The isomerase and hydratase reaction mechanism of the crotonase active site of the multifunctional enzyme (type-1), as deduced from structures of complexes with 3S-hydroxy-acyl-CoA

FEBS Journal

Volumn 280, Issue 13, 2013, Pages 3160-3175

  Kasaragod, Prasad ^a   Schmitz, Werner ^b   Hiltunen, Jukka K ^a   Wierenga, Rik K ^a  

^a UNIVERSITY OF OULU   (Finland)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

3S hydroxy acyl CoA; crotonase; hydratase; isomerase; oxyanion hole

Indexed keywords

3 HYDROXYACYL COENZYME A DEHYDROGENASE; CATALASE; ENOYL COENZYME A HYDRATASE; ENOYL COENZYME A ISOMERASE; GLUTAMIC ACID; ISOMERASE; MULTIFUNCTIONAL ENZYME TYPE 1; PROTON; UNCLASSIFIED DRUG; WATER;

AMINO TERMINAL SEQUENCE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; COMPLEX FORMATION; CONFERENCE PAPER; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME MECHANISM; ENZYME STRUCTURE; PRIORITY JOURNAL;

3-HYDROXYACYL COA DEHYDROGENASES; ACYL COENZYME A; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BIOCATALYSIS; CARBON-CARBON DOUBLE BOND ISOMERASES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DATABASES, PROTEIN; ENOYL-COA HYDRATASE; GLUTAMIC ACID; HYDROLYSIS; ISOMERASES; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; MULTIENZYME COMPLEXES; MUTANT PROTEINS; RATS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; STEREOISOMERISM; SUBSTRATE SPECIFICITY;

RATTUS;

EID: 84879249536     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12150     Document Type: Conference Paper

References (57)

1. Poirier Y, Antonenkov VD, Glumoff T, &, Hiltunen JK, (2006) Peroxisomal beta-oxidation-a metabolic pathway with multiple functions. Biochim Biophys Acta 1763, 1413-1426. (Pubitemid 44883386)
2. Kiema TR, Taskinen JP, Pirila PL, Koivuranta KT, Wierenga RK, &, Hiltunen JK, (2002) Organization of the multifunctional enzyme type 1: interaction between N- and C-terminal domains is required for the hydratase-1/isomerase activity. Biochem J 367, 433-441. (Pubitemid 35216817)
3. Holden HM, Benning MM, Haller T, &, Gerlt JA, (2001) The crotonase superfamily: divergently related enzymes that catalyze different reactions involving acyl coenzyme a thioesters. Acc Chem Res 34, 145-157. (Pubitemid 32167864)
4. Hamed RB, Batchelar ET, Clifton IJ, &, Schofield CJ, (2008) Mechanisms and structures of crotonase superfamily enzymes-how nature controls enolate and oxyanion reactivity. Cell Mol Life Sci 65, 2507-2527.
5. Barycki JJ, O'Brien LK, Strauss AW, &, Banaszak LJ, (2000) Sequestration of the active site by interdomain shifting. Crystallographic and spectroscopic evidence for distinct conformations of L-3-hydroxyacyl-CoA dehydrogenase. J Biol Chem 275, 27186-27196.
6. Taskinen JP, Kiema TR, Hiltunen JK, &, Wierenga RK, (2006) Structural studies of MFE-1: the 1.9 A crystal structure of the dehydrogenase part of rat peroxisomal MFE-1. J Mol Biol 355, 734-746. (Pubitemid 41819106)
7. Taskinen JP, Kiema TR, Koivuranta KT, Wierenga RK, &, Hiltunen JK, (2002) Crystallization and characterization of the dehydrogenase domain from rat peroxisomal multifunctional enzyme type 1. Acta Crystallogr D Biol Crystallogr 58, 690-693. (Pubitemid 34395038)
8. Kasaragod P, Venkatesan R, Kiema TR, Hiltunen JK, &, Wierenga RK, (2010) Crystal structure of liganded rat peroxisomal multifunctional enzyme type 1: a flexible molecule with two interconnected active sites. J Biol Chem 285, 24089-24098.
9. Haataja TJ, Koski MK, Hiltunen JK, &, Glumoff T, (2011) Peroxisomal multifunctional enzyme type 2 from the fruitfly: dehydrogenase and hydratase act as separate entities, as revealed by structure and kinetics. Biochem J 435, 771-781.
10. Fould B, Garlatti V, Neumann E, Fenel D, Gaboriaud C, &, Arlaud GJ, (2010) Structural and functional characterization of the recombinant human mitochondrial trifunctional protein. Biochemistry 49, 8608-8617.
11. He XY, &, Yang SY, (1997) Glutamate-119 of the large alpha-subunit is the catalytic base in the hydration of 2-trans-enoyl-coenzyme A catalyzed by the multienzyme complex of fatty acid oxidation from Escherichia coli. Biochemistry 36, 11044-11049.
12. Yang S, He X, &, Schulz H, (1995) Glutamate 139 of the large alpha-subunit is the catalytic base in the dehydration of both D- and L-3-hydroxyacyl-coenzyme A but not in the isomerization of Delta3, Delta2-enoyl-coenzyme A Catalyzed by the multienzyme complex of fatty acid oxidation from Escherichia coli. Biochemistry 34, 6441-6447.
13. Hiltunen JK, Palosaari PM, &, Kunau WH, (1989) Epimerization of 3-hydroxyacyl-CoA esters in rat liver. Involvement of two 2-enoyl-CoA hydratases. J Biol Chem 264, 13536-13540. (Pubitemid 19198432)
14. Ferdinandusse S, Denis S, Van Roermund CW, Wanders RJ, &, Dacremont G, (2004) Identification of the peroxisomal beta-oxidation enzymes involved in the degradation of long-chain dicarboxylic acids. J Lipid Res 45, 1104-1111. (Pubitemid 38679506)
15. Nguyen SD, Baes M, &, Van Veldhoven PP, (2008) Degradation of very long chain dicarboxylic polyunsaturated fatty acids in mouse hepatocytes, a peroxisomal process. Biochim Biophys Acta 1781, 400-405.
16. Houten SM, Denis S, Argmann CA, Jia Y, Ferdinandusse S, Reddy JK, &, Wanders RJ, (2012) Peroxisomal L-bifunctional enzyme (Ehhadh) is essential for the production of medium-chain dicarboxylic acids. J Lipid Res 53, 1296-1303.
17. Kurosawa T, Sato M, Nakano H, Fujiwara M, Murai T, Yoshimura T, &, Hashimoto T, (2001) Conjugation reactions catalyzed by bifunctional proteins related to beta-oxidation in bile acid biosynthesis. Steroids 66, 107-114. (Pubitemid 32012556)
18. Cuebas DA, Phillips C, Schmitz W, Conzelmann E, &, Novikov DK, (2002) The role of alpha-methylacyl-CoA racemase in bile acid synthesis. Biochem J 363, 801-807. (Pubitemid 34526402)
19. Savolainen K, Kotti TJ, Schmitz W, Savolainen TI, Sormunen RT, Ilves M, Vainio SJ, Conzelmann E, &, Hiltunen JK, (2004) A mouse model for alpha-methylacyl-CoA racemase deficiency: adjustment of bile acid synthesis and intolerance to dietary methyl-branched lipids. Hum Mol Genet 13, 955-965. (Pubitemid 38628431)
20. Partanen ST, Novikov DK, Popov AN, Mursula AM, Hiltunen JK, &, Wierenga RK, (2004) The 1.3 A crystal structure of human mitochondrial Delta3-Delta2-enoyl-CoA isomerase shows a novel mode of binding for the fatty acyl group. J Mol Biol 342, 1197-1208. (Pubitemid 39207897)
21. Hubbard PA, Yu W, Schulz H, &, Kim JJ, (2005) Domain swapping in the low-similarity isomerase/hydratase superfamily: the crystal structure of rat mitochondrial Delta3, Delta2-enoyl-CoA isomerase. Protein Sci 14, 1545-1555. (Pubitemid 41007918)
22. Mursula AM, Hiltunen JK, &, Wierenga RK, (2004) Structural studies on delta(3)-delta(2)-enoyl-CoA isomerase: the variable mode of assembly of the trimeric disks of the crotonase superfamily. FEBS Lett 557, 81-87. (Pubitemid 38115873)
23. Engel CK, Mathieu M, Zeelen JP, Hiltunen JK, &, Wierenga RK, (1996) Crystal structure of enoyl-coenzyme A (CoA) hydratase at 2.5 angstroms resolution: a spiral fold defines the CoA-binding pocket. EMBO J 15, 5135-5145. (Pubitemid 26336195)
24. Palosaari PM, &, Hiltunen JK, (1990) Peroxisomal bifunctional protein from rat liver is a trifunctional enzyme possessing 2-enoyl-CoA hydratase, 3-hydroxyacyl-CoA dehydrogenase & delta 3, delta 2-enoyl-CoA isomerase activities. J Biol Chem 265, 2446-2449.
25. Kiema TR, Engel CK, Schmitz W, Filppula SA, Wierenga RK, &, Hiltunen JK, (1999) Mutagenic and enzymological studies of the hydratase and isomerase activities of 2-enoyl-CoA hydratase-1. Biochemistry 38, 2991-2999.
26. Yang SY, &, Elzinga M, (1993) Association of both enoyl coenzyme A hydratase and 3-hydroxyacyl coenzyme A epimerase with an active site in the amino-terminal domain of the multifunctional fatty acid oxidation protein from Escherichia coli. J Biol Chem 268, 6588-6592. (Pubitemid 23099361)
27. Goepfert S, Vidoudez C, Tellgren-Roth C, Delessert S, Hiltunen JK, &, Poirier Y, (2008) Peroxisomal Delta(3), Delta(2)-enoyl CoA isomerases and evolution of cytosolic paralogues in embryophytes. Plant J 56, 728-742.
28. Zhang D, Yu W, Geisbrecht BV, Gould SJ, Sprecher H, &, Schulz H, (2002) Functional characterization of Delta3, Delta2-enoyl-CoA isomerases from rat liver. J Biol Chem 277, 9127-9132. (Pubitemid 34952989)
29. Gurvitz A, Mursula AM, Firzinger A, Hamilton B, Kilpelainen SH, Hartig A, Ruis H, Hiltunen JK, &, Rottensteiner H, (1998) Peroxisomal Delta3-cis-Delta2-trans-enoyl-CoA isomerase encoded by ECI1 is required for growth of the yeast Saccharomyces cerevisiae on unsaturated fatty acids. J Biol Chem 273, 31366-31374. (Pubitemid 28533154)
30. Bell AF, Feng Y, Hofstein HA, Parikh S, Wu J, Rudolph MJ, Kisker C, Whitty A, &, Tonge PJ, (2002) Stereoselectivity of enoyl-CoA hydratase results from preferential activation of one of two bound substrate conformers. Chem Biol 9, 1247-1255. (Pubitemid 35352772)
31. Bahnson BJ, Anderson VE, &, Petsko GA, (2002) Structural mechanism of enoyl-CoA hydratase: three atoms from a single water are added in either an E1cb stepwise or concerted fashion. Biochemistry 41, 2621-2629. (Pubitemid 34168931)
32. Pihko P, Rapakko S, &, Wierenga RK, (2009) Oxyanion holes and their mimics. In Hydrogen Bonding in Organic Synthesis (, Pihko P, ed.), pp. 43-71. Wiley-VCH Verlag, Weinheim, Germany.
33. Papai I, Hamza A, Pihko PM, &, Wierenga RK, (2011) Stereoelectronic requirements for optimal hydrogen-bond-catalyzed enolization. Chemistry 17, 2859-2866.
34. Hamed RB, Gomez-Castellanos JR, Thalhammer A, Harding D, Ducho C, Claridge TD, &, Schofield CJ, (2011) Stereoselective C-C bond formation catalysed by engineered carboxymethylproline synthases. Nat Chem 3, 365-371.
35. He XY, Yang SY, &, Schulz H, (1992) Inhibition of enoyl-CoA hydratase by long-chain L-3-hydroxyacyl-CoA and its possible effect on fatty acid oxidation. Arch Biochem Biophys 298, 527-531.
36. Barycki JJ, O'Brien LK, Strauss AW, &, Banaszak LJ, (2001) Glutamate 170 of human l-3-hydroxyacyl-CoA dehydrogenase is required for proper orientation of the catalytic histidine and structural integrity of the enzyme. J Biol Chem 276, 36718-36726.
37. Hiltunen JK, Mursula AM, Rottensteiner H, Wierenga RK, Kastaniotis AJ, &, Gurvitz A, (2003) The biochemistry of peroxisomal beta-oxidation in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 27, 35-64. (Pubitemid 36412186)
38. Engel CK, Kiema TR, Hiltunen JK, &, Wierenga RK, (1998) The crystal structure of enoyl-CoA hydratase complexed with octanoyl-CoA reveals the structural adaptations required for binding of a long chain fatty acid-CoA molecule. J Mol Biol 275, 847-859. (Pubitemid 28077700)
39. Ishikawa M, Tsuchiya D, Oyama T, Tsunaka Y, &, Morikawa K, (2004) Structural basis for channelling mechanism of a fatty acid beta-oxidation multienzyme complex. EMBO J 23, 2745-2754. (Pubitemid 39013547)
40. Feng Y, Hofstein HA, Zwahlen J, &, Tonge PJ, (2002) Effect of mutagenesis on the stereochemistry of enoyl-CoA hydratase. Biochemistry 41, 12883-12890. (Pubitemid 35192518)
41. Zhang H, Machutta CA, &, Tonge PJ, (2010) Fatty acid biosynthesis and oxidation. In Comprehensive Natural Products II (, Mander L, &, Liu H-W, eds), pp. 231-275. Elsevier, Oxford.
42. Qin YM, Haapalainen AM, Conry D, Cuebas DA, Hiltunen JK, &, Novikov DK, (1997) Recombinant 2-enoyl-CoA hydratase derived from rat peroxisomal multifunctional enzyme 2: role of the hydratase reaction in bile acid synthesis. Biochem J 328, 377-382. (Pubitemid 27515576)
43. Tsuchida S, Kawamoto K, Nunome K, Hamaue N, Yoshimura T, Aoki T, &, Kurosawa T, (2011) Analysis of enoyl-coenzyme A hydratase activity and its stereospecificity using high-performance liquid chromatography equipped with chiral separation column. J Oleo Sci 60, 221-228.
44. Bell AF, Wu J, Feng Y, &, Tonge PJ, (2001) Involvement of glycine 141 in substrate activation by enoyl-CoA hydratase. Biochemistry 40, 1725-1733. (Pubitemid 32144043)
45. D'Ordine RL, Pawlak J, Bahnson BJ, &, Anderson VE, (2002) Polarization of cinnamoyl-CoA substrates bound to enoyl-CoA hydratase: correlation of (13)C NMR with quantum mechanical calculations and calculation of electronic strain energy. Biochemistry 41, 2630-2640. (Pubitemid 34168932)
46. Mohrig JR, Moerke KA, Cloutier DL, Lane BD, Person EC, &, Onasch TB, (1995) Importance of historical contingency in the stereochemistry of hydratase-dehydratase enzymes. Science 269, 527-529.
47. Corey EJ, &, Sneen RA, (1956) Stereoelectronic control in enolization-ketonization reactions. J Am Chem Soc 78, 6269-6278.
48. Ho SN, Hunt HD, Horton RM, Pullen JK, &, Pease LR, (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59. (Pubitemid 19125653)
49. Kabsch W, (2010) Xds. Acta Crystallogr D Biol Crystallogr 66, 125-132.
50. Leslie AGW, (1992) Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography 26.
51. Evans P, (2006) Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62, 72-82.
52. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, et al,. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67, 235-242.
53. Murshudov GN, Vagin AA, &, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53, 240-255. (Pubitemid 27235885)
54. Emsley P, &, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126-2132. (Pubitemid 41742764)
55. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, Wang X, Murray LW, Arendall WB III, Snoeyink J, &, Richardson JS, et al,. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35, W375-W383.
56. Krissinel E, &, Henrick K, (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr 60, 2256-2268. (Pubitemid 41742778)
57. Schrodinger L, (2010) The PyMOL Molecular Graphics System, Version 1.5.0.4.