Domain swapping in the low-similarity isomerase/hydratase superfamily: The crystal structure of rat mitochondrial Δ3,Δ2- enoyl-CoA isomerase

Protein Science

Volumn 14, Issue 6, 2005, Pages 1545-1555

  Hubbard, Paul A ^a   Yu, Wenfeng ^b   Schulz, Horst ^b   Kim, Jung Ja P ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

Crystal structure; Domain swapping; Enoyl coA isomerase; Fatty acid metabolism; Low similarity isomerase hydratase superfamily

Indexed keywords

1,4 DIHYDROXY 2 NAPHTHOYL COENZYME A SYNTHASE; ACID; BASE; DELTA 3,DELTA 2 ENOYL COENZYME A ISOMERASE; DIMER; ENOYL COENZYME A HYDRATASE; GLUTAMIC ACID; HYDROLYASE; ISOENZYME; ISOMERASE; MITOCHONDRIAL ENZYME; MONOMER; POLYPEPTIDE; PROTON; SYNTHETASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ENZYME LOCALIZATION; ENZYME STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTON TRANSPORT; RAT; STEREOCHEMISTRY;

AMINO ACID SEQUENCE; ANIMALS; CARBON-CARBON DOUBLE BOND ISOMERASES; CRYSTALLOGRAPHY, X-RAY; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; RATS; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 22444431672     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.041303705     Document Type: Article

References (45)

1. Abrahams, J.P. and Leslie, A.G.W. 1996. Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogr. D Biol. Crystallogr. 52: 30-42.
2. Bahnson, B.J., Anderson, V.E., and Petsko, G.A. 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.
3. Bell,A.F., Wu, J., Feng,Y., and Tonge, P.J. 2001. Involvement of glycine 141 in substrate activation by enoyl-CoA hydratase. Biochemistry 40: 1725-1733.
4. Bell, A.F., Feng, Y., Hofstein, H.A., Parikh, S., Wu, J., Rudolph, M.J., Kisker, C., Whitty, A., and Tonge, P.J. 2002. Stereoselectivity of enoyl-CoA hydratase results from preferential activation of one of two bound substrate conformers. Chem. Biol. 9: 1247-1255.
5. Bennett, M.J., Choe, S., and Eisenberg, D. 1994. Domain swapping: Entangling alliances between proteins. Proc. Natl. Acad. Sci. 91: 3127-3131.
6. Benning, M.M., Taylor, K.L., Liu, R.-Q., Yang, G., Xiang, H., Wesenberg, G., Dunaway-Mariano, D., and Holden, H.M. 1996. Structure of 4-chlorobenzoyl coenzyme A dehalogenase determined to 1.8 Å resolution: An enzyme catalyst generated via adaptive mutation. Biochemistry 35: 8103-8109.
7. Benning, M.M., Haller, T., Gerlt, J.A., and Holden, H.M. 2000. New reactions in the crotonase superfamily: Structure of methylmalonyl CoA decarboxylase from Escherichia coli. Biochemistry 39: 4630-4639.
8. Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N., and Bourne, P.E. 2000. The Protein Data Bank. Nucleic Acids Res. 28: 235-242.
9. Brunger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S., et al. 1998. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54: 905-921.
10. Bucklers, L., Umani-Ronchi, A., Retey, J., and Arigoni, D. 1970. Stereochemistry of the enzymatic dehydration of butyryl-CoA [German]. Experientia 26: 931-933.
11. Chen, L.S., Jin, S.J., and Tserng, K.Y. 1994. Purification and mechanism of Δ 3,Δ 5-t-2,t-4-dienoyl-CoA isomerase from rat liver. Biochemistry 33: 10527-10534.
12. Engel, C.K., Mathieu, M., Zeelen, J.P., Hiltunen, J.K., and Wierenga, R.K. 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.
13. Engel, C.K., Kiema, T.R., Hiltunen, J.K., and Wierenga, R.K. 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.
14. Fillgrove, K.L. and Anderson, V.E. 2000. Orientation of coenzyme A substrates, nicotinamide and active site functional groups in (Di)enoylcoenzyme A reductases. Biochemistry 39: 7001-7011.
15. Fong, J.C. and Schulz, H. 1977. Purification and properties of pig heart crotonase and the presence of short chain and long chain enoyl coenzyme A hydratases in pig and guinea pig tissues. J. Biol. Chem. 252: 542-547.
16. Geisbrecht, B.V., Zhu, D., Schulz, K., Nau, K., Morrell, J.C., Geraghty, M., Schulz, H., Erdmann, R., and Gould, S.J. 1998. Molecular characterization of Saccharomyces cerevisiae Δ3, Δ2-enoyl-CoA isomerase. J. Biol. Chem. 273: 33184-33191.
17. Gurvitz, A., Mursula, A.M., Firzinger, A., Hamilton, B., Kilpelainen, S.H., Hartig, A., Ruis, H., Hiltunen, J.K., and Rottensteiner, H. 1998. Peroxisomal Δ3-cis-Δ2-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.
18. Holden, H.M., Benning, M.M., Haller, T., and Gerlt, J.A. 2001. The crotonase superfamily: Divergently related enzymes that catalyze different reactions involving acyl coenzyme a thioesters. Acc. Chem. Res. 34: 145-157.
19. Jones, T.A., Zou, J.Y., Cowan, S.W., and Kjeldgaard, M. 1991. Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47: 110-119.
20. Kiema, T.R., Engel, C.K., Schmitz, W., Filppula, S.A., Wierenga, R.K., and Hiltunen, J.K. 1999. Mutagenic and enzymological studies of the hydratase and isomerase activities of 2-enoyl-CoA hydratase-1. Biochemistry 38: 2991-2999.
21. Kurimoto, K., Fukai, S., Nureki, O., Muto, Y., and Yokoyama, S. 2001. Crystal structure of human AUH protein, a single-stranded RNA binding homolog of enoyl-CoA hydratase. Structure 9: 1253-1263.
22. Levitt, M. and Gerstein, M. 1998. A unified statistical framework for sequence comparison and structure comparison. Proc. Natl. Acad. Sci. 95: 5913-5920.
23. McRee, D.E. 1999. Practical protein crystallography, 2nd ed. Academic Press, San Diego, CA.
24. Modis, Y., Filppula, S.A., Novikov, D.K., Norledge, B., Hiltunen, J.K., and Wierenga, R.K. 1998. The crystal structure of dienoyl-CoA isomerase at 1.5 A° resolution reveals the importance of aspartate and glutamate sidechains for catalysis. Structure 6: 957-970.
25. Muller-Newen, G. and Stoffel, W. 1993. Site-directed mutagenesis of putative active-site amino acid residues of 3,2-trans-enoyl-CoA isomerase, conserved within the low-homology isomerase/hydratase enzyme family. Biochemistry 32: 11405-11412.
26. Muller-Newen, G., Janssen, U., and Stoffel, W. 1995. Enoyl-CoA hydratase and isomerase form a superfamily with a common active-site glutamate residue. Eur. J. Biochem. 228: 68-73.
27. Mursula, A.M., van Aalten, D.M., Hiltunen, J.K., and Wierenga, R.K. 2001. The crystal structure of Δ(3)-Δ(2)-enoyl-CoA isomerase. J. Mol. Biol. 309: 845-853.
28. Mursula, A.M., Hiltunen, J.K., and Wierenga, R.K. 2004. Structural studies on Δ(3)-Δ(2)-enoyl-CoA isomerase: The variable mode of assembly of the trimeric disks of the crotonase superfamily. FEBS Lett. 557: 81-87.
29. Nicholls, A., Sharp, K.A., and Honig, B. 1991. Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11: 281-296.
30. Otwinowski, Z. and Minor, W. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276: 307-326.
31. Palosaari, P.M., Kilponen, J.M., Sormunen, R.T., Hassinen, I.E., and Hiltunen, J.K. 1990. Δ 3,Δ 2-enoyl-CoA isomerases. Characterization of the mitochondrial isoenzyme in the rat. J. Biol. Chem. 265: 3347-3353.
32. Partanen, S.T., Novikov, D.K., Popov, A.N., Mursula, A.M., Hiltunen, J.K., and Wierenga, R.K. 2004. The 1.3 A° crystal structure of human mitochondrial Δ3-Δ2-enoyl-CoA isomerase shows a novel mode of binding for the fatty acyl group. J. Mol. Biol. 342: 1197-1208.
33. Pearson, W.R. and Lipman, D.J. 1988. Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. 85: 2444-2448.
34. Pflugrath, J.W. 1999. The finer things in X-ray diffraction data collection. Acta Crystallogr. D Biol. Crystallogr. 55 (Pt. 10): 1718-1725.
35. Read, R.J. 1986. Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Crystallogr. A 42: 140-149.
36. Sa°li, A. and Blundell, T.L. 1993. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234: 779-815.
37. Schulz, H. and Kunau, W.-H. 1987. β-oxidation of unsaturated fatty acids: A revised pathway. Trends Biochem. Sci. 12: 403-406.
38. Stoffel,W.,Ditzer, R., and Caeser,H. 1964. Der stoffwechsel der ungesättigen fettsäuren. III. Zur β-oxidation der mono-und polyenfettsaβuren. Der mechanismus der enzymatischen reaktionen an 3-cis-enoyl-CoA-verbindungen. Hoppe Seylers Z. Physiol. Chem. 339: 167-181.
39. Todd, A.E., Orengo, C.A., and Thornton, J.M. 2002. Plasticity of enzyme active sites. Trends Biochem. Sci. 27: 419-426.
40. Truglio, J.J., Theis, K., Feng, Y., Gajda, R., Machutta, C., Tonge, P.J., and Kisker, C. 2003. Crystal structure of Mycobacterium tuberculosis MenB, a key enzyme in vitamin K2 biosynthesis. J. Biol. Chem. 278: 42352-42360.
41. van den Akker, F. and Hol, W.G. 1999. Difference density quality (DDQ): A method to assess the global and local correctness of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 55: 206-218.
42. Wallace, A.C., Laskowski, R.A., and Thornton, J.M. 1995. LIGPLOT: A program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8: 127-134.
43. Whittingham, J.L., Turkenburg, J.P., Verma, C.S., Walsh, M.A., and Grogan, G. 2003. The 2-A° crystal structure of 6-oxo camphor hydrolase. New structural diversity in the crotonase superfamily. J. Biol. Chem. 278: 1744-1750.
44. Zhang, W., Wei, Y., Luo, L., Taylor, K.L., Yang, G., Dunaway-Mariano, D., Benning, M.M., and Holden, H.M. 2001. Histidine 90 function in 4-chlorobenzoyl-coenzyme a dehalogenase catalysis. Biochemistry 40: 13474-13482.
45. Zhang, D., Yu, W., Geisbrecht, B.V., Gould, S.J., Sprecher, H., and Schulz, H. 2002. Functional characterization of D3,D2-enoyl-CoA isomerases from rat liver. J. Biol. Chem. 277: 9127-9132.