and T. A. Dix, J. Am. Chem. Soc. 115, 10275 (1993); T. M Krygowsk and W. R. Fawcett, ibid 97 2143 (1975); A Allerhand and P. R. Schleyer, ibid 85 371 (1963), E. B. Nadler and Z. Rappoport, ibid 111, 213 (1989)]
54. W. P. Jencks, Adv. Enzymol. 43, 219 (1975)
55. J. P. Guthrie and R. Kluger, J. Am. Chem. Soc. 115, 11569 (1993); A. Warshel, Proc. Natl Acad. Sci. U.S.A. 75, 5250 (1978); Biochemistry 20, 3167 (1981); S Rao, U. C. Singh, P. A Bash, P A. Kollman, Nature 328, 551 (1987); D. Herschlag. F. Eckstein, T. R. Cech, Biochemistry 32, 8312 (1993).
56. J. P. Guthrie and R. Kluger, J. Am. Chem. Soc. 115, 11569 (1993); A. Warshel, Proc. Natl Acad. Sci. U.S.A. 75, 5250 (1978); Biochemistry 20, 3167 (1981); S Rao, U. C. Singh, P. A Bash, P A. Kollman, Nature 328, 551 (1987); D. Herschlag. F. Eckstein, T. R. Cech, Biochemistry 32, 8312 (1993).
57. J. P. Guthrie and R. Kluger, J. Am. Chem. Soc. 115, 11569 (1993); A. Warshel, Proc. Natl Acad. Sci. U.S.A. 75, 5250 (1978); Biochemistry 20, 3167 (1981); S Rao, U. C. Singh, P. A Bash, P A. Kollman, Nature 328, 551 (1987); D. Herschlag. F. Eckstein, T. R. Cech, Biochemistry 32, 8312 (1993).
58. J. P. Guthrie and R. Kluger, J. Am. Chem. Soc. 115, 11569 (1993); A. Warshel, Proc. Natl Acad. Sci. U.S.A. 75, 5250 (1978); Biochemistry 20, 3167 (1981); S Rao, U. C. Singh, P. A Bash, P A. Kollman, Nature 328, 551 (1987); D. Herschlag. F. Eckstein, T. R. Cech, Biochemistry 32, 8312 (1993).
59. J. P. Guthrie and R. Kluger, J. Am. Chem. Soc. 115, 11569 (1993); A. Warshel, Proc. Natl Acad. Sci. U.S.A. 75, 5250 (1978); Biochemistry 20, 3167 (1981); S Rao, U. C. Singh, P. A Bash, P A. Kollman, Nature 328, 551 (1987); D. Herschlag. F. Eckstein, T. R. Cech, Biochemistry 32, 8312 (1993).
60. C. D Waldburger, J F Schildbach, R. T Sauer, Nature Struct. Biol. 2, 122 (1995); S. Dao-pin, D E Anderson, W. A. Baase, F. W Dahlquist, B. W. Matthews, Biochemistry 30, 11521 (1991); M. Gilson andB Honig,Proc. Natl. Acad Sci. U.S A 86 1524 (1989)
61. C. D Waldburger, J F Schildbach, R. T Sauer, Nature Struct. Biol. 2, 122 (1995); S. Dao-pin, D E Anderson, W. A. Baase, F. W Dahlquist, B. W. Matthews, Biochemistry 30, 11521 (1991); M. Gilson andB Honig,Proc. Natl. Acad Sci. U.S A 86 1524 (1989)
62. C. D Waldburger, J F Schildbach, R. T Sauer, Nature Struct. Biol. 2, 122 (1995); S. Dao-pin, D E Anderson, W. A. Baase, F. W Dahlquist, B. W. Matthews, Biochemistry 30, 11521 (1991); M. Gilson andB Honig,Proc. Natl. Acad Sci. U.S A 86 1524 (1989)
63. H. Tong and L. Davis, Biochemistry 34, 3362 (1995).
64. K. C. Usher, S. J. Remington, D. P. Martin, D. G Drueckhammer, ibid. 33, 7753 (1994); B. Schwartz, D. G. Drueckhammer, K. C. Usher, S. J Remington, ibid. 34, 15159 (1995)
65. K. C. Usher, S. J. Remington, D. P. Martin, D. G Drueckhammer, ibid. 33, 7753 (1994); B. Schwartz, D. G. Drueckhammer, K. C. Usher, S. J Remington, ibid. 34, 15159 (1995)
66. For an enzyme to take advantage of the greater increase of H-bond strength in nonaqueous environments, binding interactions away from the site of electronic rearrangement are presumably required to localize the H-bonding groups in the low-dielectric active site; this situation is not intrinsically favorable (20, 32)
67. water to compare the results in the different solvents (42)
68. S. Shan and D. Herschlag, in preparation.
69. W. S Matthews et al., J. Am. Chem. Soc. 97.7006 (1975); F G. Bordwell, Acc. Chem. Res. 21, 466 (1988).
70. W. S Matthews et al., J. Am. Chem. Soc. 97.7006 (1975); F G. Bordwell, Acc. Chem. Res. 21, 466 (1988).
71. F G Bordwell, J. C. Branca, D. L Hughes, W N Olmstead, J. Org. Chem 45, 3305 (1980)
72. F. G Bordwell, R. J McCallum, W. N. Olmstead, ibid. 49, 1424 (1984).
73. water > 2, where the proton transfers occur at much higher phenol concentrations than are required for complex formation with the nitrophenolate Control experiments with sterically hindered phenols (2,6-dt-tert-butylphenol and 2,6-di-tert-butyl-4-nrtrophenol) did not produce the spectral shift described in (23), even at concentrations up to 1 M This finding ruled out complications from general solvent effects by addition of phenols to the phenolate solution and suggested that H bonding is responsible for complexation. Addition of increasing concentrations of a nonconjugate phenol to a solution containing a preformed homoconjugate nitrophenol-nitrophenolate complex leads to loss of the homoconjugate complex and formation of the heteroconjugate complex, as judged by modest spectral shifts The concentration dependence of these changes was consistent with the relative stability of the H-bonded species obtained from the direct measurements described in (23).
74. a scales is expected to be somewhat greater (43).
75. D. A Bors, M. J Kaufman, A. Streitwieser Jr., J. Am. Chem. Soc. 107, 6975 (1985).
76. 2O ratios (1/9 → 9/1). The small amount of water added did not affect the observed downfield chemical shift of the H-bonded proton. Values are reported as mean ± 2 SD.
77. X. meta])
78. G Kortum, W. Vogel, K. Andrussow, Dissociation Constants of Organic Acids in Aqueous Solution (Butterworths, London, 1961).
79. We thank J Brauman, J. Klinman, and J Kirsch for discussions and helpful suggestions, the Bordweil group for technical help, and the Herschlag lab for comments on the manuscript. This work is supported by grants from the Lucille P. Markey Charitable Trust arid the Chicago Community Trust to D.H D.H. is a Lucille P Markey Scholar and a Searle Scholar