Homology Modelling and in Silico Substrate Binding Analysis of a Rhizobium sp. RC1 Haloalkanoic Acid Permease
DOI:
https://doi.org/10.18034/mjmbr.v7i1.485Keywords:
Docking, Haloacids, Homology modelling, Permease, Rhizobium sp. RC1Abstract
Rhizobium sp. RC1 grows on haloalkanoic acid (haloacid) pollutants and expresses a haloacid permease (DehrP) which mediates the uptake of haloacids into the cells. For the first time, we report the homology model and docking analysis of DehrP and proposed its putative binding residues. The Protein Data Bank for protein of similar sequence. Ligand structures were retrieved from the ChemSpider database. The 3-dimensional (3-D) structure of DehrP was modelled based on the structure of Staphylococcus epidermidis glucose: H+ symporter (GlcPse) by Phyre2, refined by 3Drefine and evaluated by ProSA z-score, ERRAT and RAMPAGE. Docking of monobromoacetate, monochloroacetate, dibromoacetate, dichloroacetate, trichloroacetate, and 2,2-dichloropropionate ligands was done with AutoDock vina1.1.2. The 3-D structure of DehrP protein has twelve transmembrane helices. The overall quality factor of the model is ∼91%, with 93.6% of the residues in the favored region and the z-score is within the ≤ 10 limit. The putative H+ binding site residues are Gln133, Asp36, and Arg130. Docking analysis showed that Glu33, Trp34, Phe37, Phe38, Gln165, and Glu370 are potential haloacid interacting residues. DehrP-haloacid complexes had a binding affinity between -2.9 to -4.0 kcal/mol. DehrP has both putative H+ and haloacid binding sites that are most likely involved in the co-transport of H+ and haloacids. DehrP interacts with haloacids majorly through van der Waals and halogen bond interactions and has greater affinity for 2,2-dichloropropionate and could be a specialized chloropropionate uptake system. Site-directed mutagenasis of DehrP binding residues could improve its haloacid binding affinity.
Downloads
References
Abramson, J., Kaback, H.R. and Iwata, S. (2004), "Structural comparison of lactose permease and the glycerol-3-phosphate antiporter: members of the major facilitator superfamily", Current Opinion in Structural Biology, Vol. 14, No. 4, pp. 413-419. DOI: https://doi.org/10.1016/j.sbi.2004.07.005
Abramson, J., Smirnova, I., Kasho, V., Verner, G., Kaback, H.R. and Iwata, S. (2003), "Structure and mechanism of the lactose permease of Escherichia coli", Science, Vol. 301, No. 5633, pp. 610-615. DOI: https://doi.org/10.1126/science.1088196
Allison N., S., A. and Cooper, R. (1983), "The dehalogenases of a 2, 2-dichloropropionate degrading bacterium.", Journal of General Microbiology, Vol. 129, No. 5, pp. 1283–1293.
Altschup, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990), "Basic local alignment search tool", Journal of Molecular Biology, Vol. 215, No. 3, pp. 403-410. DOI: https://doi.org/10.1016/S0022-2836(05)80360-2
Berry, E.K.M., Allison, N., Skinner, A.J. and Cooper, R.A. (1979), "Degradation of the Selective Herbicide 2,2-Dichloropropionate (Dalapon) by a Soil Bacterium", Microbiology, Vol. 110, No. 1, pp. 39-45.
Berthiaume, C., Gilbert, Y., Fournier‐Larente, J., Pluchon, C., Filion, G., Jubinville, E., et al. (2014), "Identification of dichloroacetic acid degrading Cupriavidus bacteria in a drinking water distribution network model", Journal of Applied Microbiology, Vol. 116, No. 1, pp. 208-221. DOI: https://doi.org/10.1111/jam.12353
Bhattacharya, D., Nowotny, J., Cao, R. and Cheng, J. (2016), "3Drefine: an interactive web server for efficient protein structure refinement", Nucleic Acids Research, Vol. 44, No. W1, pp. W406-409.
BIOVIA, D.S. (2016), "Discovery Studio Modeling Environment, Release 2017", Dassault Systèmes, San Diego, CA., Vol., No.
Bois, F., Beney, C., Boumendjel, A., Mariotte, A.-M., Conseil, G. and Di Pietro, A. (1998), "Halogenated Chalcones with High-Affinity Binding to P-Glycoprotein: Potential Modulators of Multidrug Resistance", Journal of Medicinal Chemistry, Vol. 41, No. 21, pp. 4161-4164. DOI: https://doi.org/10.1021/jm9810194
Chaudhry, G.R. and Chapalamadugu, S. (1991), "Biodegradation of halogenated organic compounds", Microbiological Reviews, Vol. 55, No. 1, pp. 59-79. DOI: https://doi.org/10.1128/MMBR.55.1.59-79.1991
Colovos, C. and Yeates, T.O. (1993), "Verification of protein structures: patterns of nonbonded atomic interactions", Protein Science : A Publication of the Protein Society, Vol. 2, No. 9, pp. 1511-1519. DOI: https://doi.org/10.1002/pro.5560020916
Consortium, U. (2015), "UniProt: a hub for protein information", Nucleic Acids Research, Vol. 43, No. Database issue, pp. D204-212.
Dang, S., Sun, L., Huang, Y., Lu, F., Liu, Y., Gong, H., et al. (2010), "Structure of a fucose transporter in an outward-open conformation", Nature, Vol. 467, No. 7316, pp. 734-738. DOI: https://doi.org/10.1038/nature09406
Effendi, A.J., Greenaway, S.D. and Dancer, B.N. (2000), "Isolation and Characterization of 2,3-Dichloro-1-Propanol-Degrading Rhizobia", Applied and Environmental Microbiology, Vol. 66, No. 7, pp. 2882-2887. DOI: https://doi.org/10.1128/AEM.66.7.2882-2887.2000
Hardegger, L.A., Kuhn, B., Spinnler, B., Anselm, L., Ecabert, R., Stihle, M., et al. (2011), "Systematic investigation of halogen bonding in protein–ligand interactions", Angewandte Chemie International Edition, Vol. 50, No. 1, pp. 314-318. DOI: https://doi.org/10.1002/anie.201006781
Hashiramoto, M., Kadowaki, T., Clark, A. E., Muraoka, A., Momomura, K., Sakura, H., Tobe, K., Akanuma, Y., Yazaki, Y., Holman, G. D. and Kasuga, M. (1992), "Site-directed mutagenesis of GLUT1 in helix 7 residues 282 results in perturbation of exofacial ligand binding", The Journal of Biological Chemistry, Vol. 267, No. 25, pp. 17502–17507.
Higgins, T.P., Hope, S.J., Effendi, A.J., Dawson, S. and Dancer, B.N. (2005), "Biochemical and molecular characterisation of the 2,3-dichloro-1-propanol dehalogenase and stereospecific haloalkanoic dehalogenases from a versatile Agrobacterium sp", Biodegradation, Vol. 16, No. 5, pp. 485-492. DOI: https://doi.org/10.1007/s10532-004-5670-5
Huang, Y., Lemieux, M.J., Song, J., Auer, M. and Wang, D.N. (2003), "Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli", Science, Vol. 301, No. 5633, pp. 616-620. DOI: https://doi.org/10.1126/science.1087619
Huyop, F.Z., Cooper, A.R.A. (2003), "A Potential Use of Dehalogenase D (DehD) from Rhizobium sp. for Industrial Process", Jurnal.Teknologi, Vol. 39, No. (C), pp. 1-8. DOI: https://doi.org/10.11113/jt.v39.450
Iancu, C.V., Zamoon, J., Woo, S.B., Aleshin, A. and Choe, J.Y. (2013), "Crystal structure of a glucose/H+ symporter and its mechanism of action", Proceedings of the National Academy of Sciences U.S.A, Vol. 110, No. 44, pp. 17862-17867. DOI: https://doi.org/10.1073/pnas.1311485110
Janssen, D.B., Scheper, A., Dijkhuizen, L. and Witholt, B. (1985), "Degradation of halogenated aliphatic compounds by Xanthobacter autotrophicus GJ10", Applied and Environmental Microbiology, Vol. 49, No. 3, pp. 673-677. DOI: https://doi.org/10.1128/AEM.49.3.673-677.1985
Jing, N., Wahab, R.A., Hamdan, S. and Huyop, F. (2010), "Cloning and DNA Sequence Analysis of the Haloalkanoic Permease Uptake Gene from Rhizobium sp. RC 1", Biotechnology, Vol. 9, No. 3, pp. 319-325. DOI: https://doi.org/10.3923/biotech.2010.319.325
Kelley, L.A., Mezulis, S., Yates, C.M., Wass, M.N. and Sternberg, M.J. (2015), "The Phyre2 web portal for protein modeling, prediction and analysis", Nature Protocols, Vol. 10, No. 6, pp. 845-858. DOI: https://doi.org/10.1038/nprot.2015.053
Leigh, J., Skinner, A. and Cooper, R. (1986), "Isolation and partial characterisation of dehalogenase-deficient mutants of a Rhizobium sp", FEMS microbiology letters, Vol. 36, No. 2-3, pp. 163-166. DOI: https://doi.org/10.1111/j.1574-6968.1986.tb01688.x
Leigh, J.A., Skinner, A.J. and Cooper, R.A. (1988), "Partial purification, stereospecificity and stoichiometry of three dehalogenases from a Rhizobium species", FEMS microbiology letters, Vol. 49, No. 3, pp. 353-356. DOI: https://doi.org/10.1111/j.1574-6968.1988.tb02756.x
Liò, P. and Bishop, M. (2008), "Modeling sequence evolution", Bioinformatics: Data, Sequence Analysis and Evolution, Vol., No., pp. 255-285.
Lovell, S.C., Davis, I.W., Arendall, W.B., 3rd, de Bakker, P.I., Word, J.M., Prisant, M.G., et al. (2003), "Structure validation by Calpha geometry: phi, psi and Cbeta deviation", Proteins, Vol. 50, No. 3, pp. 437-450. DOI: https://doi.org/10.1002/prot.10286
Matter, H., Nazare, M., Gussregen, S., Will, D.W., Schreuder, H., Bauer, A., et al. (2009), "Evidence for C-Cl/C-Br...pi interactions as an important contribution to protein-ligand binding affinity", Angewandte Chemie International Edition in English, Vol. 48, No. 16, pp. 2911-2916. DOI: https://doi.org/10.1002/anie.200806219
Morris, G.M., Goodsell, D.S., Halliday, R.S., Huey, R., Hart, W.E., Belew, R.K., et al. (1998), "Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function", Journal of computational chemistry, Vol. 19, No. 14, pp. 1639-1662. DOI: https://doi.org/10.1002/(SICI)1096-987X(19981115)19:14<1639::AID-JCC10>3.0.CO;2-B
Morris, G.M., Huey, R., Lindstrom, W., Sanner, M.F., Belew, R.K., Goodsell, D.S., et al. (2009), "AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility", Journal of computational chemistry, Vol. 30, No. 16, pp. 2785-2791. DOI: https://doi.org/10.1002/jcc.21256
Mueckler, M. and Makepeace, C. (2009), "Model of the Exofacial Substrate-Binding Site and Helical Folding of the Human Glut1 Glucose Transporter Based on Scanning Mutagenesis", Biochemistry, Vol. 48, No. 25, pp. 5934-5942. DOI: https://doi.org/10.1021/bi900521n
Mueckler, M., Weng, W. and Kruse, M. (1994), "Glutamine 161 of Glut1 glucose transporter is critical for transport activity and exofacial ligand binding", The Journal of Biology Chemistry, Vol. 269, No. 32, pp. 20533-20538.
Musa, M.A. (2017), "Computational Analysis of Putative Haloalkanoic Permease (DehrP) from Rhizobium sp. RC1", Masters dissertation, Universiti Teknologi Malaysia, Malaysia..
Newstead, S., Drew, D., Cameron, A.D., Postis, V.L., Xia, X., Fowler, P.W., et al. (2011), "Crystal structure of a prokaryotic homologue of the mammalian oligopeptide-proton symporters, PepT1 and PepT2", The EMBO Journal, Vol. 30, No. 2, pp. 417-426. DOI: https://doi.org/10.1038/emboj.2010.309
Olsen, J., Seiler, P., Wagner, B., Fischer, H., Tschopp, T., Obst-Sander, U., et al. (2004), "A fluorine scan of the phenylamidinium needle of tricyclic thrombin inhibitors: effects of fluorine substitution on pKa and binding affinity and evidence for intermolecular C-F[three dots, centered]CN interactions", Organic and Biomolecular Chemistry, Vol. 2, No. 9, pp. 1339-1352. DOI: https://doi.org/10.1039/B402515F
Pence, H.E. and Williams, A. (2010), "ChemSpider: An Online Chemical Information Resource", Journal of Chemical Education, Vol. 87, No. 11, pp. 1123-1124. DOI: https://doi.org/10.1021/ed100697w
Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., et al. (2004), "UCSF Chimera—a visualization system for exploratory research and analysis", Journal of computational chemistry, Vol. 25, No. 13, pp. 1605-1612. DOI: https://doi.org/10.1002/jcc.20084
Plewa, M.J., Simmons, J.E., Richardson, S.D. and Wagner, E.D. (2010), "Mammalian cell cytotoxicity and genotoxicity of the haloacetic acids, a major class of drinking water disinfection by-products", Environmental and Molecular Mutagenesis, Vol. 51, No. 8-9, pp. 871-878. DOI: https://doi.org/10.1002/em.20585
Saier, M.H., Reddy, V.S., Tsu, B.V., Ahmed, M.S., Li, C. and Moreno-Hagelsieb, G. (2016), "The Transporter Classification Database (TCDB): recent advances", Nucleic Acids Research, Vol. 44, No. Database issue, pp. D372-D379.
Sanderson, N.M., Qi, D., Steel, A. and Henderson, P.J.F. (1998), "Effect of the D<sup>32</sup>N and N<sup>300</sup>F mutations on the activity of the bacterial sugar transport protein, GalP", Biochemical Society Transactions, Vol. 26, No. 3, pp. S306.
Schaffer, A.A., Aravind, L., Madden, T.L., Shavirin, S., Spouge, J.L., Wolf, Y.I., et al. (2001), "Improving the accuracy of PSI-BLAST protein database searches with composition-based statistics and other refinements", Nucleic Acids Research, Vol. 29, No. 14, pp. 2994-3005. DOI: https://doi.org/10.1093/nar/29.14.2994
Shenoy, S.R. and Jayaram, B. (2010), "Proteins: sequence to structure and function--current status", Current Protein and Peptide Science, Vol. 11, No. 7, pp. 498-514. DOI: https://doi.org/10.2174/138920310794109094
Sievers, F., Wilm, A., Dineen, D., Gibson, T.J., Karplus, K., Li, W., et al. (2011), "Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega", Molecular systems biology, Vol. 7, No. 1, pp. 539.
Sirimulla, S., Bailey, J.B., Vegesna, R. and Narayan, M. (2013), "Halogen interactions in protein–ligand complexes: implications of halogen bonding for rational drug design", Journal of chemical information and modeling, Vol. 53, No. 11, pp. 2781-2791. DOI: https://doi.org/10.1021/ci400257k
Slater, J.H., Lovatt, D., Weightman, A. J., Senior, E. and Bull, A. T. (1979), "The growth of Pseudomonas putida on chlorinated aliphatic acids and its dehalogenase activity", Journal of General Microbiology, Vol. 114, No., pp. 125-136. DOI: https://doi.org/10.1099/00221287-114-1-125
Solcan, N., Kwok, J., Fowler, P.W., Cameron, A.D., Drew, D., Iwata, S., et al. (2012), "Alternating access mechanism in the POT family of oligopeptide transporters", The EMBO Journal, Vol. 31, No. 16, pp. 3411-3421. DOI: https://doi.org/10.1038/emboj.2012.157
Stringfellow, J.M., Cairns, S.S., Cornish, A. and Cooper, R.A. (1997), "Haloalkanoate Dehalogenase II (DehE) of a Rhizobium sp. — Molecular Analysis of the Gene and Formation of Carbon Monoxide from Trihaloacetate by the Enzyme", European Journal of Biochemistry, Vol. 250, No. 3, pp. 789-793. DOI: https://doi.org/10.1111/j.1432-1033.1997.00789.x
Strotmann, U.J., Pentenga, M. and Janssen, D.B. (1990), "Degradation of 2-chloroethanol by wild type and mutants of Pseudomonas putida US2", Archives of Microbiology, Vol. 154, No. 3, pp. 294-300. DOI: https://doi.org/10.1007/BF00248970
Su, X., Deng, L., Kong, K.F. and Tsang, J.S. (2013), "Enhanced degradation of haloacid by heterologous expression in related Burkholderia species", Biotechnology and Bioengineering, Vol. 110, No. 10, pp. 2687-2696. DOI: https://doi.org/10.1002/bit.24917
Su, X., Kong, K.-F. and Tsang, J.S.H. (2012), "Transports of acetate and haloacetate in Burkholderia species MBA4 are operated by distinct systems", BMC Microbiology, Vol. 12, No. 1, pp. 267.
Su, X. and Tsang, J.S. (2013), "Existence of a robust haloacid transport system in a Burkholderia species bacterium", Biochimica et Biophysica Acta, Vol. 1828, No. 2, pp. 187-192. DOI: https://doi.org/10.1016/j.bbamem.2012.09.017
Sun, L., Zeng, X., Yan, C., Sun, X., Gong, X., Rao, Y., et al. (2012), "Crystal structure of a bacterial homologue of glucose transporters GLUT1-4", Nature, Vol. 490, No. 7420, pp. 361-366. DOI: https://doi.org/10.1038/nature11524
Trott, O. and Olson, A.J. (2010), "AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization and multithreading", Journal of computational chemistry, Vol. 31, No. 2, pp. 455-461.
Tsang, J.S.H., Sallis, P.J., Bull, A.T. and Hardman, D.J. (1988), "A monobromoacetate dehalogenase from Pseudomonas cepacia MBA4", Archives of Microbiology, Vol. 150, No. 5, pp. 441-446. DOI: https://doi.org/10.1007/BF00422284
Tse, Y.M., Yu, M. and Tsang, J.S. (2009), "Topological analysis of a haloacid permease of a Burkholderia sp. bacterium with a PhoA-LacZ reporter", BMC Microbiology, Vol. 9, No., pp. 233.
van der Ploeg, J. and Janssen, D.B. (1995), "Sequence analysis of the upstream region of dhlB, the gene encoding haloalkanoic acid dehalogenase of Xanthobacter autotrophicus GJ10", Biodegradation, Vol. 6, No. 3, pp. 257-263. DOI: https://doi.org/10.1007/BF00700465
Voth Regier, A. and Ho Shing, P. (2007), "The Role of Halogen Bonding in Inhibitor Recognition and Binding by Protein Kinases", Current Topics in Medicinal Chemistry, Vol. 7, No. 14, pp. 1336-1348. DOI: https://doi.org/10.2174/156802607781696846
Wiederstein, M. and Sippl, M.J. (2007), "ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins", Nucleic Acids Research, Vol. 35, No. Web Server issue, pp. W407-W410.
Wilcken, R., Liu, X., Zimmermann, M.O., Rutherford, T.J., Fersht, A.R., Joerger, A.C., et al. (2012), "Halogen-Enriched Fragment Libraries as Leads for Drug Rescue of Mutant p53", Journal of the American Chemical Society, Vol. 134, No. 15, pp. 6810-6818. DOI: https://doi.org/10.1021/ja301056a
Yan, N. (2013), "Structural advances for the major facilitator superfamily (MFS) transporters", Trends in biochemical sciences, Vol. 38, No. 3, pp. 151-159. DOI: https://doi.org/10.1016/j.tibs.2013.01.003
Yin, Y., He, X., Szewczyk, P. and Chang, G. (2006), "Structure of the multidrug transporter EmrD from Escherichia coli", Journal of Science, Vol. 312, No. 5774, pp. 741-744.
Yu, M., Faan, Y.W., Chung, W.Y. and Tsang, J.S. (2007), "Isolation and characterization of a novel haloacid permease from Burkholderia cepacia MBA4", Applied Environmental Microbiology, Vol. 73, No. 15, pp. 4874-4880. DOI: https://doi.org/10.1128/AEM.00576-07
-- 0 --
Published
Issue
Section
License
How to Cite
