Intermediate trapping and Laue X-ray diffraction: Potential for enzyme mechanism, dynamics, and inhibitor screening

Pharmacology and Therapeutics

Volumn 70, Issue 3, 1996, Pages 215-256

  Stoddard, Barry L ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

Author keywords

crystallography; enzyme mechanism; inhibitor screening; intermediates; Laue diffraction

Indexed keywords

ENZYME INHIBITOR; FLUOROURACIL;

CATALYSIS; CRYSTALLIZATION; DRUG DESIGN; DRUG DEVELOPMENT; DRUG STRUCTURE; DRUG TARGETING; ENZYME ACTIVITY; PRIORITY JOURNAL; REVIEW; THEORETICAL STUDY; X RAY DIFFRACTION;

EID: 0029777433     PISSN: 01637258     EISSN: None     Source Type: Journal    
DOI: 10.1016/0163-7258(96)00058-7     Document Type: Review

References (95)

1. Alber, T., Petsko, G. A. and Tsernoglou, D. (1976) Crystal structure of elastase-substrate complex at -55°C. Nature 263: 297-300.
2. Appelt, K., Bacquet, R. J., Barlett, C. A., Booth, C. L. J., Freer, S. T., Fuhry, M. A., Gehring, M. R., Herrmann, S. M., Howland, E. F., Janson, C. A., Jones, T. R., Kan, C-C., Kathardekar, V., Lewis, K. K., Marzoni, G. P., Matthews, D. A., Mohr, C., Moomaw, E. W., Morse, C. A., Oatley, S. J., Ogden, R. C., Reddy, M. R., Reich, S. H., Schoettlin, W. S., Smith, W. W., Varney, M. D., Villafranca, J. E., Ward, R. W., Webber, S., Webber, S. E., Welsh, K. M. and White, J. (1991) Design of enzyme inhibitors using iterative protein crystallographic analysis. J. Med. Chem. 34: 1925-1934.
3. Bennett, W. S., Jr. and Steitz, T. A. (1980) Structure of a complex between yeast hexokinase A and glucose. J. Mol. Biol. 140: 211-230.
4. Bolduc, J., Dyer, D., Lee, M., Scott, W. G., Singer, P., Sweet, R. M., Koshland, D. E., Jr. and Stoddard, B. L. (1995) Mutagenesis and laue structures of enzyme intermediates: isocitrate dehydrogenase. Science 268: 1312-1318.
5. Brubaker, M. J., Dyer, D. H., Stoddard, B. L. and Koshland, D. E., Jr. (1996) Synthesis, kinetics, and structural studies of a photolabile caged isocitrate: a catalytic trigger for isocitrate dehydrogenase. Biochemistry, in press.
6. Campbell, J. W., Habash, J., Helliwell, J. R. and Moffat, K. (1986) Laue diffraction. Inf. Q. Protein Cryst., Daresbury Lab 18: 23-31.
7. Campbell, J. W., Clifton, I. J., Greenhough, T. J., Hajdu, J., Harrison, S. C., Liddington, R. C. and Shrive, A. K. (1990) Calcium binding sites in tomato bushy stunt virus visualized by Laue crystallography. J. Mol. Biol. 214: 627-632.
8. Chen, C. C. H. and Herzberg, O. (1992) Inhibition of b-lactamase by clavulanate: trapped intermediates in cryocrystallographic studies. J. Mol. Biol. 224: 1103-1113.
9. Cherfils, J., Duquerroy, S. and Janin, J. (1991) Protein-protein recognition analyzed by docking simulation. Proteins Struc. Funct. Genet. 11: 271-280.
10. Christianson, D. W. and Lipscomb, W. N (1986) X-ray crystallographic investigation of substrate binding to carboxypeptidase A at subzero temperature. Proc. Natl. Acad. Sci. USA 83: 7568-7572.
11. Cleland, W. C. (1979) Statistical analysis of enzyme kinetic data. Methods Enzymol. 63: 103-138.
12. Corrie, J. E. T., Katayama, Y., Reid, G. P., Anson, M. and Trentham, D. R. (1992) The development and application of photosensitive caged compounds to aid time-resolved structure determination of macromolecules. In: Time-Resolved Macromolecular Crystallography, pp. 65-76, Cruickshank, D. W. J., Helliwell, J. R. and Johnson, L. N. (eds.) Oxford University Press Inc., New York and Oxford.
13. Cruikshank, D. W. J., Helliwell, J. R. and Moffat, K. (1987) Multiplicity distribution of reflections in Laue diffraction. Acta Crystallogr. A 43: 656-674.
14. Cruickshank, D. W. J., Helliwell, J. R. and Moffat, K. (1991) Angular distribution of reflections in Laue diffraction. Acta Crystallogr. A 47: 352-373.
15. Ding, X., Rasmussen, B. F., Petsko, G. A. and Ringe, D. (1994) Direct structural observation of an acyl-enzyme intermediate in the hydrolysis of an ester substrate by elastase. Biochemistry 33: 9285-9293.
16. Duke, E. M. H., Wakatsuki, S., Hadfield, A. and Johnson, L. N. (1994) Laue and monochromatic diffraction studies on catalysis in phosphorylase b crystals. Protein Sci. 3: 1178-1196.
17. Farber, G. K. (1995) It's show time. Curr. Biol. 5: 1088-1090.
18. Farber, G. K., Machin, P. A., Almo, S. C., Petsko, G. A. and Hajdu, J. (1988) X-ray laue diffraction from crystals of xylose isomerase. Proc. Natl. Acad. Sci. USA 85: 112-115.
19. Fauman, E. B., Rutenber, E. E., Maley, G. F., Maley, F. and Stroud, R. M. (1994) Water-mediated substrate/product discrimination: the product complex of thymidylate synthase at 1.83 Å. Biochemistry 33: 1502-1511.
20. Ferre-D'Amare, A. and Burley, S. K. (1994) Use of dynamic light scattering to assess crystallizability of macromolecules and macromolecular assemblies. Structure 2: 357-359.
21. Finer-Moore, J., Fauman, E. B., Foster, P. G., Perry, K. M., Santi, D. V. and Stroud, R. M. (1993) Refined structures of substrate-bound and phosphate-bound thymidylate synthase from Lactobacillus casei. J. Mol. Biol. 232: 1101-1116.
22. Fink, A. L. and Petsko, G. A. (1981) X-ray cryoenzymology. Adv. Enzymol. 52: 177-246.
23. Fleischer, M. (1993) Antifolate analogs: mechanism of action, analytical methodology, and clinical efficacy. Then Drug Monit. 15: 521-526.
24. Fletterick, R. J., Bates, D. J. and Steitz, T. A. (1975) The structure of a yeast hexokinase monomer and its complexes with substrates at 2.7 Å resolution. Proc. Natl. Acad. Sci. USA 72: 38-42.
25. Friedrich, W., Knipping, P. and Laue, M. (1912) Interferenzerscheinungen bei Rontgenstrahlen. Proc. Acad. Bavarian Sci.: 303-322.
26. Fulop, V., Phizackerley, R. P., Soltis, S. M., Clifton, I. J., Wakatsuki, S., Erman, J., Hajdu, J. and Edwards, S. L. (1994) Laue diffraction study on the structure of cytochrome c peroxidase compound I. Structure 2: 201-208.
27. Gerstein, M., Lesk, A. M. and Chothia, C. (1994) Structural mechanisms for domain movements in proteins. Biochemistry 33: 6739-6749.
28. Goodford, P. J. (1985) A computational procedure for determining energetically favorable binding sites on biologically important macromolecuies. J. Med. Chem. 28: 849-857.
29. Goodsell, D. and Dickerson, R. E. (1986) Isohelical analysis of DNA groove-binding drugs. J. Med. Chem. 29: 727-733.
30. Goodsell, D. S. and Olson, A. J. (1990) Automated docking of substrates to proteins by simulated annealing. Proteins Struc. Funct. Genet. 8: 195-202.
31. Grissom, C. B. and Cleland, W. W. (1988) Isotope effect studies of the chemical mechanism of pig heart NADP isocitrate dehydrogenase. Biochemistry 27: 2934-2943.
32. Hadfield, A. and Hajdu, J. (1993) A fast and portable microspectrophotometer for protein crystallography. J. Appl. Crystallogr. 26: 839-842.
33. Hajdu, J. and Johnson, L. N. (1990) Progress with Laue diffraction studies on protein and virus crystals. Biochemistry 29: 1669-1678.
34. Hajdu, J., Acharya, K. R., Stuart, D. I., McLaughlin, P. J., Barford, D., Klein, H. and Johnson, L. N. (1986) Time-resolved structural studies on catalysis in the crystal with glycogen phosphorylase. Biochem. Soc. Trans. 14: 538-541.
35. Hajdu, J., Acharya, K. R., Stuart, D. I., McLaughlin, P. J., Barford, D., Klein, H., Oikonomakos, N. G. and Johnson, L. N. (1987a) Catalysis in the crystal: synchrotron radiation studies with glycogen phosphorylase b. EMBO J. 6: 539-546.
36. Hajdu, J., Machin, P. A., Campbell, J. W., Greenhough, T. J., Clifton, I. J., Zurek, S., Cover, S., Johnson, L. N. and Elder, M. (1987b) Millisecond x-ray diffraction and the first electron density map from Laue photographs of a protein crystal. Nature 329: 115-116.
37. Hajdu, J., Almo, S. C., Farber, G. K., Prater, J. K., Petsko, G. A., Wakatsuki, S., Clifton, I. J. and Fulop, V. (1991) On the limitations of the laue method when applied to crystals of macromolecules. In: Crystallographic Computing 5, pp. 29-49, Moras, D., Podjarny, A. D. and Thierry, J. C. (eds.) Oxford University Press, New York.
38. Hardy, L. W., Finer-Moore, J. S., Montfort, W. R., Jones, M. O., Santi, D. V. and Stroud, R. M. (1987) Atomic structure of thymidylate synthase: target for rational drug design. Science 235: 448-455.
39. Hedman, B., Hodgson, K., Helliwell, J. R., Liddington, R. C. and Papiz, M. Z. (1985) Protein microcrystal diffraction and the effects of radiation damage with ultra-high flux synchrotron radiation. Proc. Natl. Acad. Sci. USA 82: 7604-7606.
40. Helliwell, J. R. (1984) Synchrotron x-radiation protein crystallography-instrumentation, methods, and applications. Rep. Prog. Phys. 47: 1403-1497.
41. Helliwell, J. R. (1985) Protein crystallography with synchrotron radiation. J. Mol. Struct. 130: 63-91.
42. Helliwell, J. R. (1992) Macromolecular Crystallography With Synchrotron Radiation. Cambridge University Press, Inc., New York and Cambridge.
43. Helliwell, J. R., Habash, J., Cruickshank, D. W. J., Harding, M. M., Greenhough, T. J., Campbell, J. W., Clifton, I. J., Elder, M., Machin, P. A., Papiz, M. Z. and Zurek, S. (1989) The recording and analysis of synchrotron x-radiation Laue diffraction photographs. J. Appl. Crystallogr. 22: 483-497.
44. Howell, P. L., Warren, C., Amatayakul-Chantler, S., Petsko, G. A. and Hajdu, J. (1992) Activity of crystalline turkey egg white lysozyme. Proteins Struc. Funct. Genet. 12: 91-99.
45. Hurley, J. H., Thorsness, P. E., Ramalingam, V., Helmers, N. H., Koshland, D. E., Jr. and Stroud, R. M. (1989) Structure of a bacterial enzyme regulated by phosphorylation, isocitrate dehydrogenase. Proc. Natl. Acad. Sci. USA 86: 8635-8639.
46. Hurley, J. H., Dean, A. M., Sohl, J. L., Koshland, D. E., Jr. and Stroud, R. M. (1990a) Regulation of an enzyme by phosphorylation at the active site. Science 249: 1012-1016.
47. Hurley, J. H., Dean, A. M., Thorsness, P. E., Koshland, D. E., Jr. and Stroud, R. M. (1990b) Regulation of isocitrate dehydrogenase by phosphorylation involves no long-range conformational change in the free enzyme. J. Biol. Chem. 265: 3599-3602.
48. Hurley, J. H., Dean, A. M., Koshland, D. E., Jr. and Stroud, R. M. (1991) Catalytic mechanism of NADP-dependent isocitrate dehydrogenase: implications from the structures of magnesium-isocitrate and NADP complexes. Biochemistry 30: 8671-8678.
49. Joseph, D., Petsko, G. A. and Karplus, M. (1990) Anatomy of a conformational change: hinged 'Lid' motion of the triosephosphate isomerase loop. Science 249: 1425-1428.
50. Kalman, Z. H. (1979) Derivation of integrated reflected energy formulas. Acta Crystallogr. A 35: 634-641.
51. Kamb, A., Finer-Moore, J. S. and Stroud, R. M. (1992) Cofactor triggers the conformational change in thymidylate synthase: implications for an ordered binding mechanism. Biochemistry 31: 12876-12884.
52. Kirkpatrick, S., Gelatt, C. D., Jr. and Vecchi, M. P. (1983) Optimization by simulated annealing. Science 220: 671-680.
53. Kuntz, I. D. (1992) Structure-based strategies for drug design and discovery. Science 257: 1078-1082.
54. Kuntz, I. D., Blaney, J. M., Oatley, S. J., Langridge, R. and Ferrin, T. E. (1982) A geometric approach to macromolecule-ligand interactions. J. Biol. Chem. 161: 269-288.
55. Laskowski, R. A., MacArthur, M. W., Moss, D. S. and Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 26: 283-291.
56. Laue, M. (1912) Eine quantitative prufung der theorie fur the interferenzerscheinungen bei Rontgenstrahlen. Proc. Acad. Bavarian Sci. 363-373.
57. Lolis, E., Alber, T., Davenport, R. C., Rose, D., Hartman, F. C. and Petsko, G. A. (1990) Structure of yeast triosephosphate isomerase at 1.9-Å resolution. Biochemistry 29: 6609-6618.
58. Makinen, M. W. and Fink, A. L. (1977) Reactivity and cryoenzymology of enzymes in the crystalline state. Annu. Rev. Biophys. Bioeng. 6: 301-343.
59. Margaritondo, G. (1988) Introduction to Synchrotron Radiation. Oxford University Press, Inc., New York and Oxford.
60. Matthews, B.W. (1968) Solvent content of protein crystals. J. Mol. Biol. 33: 491-497.
61. Matthews, D. A., Appelt, K., Oatley, S. J. and Xuong, N. H. (1990a) Crystal structure of Escherichia coli thymidylate synthase containing bound 5-fluoro-2′-deoxyuridylate and 10-propargyl-5,8-dideazafolate. J. Mol. Biol. 214: 923-936.
62. Matthews, D. A., Villafranca, J. E., Janson, C. A., Smith, W. W., Welsh, K. and Freer, S. (1990b) Stereochemical mechanism of action for thymidylate synthase based on the x-ray structure of the covalent inhibitor ternary complex with 5-fluoro-2′-deoxyuridylate and 5,10-methylenetetrahydrofolate. J. Mol. Biol. 214: 937-948.
63. Meng, E. C., Shoichet, B. K. and Kuntz, I. D. (1992) Automated docking with grid-based energy evaluation. J. Comp. Chem. 13: 505-512.
64. Moffat, K. (1989) Time-resolved macromolecular crystallography. Annu. Rev. Biophys. Biophys. Chem. 18: 309-332.
65. Moffat, K., Szebenyi, D. M. E. and Bilderback, D. H. (1984) X-ray laue diffraction from protein crystals. Science 223: 1423-1425.
66. Moffat, K., Bilderback, D., Schildkamp, W. and Volz, K. (1986) Laue diffraction from biological samples. Nucl. Instrum. Methods A246: 627-635.
67. Montfort, W. R., Perry, K. M., Fauman, E. B., Finer-Moore, J. S., Maley, G. F., Hardy, L., Maley, F. and Stroud, R. M. (1990) Structure, multiple site binding, and segmental accommodation in thymidylate synthase on binding dUMP and an anti-folate. Biochemistry 29: 6964-6977.
68. Morris, S. M. (1993) The genetic toxicology of 5-fluoropyrimidines and 5-chlorouracil. Mutat. Res. 297: 39-51.
69. O' Hara, P., Goodwin, P. and Stoddard, B. L. (1995) Direct measurement of diffusion rates in enzyme crystals by video absorbance spectroscopy. J. Appl. Crystallogr. 28: 829-833.
70. Perry, K. M., Fauman, E. B., Finer-Moore, J. S., Montfort, W. R., Maley, G. F., Maley, F. and Stroud, R. M. (1990) Plastic adaptation toward mutations in proteins: structural comparison of thymidylate synthases. Proteins 8: 315-333.
71. Rasmussen, B. F., Stock, A. M., Ringe, D. and Petsko, G. A. (1992) Crystalline ribonuclease A loses function below the dynamic transition at 220K. Nature 357: 423-426.
72. Reynolds, C. D., Stowell, B., Joshi, K. K., Harding, M. M., Maginn, S. J. and Dodson, G. G. (1988) Preliminary study of a phasetransformation in insulin crystals using synchrotron radiation Laue diffraction. Acta Crystallogr. B 44: 512-515.
73. Rodgers, D. W. (1994) Cryocrystallography. Structure 2: 1135-1140.
74. Röntgen, W. C. (1898) Abdruck der 1. und 2. Originalmitteilung von 1895, uber eine neue art von strahlen, und der 3. Mitteilung von 1897, weitere beobachtungen uber die eigenschaften der x-strahlen. Ann. Phys. Chem. 64: 1-37.
75. Schlichting, I., Rapp, G., John, J., Wittinghofer, A., Pai, E. F. and Goody, R. S. (1989) Biochemical and crystallogaphic characterization of a complex of c-Ha-ras p21 and caged GTP with flash photolysis. Proc. Natl. Acad. Sci. USA 86: 7687-7690.
76. Schlichting, I., Almo, S. C., Rapp, G., Wilson, K., Petratos, K., Lentfer, A., Wittinghofer, A., Kabsch, W., Pai, E. F., Petsko, G. A. and Goody, R. S. (1990) Time-resolved x-ray crystallographic study of the conformational change in Ha-Ras p21 protein on GTP hydrolysis. Nature 345: 309-315.
77. Schlichting, I., Berendzen, J., Phillips, G. N., Jr. and Sweet, R. M. (1994) Crystal structure of photolyzed carbonmonoxymyoglobin. Nature 371: 808-812.
78. Shoichet, B. K. and Kuntz, I. D. (1991) Protein docking and complementarity. J. Mol. Biol. 221: 327-346.
79. Shoichet, B. K., Stroud, R. M., Santi, D. V., Kuntz, I. D. and Perry, K. M. (1993) Structure-based discovery of inhibitors of thymidylate synthase. Science 259: 1445-1450.
80. Singer, P., Smalas, A., Carty, R. P., Mangel, W. F. and Sweet, R. M. (1992) The hydrolytic water molecule in trypsin, revealed by time-resolved Laue crystallography. Science 259: 669-673.
81. Stoddard, B. L. and Farber, G. K. (1995) Direct measurement of reactivity in the protein crystal by steady-state kinetic studies. Structure 3: 991-996.
82. Stoddard, B. L. and Koshland, D. E., Jr. (1992) Prediction of the structure of a receptor-protein complex using a binary docking method. Nature 358: 774-776.
83. Stoddard, B., Bruhnke, J., Koenigs, P., Porter, N., Ringe, D. and Petsko, G. (1990a) Photolysis and deacylation of inhibited chymotrypsin. Biochemistry 29: 8042-8051.
84. Stoddard, B., Bruhnke, J., Porter, N., Ringe, D. and Petsko, G. (1990b) Structure and activity of two photoreversible cinnamates bound to chymotrypsin. Biochemistry 29: 4871-4879.
85. Stoddard, B. L., Koenigs, P., Porter, N., Petratos, K., Petsko, G. A. and Ringe, D. (1991) Observation of the light-triggered binding of pyrone to chymotrypsin by Laue x-ray crystallography. Proc. Natl. Acad. Sci. USA 88: 5503-5507.
86. Szebenyi, D. M. E., Bilderback, D. H., LeGrand, A., Moffat, K., Schildkamp, W., Temple, B. S. and Teng, T.-Y. (1988) Quantitative analysis of Laue diffraction patterns recorded with a 120 picosecond exposure from an x-ray undulator. Trans. Am. Crystallogr. Assoc. 24: 167-172.
87. Teng, T.-Y., Srajer, V. and Moffat, K. (1994) Photolysis-induced structural changes in single crystals of carbonmonoxymyoglobin at 40K. Nature Struct. Biol. 1: 701-705.
88. Tilton, R. F., Jr., Dewan, J. C. and Petsko, G. A. (1992) Effects of temperature on protein structure and dynamics: x-ray crystallographic studies of the protein ribonuclease A at nine different temperatures from 98 to 320°K. Biochemistry 31: 2469-2481.
89. Varney, M. D., Marzoni, G. P., Palmer, C. L., Deal, J. G., Webber, S., Welsh, K. M., Bacquet, R. J., Bartlett, C. A., Morse, C. A., Booth, C. L. J., Herrmann, S. M., Howland, E. F., Ward, R. W. and White, J. (1992) Crystal-structure-based design and synthesis of benz-[cd]indole-containing inhibitors of thymidylate synthase. J. Med. Chem. 35: 663-676.
90. Weichsel, A. and Montfort, W. R. (1995) Ligand-induced distortion of an active site in thymidylate synthase upon binding anticancer drug 1843U89. Nature Struct. Biol. 2: 1095-1101.
91. Wodak, S. J. and Janin, J. (1978) Computer analysis of protein-protein interaction. J. Mol. Biol. 124: 323-342.
92. Wyckoff, H. and Richards, F. M. (1967) Design of a diffractometer and flow cell system for x-ray analysis of crystalline proteins with applications to the crystal chemistry of ribonuclease S. J. Mol. Biol. 27: 563-578.
93. Wyckoff, H. W., Doscher, M., Tsernoglou, D., Inagami, T., Johnson, L. N., Hardman, K. D., Allewell, N. M., Kelly, D. M. and Richards, F. M. (1967) Design of a diffractometer and flow cell system for X-ray analysis of crystalline proteins with applications to the crystal chemistry of ribonuclease-S. J. Mol. Biol. 27: 563-578.
94. Yennewar, N. H., Yennawar, H. P. and Farber, G. K. (1994) X-ray crystal structure of γ-chymotrypsin in hexane. Biochemistry 33: 7326-7336.
95. Yennewar, H. P., Yennawar, N. H. and Farber, G. K. (1995) A structural explanation for enzyme memory in nonaqueous solvents. J. Am. Chem. Soc. 117: 577-585.