Molecular recognition of aldehydes by aldehyde dehydrogenase and mechanism of nucleophile activation

Proteins: Structure, Function and Genetics

Volumn 57, Issue 4, 2004, Pages 758-771

  Wymore, Troy ^a   Hempel, John ^b   Cho, Samuel S ^c   MacKerell Jr , Alexander D ^c   Nicholas Jr , Hugh B ^a   Deerfield II, David W ^a  

^a PITTSBURGH SUPERCOMPUTING CENTER   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF PHARMACY   (United States)

Author keywords

Aldehydes; Enzyme mechanism; Force field parameterization; General base; Hybrid QM MM potentials; Molecular dynamics simulation; Molecular mechanics; Thiolate

Indexed keywords

ALDEHYDE; ALDEHYDE DEHYDROGENASE; BENZALDEHYDE; CYSTEINE; GLUTAMIC ACID; WATER;

ARTICLE; CALCULATION; CHEMICAL STRUCTURE; COMPLEX FORMATION; CONFORMATION; ENZYME MECHANISM; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; RAT; SIMULATION;

ALDEHYDE DEHYDROGENASE; ALDEHYDES; BENZALDEHYDES; BINDING SITES; COMPUTER SIMULATION; HYDROGEN BONDING; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 10344242388     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/prot.20256     Document Type: Article

References (55)

1. Lindahl R. Aldehyde dehydrogenases and their role in carcinogenesis. Crit Rev Biochem Mol Biol 1992;27:283-335.
2. Sladek NE. Aldehyde dehydrogenase-mediated cellular relative insensitivity to the oxazaphosphorines. Curr Pharm Des 1999;5:607-625.
3. Liu Z, Sun Y, Rose J, Chung Y, Hsiao C, Chang W, Kuo I, Perozich J, Lindahl R, Hempel J, Wang B-C. The first structure of an aldehyde dehydrogenase reveals novel interactions between NAD and the Rossman fold. Nat Struct Biol 1997;4:317-326.
4. Hempel J, Kuo I, Perozich J, Wang B-C, Lindahl R, Nicholas H. ALDH: maintaining critical active site geometry at motif 8 in the class 3 enzyme. Eur J Biochem 2001;268:722-726.
5. Mann CJ, Weiner H. Differences in the roles of conserved glutamic acid residues in the active site of human class 3 and class 2 aldehyde dehydrogenases. Prot Sci 1999;8:1922-1929.
6. DeLaurenzi V, Rogers GR, Hamrock DL, Marekov LN, Steinert PM, Compton JG, Marekova N, Rizzo WB. Sjögren-Larsson syndrome is caused by mutations in the fatty acid aldehyde dehydrogenase gene. Nature Genet 1996;12:52-57.
7. Jones KH, Lindahl R, Baker DC, Timkovich R. Hydride transfer stereospecificity of rat liver aldehyde dehydrogenases. J Biol Chem 1987;262:10911-10913.
8. Hempel J, Perozich J, Chapman T, Rose J, Boesch JS, Liu Z-J, Lindahl R, Wang BC. Aldehyde Dehydrogenase catalytic mechanism: a proposal. In: Weiner H, editor. Enzymology and molecular biology of carbonyl metabolism 7. New York: Plenum Press; 1999. p. 53-59.
9. Hempel J, Nicholas H, Lindahl R. Aldehyde dehydrogenases: widespread structural and functional diversity within a shared framework. Prot Sci 1993;2:1890-1900.
10. Dryjanski M, Kosley LL, Pietruszko R. N-Tosyl-L-phenylalanine chloromethyl ketone, a serine protease inhibitor, identifies glutamate 398 at the coenzyme-binding site of human aldehyde dehydrogenase. Evidence for a second "naked anion" at the active site. Biochemistry 1998;37:14151-14156.
11. MacKerell AD Jr, MacWright RS, Pietruszko R. Bromoacetophenone as an affinity reagent for human liver aldehyde dehydrogenase. Biochemistry 1986;25:5182-5189.
12. Abriola DP, Fields R, Stein S, MacKerell AD Jr, Pietruszko R. Active site of human liver aldehyde dehydrogenase. Biochemistry 1987;26:5679-5684.
13. Wang, X, Weiner H. Involvement of glutamate 268 in the active site of human liver mitochondrial (class 2) aldehyde dehydrogenase as probed by site-directed mutagenesis. Biochemistry 1995;34:237-243.
14. Ni L, Sheikh S, Weiner H. Involvement of Glutamate 399 and Lysine 192 in the mechanism of human liver mitochondrial aldehyde dehydrogenase. J Biol Chem 1997;272:18823-18826.
15. Perozich J, Nicholas H, Wang B, Lindahl R, Hempel J. Relationships within the aldehyde dehydrogenase extended family. Prot Sci 1999;8:137-146.
16. Yang A, Gunner M, Sampogna R, Sharp K, Honig B. On the calculation of pKas in proteins. Proteins 1993;15:252-265.
17. Feig M, Onufriev A, Lee MS, Im W, Case DA, Brooks III CL. Performance comparison of generalized born and poisson methods in the calculation of electrostatic solvation energies for protein structures. J Comp Chem 2004;25:265-284.
18. Burgi HB, Dunitz JD, Shelter EJ. Geometrical reaction coordinates. II. Nucleophilic addition to a carbonyl group. J Am Chem Soc 1973;95:5065-5067.
19. Burgi HB, Dunitz JD, Shefter E. Chemical reaction paths. IV. Aspects of O-C=O interactions in crystals. Acta Cryst B 1974;30:1517-1527.
20. Chakrabarti P, Pal D. An electrophile-nucleophile interaction in metalloprotein structures. Prot Sci 1997;6:851-859.
21. Bruice TC, Benkovic SJ. Chemical basis for enzyme catalyis. Biochemistry 2000;39:6267-6274.
22. Shurki A, Štrajbl M , Villá J, Warshel A. How much do enzymes really gain by restraining their reacting fragments? J Am Chem Soc 2002;124:4097-4107.
23. Štrajbl M, Shurki A, Kato M, Warshel A. Apparent NAC effect in chorismate mutase reflects electrostatic transition state stabilization. J Am Chem Soc 2003;125;10228-10237.
24. Warshel A, Levitt M. Theoretical studies of enzymic reactions: dielectric, electrostatic and steric stabilization of the carbonium ion in the reaction of lysozyme. J Mol Biol 1976;103:227-249.
25. Field MJ. Simulating enzyme reactions: challenges and perspectives. J Comput Chem 2002;23:48-58.
26. Gao J, Truhlar DG. Quantum mechanical methods for enzyme kinetics. Annu Rev Phys Chem 2002;53:467-505.
27. Warshel A. Computer simulations of enzyme catalysis:methods, progress, and insights. Ann Rev Biophys Biomol Struct 2003;32:425-443.
28. MacKerell, AD Jr, Banavali NB, Foloppe N. Development and current status of the CHARMM force field for nucleic acids. Biopolymers 2001;56:257-265.
29. MacKerell AD Jr, Bashford D, Bellott M, Dunbrack Jr. RL, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S, Joseph-McCarthy D, Kuchnir L, Kuczera K, Lau FTK, Mattos C, Michnick S, Ngo T, Nguyen DT, Prodhom B, Reiher III WE, Roux B, Schlenkrich M, Smith JC, State R, Straub J, Watanabe M, Wiorkiewicz-Kuczera J, Yin D, Karplus M. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 1998;102:3586-3616.
30. Foloppe N, MacKerell AD Jr. All-atom empirical force field for nucleic acids: 1. Parameter optimization based on small molecule and condensed phase macromolecular target data. J Comp Chem 2000;21:86-104.
31. Feller SE, MacKerell AD Jr. An improved empirical potential energy function for molecular simulations of phospholipids. J Phys Chem B 2000;104:7510-7515.
32. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. The Protein Data Bank. Nucleic Acids Res 2000;28:235-242.
33. Brooks BR, Bruccoleri RE, Olafson BD, States DJ, Swaminathan S, Karplus M. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J Comput Chem 1983;4:187-217.
34. Pavelites JJ, Bash PA, Gao J, MacKerell AD Jr. Molecular mechanics force field for NAD+, NADH, and the pyrophosphate groups of nucleotides. J Comp Chem 1997;18:221-239.
35. Brunger AT, Karplus M. Polar hydrogen positions in proteins: empirical energy placement and neutron diffraction comparison. Proteins 1988;4:148-156.
36. Ryckaert J-P, Cicotti G, Berendsen HJC. Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys 1977;23:327-341.
37. Darden T, York D, Pedersen L. Particle mesh ewald: an N × log(N) method for ewald sums in large systems. J Chem Phys 1993;98:10089-10092.
38. Perez-Miller SJ, Hurley TD. Coenzyme isomerization is integral to catalysis in aldehyde dehydeogenase. Biochemistry 2003;42:7100-7109.
39. Cobessi D, Tete-Favier F, Marchal S, Branlant G, Aubry A. Structural and biochemical investigations of the catalytic mechanism of an NADP-dependent aldehyde dehydrogenase from streptococcus mutans. J Mol Biol 2000;300:141-152.
40. Reddy SY, Kahn K, Zheng Y, Bruice TC. Protein engineering of nitrile hydratase activity of papain: molecular dynamics study of a mutant and wild-type enzyme. J Am Chem Soc 2002;124:12979-12990.
41. Swanson JMJ, Henchman RH, McCammon JA. Revisiting free energy calculations: a theoretical connection to MM/PBSA and direct calculation of the association free energy. Biophys J 2004;86:67-74.
42. Field MJ, Albe M, Bret C, Proust-De Martin F, Thomas A. The DYNAMO library for molecular simulations using hybrid quantum mechanical and molecular mechanical potentials. J Comput Chem 2000;21:1088-1100
43. Jorgensen WL, Maxwell DS, Tirado-Rives J. Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J Am Chem Soc 1996;118:11225-11236.
44. Stewart JJP. Optimization of parameters for semiempirical methods. I. Methods. J Comp Chem 1989;10:209-220.
45. Gonzalez-Lafront A, Truong TN, Truhlar DG. Direct dynamics calculations with neglect of diatomic differential overlap molecular orbital theory with specific reaction parameters. J Phys Chem 1991;95:4618-4627.
46. Repasky MP, Chandrasekhar J, Jorgensen WL. PDDG/PM3 and PDDG/MNDO: improved semiemperical methods. J Comput Chem 2002;23:1601-1622.
47. Karplus M. Aspects of protein reaction dynamics: deviations from simple behavior. J Phys Chem B 2000;104:11-27.
48. Kumar S, Bouzida D, Swendsen RH, Kollman PA, Rosenberg JM. The weighted histogram analysis method for free energy calculations on biomolecules. I. The method. J Comp Chem 1992;13:1011-1021.
49. PSI-Plot, Version 7.0. New York: Poly Software International; 2002.
50. Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamics. J Mol Graph 1996;14:33-38.
51. Wymore T, Deerfield II DW, Field MJ, Nicholas HB, Hempel J. Initial events in class 3 aldehyde dehydrogenase: MM and QM/MM simulations. Chem Biol Int 2003;143-144:75-84.
52. Kraut DA, Carroll KS, Herschlag D. Challenges in enzyme mechanism and energetics. Ann Rev Biochem 2003;72:517-571.
53. Pliego Jr. J, Riveros JM. Gibbs energy of solvation of organic ions in aqueous and dimethyl sulfoxide solutions. Phys Chem Chem Phys 2002;4:1622-1627.
54. Olsson MHM, Hong G, Warshel A. Frozen density functional free energy simulations of redox proteins: computational studies of the reduction potential of plastocyanin and rusticyanin. J Am Chem Soc 2003;125:5025-5039.
55. Štrajbl M, Florian J, Warshel A. Ab initio evaluation of the free energy surfaces for the general base/acid catalyzed thiolysis of formamide and the hydrolysis of methyl thiolformate: a reference solution reaction for studies of cysteine proteases. J Phys Chem B 2001;105:4471-4484.