The ω-loop lid domain of phosphoenolpyruvate carboxykinase is essential for catalytic function

Biochemistry

Volumn 51, Issue 47, 2012, Pages 9547-9559

  Johnson, Troy A ^a,c   Holyoak, Todd ^a,b  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WATERLOO   (Canada)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; CATALYTIC CYCLES; CATALYTIC FUNCTIONS; CHEMICAL CONVERSIONS; CONFORMATIONAL EQUILIBRIUM; GLUCONEOGENESIS; GLYCERONEOGENESIS; GLYCINE RESIDUES; KINETIC ACTIVITY; KINETIC ANALYSIS; METABOLIC ENZYMES; MOBILE DOMAINS; MUTANT ENZYMES; PHOSPHOENOLPYRUVATE CARBOXYKINASE; REACTIVE INTERMEDIATE; STRUCTURAL CHARACTERIZATION;

AMINO ACIDS; CATALYSIS; CONFORMATIONS; METABOLISM; REACTION INTERMEDIATES;

ENZYMES;

GLYCINE; PHOSPHOENOLPYRUVATE CARBOXYKINASE (ATP);

ANIMAL TISSUE; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME KINETICS; GLUCONEOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTON TRANSPORT; RAT;

ANIMALS; CATALYSIS; CATALYTIC DOMAIN; CYTOSOL; MODELS, MOLECULAR; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RATS;

EID: 84870165873     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi301278t     Document Type: Article

References (38)

1. Ma, B. and Nussinov, R. (2010) Enzyme dynamics point to stepwise conformational selection in catalysis Curr. Opin. Chem. Biol. 14, 652-659
2. Fetrow, J. (1995) Omega loops: Nonregular secondary structures significant in protein function and stability FASEB J. 9, 708-717
3. Malabanan, M. M., Amyes, T. L., and Richard, J. P. (2010) A role for flexible loops in enzyme catalysis Curr. Opin. Struct. Biol. 20, 702-710
4. Holyoak, T., Sullivan, S. M., and Nowak, T. (2006) Structural Insights into the Mechanism of PEPCK Catalysis Biochemistry 45, 8254-8263
5. Banerjee, S., Pieper, U., Kapadia, G., Pannell, L. K., and Herzberg, O. (1998) Role of the ω-Loop in the Activity, Substrate Specificity, and Structure of Class A β-Lactamase Biochemistry 37, 3286-3296
6. Pompliano, D. L., Peyman, A., and Knowles, J. R. (1990) Stabilization of a reaction intermediate as a catalytic device: Definition of the functional role of the flexible loop in triosephosphate isomerase Biochemistry 29, 3186-3194
7. Kato, H., Tanaka, T., Yamaguchi, H., Hara, T., Nishioka, T., Katsube, Y., and Oda, J.-i. (1994) Flexible Loop That Is Novel Catalytic Machinery in a Ligase. Atomic Structure and Function of the Loopless Glutathione Synthetase Biochemistry 33, 4995-4999
8. Larson, E. M., Larimer, F. W., and Hartman, F. C. (1995) Mechanistic insights provided by deletion of a flexible loop at the active site of ribulose-1,5-bisphosphate carboxylase/oxygenase Biochemistry 34, 4531-4537
9. Sampson, N. S., Kass, I. J., and Ghoshroy, K. B. (1998) Assessment of the Role of an ω Loop of Cholesterol Oxidase: A Truncated Loop Mutant Has Altered Substrate Specificity Biochemistry 37, 5770-5778
10. Kempf, J. G., Jung, J. Y., Ragain, C., Sampson, N. S., and Loria, J. P. (2007) Dynamic requirements for a functional protein hinge J. Mol. Biol. 368, 131-149
11. Sullivan, S. M. and Holyoak, T. (2008) Enzymes with lid-gated active sites must operate by an induced fit mechanism instead of conformational selection Proc. Natl. Acad. Sci. U.S.A. 105, 13829-13834
12. Malabanan, M. M., Amyes, T. L., and Richard, J. P. (2011) Mechanism for Activation of Triosephosphate Isomerase by Phosphite Dianion: The Role of a Ligand-Driven Conformational Change J. Am. Chem. Soc. 133, 16428-16431
13. Sullivan, S. M. and Holyoak, T. (2007) Structures of rat cytosolic PEPCK: Insight into the mechanism of phosphorylation and decarboxylation of oxaloacetic acid Biochemistry 46, 10078-10088
14. Johnson, T. A. and Holyoak, T. (2010) Increasing the conformational entropy of the ω-loop lid domain in phosphoenolpyruvate carboxykinase impairs catalysis and decreases catalytic fidelity Biochemistry 49, 5176-5187
15. McNicholas, S., Potterton, E., Wilson, K. S., and Noble, M. E. M. (2011) Presenting your structures: The CCP4mg molecular-graphics software Acta Crystallogr. D67, 386-394
16. Yang, J., Kalhan, S. C., and Hanson, R. W. (2009) What is the metabolic role of phosphoenolpyruvate carboxykinase? J. Biol. Chem. 284, 27025-27029
17. Colombo, G., Carlson, G. M., and Lardy, H. A. (1981) Phosphoenolpyruvate carboxykinase (guanosine 5′-triphosphate) from rat liver cytosol. Dual-cation requirement for the carboxylation reaction Biochemistry 20, 2749-2757
18. Lee, M. H., Hebda, C. A., and Nowak, T. (1981) The role of cations in avian liver phosphoenolpyruvate carboxykinase catalysis. Activation and regulation J. Biol. Chem. 256, 12793-12801
19. 2+ substrate complexes J. Biol. Chem. 257, 5515-5522
20. Carlson, G. M. and Holyoak, T. (2009) Structural insights into the mechanism of phosphoenolpyruvate carboxykinase catalysis J. Biol. Chem. 284, 27037-27041
21. 2+-oxalate ternary complex of Escherichia coli PEP carboxykinase Nat. Struct. Biol. 3, 355-363
22. Griffith, O. W. and Weinstein, C. L. (1987) β-Sulfopyruvate Methods Enzymol. 143, 221-223
23. Vagin, A. and Teplyakov, A. (1997) MOLREP: An Automated Program for Molecular Replacement J. Appl. Crystallogr. 30, 1022-1025
24. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: Programs for protein crystallography Acta Crystallogr. 50, 760-763
25. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot Acta Crystallogr. D66, 486-501
26. Chen, V. B., Arendall, W. B., III, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: All-atom structure validation for macromolecular crystallography Acta Crystallogr. D66, 12-21
27. Henzler-Wildman, K. A., Thai, V., Lei, M., Ott, M., Wolf-Watz, M., Fenn, T., Pozharski, E., Wilson, M. A., Petsko, G. A., Karplus, M., Hubner, C. G., and Kern, D. (2007) Intrinsic motions along an enzymatic reaction trajectory Nature 450, 838-844
28. Williams, J. C. and McDermott, A. E. (1995) Dynamics of the flexible loop of triosephosphate isomerase: The loop motion is not ligand gated Biochemistry 34, 8309-8319
29. Xiang, J., Jung, J.-y., and Sampson, N. S. (2004) Entropy Effects on Protein Hinges: The Reaction Catalyzed by Triosephosphate Isomerase Biochemistry 43, 11436-11445
30. Johnson, T. A., Qiu, J., Plaut, A. G., and Holyoak, T. (2009) Active-Site Gating Regulates Substrate Selectivity in a Chymotrypsin-like Serine Protease The Structure of Haemophilus influenzae Immunoglobulin A1 Protease J. Mol. Biol. 389, 559-574
31. Sampson, N. S. and Knowles, J. R. (1992) Segmental motion in catalysis: Investigation of a hydrogen bond critical for loop closure in the reaction of triosephosphate isomerase Biochemistry 31, 8488-8494
32. Sampson, N. S. and Knowles, J. R. (1992) Segmental movement: Definition of the structural requirements for loop closure in catalysis by triosephosphate isomerase Biochemistry 31, 8482-8487
33. Desai, B. J., Wood, B. M., Fedorov, A. A., Fedorov, E. V., Goryanova, B., Amyes, T. L., Richard, J. P., Almo, S. C., and Gerlt, J. A. (2012) Conformational Changes in Orotidine 5′-Monophosphate Decarboxylase: A Structure-Based Explanation for How the 5′-Phosphate Group Activates the Enzyme Biochemistry 51, 8665-8678
34. Amyes, T. L., ODonoghue, A. C., and Richard, J. P. (2001) Contribution of phosphate intrinsic binding energy to the enzymatic rate acceleration for triosephosphate isomerase J. Am. Chem. Soc. 123, 11325-11326
35. Stiffin, R., Sullivan, S. M., Carlson, G. M., and Holyoak, T. (2008) Differential inhibition of cytosolic PEPCK by substrate analogues. Kinetic and structural characterization of inhibitor recognition Biochemistry 47, 2099-2109
36. Sullivan, S. M. and Holyoak, T. (2007) Structures of rat cytosolic PEPCK: Insight into the mechanism of phosphorylation and decarboxylation of oxaloacetic acid Biochemistry 46, 10078-10088
37. Pompliano, D. L., Peyman, A., and Knowles, J. R. (1990) Stabilization of a reaction intermediate as a catalytic device: Definition of the functional role of the flexible loop in triosephosphate isomerase Biochemistry 29, 3186-3194
38. Noce, P. S. and Utter, M. F. (1975) Decarboxylation of oxalacetate to pyruvate by purified avian liver phosphoenolpyruvate carboxykinase J. Biol. Chem. 250, 9099-9105