The X-ray structure of a transition state analog complex reveals the molecular origins of the catalytic power and substrate specificity of acetylcholinesterase

Journal of the American Chemical Society

Volumn 118, Issue 10, 1996, Pages 2340-2346

  Harel, Michal ^a   Quinn, Daniel M ^c   Nair, Haridasan K ^c,d   Silman, Israel ^a   Sussman, Joel L ^a,b  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b BROOKHAVEN NATIONAL LABORATORY   (United States)

^c E11 SSH   (United States)

^d Clarion Pharmaceuticals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYST ACTIVITY; CRYSTALLOGRAPHY; HYDROGEN BONDS; MOLECULAR STRUCTURE; X RAY DIFFRACTION ANALYSIS;

ACETYLCHOLINESTERASE; CATALYTIC POWER; SUBSTRATE SPECIFICITY; TRANSITION STATE COMPLEX; TRIMETHYLAMMONIO TRIFLUOROACETOPHENONE;

ENZYMES;

ACETYLCHOLINESTERASE;

ARTICLE; ENZYME BINDING; ENZYME STRUCTURE; NONHUMAN; THERMODYNAMICS; TORPEDO CALIFORNICA; X RAY CRYSTALLOGRAPHY;

EID: 15844422678     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja952232h     Document Type: Article

References (82)

1. Abbreviations: ACh, acetylcholine; AChE, acetylcholinesterase; ATCh. (acetylthio)choline; EDR. edrophonium; TcAChE, Torpedo californica AChE. Single letter amino acid codes used: A, alanine; C, cysteine; D, aspartate: E. glutamate: F. phenylalanine: G, glycine; H, histidine: L, leucine; S. serine; V, valine; W, tryptophan: Y, tyrosine. The sequence numbering of TcAChE is used throughout this paper when amino acid residues of any AChE are discussed.
2. Rosenberry, T. L. Adv. Enzymol. Relar. Areas Mol. Biol. 1975, 43, 103-218.
3. Taylor, P. In Pharmacological Basis of Therapeutics: Gilman, A. G., Goodman, L. S., Murad, F., Eds.; MacMillan: New York, 1985: pp 110-129.
4. Quinn, D. M. Chem. Rev. 1987, 87, 955-979.
5. Bazelyansky, M.; Robey, E; Kirsch, J. F. Biochemistry 1986, 25, 125-130.
6. Hasinoff, B. B. Biochim. Biophys. Acta 1982. 704. 52-58.
7. Nolte, H.-J.; Rosenberry, T. L.; Neumann, E. Biochemistry 1980, 19, 3705-3711.
8. Froede, H. C.; Wilson. I. B. In The Enzvmes, 3rd ed.; Boyer, P. D., Ed.; Academic Press: New York. 1971; Vol. 5, pp 87-114.
9. Sussman, J. L.; Harel, M.; Frolow, F.: Oefner, C.; Goldman, A.; Toker, L.: Silman, I. Science 1991, 253, 872-879.
10. Stroud, R. M. Sci. Am. 1974, 231, 74-88.
11. Blow, D. M. Acc, Chem. Res. 1976, 9, 145-152.
12. Kraut, J. Anna. Rev. Biochem. 1977, 46, 331-358.
13. Polgar, L- In Hydrolync Enzymes; Neuberger, A., Brockletiurst, K., Eds.: Elsevier: Amsterdam. 1987; pp 159-200.
14. Gentry, M. K.; Doctor, B. P. In Cholinesterases: Structure, Function, Mechanism, Genetics, and Cell Biology; Massoulié. J., Bacou, F., Barnard, E., Chatonnet, A., Doctor, B. P., Quinn, D. M., Eds.; American Chemical Society: Washington, DC, 1991; pp 394-398.
15. Sussman, J.; Harel, M.; Silman. I. In Membrane Proteins: Structures, Interactions and Models; Pullman. A., et al., Eds.; Kluwer Academic Publishers: The Netherlands, 1992; pp 161-175.
16. Sussman, J.; Silman, I. Curr. Opin. Struct. Biol. 1992, 2, 721 - 729.
17. Silman, L; Krejci, E.; Duval, N.; Bon, S.; Chanal, P.; Harel, M.; Sussman, J.; Massoulié, J. In Multidisciplinary Approaches to Cholineslerase Functions; Shafferman, A., Velan, B., Eds.; Plenum: New York, 1992; pp 177-183.
18. Harel, M.; Sussman, J. L.; Krejci, E.: Bon, S.; Chanal, P.; Massoulié, J.; Silman, I. Proc. Natl. Acad. Sci. U.S.A. 1992, 89, 10827-10831.
19. Harel, M.; Schalk, L; Ehret-Sabatier, L.; Bouet, F.; Goeldner, M.; Hirth, C.; Axelsen, P. H.; Silman, I.; Sussman, J. L. Proc. Natl. Acad. Sci. U.S.A. 1993, 90, 9031-9035.
20. Weise, C.; Kreienkamp, H. J.; Raba. R.; Pedak, A.; Aaviksaar, A.; Hucho, R EMBO J. 1990, 9, 3385-3388.
21. Shafferman, A.; Kronman, C.; Flashner, Y.; Leitner, M.; Grosfeld, H.; Ordentlich, A.; Gozes, Y.; Cohen, S.; Ariel, N.; Barak, D.; Harel, M.; Silman, L; Sussman, J. L.: Velan, B. J. Biol. Chem. 1992, 267, 17640-17648.
22. Shafferman, A.; Velan, B.; Ordentlich, A.; Kronman, C.; Grosfeld, H.; Leitner, M.; Flashner, Y.; Cohen, S.: Barak, D.; Ariel, N. In Multidisciplinary Approaches to Cholinesterase Functions; Shafferman, A., Velan, B., Eds.; Plenum: New York, 1992; pp 165-175.
23. Radié, Z.; Gibney, G.; Kawamoto, S.; MacPhee-Quigley, K.; Bongiorno, C.; Taylor, P. Biochemistry 1992, 31, 9760-9767.
24. Radié, Z.; Pickering, N. A.; Vellom, D. C.; Camp, S.; Taylor, P. Biochemistry 1993, 32, 12074-12084.
25. Ordentlich, A.; Barak, D.; Kronman, C.; Flashner, Y.; Leitner, M.; Segall, Y.; Ariel, N.; Cohen, S.; Velan, B.; Shafferman, A. J. Biol. Chem. 1993, 268, 17083-17095.
26. Selwood, T.; Feaster, S. R.; States, M. J.; Pryor, A. N.; Quinn, D. M. J. Am. Chem. Soc. 1993, 115, 10477-10482.
27. Massoulié, J.; Pezzementi, L.; Bon, S.; Krejci, E.; Vallette, F.-M. Prog. Neurobiol. 1993, 41, 33-91.
28. Taylor, P.; Radié, Z. Annu. Rev. Pharmacol. ToxicoL 1994, 34, 281 - 320.
29. Pauling, L. Am. Sci. 1948, 36, 51-58.
30. Fersht, A. R. Proc. R. Soc. London. B 1974, 187, 397-407.
31. Schowen, R. L. In Transition States of Biochemical Processes; Candour, R. D., Schowen, R. L., Eds.; Plenum: New York, 1978; pp 77-114.
32. Wolfenden, R. In Transition States of Biochemical Processes; Candour, R. D., Schowen, R. L., Eds.: Plenum: New York, 1978: pp 555-578.
33. Glasstone, S.; Laidler, K. J.; Eyring, H. The Theory of Rate Processes; McGraw-Hill: New York, 1941.
34. -1.
35. Wolfenden, R. Nature 1969, 223, 704-705.
36. Lienhard, G. E. Science 1973, 180, 149-154.
37. Allen, K. N.; Abeles, R. H. Biochemistry 1989, 28, 8466-8473.
38. Brodbeck, U.; Schweikert, K.; Gentinetta, R.: Ronenberg, M. Biochim. Biophys. Acta 1979, 567, 357-369.
39. Dafforn, A.; Neenan, J. P.; Ash, C. E.; Betts, L.; Finke, J. M.; Garman, J. A.; Pao, M.; Walsh, K.; Williams, R. R. Biochem. Biophys. Res. Commun. 1982, 104, 597-602.
40. Gelb, M. H.; Svaren, J. P.; Abeles, R. H. Biochemistry 1985, 24, 1813-1817.
41. Linderman, R. J.; Leazer, J.: Roe, R. M.; Venkatsh, K.: Selinsky, B. S.; London, R. E. Pest. Biochem. Physiol. 1988, 31, 187-194.
42. Nair, H. K.; Lee, K.; Quinn, D. M. J. Am. Chem. Soc. 1993. 115, 9939-9941.
43. Nair, H. K.; Seravalli, J.; Arbuckle, T.: Quinn, D. M. Biochemistry 1994, 33, 8566-8576.
44. Free energy changes were calculated at 298-2 K according to ΔΔG = -RT In(f). where f is a numerical factor, such as the catalytic acceleration effected by AChE or the effect of a particular active site mutant.
45. Schowen, K. B.; Smissman, E. E.; Stephen, W. F., Jr. J. Med. Chem. 1975, 18, 292-300.
46. Smissman, E. E.: Nelson, W. L.: LaPidus, J. B.; Day, J. L. J. Med, Chem. 1966, 9, 458-465.
47. Smissman, E. E.; Parker, G. R. J. Med. Chem. 1973, 16, 23-27.
48. Stephen, W. F.; Smissman, E. E.; Schowen, K. B.; Self, G. W. J. Med. Chem. 1972, 75, 241-243.
49. Sundaralingam, M. Nature 1968, 217, 35-37.
50. Cushley, R. J.; Mautner, H. G. Tetrahedron 1970, 26, 2151-2159.
51. Datta, N.; Mondai, P.; Pauling, P. Acta Crystallogr., Sect. B 1980, 36, 906-909.
52. Partington, P.; Feeney, J.; Burgen, A. S. V. Mol. Pharmacol. 1972, 8, 269-277.
53. Gerlt, J. A.; Gassraan, P. G. Biochemistry 1993, 32, 11943-11952.
54. Henderson, R. J. Mol. Biol 1970, 54, 341-354.
55. Marquart, M.; Walter, J.; Deisenhofer, J.; Bode, W.; Huber, R. Acta Crystallogr., Sect. B 1983, 39, 480-490.
56. Robertus, J. D.; Kraut, J.; Alden, R. A.; Birktoft, J. J. Biochemistry 1972, 11, 4293-4303.
57. Grochulski, P.; Bouthillier, F.; Kazlauskas, R. J.; Serreqi, A. N.; Schrag, J. D.; Ziomek, E.; Cygler, M. Biochemistry 1994, 33, 3494-3500.
58. Brzozowski, A. M.; Derewenda, U.; Derewenda, Z. S.; Dodson, G. G., Lawson, D. M.; Turkenburg, J. P.; Bjorkling, F.; Huge-Jensen, B., Patkar, S. A.; Thim, L. Nature 1991, 351, 491-494.
59. Derewenda, U.; Brzozowski, A. M.; Lawson, D. L.; Derewenda, Z. S. Biochemistry 1992, 31, 1532-1541.
60. Ollis, D. L..; Cheah, E.; Cygler, M.; Dijkstra, B.; Frolow, F.; Franken, S. M.; Harel, M.; Remington, S. J.: Silman, I.; Schrag, J. D.; Sussman, J. L.; Verscheuren, K. H. G.; Goldman, A. Protein Eng. 1992, 5, 197-211.
61. Pryor, A. N.; Selwood, T.; Leu, L.-S.; Andracki, M. A.; Lee, B. H.; Rao, M.; Rosenberry, T.; Doctor, B. P.; Silman, I.; Quitm, D. M. J. Am. Chem. Soc. 1992, 114, 3896-3900.
62. Quinn, D. M.; Swanson, M. L. J. Am, Chem. Soc. 1984, 706, 1883-1884.
63. Rosenberry, T. L. Proc. Natl. Acad. Sci. U.S.A. 1975, 72, 3834-3838.
64. Acheson, S. A.; Barlow, P. N.; Lee, G. C.; Swanson, M. L.; Quinn, D. M. J. Am. Chem. Soc. 1987, 109, 246-252.
65. Acheson, S. A.: Dedopoulou, D.; Quinn, D. M. J. Am. Chem. Soc. 1987, 109, 239-245.
66. Barlow, P. N.; Acheson, S. A.; Swanson, M. L.; Quinn, D. M. J. Am. Chem. Soc. 1987, 109, 253-257.
67. Acheson, S. A.; Quinn, D. M. Biochim. Biophys. Acta 1990, 1040, 199-205.
68. Kovach, I. M.: Larson, M.; Schowen, R. L. J. Am. Chem. Soc. 1986, 108, 3054-3056.
69. Liang, T.-C.; Abeles, R. H. Biochemistry 1987, 26, 7603-7608.
70. Adebodun, F.; Jordan, F. J. Cell Biochem. 1989, 40, 249-260.
71. Carter P.; Wells, J. A. Nature 1988, 332, 564-568.
72. Kim, K. S.; Lee, J. Y.: Lee, S. J.; Ha, T.-K.; Kim, D. H. J. Am, Chem. Soc. 1994, 116, 7399-7400.
73. Dougherty, D. A.; Stauffer, D. A. Science 1990, 250, 1558-1560.
74. Kearney, P. C.; Mizoue, L. S.; Kumpf, R. A.; Forman, J. E.; McCurdy, A.; Dougherty, D. A. J. Am. Chem. Soc. 1993, 115, 9907-9919.
75. Hansch, C.; Leo, A. Substituent Constants for Correlation Analysis in Chemistry and Bialogy; John Wiley & Sons: New York, 1989.
76. Bencsura, A.; Enyedy, I.; Kovach, I. M. Biochemistry 1995, 34, 8989.
77. Bohme, D. K.; Mackay, G. I. J. Am. Chem. Soc. 1981, 103, 978-979.
78. Madura, J. D.: Joreensen, W. L. J. Am. Chem. Soc. 1986, 108, 2517-2527.
79. Baer, S.; Brinkman, E. A.; Brauman, J. I. J. Am. Chem. Soc. 1991, 113, 805-812.
80. Brünger, A. T. X-PLOR Version 3.1, A System for Crystallography and NMK; Yale University Press: New Haven and London, 1992; 3, 1 Manual.
81. Chothia, C.; Pauling, P. Nature 1968, 290, 1156-1157.
82. Bernstein, F. C.; Koetzle, T. F.; Williams, G. J. B.; Meyer, E. F., Jr.; Brice, M. D.; Rodgers, J. R.; Kennard, O.; Shimanouchi, T.; Tasumi, M. J. MoL Biol. 1977, 112, 535-542.