Thermodynamic analysis shows conformational coupling and dynamics confer substrate specificity in fructose-1,6-bisphosphate aldolase

Biochemistry

Volumn 46, Issue 45, 2007, Pages 13010-13018

  Pezza, John A ^a,c   Stopa, Jack D ^a   Brunyak, Elizabeth M ^a   Allen, Karen N ^b   Tolan, Dean R ^a  

^a Boston University   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; CONFORMATIONS; SUBSTRATES; THERMODYNAMIC PROPERTIES;

COUPLING ENERGY; DISTAL SURFACE PATCH (DSP); ENZYME DYNAMICS; ISOZYME SPECIFICITY;

ENZYME KINETICS;

FRUCTOSE BISPHOSPHATE ALDOLASE; ISOENZYME;

ARTICLE; CATALYSIS; ENZYME SPECIFICITY; ENZYME STRUCTURE; MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; THERMODYNAMICS;

FRUCTOSE-BISPHOSPHATE ALDOLASE; ISOENZYMES; KINETICS; MODELS, MOLECULAR; PROTEIN CONFORMATION; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

EID: 36048968561     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700713s     Document Type: Article

References (58)

1. Hammes-Schiffer, S., and Benkovic, S. J. (2006) Relating protein motion to catalysis, Annu. Rev. Biochem. 75, 519-541.
2. Schnell, J. R., Dyson, H. J., and Wright, P. E. (2004) Structure, dynamics, and catalytic function of dihydrofolate reductase, Annu. Rev. Biophys. Biomol. Struct. 33, 119-140.
3. Wand, A. J. (2001) Dynamic activation of protein function: A view emerging from NMR spectroscopy, Nat. Struct. Biol. 8, 926-931.
4. Gunasekaran, K., Ma, B., and Nussinov, R. (2004) Is allostery an intrinsic property of all dynamic proteins, Proteins 57, 433-443.
5. Cooper, A., and Dryden, D. T. (1984) Allostery without conformational change. A plausible model, Eur. Biophys. J. 11, 103-109.
6. Lockless, S. W., and Ranganathan, R. (1999) Evolutionarily conserved pathways of energetic connectivity in protein families, Science 286, 295-299.
7. Labeikovsky, W., Eisenmesser, E. Z., Bosco, D. A., and Kern, D. (2007) Structure and Dynamics of Pin1 During Catalysis by NMR, J. Mol. Biol. 367, 1370-1381.
8. Miller, G. P., and Benkovic, S. J. (1998) Stretching exercises: Flexibility in dihydrofolate reductase catalysis, Chem. Biol. 5, R105-R113.
9. Huang, Z., Wagner, C. R., and Benkovic, S. J. (1994) Nonadditivity of mutational effects at the folate binding site of Escherichia coli dihydrofolate reductase, Biochemistry 33, 11576-11585.
10. Liang, Z. X., Tsigos, I., Lee, T., Bouriotis, V., Resing, K. A., Ahn, N. G., and Klinman, J. P. (2004) Evidence for increased local flexibility in psychrophilic alcohol dehydrogenase relative to its thermophilic homologue, Biochemistry 43, 14676-14683.
11. Liang, Z. X., Lee, T., Resing, K. A., Ahn, N. G., and Klinman, J. P. (2004) Thermal-activated protein mobility and its correlation with catalysis in thermophilic alcohol dehydrogenase, Proc. Natl. Acad. Sci. U.S.A. 101, 9556-9561.
12. Liang, Z. X., and Klinman, J. P. (2004) Structural bases of hydrogen tunneling in enzymes: Progress and puzzles, Curr. Opin. Struct. Biol. 14, 648-655.
13. Tsai, Y. C., and Johnson, K. A. (2006) A new paradigm for DNA polymerase specificity, Biochemistry 45, 9675-9687.
14. Horecker, B. L., Tsolas, O., and Lai, C. Y. (1975) Aldolases, in The Enzymes (Boyer, P. D., Ed.) pp 213-258, Academic Press, New York.
15. Lebherz, H. G., and Rutter, W. J. (1969) Distribution of fructose diphosphate aldolase variants in biological systems, Biochemistry 8, 109-121.
16. Kusakabe, T., Motoki, K., and Hori, K. (1994) Human aldolase C: Characterization of the recombinant enzyme expressed in Escherichia coli, J. Biochem. 115, 1172-1177.
17. Penhoet, E. E., and Rutter, W. J. (1971) Catalytic and immunochemical properties of homomeric and heteromeric combinations of aldolase subunits, J. Biol. Chem. 246, 318-323.
18. Hers, H.-G. (1957) Le Métabolisme du Fructose, Editions Arsica, Brussels.
19. Choi, K. H., Shi, J., Hopkins, C. E., Tolan, D. R., and Allen, K. N. (2001) Snapshots of catalysis: The structure of fructose-1,6-(bis)phosphate aldolase covalently bound to the substrate dihydroxyacetone phosphate, Biochemistry 40, 13868-13875.
20. Rose, I. A., Warms, J. V. B., and Kuo, D. J. (1987) Concentration and partitioning of intermediates in the fructose bisphosphate aldolase reaction. Comparison of the muscle and liver enzymes, J. Biol. Chem. 262, 692-701.
21. Rose, I. A., O'Connell, E. L., and Mehler, A. H. (1965) Mechanism of the aldolase reaction, J. Biol. Chem. 240, 1758-1765.
22. Gamblin, S. J., Davies, G. J., Grimes, J. M., Jackson, R. M., Littlechild, J. A., and Watson, H. C. (1991) Activity and specificity of human aldolases, J. Mol. Biol. 219, 573-576.
23. Dalby, A., Tolan, D. R., and Littlechild, J. A. (2001) Crystal structure of human liver fructose 1,6-bisphosphate aldolase, Acta Crystallogr. D57, 1526-1533.
24. Arakaki, T. L., Pezza, J. A., Cronin, M. A., Hopkins, C. E., Zimmer, D. B., Tolan, D. R., and Allen, K. N. (2004) Structure of human brain fructose 1,6-bisphosphate aldolase: Linking isozyme structure with function, Protein Sci. 13, 3077-3084.
25. Pezza, J. A., Choi, K. H., Berardini, T. Z., Beernink, P. T., Allen, K. N., and Tolan, D. R. (2003) Spatial clustering of isozyme-specific residues reveals unlikely determinants of isozyme specificity in fructose 1,6-bisphosphate aldolase, J. Biol. Chem. 278, 17307-17313.
26. Ackers, G. K., Doyle, M. L., Myers, D., and Daugherty, M. A. (1992) Molecular code for cooperativity in hemoglobin, Science 255, 54-63.
27. Cronin, C. N., and Kirsch, J. F. (1988) Role of arginine-292 in the substrate specificity of aspartate aminotransferase as examined by site-directed mutagenesis, Biochemistry 27, 4572-4579.
28. Ho, S., Hunt, H., Horton, R., Pullen, J., and Pease, L. (1989) Site-directed mutagenesis by overlapping extension using the polymerase chain reaction, Gene 77, 51-59.
29. Morris, A. J., and Tolan, D. R. (1993) Site-directed mutagenesis identifies aspartate 33 as a previously unidentified critical residue in the catalytic mechanism of rabbit aldolase A, J. Biol. Chem. 268, 1095-1100.
30. Beernink, P. T., and Tolan, D. R. (1992) Construction of a high-copy "ATG vector" for expression in Escherichia coli, Protein Expression Purif. 3, 332-336.
31. Hopkins, C. E., O'Conner, P. B., Allen, K. N., Costello, C. E., and Tolan, D. R. (2002) Chemical-modification rescue assessed by mass spectrometry demonstrates γ-thia-lysine yields the same activity as lysine in aldolase, Protein Sci. 11, 1591-1599.
32. Pezza, J. A., Allen, K. N., and Tolan, D. R. (2004) Intein-mediated purification of a recombinantly expressed peptide, Chem. Commun., 2412-2413.
33. Racker, E. (1947) Spectrophotometric measurement of hexokinase and phosphohexokinase activity, J. Biol. Chem. 167, 843-854.
34. Kobashi, K., and Horecker, B. L. (1967) Reversible inactivation of rabbit muscle aldolase by o-phenanthroline, Arch. Biochem. Biophys. 121, 178-186.
35. Connolly, M. L. (1983) Analytical molecular surface calculation, J. Appl. Crystallogr. 16, 548-558.
36. Morris, A. J., and Tolan, D. R. (1994) Lysine-146 of rabbit muscle aldolase is essential for cleavage and condensation of the C3-C4 bond of fructose 1,6-bis(phosphate), Biochemistry 33, 12291-12297.
37. Wilkinson, A. J., Fersht, A. R., Blow, D. M., and Winter, G. (1983) Site-directed mutagenesis as a probe of enzyme structure and catalysis: Tyrosyl-tRNA synthetase cysteine-35 to glycine-35 mutation, Biochemistry 22, 3581-3586.
38. Carter, P. J., Winter, G., Wilkinson, A. J., and Fersht, A. R. (1984) The use of double mutants to detect structural changes in the active site of the tyrosy 1-tRNA synthetase (Bacillus stearothermophilus), Cell 38, 835-840.
39. Ackers, G. K., and Smith, F. R. (1985) Effects of site-specific amino acid modification on protein interactions and biological function, Annu. Rev. Biochem. 54, 597-629.
40. Wells, J. A. (1990) Additivity of mutational effects in proteins, Biochemistry 29, 8509-8517.
41. Sygusch, J., Beaudry, D., and Allaire, M. (1987) Molecular architecture of rabbit skeletal muscle aldolase at 2.7-Å resolution, Proc. Natl. Acad. Sci. U.S.A. 84, 7846-7850.
42. Blom, N., and Sygusch, J. (1997) Product binding and role of the C-terminal region in class I D-fructose 1,6-bisphosphate aldolase, Nat. Struct. Biol. 4, 36-39.
43. St-Jean, M., Lafrance-Vanasse, J., Liotard, B., and Sygusch, J. (2005) High resolution reaction intermediates of rabbit muscle fructose-1,6- bisphosphate aldolase: Substrate cleavage and induced fit, J. Biol. Chem. 280, 27262-27270.
44. Maurady, A., Zdanov, A., de Moissac, D., Beaudry, D., and Sygusch, J. (2002) A conserved glutamate residue exhibits multifunctional catalytic roles in D-fructose-1,6-bisphosphate aldolases, J. Biol. Chem. 277, 9474-9483.
45. Rutter, W. J., Richards, O. C., and Woodfin, B. M. (1961) Comparative studies of liver and muscle aldolase. I. Effect of carboxypeptidase on catalytic activity, J. Biol. Chem. 236, 3193-3197.
46. Dreschler, E. R., Boyer, P. D., and Kowalsky, A. G. (1959) The catalytic activity of carboxypeptidase-degraded aldolase, J. Biol. Chem. 234, 2627-2634.
47. Heyduk, T., Michalczyk, R., and Kochman, M. (1991) Long-range effects and conformational flexibility of aldolase, J. Biol. Chem. 266, 15650-15655.
48. Kay, L. E. (1998) Protein dynamics from NMR, Nat. Struct. Biol. 5 (Suppl.), 513-517.
49. Boehr, D. D., Dyson, H. J., and Wright, P. E. (2006) An NMR perspective on enzyme dynamics, Chem. Rev. 106, 3055-3079.
50. Berthiaume, L., Tolan, D. R., and Sygusch, J. (1993) Differential usage of the carboxyl-terminal region among aldolase isozymes, J. Biol. Chem. 268, 10826-10835.
51. Motoki, K., Kitajima, Y., and Hori, K. (1993) Isozyme-specific modules on human aldolase A molecule: Isozyme group-specific sequences 1 and 4 are required for showing characteristics as aldolase A, J. Biol. Chem. 268, 1677-1683.
52. Kitajima, Y., Takasaki, Y., Takahashi, I., and Hori, K. (1990) Construction and properties of active chimeric enzymes between human aldolases A and B. Analysis of molecular regions which determine isozyme-specific functions, J. Biol. Chem. 265, 17493-17498.
53. Takasaki, Y., Kitajima, Y., Takahashi, I., Sakakibara, M., Mukai, T., and Hori, K. (1990) Structural studies on aldolase isozymes through protein engineering, Prog. Clin. Biol. Res. 344, 935-953.
54. Takasaki, Y., and Hori, K. (1992) Studies on chimeric fusion proteins of human aldolase isozymes A and B, Protein Eng. 5, 101-104.
55. Rajagopalan, P. T., Lutz, S., and Benkovic, S. J. (2002) Coupling interactions of distal residues enhance dihydrofolate reductase catalysis: Mutational effects on hydride transfer rates, Biochemistry 41, 12618-12628.
56. Dalby, A., Dauter, Z., and Littlechild, J. A. (1999) Crystal structure of human muscle aldolase complexed with fructose 1,6-bisphosphate: Mechanistic implications, Protein Sci. 8, 291-297.
57. Choi, K. H., Mazurkie, A. S., Morris, A. J., Utheza, D., Tolan, D. R., and Allen, K. N. (1999) Structure of a fructose-1,6-bis-(phosphate) aldolase liganded to its natural substrate in a cleavage-defective mutant at 2.3 Å, Biochemistry 38, 12655-12664.
58. DeLano, W. L. (2002) PyMOL, version 0.97, DeLano Scientific, San Carlos, CA.