196
Views
2
CrossRef citations to date
0
Altmetric
Research Article

Structural characterization of a Δ3, Δ2-enoyl-CoA isomerase from Pseudomonas aeruginosa: implications for its involvement in unsaturated fatty acid metabolism

, , , , , , , , , , , , , & show all
Pages 2695-2702 | Received 22 Mar 2018, Accepted 14 Jun 2018, Published online: 17 Nov 2018

References

  • Amari, D., Marques, C. & Davies, D. (2013). The putative enoyl-coenzyme A hydratase DspI is required for production of the Pseudomonas aeruginosa biofilm dispersion autoinducer cis-2-decenoic acid. Journal of Bacteriology, 195, 4600–4610.
  • Bell, A. F., Feng, Y., Hofstein, H. A., Parikh, S., Wu, J., Rudolph, … Tonge, P. J. (2002). Stereoselectivity of enoyl-CoA hydratase results from preferential activation of one of two bound substrate conformers. Chemistry & Biology, 9, 1247–1255.
  • Bhaswant, M., Poudyal, H. & Brown, L. (2015). Mechanisms of enhanced insulin secretion and sensitivity with n-3 unsaturated fatty acids. Journal of Nutritional Biochemistry, 26, 571–584.
  • Boon, C., Deng, Y., Wang, L., He, Y., Xu, J., Fan, Y., … Zhang, L. (2008). A novel DSF-like signal from Burkholderia cenocepacia interferes with Candida albicans morphological transition. ISME Journal, 2, 27–36.
  • Chatterjee, S., Wistrom, C. & Lindow, S. (2008). A cell-cell signaling sensor is required for virulence and insect transmission of Xylella fastidiosa. Proceedings of the National Academy of Sciences of the United States of America, 105, 2670–2675.
  • Cheng, Z., He, Y.-W., Lim, S. C., Qamra, R., Walsh, M. A., Zhang, L.-H. & Song, H. (2010). Structural basis of the sensor-synthase interaction in autoinduction of the quorum sensing signal DSF biosynthesis. Structure, 18, 1199–1209.
  • Davies, D. & Marques, C. (2009). A fatty acid messenger is responsible for inducing dispersion in microbial biofilms. Journal of Bacteriology, 191, 1393–1403.
  • Deep, A., Chaudhary, U. & Gupta, V. (2011). Quorum sensing and bacterial pathogenicity: From molecules to disease. Journal of Laboratory Physicians, 3, 4–11.
  • Deng, Y., Wu, J., Tao, F. & Zhang, L. (2011). Listening to a new language: DSF-based quorum sensing in Gram-negative bacteria. Chemical Reviews, 111, 160–173.
  • Engel, C., Kiema, T., Hiltunen, J. & Wierenga, R. (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. Journal of Molecular Biology, 275, 859–847.
  • Hamed, R., Batchelar, E., Clifton, I. & Schofield, C. (2008). Mechanisms and structures of crotonase superfamily enzymes–how nature controls enolate and oxyanion reactivity. Cellular and Molecular Life Sciences, 65, 2507–2527.
  • Hamed, R. B., Batchelar, E. T., Clifton, I. & Schofield, C. J. (2008). Mechanisms and structures of crotonase superfamily enzymes–how nature controls enolate and oxyanion reactivity. Cellular and Molecular Life Sciences, 65, 2507–2527.
  • Hiltunen, J. K. & Qin, Y.-M. (2000). beta-oxidation - strategies for the metabolism of a wide variety of acyl-CoA esters. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids, 1484, 117–128.
  • Huang, T. & Lee Wong, A. (2007). Extracellular fatty acids facilitate flagella-independent translocation by Stenotrophomonas maltophilia. Research in Microbiology, 158, 702–711.
  • Hubbard, P., Yu, W., Schulz, H. & Kim, J. (2005). Domain swapping in the low-similarity isomerase/hydratase superfamily: The crystal structure of rat mitochondrial Delta3, Delta2-enoyl-CoA isomerase. Protein Science, 14, 1545–1555.
  • Kiema, T., Engel, C., Schmitz, W., Filppula, S., Wierenga, R. & Hiltunen, J. (1999). Mutagenic and enzymological studies of the hydratase and isomerase activities of 2-enoyl-CoA hydratase-1. Biochemistry, 38, 2991–2999.
  • Konc, J., Miller, B., Štular, T., Lešnik, S., Woodcock, H., Brooks, B. & Janežič, D. (2015). ProBiS-CHARMMing: Web interface for prediction and optimization of ligands in protein binding sites. Journal of Chemical Information and Modeling, 55, 2308–2314.
  • Kozlikova, B., Sebestova, E., Sustr, V., Brezovsky, J., Strnad, O., Daniel, L., … Sochor, J. (2014). CAVER Analyst 1.0: Graphic tool for interactive visualization and analysis of tunnels and channels in protein structures. Bioinformatics, 30, 2684–2685.
  • Li, C., Yang, M., Liu, L., Li, T., Peng, C., He, L., … Bao, R. (2018). Mechanistic insights into the allosteric regulation of aspartate kinase. Biochemical Journal, 475, 1107–1119.
  • Liu, L., Li, T., Cheng, X., Peng, C., Li, C., He, L., … Bao, R. (2018). Structural and functional studies on Pseudomonas aeruginosa DspI: Implications for its role in DSF biosynthesis. Scienctific Reports, 8, 3928.
  • Müller-Newen, G., Janssen, U. & Stoffel, W. (1995). Enoyl-CoA hydratase and isomerase form a superfamily with a common active-site glutamate residue. European Journal of Biochemistry, 228, 68–73.
  • Müller-Newen, G. & 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.
  • Marques, C., Davies, D. & Sauer, K. (2015). Control of biofilms with the fatty acid signaling molecule cis-2-decenoic acid. Pharmaceuticals (Basel), 8, 816–835.
  • Modis, Y., Filppula, S., Novikov, D., Norledge, B., Hiltunen, J. & Wierenga, R. (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.
  • Mursula, A., Hiltunen, J. & Wierenga, R. (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 Letters, 557, 81–87.
  • Mursula, A., van Aalten, D., Hiltunen, J. & Wierenga, R. (2001). The crystal structure of delta(3)-delta(2)-enoyl-CoA isomerase. Journal of Molecular Biology, 309, 845–853.
  • Mursula, A. M., van Aalten, D. M., Hiltunen, J. K. & Wierenga, R. K. (2001). The crystal structure of delta(3)-delta(2)-enoyl-CoA isomerase. Journal of Molecular Biology, 309, 845–853.
  • Niesen, F., Berglund, H. & Vedadi, M. (2007). The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nature Protocols, 2, 2212–2221.
  • Onwukwe, G., Koski, M., Pihko, P., Schmitz, W. & Wierenga, R. (2015). Structures of yeast peroxisomal Δ(3),Δ(2)-enoyl-CoA isomerase complexed with acyl-CoA substrate analogues: The importance of hydrogen-bond networks for the reactivity of the catalytic base and the oxyanion hole. Acta Crystallographica Section D: Biological Crystallography, 71, 2178–2191.
  • Onwukwe, G., Kursula, P., Koski, M., Schmitz, W. & Wierenga, R. (2015). Human Δ³,Δ2-enoyl-CoA isomerase, type 2: A structural enzymology study on the catalytic role of its ACBP domain and helix-10. FEBS Journal, 282, 746–768.
  • Partanen, S., Novikov, D., Popov, A., Mursula, A., Hiltunen, J. & Wierenga, R. (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. Journal of Molecular Biology, 342, 1197–1208.
  • Rahmani-Badi, A., Sepehr, S., Fallahi, H. & Heidari-Keshel, S. (2015). Dissection of the cis-2-decenoic acid signaling network in Pseudomonas aeruginosa using microarray technique. Frontiers in Microbiology, 6, 383.
  • Robert, X. & Gouet, P. (2014). Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Research, 42, W320–W324.
  • Ryan, R. P., An, S.-q., Allan, J. H., McCarthy, Y. & Dow, J. M. (2015). The DSF family of cell-cell signals: An expanding class of bacterial virulence regulators. PLoS Pathogens, 11, e1004986.
  • Ryan, R. & Dow, J. (2011). Communication with a growing family: Diffusible signal factor (DSF) signaling in bacteria. Trends in Microbiology, 19, 145–152.
  • Singh, P. K., Schaefer, A. L., Parsek, M. R., Moninger, T. O., Welsh, M. J. & Greenberg, E. (2000). Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature, 407, 762–764.
  • Slater, H., Alvarez-Morales, A., Barber, C., Daniels, M. & Dow, J. (2000). A two-component system involving an HD-GYP domain protein links cell-cell signalling to pathogenicity gene expression in Xanthomonas campestris. Molecular Microbiology, 38, 986–1003.
  • Srivastava, S., Chaudhary, S., Thukral, L., Shi, C., Gupta, R., Gupta, R., … Gokhale, R. (2015). Unsaturated lipid assimilation by mycobacteria requires auxiliary cis-trans enoyl CoA isomerase. Chemistry & Biology, 22, 1577–1587.
  • Thowthampitak, J., Shaffer, B., Prathuangwong, S. & Loper, J. (2008). Role of rpfF in virulence and exoenzyme production of Xanthomonas axonopodis pv. glycines, the causal agent of bacterial pustule of soybean. Phytopathology, 98, 1252–1260.
  • Twomey, K. B., O'Connell, O. J., McCarthy, Y., Dow, J. M., O'Toole, G. A., Plant, B. J. & Ryan, R. P. (2012). Bacterial cis-2-unsaturated fatty acids found in the cystic fibrosis airway modulate virulence and persistence of Pseudomonas aeruginosa. The ISME Journal, 6, 939–950.
  • Wan, K., Wang, S., Brown, C., Yu, V., Entzeroth, M., Lane, D. & Lee, M. (2009). Differential scanning fluorimetry as secondary screening platform for small molecule inhibitors of Bcl-XL. Cell Cycle, 8, 3943–3952.
  • Zhang, D., Yu, W., Geisbrecht, B., Gould, S., Sprecher, H. & Schulz, H. (2002). Functional characterization of Delta3,Delta2-enoyl-CoA isomerases from rat liver. Journal of Biological Chemistry., 277, 9127–9132.
  • Zheng, C., Yoo, J., Lee, T., Cho, H., Kim, Y. & Kim, W. (2005). Fatty acid synthesis is a target for antibacterial activity of unsaturated fatty acids. FEBS Letters, 579, 5157–5162.
  • Zhou, L., Zhang, L., Cámara, M. & He, Y. (2017). The DSF family of quorum sensing signals: Diversity, biosynthesis, and turnover. Trends in Microbiology, 25, 293–303.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.