Protein-protein interactions in the β-oxidation part of the phenylacetate utilization pathway: Crystal structure of the PaaF-PaaG hydratase-isomerase complex

Journal of Biological Chemistry

Volumn 287, Issue 45, 2012, Pages 37986-37996

  Grishin, Andrey M ^a   Ajamian, Eunice ^b   Zhang, Linhua ^b   Rouiller, Isabelle ^b   Bostina, Mihnea ^b   Cygler, Miroslaw ^a,b  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DEGRADATION PATHWAYS; ENZYME COMPLEXES; PHENYLACETATE; PROTEIN-PROTEIN INTERACTIONS;

ENZYMES;

PROTEINS;

HYDROLYASE; PHENYLACETIC ACID; PROTEIN PAAF; PROTEIN PAAG; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE;

ARTICLE; CATALYSIS; COMPLEX FORMATION; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME PURIFICATION; ENZYME STRUCTURE; FATTY ACID OXIDATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ACETYL COENZYME A; CARBON-CARBON DOUBLE BOND ISOMERASES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; ENOYL-COA HYDRATASE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MICROSCOPY, ELECTRON; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR STRUCTURE; MULTIPROTEIN COMPLEXES; OPERON; OXIDATION-REDUCTION; PHENYLACETATES; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; WATER;

PAA;

EID: 84868325957     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.388231     Document Type: Article

References (39)

1. Cao, B., Nagarajan, K., and Loh, K. C. (2009) Biodegradation of aromatic compounds. Current status and opportunities for biomolecular approaches. Appl. Microbiol. Biotechnol. 85, 207-2288
2. Gibson, J., and Harwood, C. S. (2002) Metabolic diversity in aromatic compound utilization by anaerobic microbes. Annu. Rev. Microbiol. 56, 345-3699
3. Fuchs, G. (2008) Anaerobic metabolism of aromatic compounds. Ann. N.Y. Acad. Sci. 1125, 82-999
4. Egland, P. G., Pelletier, D. A., Dispensa, M., Gibson, J., and Harwood, C. S. (1997) A cluster of bacterial genes for anaerobic benzene ring biodegradation. Proc. Natl. Acad. Sci. U.S.A. 94, 6484-64899
5. Ferrández, A., Miñambres, B., García, B., Olivera, E. R., Luengo, J. M., García, J. L., and Díaz, E. (1998) Catabolism of phenylacetic acid in Escherichia coli. Characterization of a new aerobic hybrid pathway. J. Biol. Chem. 273, 25974-259866
6. Teufel, R., Mascaraque, V., Ismail, W., Voss, M., Perera, J., Eisenreich, W., Haehnel, W., and Fuchs, G. (2010) Bacterial phenylalanine and phenylacetate catabolic pathway revealed. Proc. Natl. Acad. Sci. U.S.A. 107, 14390-143955
7. Rather, L. J., Knapp, B., Haehnel, W., and Fuchs, G. (2010) Coenzyme A-dependent aerobic metabolism of benzoate via epoxide formation. J. Biol. Chem. 285, 20615-206244
8. El-Said Mohamed, M. (2000) Biochemical and molecular characterization of phenylacetate-coenzyme A ligase, an enzyme catalyzing the first step in aerobic metabolism of phenylacetic acid in Azoarcus evansii. J. Bacteriol. 182, 286-2944
9. Grishin, A. M., Ajamian, E., Tao, L., Zhang, L., Menard, R., and Cygler, M. (2011) Structural and functional studies of the Escherichia coli phenylacetyl-CoA monooxygenase complex. J. Biol. Chem. 286, 10735-107433
10. Nogales, J., Macchi, R., Franchi, F., Barzaghi, D., Fernández, C., García, J. L., Bertoni, G., and Díaz, E. (2007) Characterization of the last step of the aerobic phenylacetic acid degradation pathway. Microbiology 153, 357-3655
11. Kim, J. J., and Battaile, K. P. (2002) Burning fat. The structural basis of fatty acid beta-oxidation. Curr. Opin. Struct. Biol. 12, 721-7288
12. Mursula, A. M., Hiltunen, J. K., and Wierenga, R. K. (2004) Structural studies on 3-α2-enoyl-CoA isomerase. The variable mode of assembly of the trimeric disks of the crotonase superfamily. FEBS Lett. 557, 81-877
13. 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 Delta;3-Delta;2-enoyl-CoA isomerase shows a novel mode of binding for the fatty acyl group. J. Mol. Biol. 342, 1197-12088
14. Mursula, A. M., van Aalten, D. M., Hiltunen, J. K., and Wierenga, R. K. (2001) The crystal structure of Delta;3-Delta;2-enoyl-CoA isomerase. J. Mol. Biol. 309, 845-8533
15. 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, 957-9700
16. Ishikawa, M., Tsuchiya, D., Oyama, T., Tsunaka, Y., and Morikawa, K. (2004) Structural basis for channelling mechanism of a fatty acid β-oxidation multienzyme complex. EMBO J. 23, 2745-27544
17. 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, 5135-51455
18. 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, 847-8599
19. Barycki, J. J., O'Brien, L. K., Bratt, J. M., Zhang, R., Sanishvili, R., Strauss, A. W., and Banaszak, L. J. (1999) Biochemical characterization and crystal structure determination of human heart short chain L-3-hydroxyacyl-CoA dehydrogenase provide insights into catalytic mechanism. Biochemistry 38, 5786-57988
20. Haapalainen, A. M., Meriläinen, G., Pirilä, P. L., Kondo, N., Fukao, T., and Wierenga, R. K. (2007) Crystallographic and kinetic studies of human mitochondrial acetoacetyl-CoA thiolase. The importance of potassium and chloride ions for its structure and function. Biochemistry 46, 4305-43211
21. Fould, B., Garlatti, V., Neumann, E., Fenel, D., Gaboriaud, C., and Arlaud, G. J. (2010) Structural and functional characterization of the recombinant human mitochondrial trifunctional protein. Biochemistry 49, 8608-86177
22. Kasaragod, P., Venkatesan, R., Kiema, T. R., Hiltunen, J. K., and Wierenga, R. K. (2010) Crystal structure of liganded rat peroxisomal multifunctional enzyme type 1. A flexible molecule with two interconnected active sites. J. Biol. Chem. 285, 24089-240988
23. Mathieu, M., Modis, Y., Zeelen, J. P., Engel, C. K., Abagyan, R. A., Ahlberg, A., Rasmussen, B., Lamzin, V. S., Kunau, W. H., and Wierenga, R. K. (1997) The 1.8 A crystal structure of the dimeric peroxisomal 3-ketoacyl-CoA thiolase of Saccharomyces cerevisiae. Implications for substrate binding and reaction mechanism. J. Mol. Biol. 273, 714-7288
24. Kichise, T., Hisano, T., Takeda, K., and Miki, K. (2009) Crystal structure of phenylacetic acid degradation protein PaaG from Thermus thermophilus HB8. Proteins 76, 779-7866
25. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc-Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX. A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-2211
26. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-3266
27. Vagin, A., and Teplyakov, A. (1997) MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 30, 1022-10255
28. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-21322
29. Murshudov, G. N., Vagin, A. A., Lebedev, A., Wilson, K. S., and Dodson, E. J. (1999) Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallogr. D 55, 247-2555
30. Chen, V. B., Arendall, W. B., 3rd, 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. D 66, 12-211
31. Ohi, M., Li, Y., Cheng, Y., and Walz, T. (2004) Negative staining and image classification. Powerful tools in modern electron microscopy. Biol. Proced. Online 6, 23-344
32. Ludtke, S. J., Baldwin, P. R., and Chiu, W. (1999) EMAN. Semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-977
33. Hohn, M., Tang, G., Goodyear, G., Baldwin, P. R., Huang, Z., Penczek, P. A., Yang, C., Glaeser, R. M., Adams, P. D., and Ludtke, S. J. (2007) SPARX, a new environment for Cryo-EM image processing. J. Struct. Biol. 157, 47-555
34. Schüttelkopf, A. W., and van Aalten, D. M. (2004) PRODRG. A tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr. D 60, 1355-13633
35. Hamed, R. B., Batchelar, E. T., Clifton, I. J., and Schofield, C. J. (2008) Mechanisms and structures of crotonase superfamily enzymes. How nature controls enolate and oxyanion reactivity. Cell Mol. Life Sci. 65, 2507-25277
36. Hofstein, H. A., Feng, Y., Anderson, V. E., and Tonge, P. J. (1999) Role of glutamate 144 and glutamate 164 in the catalytic mechanism of enoyl-CoA hydratase. Biochemistry 38, 9508-95166
37. 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, 2991-29999
38. Teufel, R., Friedrich, T., and Fuchs, G. (2012) An oxygenase that forms and deoxygenates toxic epoxide. Nature 483, 359-3622
39. Jancarik, J., Pufan, R., Hong, C., Kim, S. H., and Kim, R. (2004) Optimum solubility (OS) screening: an efficient method to optimize buffer conditions for homogeneity and crystallization of proteins. Acta Crystallogr. D 60, 1670-16733