Crystal structures of Acetobacter aceti succinyl-coenzyme A (CoA):Acetate CoA-transferase reveal specificity determinants and illustrate the mechanism used by class i CoA-transferases

Biochemistry

Volumn 51, Issue 42, 2012, Pages 8422-8434

  Mullins, Elwood A ^a,b   Kappock, T Joseph ^a  

^a PURDUE UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETOBACTER ACETI; ACETYL-COA; ACYL TRANSFER; ACYL-COA; CLASS I; COA THIOESTER; COENZYME A; ENZYME REACTION; KEY RESIDUES; MECHANISTIC STUDIES; MICHAELIS COMPLEX; OXYANION HOLE; RATE LIMITING; SEQUENCE CONSERVATION; SUBSTRATE RECOGNITION; THIOESTERS; TRANSTHIOESTERIFICATION; WILD TYPES; X RAY CRYSTAL STRUCTURES;

ACETIC ACID; ACETOBACTER; ACID RESISTANCE; AMINO ACIDS; BINDING ENERGY; CARBOXYLATION; CITRIC ACID; ENZYMES; VOLATILE FATTY ACIDS;

SUBSTRATES;

3 OXOACID COENZYME A TRANSFERASE; ACETIC ACID; ACETOACETIC ACID; CARBOXYLIC ACID; DEXTRO LEVO METHYLSUCCINATE; FORMIC ACID; FUMARIC ACID; GLUTARIC ACID; MALIC ACID; OXALOACETIC ACID; PROPIONIC ACID; SUCCINIC ACID; UNCLASSIFIED DRUG;

ACETOBACTER ACETI; ACETOBACTERACEAE; ARTICLE; CRYSTAL STRUCTURE; ENZYME ANALYSIS; ENZYME STRUCTURE; ENZYME SUBSTRATE; EXPRESSION VECTOR; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MICHAELIS CONSTANT; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN CONFORMATION; STEADY STATE; X RAY CRYSTALLOGRAPHY;

ACETOBACTER; ACYL COENZYME A; COENZYME A-TRANSFERASES; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR;

EID: 84867801967     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300957f     Document Type: Article

References (82)

1. Jencks, W. P. (1973) In The Enzymes (Boyer, P. D., Ed.) Vol. 9, Chapter 11, pp 483-496, Academic Press, San Diego.
2. Hersh, L. B. and Jencks, W. P. (1967) Coenzyme A transferase. Kinetics and exchange reactions J. Biol. Chem. 242, 3468-3480
3. Hersh, L. B. and Jencks, W. P. (1967) Coenzyme A transferase. Isolation and properties of an enzyme-coenzyme A intermediate J. Biol. Chem. 242, 3481-3486
4. Hersh, L. B. and Jencks, W. P. (1967) Isolation of an enzyme-coenzyme A intermediate from succinyl coenzyme A-acetoacetate coenzyme A transferase J. Biol. Chem. 242, 339-340
5. Solomon, F. and Jencks, W. P. (1969) Identification of an enzyme-γ-glutamyl coenzyme A intermediate from coenzyme A transferase J. Biol. Chem. 244, 1079-1081
6. Pickart, C. M. and Jencks, W. P. (1979) Formation of stable anhydrides from CoA transferase and hydroxamic acids J. Biol. Chem. 254, 9120-9129
7. White, H. and Jencks, W. P. (1976) Mechanism and specificity of succinyl-CoA:3-ketoacid coenzyme A transferase J. Biol. Chem. 251, 1688-1699
8. White, H., Solomon, F., and Jencks, W. P. (1976) Utilization of the inactivation rate of coenzyme A transferase by thiol reagents to determine properties of the enzyme-CoA intermediate J. Biol. Chem. 251, 1700-1707
9. Moore, S. A. and Jencks, W. P. (1982) Formation of active site thiol esters of CoA transferase and the dependence of catalysis on specific binding interactions J. Biol. Chem. 257, 10893-10907
10. Fierke, C. A. and Jencks, W. P. (1986) Two functional domains of coenzyme A activate catalysis by coenzyme A transferase. Pantetheine and adenosine 3′-phosphate 5′-diphosphate J. Biol. Chem. 261, 7603-7606
11. Whitty, A., Fierke, C. A., and Jencks, W. P. (1995) Role of binding energy with coenzyme A in catalysis by 3-oxoacid coenzyme A transferase Biochemistry 34, 11678-11689
12. Bateman, K. S., Brownie, E. R., Wolodko, W. T., and Fraser, M. E. (2002) Structure of the mammalian CoA transferase from pig heart Biochemistry 41, 14455-14462
13. Tammam, S. D., Rochet, J.-C., and Fraser, M. E. (2007) Identification of the cysteine residue exposed by the conformational change in pig heart succinyl-CoA:3-ketoacid coenzyme A transferase on binding coenzyme A Biochemistry 46, 10852-10863
14. Rangarajan, E. S., Li, Y., Ajamian, E., Iannuzzi, P., Kernaghan, S. D., Fraser, M. E., Cygler, M., and Matte, A. (2005) Crystallographic trapping of the glutamyl-CoA thioester intermediate of family I CoA transferases J. Biol. Chem. 280, 42919-42928
15. Fraser, M. E., Hayakawa, K., and Brown, W. D. (2010) Catalytic role of the conformational change in succinyl-CoA:3-oxoacid CoA transferase on binding CoA Biochemistry 49, 10319-10328
16. Jencks, W. P. (1987) Economics of enzyme catalysis Cold Spring Harbor Symp. Quant. Biol. 52, 65-73
17. Heider, J. (2001) A new family of CoA-transferases FEBS Lett. 509, 345-349
18. Jonsson, S., Ricagno, S., Lindqvist, Y., and Richards, N. G. J. (2004) Kinetic and mechanistic characterization of the formyl-CoA transferase from Oxalobacter formigenes J. Biol. Chem. 279, 36003-36012
19. Berthold, C. L., Toyota, C. G., Richards, N. G. J., and Lindqvist, Y. (2008) Reinvestigation of the catalytic mechanism of formyl-CoA transferase, a class III CoA-transferase J. Biol. Chem. 283, 6519-6529
20. Fukaya, M., Takemura, H., Okumura, H., Kawamura, Y., Horinouchi, S., and Beppu, T. (1990) Cloning of genes responsible for acetic acid resistance in Acetobacter aceti J. Bacteriol. 172, 2096-2104
21. Fukaya, M., Takemura, H., Tayama, K., Okumura, H., Kawamura, Y., Horinouchi, S., and Beppu, T. (1993) The aarC gene responsible for acetic acid assimilation confers acetic acid resistance on Acetobacter aceti J. Ferment. Bioeng. 76, 270-276
22. Ohmori, S., Masai, H., Arima, K., and Beppu, T. (1980) Isolation and identification of acetic acid bacteria for submerged acetic acid fermentation at high temperature Agric. Biol. Chem. 44, 2901-2906
23. Ohmori, S., Uozumi, T., and Beppu, T. (1982) Loss of acetic acid resistance and ethanol oxidizing ability in an Acetobacter strain Agric. Biol. Chem. 46, 381-389
24. Nakano, S. and Fukaya, M. (2008) Analysis of proteins responsive to acetic acid in Acetobacter: Molecular mechanisms conferring acetic acid resistance in acetic acid bacteria Int. J. Food Microbiol. 125, 54-59
25. Francois, J. A. and Kappock, T. J. (2007) Alanine racemase from the acidophile Acetobacter aceti Protein Expression Purif. 51, 39-48
26. Azuma, Y., Hosoyama, A., Matsutani, M., Furuya, N., Horikawa, H., Harada, T., Hirakawa, H., Kuhara, S., Matsushita, K., Fujita, N., and Shirai, M. (2009) Whole-genome analyses reveal genetic instability of Acetobacter pasteurianus Nucleic Acids Res. 37, 5768-5783
27. Sakurai, K., Arai, H., Ishii, M., and Igarashi, Y. (2011) Transcriptome response to different carbon sources in Acetobacter aceti Microbiology 157, 899-910
28. Mullins, E. A., Francois, J. A., and Kappock, T. J. (2008) A specialized citric acid cycle requiring succinyl-coenzyme A (CoA):acetate CoA-transferase (AarC) confers acetic acid resistance on the acidophile Acetobacter aceti J. Bacteriol. 190, 4933-4940
29. Cole, P. A. (1996) Chaperone-assisted protein expression Structure 4, 239-242
30. Francois, J. A., Starks, C. M., Sivanuntakorn, S., Jiang, H., Ransome, A. E., Nam, J.-W., Constantine, C. Z., and Kappock, T. J. (2006) Structure of a NADH-insensitive hexameric citrate synthase that resists acid inactivation Biochemistry 45, 13487-13499
31. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72, 248-254
32. Nath, A. and Atkins, W. M. (2008) A quantitative index of substrate promiscuity Biochemistry 47, 157-166
33. Teng, T.-Y. (1990) Mounting of crystals for macromolecular crystallography in a free-standing thin film J. Appl. Crystallogr. 23, 387-391
34. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326
35. Guex, N. and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modeling Electrophoresis 18, 2714-2723
36. Adams, P. D. 2010, PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D66, 213-221
37. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot Acta Crystallogr. D66, 486-501
38. Kleywegt, G. J. (2007) Crystallographic refinement of ligand complexes Acta Crystallogr. D63, 94-100
39. DeLano, W. L. (2002) The PyMOL molecular graphics system, DeLano Scientific, Palo Alto, CA.
40. Dolinsky, T. J., Nielsen, J. E., McCammon, J. A., and Baker, N. A. (2004) PDB2PQR: An automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations Nucleic Acids Res. 32, W665-W667
41. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., and McCammon, J. A. (2001) Electrostatics of nanosystems: Application to microtubules and the ribosome Proc. Natl. Acad. Sci. U.S.A. 98, 10037-10041
42. Miroux, B. and Walker, J. E. (1996) Over-production of proteins in Escherichia coli: Mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels J. Mol. Biol. 260, 289-298
43. Francis, D. M. and Page, R. (2001) In Current Protocols in Protein Science (Coligan, J. E., Dunn, B. M., Ploegh, H. L., Speicher, D. W., and Wingfield, P. T., Eds.) Chapter 61, pp 5.24.1-5.24.29, Wiley, New York.
44. Menzel, U. and Gottschalk, G. (1985) The internal pH of Acetobacterium wieringae and Acetobacter aceti during growth and production of acetic acid Arch. Microbiol. 143, 47-51
45. 5-carboxyaminoimidazole ribonucleotide mutase (PurE) from the acidophilic bacterium Acetobacter aceti Biochemistry 45, 8193-8208
46. Mullins, E. A., Starks, C. M., Francois, J. A., Sael, L., Kihara, D., and Kappock, T. J. (2012) Formyl-coenzyme A (CoA):oxalate CoA-transferase from the acidophile Acetobacter aceti has a distinctive electrostatic surface and inherent acid stability Protein Sci. 21, 686-696
47. Buckel, W., Dorn, U., and Semmler, R. (1981) Glutaconate CoA-transferase from Acidaminococcus fermentans Eur. J. Biochem. 118, 315-321
48. Haller, T., Buckel, T., Rétey, J., and Gerlt, J. A. (2000) Discovering new enzymes and metabolic pathways: Conversion of succinate to propionate by Escherichia coli Biochemistry 39, 4622-4629
49. Selmer, T., Willanzheimer, A., and Hetzel, M. (2002) Propionate CoA-transferase from Clostridium propionicum. Cloning of gene and identification of glutamate 324 at the active site Eur. J. Biochem. 269, 372-380
50. Fleck, C. B. and Brock, M. (2008) Characterization of an acyl-CoA:carboxylate CoA-transferase from Aspergillus nidulans involved in propionyl-CoA detoxification Mol. Microbiol. 68, 642-656
51. Jacob, U., Mack, M., Clausen, T., Huber, R., Buckel, W., and Messerschmidt, A. (1997) Glutaconate CoA-transferase from Acidaminococcus fermentans: The crystal structure reveals homology with other CoA-transferases Structure 5, 415-426
52. Carson, M., Johnson, D. H., McDonald, H., Brouillette, C., and Delucas, L. J. (2007) His-tag impact on structure Acta Crystallogr. D63, 295-301
53. Wu, W.-J., Anderson, V. E., Raleigh, D. P., and Tonge, P. J. (1997) Structure of hexadienoyl-CoA bound to enoyl-CoA hydratase determined by transferred nuclear Overhauser effect measurements: Mechanistic predictions based on the X-ray structure of 4-(chlorobenzoyl)-CoA dehalogenase Biochemistry 36, 2211-2220
54. Martin, D. P., Bibart, R. T., and Drueckhammer, D. G. (1994) Synthesis of novel analogs of acetyl coenzyme A: Mimics of enzyme reaction intermediates J. Am. Chem. Soc. 116, 4660-4668
55. Bürgi, H. B., Dunitz, J. D., and Shefter, E. (1973) Geometrical reaction coordinates. II. Nucleophilic addition to a carbonyl group J. Am. Chem. Soc. 95, 5065-5067
56. Allen, S. H. G., Kellermeyer, R. W., Stjernholm, R. L., and Wood, H. G. (1964) Purification and properties of enzymes involved in the propionic acid fermentation J. Bacteriol. 87, 171-187
57. Söhling, B. and Gottschalk, G. (1996) Molecular analysis of the anaerobic succinate degradation pathway in Clostridium kluyveri J. Bacteriol. 178, 871-880
58. Scherf, U. and Buckel, W. (1991) Purification and properties of 4-hydroxybutyrate coenzyme A transferase from Clostridium aminobutyricum Appl. Environ. Microbiol. 57, 2699-2702
59. Macieira, S., Zhang, J., Velarde, M., Buckel, W., and Messerschmidt, A. (2009) Crystal structure of 4-hydroxybutyrate CoA-transferase from Clostridium aminobutyricum Biol. Chem. 390, 1251-1263
60. Mack, M. and Buckel, W. (1997) Conversion of glutaconate CoA-transferase from Acidaminococcus fermentans into an acyl-CoA hydrolase by site-directed mutagenesis FEBS Lett. 405, 209-212
61. Hammes, G. G. (2002) Multiple conformational changes in enzyme catalysis Biochemistry 41, 8221-8228
62. Koshland, D. E., Jr. (1960) The active site and enzyme action Adv. Enzymol. Relat. Subj. Biochem. 22, 45-97
63. Gandour, R. D. (1981) On the importance of orientation in general base catalysis by carboxylate Bioorg. Chem. 10, 169-176
64. Chan, K. K., Wood, B. M., Fedorov, A. A., Fedorov, E. V., Imker, H. J., Amyes, T. L., Richard, J. P., Almo, S. C., and Gerlt, J. A. (2009) Mechanism of the orotidine 5′-monophosphate decarboxylase-catalyzed reaction: Evidence for substrate destabilization Biochemistry 48, 5518-5531
65. Bruice, T. C. (2002) A view at the millennium: The efficiency of enzymatic catalysis Acc. Chem. Res. 35, 139-148
66. Kamerlin, S. C. L., Chu, Z. T., and Warshel, A. (2010) On catalytic preorganization in oxyanion holes: Highlighting the problems with the gas-phase modeling of oxyanion holes and illustrating the need for complete enzyme models J. Org. Chem. 75, 6391-6401
67. Koike, R., Amemiya, T., Ota, M., and Kidera, A. (2008) Protein structural change upon ligand binding correlates with enzymatic reaction mechanism J. Mol. Biol. 379, 397-401
68. Koike, R., Kidera, A., and Ota, M. (2009) Alteration of oligomeric state and domain architecture is essential for functional transformation between transferase and hydrolase with the same scaffold Protein Sci. 18, 2060-2066
69. Dickert, S., Pierik, A. J., Linder, D., and Buckel, W. (2000) The involvement of coenzyme A esters in the dehydration of (R)-phenyllactate to (E)-cinnamate by Clostridium sporogenes Eur. J. Biochem. 267, 3874-3884
70. Leutwein, C. and Heider, J. (2001) Succinyl-CoA:(R)-benzylsuccinate CoA-transferase: An enzyme of the anaerobic toluene catabolic pathway in denitrifying bacteria J. Bacteriol. 183, 4288-4295
71. Ricagno, S., Jonsson, S., Richards, N., and Lindqvist, Y. (2003) Formyl-CoA transferase encloses the CoA binding site at the interface of an interlocked dimer EMBO J. 22, 3210-3219
72. Gruez, A., Roig-Zamboni, V., Valencia, C., Campanacci, V., and Cambillau, C. (2003) The crystal structure of the Escherichia coli YfdW gene product reveals a new fold of two interlaced rings identifying a wide family of CoA transferases J. Biol. Chem. 278, 34582-34586
73. Macieira, S., Zhang, J., Buckel, W., and Messerschmidt, A. (2012) Crystal structure of the complex between 4-hydroxybutyrate CoA-transferase from Clostridium aminobutyricum and CoA Arch. Microbiol. 194, 157-166
74. Torres, R., Swift, R. V., Chim, N., Wheatley, N., Lan, B., Atwood, B. R., Pujol, C., Sankaran, B., Bliska, J. B., Amaro, R. E., and Goulding, C. W. (2011) Biochemical, structural and molecular dynamics analyses of the potential virulence factor RipA from Yersinia pestis PLoS One 6, e25084
75. Zhou, H.-X., Wlodek, S. T., and McCammon, J. A. (1998) Conformation gating as a mechanism for enzyme specificity Proc. Natl. Acad. Sci. U.S.A. 95, 9280-9283
76. Zhou, H.-X. and McCammon, J. A. (2010) The gates of ion channels and enzymes Trends Biochem. Sci. 35, 179-185
77. McCammon, J. A. (2011) Gated diffusion-controlled reactions BMC Biophys. 4, 4
78. Sheridan, R. P. and Allen, L. C. (1981) The active site electrostatic potential of human carbonic anhydrase J. Am. Chem. Soc. 103, 1544-1550
79. Getzoff, E. D., Tainer, J. A., Weiner, P. K., Kollman, P. A., Richardson, J. S., and Richardson, D. C. (1983) Electrostatic recognition between superoxide and copper, zinc superoxide dismutase Nature 306, 287-290
80. Ripoll, D. R., Faerman, C. H., Axelsen, P. H., Silman, I., and Sussman, J. L. (1993) An electrostatic mechanism for substrate guidance down the aromatic gorge of acetylcholinesterase Proc. Natl. Acad. Sci. U.S.A. 90, 5128-5132
81. Tan, R. C., Truong, T. N., McCammon, J. A., and Sussman, J. L. (1993) Acetylcholinesterase: Electrostatic steering increases the rate of ligand binding Biochemistry 32, 401-403
82. Korolev, S., Koroleva, O., Petterson, K., Gu, M., Collart, F., Dementieva, I., and Joachimiak, A. (2002) Autotracing of Escherichia coli acetate CoA-transferase α-subunit structure using 3.4 Å MAD and 1.9 Å native data Acta Crystallogr. D58, 2116-2121