Effect of natural polymorphism on structure and function of the Yersinia pestis outer membrane porin F (OmpF protein): a computational study

References

• Achtman, M., Zurth, K., Morelli, G., Torrea, G., Guiyoule, A., & Carniel, E. (1999). Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proceedings of the National Academy of Sciences, 96, 14043–14048. doi:10.1073/pnas.96.24.14043
   PubMed Web of Science ®Google Scholar
• Alberti, S., Rodriquez-Quinones, F., Schirmer, T., Rummel, G., Tomas, J. M., Rosenbusch, J. P., & Benedi, V. J. (1995). A porin from Klebsiella pneumoniae: Sequence homology, three-dimensional model, and complement binding. Infection and Immunity, 63, 903–910.
   PubMed Web of Science ®Google Scholar
• Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25, 3389–3402. doi:10.1093/nar/25.17.3389
   PubMed Web of Science ®Google Scholar
• Balasubramaniam, D., Arockiasamy, A., Kumar, P. D., Sharma, A., & Krishnaswamy, S. (2012). Asymmetric pore occupancy in crystal structure of OmpF porin from Salmonella typhi. Journal of Structural Biology, 178, 233–244. doi:10.1016/j.jsb.2012.04.005
   PubMed Web of Science ®Google Scholar
• Benz, R., Jones, M. D., Younas, F., Maier, E., Modi, N., Mentele, R., … Smit, J. (2015). OmpW of Caulobacter crescentus functions as an outer membrane channel for cations. PLoS One, 10, e0143557. doi:10.1371/journal.pone.0143557
   PubMed Web of Science ®Google Scholar
• Brubaker, R. R. (1972). The genus Yersinia: Biochemistry and genetics of virulence. Current Topics in Microbiology and Immunology, 57, 111–158. doi:10.1007/978-3-642-65297-4_4
   PubMedGoogle Scholar
• Bürgi, J., Xue, B., Uversky, V. N., & van der Goot, F. G. (2016). Intrinsic disorder in transmembrane proteins: Roles in signaling and topology prediction. PLoS One, 11, e0158594. doi:10.1371/journal.pone.0158594
   PubMed Web of Science ®Google Scholar
• Campen, A., Williams, R. M., Brown, C. J., Meng, J., Uversky, V. N., & Dunker, A. K. (2008). TOP-IDP-scale: A new amino acid scale measuring propensity for intrinsic disorder. Protein & Peptide Letters, 15, 956–963. doi:10.2174/092986608785849164
   PubMed Web of Science ®Google Scholar
• Chain, P. S., Carniel, E., Larimer, F. W., Lamerdin, J., Stoutland, P. O., Regala, W. M., … Garcia, E. (2004). Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proceedings of the National Academy of Sciences, 101, 13826–13831. doi:10.1073/pnas.0404012101
   PubMed Web of Science ®Google Scholar
• Cowan, S. W., Schirmer, T., Rummel, G., Steiert, M., Ghosh, R., Pauptit, R. A., … Rosenbusch, J. P. (1992). Crystal structures explain functional properties of two E. coli porins. Nature, 358, 727–733. doi:10.1038/358727a0
   PubMed Web of Science ®Google Scholar
• Cui, Y., Yu, C., Yan, Y., Li, D., Li, Y., Jombart, T., … Yang, R. (2013). Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis. Proceedings of the National Academy of Sciences, 110, 577–582. doi:10.1073/pnas.1205750110
   PubMed Web of Science ®Google Scholar
• De Biasio, A., Guarnaccia, C., Popovic, M., Uversky, V. N., Pintar, A., & Pongor, S. (2008). Prevalence of intrinsic disorder in the intracellular region of human single-pass type I proteins: The case of the notch ligand delta-4. Journal of Proteome Research, 7, 2496–2506. doi:10.1021/pr800063u
   PubMed Web of Science ®Google Scholar
• Dosztanyi, Z., Csizmok, V., Tompa, P., & Simon, I. (2005). IUPred: Web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics, 21, 3433–3434. doi:10.1093/bioinformatics/bti541
   PubMed Web of Science ®Google Scholar
• Dosztanyi, Z., Meszaros, B., & Simon, I. (2009). ANCHOR: Web server for predicting protein binding regions in disordered proteins. Bioinformatics, 25, 2745–2746. doi:10.1093/bioinformatics/btp518
   PubMed Web of Science ®Google Scholar
• Dunker, A. K., Brown, C. J., Lawson, J. D., Iakoucheva, L. M., & Obradović, Z. (2002). Intrinsic disorder and protein function. Biochemistry, 41, 6573–6582. doi:10.1021/bi012159+
   PubMed Web of Science ®Google Scholar
• Dunker, A. K., Lawson, J. D., Brown, C. J., Williams, R. M., Romero, P., Oh, J. S., … Obradovic, Z. (2001). Intrinsically disordered protein. Journal of Molecular Graphics and Modelling, 19, 26–59. doi:10.1016/s1093-3263(00)00138-8
   PubMed Web of Science ®Google Scholar
• Dunker, A. K., & Obradovic, Z. (2001). The protein trinity – Linking function and disorder. Nature Biotechnology, 19, 805–806. doi:10.1038/Nbt0901-805
   PubMed Web of Science ®Google Scholar
• Dunker, A. K., Obradovic, Z., Romero, P., Garner, E. C., & Brown, C. J. (2000). Intrinsic protein disorder in complete genomes. Genome Inform Ser Workshop Genome Inform, 11, 161–171.
   PubMedGoogle Scholar
• Dunker, A. K., Silman, I., Uversky, V. N., & Sussman, J. L. (2008). Function and structure of inherently disordered proteins. Current Opinion in Structural Biology, 18, 756–764. doi:10.1016/j.sbi.2008.10.002
   PubMed Web of Science ®Google Scholar
• Dutzler, R., Rummel, G., Albertí, S., Hernández-Allés, S., Phale, P., Rosenbusch, J., … Schirmer, T. (1999). Crystal structure and functional characterization of OmpK36, the osmoporin of Klebsiella pneumoniae. Structure, 7, 425–434. doi:10.1016/S0969-2126(99)80055-0
   PubMed Web of Science ®Google Scholar
• Dyson, H. J., & Wright, P. E. (2002). Coupling of folding and binding for unstructured proteins. Current Opinion in Structural Biology, 12, 54–60. doi:10.1016/s0959-440x(02)00289-0
   PubMed Web of Science ®Google Scholar
• Dyson, H. J., & Wright, P. E. (2005). Intrinsically unstructured proteins and their functions. Nature Reviews Molecular Cell Biology, 6, 197–208. doi:10.1038/nrm1589
   PubMed Web of Science ®Google Scholar
• Fan, X., & Kurgan, L. (2014). Accurate prediction of disorder in protein chains with a comprehensive and empirically designed consensus. Journal of Biomolecular Structure and Dynamics, 32, 448–464. doi:10.1080/07391102.2013.775969
   PubMed Web of Science ®Google Scholar
• Galdiero, M., Vitiello, M., & Galdiero, S. (2003). Eukaryotic cell signaling and transcriptional activation induced by bacterial porins. FEMS Microbiology Letters, 226, 57–64. doi:10.1016/S0378-1097(03)00562-7
   PubMed Web of Science ®Google Scholar
• Ganguly, B., Tewari, K., & Singh, R. (2015). Homology modeling, functional annotation and comparative genomics of outer membrane protein H of Pasteurella multocida. Journal of Theoretical Biology, 386, 18–24. doi:10.1016/j.jtbi.2015.08.028
   PubMed Web of Science ®Google Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14, 33–38, 27–38. doi:10.1016/0263-7855(96)00018-5
   PubMed Web of Science ®Google Scholar
• Hutsul, J. A., & Worobec, E. (1997). Molecular characterization of the Serratia marcescens OmpF porin, and analysis of S. marcescens OmpF and OmpC osmoregulation. Microbiology, 143, 2797–2806. doi:10.1099/00221287-143-8-2797
   PubMed Web of Science ®Google Scholar
• Issaeva, M. P., Guzev, K. V., Novikova, O. D., Solovjeva, T. F., Degtyarev, S., & Rasskazov, V. A. (2003). Porin from Yersinia pseudotuberculosis: Cloning and analysis of primary structure. Advances in Experimental Medicine and Biology, 529, 257–260. doi:10.1007/0-306-48416-1_50
   PubMed Web of Science ®Google Scholar
• Jap, B. K., & Walian, P. J. (1996). Structure and functional mechanism of porins. Physiological Reviews, 76, 1073–1088.
   PubMed Web of Science ®Google Scholar
• Khomenko, V. A., Portniagina, O., Novikova, O. D., Isaeva, M. P., Kim, N., Likhatskaia, G. N., … Solov’eva, T. F. (2008). Isolation and characterization of recombinant OmpF-like porin from the Yersinia pseudotuberculosis outer membrane. Bioorganicheskaia Khimiia, 34, 177–184. doi:10.1134/s1068162008020040
   PubMed Web of Science ®Google Scholar
• Kislichkina, A. A., Bogun, A. G., Kadnikova, L. A., Maiskaya, N. V., Platonov, M. E., Anisimov, N. V. … Anisimov, A. P. (2015). Nineteen whole-genome assemblies of Yersinia pestis subsp. microtus, including representatives of Biovars caucasica, talassica, hissarica, altaica, xilingolensis, and ulegeica. Genome announcements, 3(6), e01342-15. doi:10.1128/genomeA.01342-15
   PubMedGoogle Scholar
• Koebnik, R., Locher, K. P., & Van Gelder, P. (2000). Structure and function of bacterial outer membrane proteins: Barrels in a nutshell. Molecular Microbiology, 37, 239–253. doi:10.1046/j.1365-2958.2000.01983.x
   PubMed Web of Science ®Google Scholar
• Krojer, T., Sawa, J., Schäfer, E., Saibil, H. R., Ehrmann, M., & Clausen, T. (2008). Structural basis for the regulated protease and chaperone function of DegP. Nature, 453, 885–890. doi:10.1038/nature07004
   PubMed Web of Science ®Google Scholar
• Likhatskaya, G. N., Solov’eva, T. F., Novikova, O. D., Issaeva, M. P., Gusev, K. V., Kryzhko, I. B., … Nurminski, E. A. (2005). Homology models of the Yersinia Pseudotuberculosis and Yersinia Pestis general porins and comparative analysis of their functional and antigenic regions. Journal of Biomolecular Structure and Dynamics, 23, 163–174. doi:10.1080/07391102.2005.10507056
   PubMed Web of Science ®Google Scholar
• Lou, H., Chen, M., Black, S. S., Bushell, S. R., Ceccarelli, M., Mach, T., & Naismith, J. H. (2011). Altered antibiotic transport in OmpC mutants isolated from a series of clinical strains of multi-drug resistant E. coli. PLoS One, 6, e25825. doi:10.1371/journal.pone.0025825
   PubMed Web of Science ®Google Scholar
• Luthra, A., Anand, A., Hawley, K. L., LeDoyt, M., La Vake, C. J., Caimano, M. J., … Radolf, J. D. (2015). A homology model reveals novel structural features and an immunodominant surface loop/opsonic target in the Treponema pallidum BamA Ortholog TP_0326. Journal of Bacteriology, 197, 1906–1920. doi:10.1128/JB.00086-15
   PubMed Web of Science ®Google Scholar
• Mészáros, B., Simon, I., & Dosztányi, Z. (2009). Prediction of protein binding regions in disordered proteins. PLoS Computational Biology, 5, e1000376. doi:10.1371/journal.pcbi.1000376
   PubMed Web of Science ®Google Scholar
• Mohan, A., Sullivan Jr, W. J., Radivojac, P., Dunker, A. K., & Uversky, V. N. (2008). Intrinsic disorder in pathogenic and non-pathogenic microbes: Discovering and analyzing the unfoldomes of early-branching eukaryotes. Molecular BioSystems, 4, 328–340. doi:10.1039/b719168e
   PubMed Web of Science ®Google Scholar
• Moraes, T. F., Bains, M., Hancock, R. E., & Strynadka, N. C. (2007). An arginine ladder in OprP mediates phosphate-specific transfer across the outer membrane. Nature Structural & Molecular Biology, 14, 85–87. doi:10.1038/nsmb1189
   PubMed Web of Science ®Google Scholar
• Nikaido, H. (2003). Molecular Basis of bacterial outer membrane permeability revisited. Microbiology and Molecular Biology Reviews, 67, 593–656. doi:10.1128/MMBR.67.4.593-656.2003
   PubMed Web of Science ®Google Scholar
• Niramitranon, J., Sansom, M. S., & Pongprayoon, P. (2016). Why do the outer membrane proteins OmpF from E. coli and OprP from P. aeruginosa prefer trimers? Simulation studies Journal of Molecular Graphics and Modelling, 65, 1–7. doi:10.1016/j.jmgm.2016.02.002
   PubMed Web of Science ®Google Scholar
• Novikov, O. D., Fedoreeva, L. I., Khomenko, V. A., Portniagina, O., Ermak, I. M., Likhatskaia, G. N., … Ovodov Iu, S. (1993). Effect of the method of extracting the pore-forming protein from Yersinia pseudotuberculosis on its macromolecular organization. Bioorganicheskaia Khimiia, 19, 536–547.
   PubMed Web of Science ®Google Scholar
• Obradovic, Z., Peng, K., Vucetic, S., Radivojac, P., & Dunker, A. K. (2005). Exploiting heterogeneous sequence properties improves prediction of protein disorder. Proteins: Structure, Function, and Bioinformatics, 61, 176–182. doi:10.1002/prot.20735
   PubMed Web of Science ®Google Scholar
• Oldfield, C. J., Cheng, Y., Cortese, M. S., Romero, P., Uversky, V. N., & Dunker, A. K. (2005). Coupled folding and binding with alpha-helix-forming molecular recognition elements. Biochemistry, 44, 12454–12470. doi:10.1021/bi050736e
   PubMed Web of Science ®Google Scholar
• Oldfield, C. J., & Dunker, A. K. (2014). Intrinsically disordered proteins and intrinsically disordered protein regions. Annual Review of Biochemistry, 83, 553–584. doi:10.1146/annurev-biochem-072711-164947
   PubMed Web of Science ®Google Scholar
• Parkhill, J., Wren, B. W., Thomson, N. R., Titball, R. W., Holden, M. T., Prentice, M. B., … Barrell, B. G. (2001). Genome sequence of Yersinia pestis, the causative agent of plague. Nature, 413, 523–527. doi:10.1038/35097083
   PubMed Web of Science ®Google Scholar
• Peng, K., Radivojac, P., Vucetic, S., Dunker, A. K., & Obradovic, Z. (2006). Length-dependent prediction of protein intrinsic disorder. BMC Bioinformatics, 7, 208. doi:10.1186/1471-2105-7-208
   PubMed Web of Science ®Google Scholar
• Peng, K., Vucetic, S., Radivojac, P., Brown, C. J., Dunker, A. K., & Obradovic, Z. (2005). Optimizing long intrinsic disorder predictors with protein evolutionary information. Journal of Bioinformatics and Computational Biology, 3, 35–60. doi:10.1142/s0219720005000886
   PubMedGoogle Scholar
• Peng, Z., Yan, J., Fan, X., Mizianty, M. J., Xue, B., Wang, K., … Kurgan, L. (2015). Exceptionally abundant exceptions: Comprehensive characterization of intrinsic disorder in all domains of life. Cellular and Molecular Life Sciences, 72, 137–151. doi:10.1007/s00018-014-1661-9
   PubMed Web of Science ®Google Scholar
• Peng, Z. L., & Kurgan, L. (2012). Comprehensive comparative assessment of in-silico predictors of disordered regions. Current Protein & Peptide Science, 13, 6–18. doi:10.2174/138920312799277938
   PubMed Web of Science ®Google Scholar
• Phale, P. S., Philippsen, A., Kiefhaber, T., Koebnik, R., Phale, V. P., Schirmer, T., & Rosenbusch, J. P. (1998). Stability of trimeric OmpF porin: The contributions of the latching loop L2. Biochemistry, 37, 15663–15670. doi:10.1021/bi981215c
   PubMed Web of Science ®Google Scholar
• Phale, P. S., Philippsen, A., Widmer, C., Phale, V. P., Rosenbusch, J. P., & Schirmer, T. (2001). Role of charged residues at the OmpF porin channel constriction probed by mutagenesis and simulation. Biochemistry, 40, 6319–6325. doi:10.1021/bi010046k
   PubMed Web of Science ®Google Scholar
• Platonov, M. E., Evseeva, V. V., Dentovskaya, S. V., & Anisimov, A. P. (2013). Molecular typing of Yersinia pestis. Molecular Genetics, Microbiology and Virology, 2013, 3–12. doi:10.3103/s0891416813020067
   Web of Science ®Google Scholar
• Prilusky, J., Felder, C. E., Zeev-Ben-Mordehai, T., Rydberg, E. H., Man, O., Beckmann, J. S., … Sussman, J. L. (2005). FoldIndex: A simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics, 21, 3435–3438. doi:10.1093/bioinformatics/bti537
   PubMed Web of Science ®Google Scholar
• Romero, P., Obradovic, Z., Li, X., Garner, E. C., Brown, C. J., & Dunker, A. K. (2001). Sequence complexity of disordered protein. Proteins: Structure, Function, and Genetics, 42, 38–48. doi:10.1002/1097-0134(20010101)42:1
   PubMed Web of Science ®Google Scholar
• Roy, A., Kucukural, A., & Zhang, Y. (2010). I-TASSER: A unified platform for automated protein structure and function prediction. Nature Protocols, 5, 725–738. doi:10.1038/nprot.2010.5
   PubMed Web of Science ®Google Scholar
• Schulz, G. E. (2005). The structures of general porins. In R. Benz (Ed.), Bacterial and Eukaryotic Porins, (pp. 25–40): Wiley-VCH Verlag GmbH & Co. KGaA.
   Google Scholar
• Shatsky, M., Nussinov, R., & Wolfson, H. J. (2004). A method for simultaneous alignment of multiple protein structures. Proteins: Structure, Function, and Bioinformatics, 56, 143–156. doi:10.1002/prot.10628
   PubMed Web of Science ®Google Scholar
• Sidorova, O. V., Isaeva, M. P., Khomenko, V. A., Portniagina, O., Likhatskaia, G. N., Kim, N., … Solov’eva, T. F. (2012). Yersinia pseudotuberculosis mutant OmpF porins with deletions of the external loops: Genetic constructions design, expression, isolation and refolding. Bioorganicheskaia Khimiia, 38, 156–165. doi:10.1134/s1068162012010189
   PubMed Web of Science ®Google Scholar
• Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W., … Higgins, D. G. (2011). Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology, 7, 539. doi:10.1038/msb.2011.75
   PubMed Web of Science ®Google Scholar
• Sigalov, A. B., Aivazian, D. A., Uversky, V. N., & Stern, L. J. (2006). Lipid-binding activity of intrinsically unstructured cytoplasmic domains of multichain immune recognition receptor signaling subunits. Biochemistry, 45, 15731–15739. doi:10.1021/bi061108f
   PubMed Web of Science ®Google Scholar
• Skurnik, M., Peippo, A., & Ervela, E. (2000). Characterization of the O-antigen gene clusters of Yersinia pseudotuberculosis and the cryptic O-antigen gene cluster of Yersinia pestis shows that the plague bacillus is most closely related to and has evolved from Y. pseudotuberculosis serotype O:1b. Molecular Microbiology, 37, 316–330. doi:mmi1993[pii]
   PubMed Web of Science ®Google Scholar
• Solov’eva, T. F., Likhatskaya, G. N., Khomenko, V. A., Stenkova, A. M., Kim, N. Y., Portnyagina, O. Y., … Isaeva, M. P. (2011). A novel OmpY porin from Yersinia pseudotuberculosis: Structure, channel-forming activity and trimer thermal stability. Journal of Biomolecular Structure and Dynamics, 28, 517–533. doi:10.1080/07391102.2011.10508592
   PubMed Web of Science ®Google Scholar
• Tompa, P. (2002). Intrinsically unstructured proteins. Trends in Biochemical Sciences, 27, 527–533. doi:10.1016/s0968-0004(02)02169-2
   PubMed Web of Science ®Google Scholar
• Tompa, P. (2003). The functional benefits of protein disorder. Journal of Molecular Structure: THEOCHEM, 666–667, 361–371. doi:10.1016/j.theochem.2003.08.047
   Web of Science ®Google Scholar
• Tompa, P. (2012). Intrinsically disordered proteins: A 10-year recap. Trends in Biochemical Sciences, 37, 509–516. doi:10.1016/j.tibs.2012.08.004
   PubMed Web of Science ®Google Scholar
• Turoverov, K. K., Kuznetsova, I. M., & Uversky, V. N. (2010). The protein kingdom extended: Ordered and intrinsically disordered proteins, their folding, supramolecular complex formation, and aggregation. Progress in Biophysics and Molecular Biology, 102, 73–84. doi:10.1016/j.pbiomolbio.2010.01.003
   PubMed Web of Science ®Google Scholar
• Uversky, V. N. (2013). Unusual biophysics of intrinsically disordered proteins. Biochimica et Biophysica Acta (BBA) – Proteins and Proteomics, 1834, 932–951. doi:10.1016/j.bbapap.2012.12.008
   PubMed Web of Science ®Google Scholar
• Uversky, V. N., Davé, V., Iakoucheva, L. M., Malaney, P., Metallo, S. J., Pathak, R. R., & Joerger, A. C. (2014). Pathological unfoldomics of uncontrolled chaos: Intrinsically disordered proteins and human diseases. Chemical Reviews, 114, 6844–6879. doi:10.1021/cr400713r
   PubMed Web of Science ®Google Scholar
• Uversky, V. N., & Dunker, A. K. (2010). Understanding protein non-folding. Biochimica et Biophysica Acta (BBA) – Proteins and Proteomics, 1804, 1231–1264. doi:10.1016/j.bbapap.2010.01.017
   PubMed Web of Science ®Google Scholar
• Uversky, V. N., Gillespie, J. R., & Fink, A. L. (2000). Why are “natively unfolded” proteins unstructured under physiologic conditions? Proteins: Structure, Function, and Genetics, 41, 415–427. doi:10.1002/1097-0134(20001115)41:3<415:aid-prot130>3.0.co;2-7
   PubMed Web of Science ®Google Scholar
• Uversky, V. N., Oldfield, C. J., & Dunker, A. K. (2008). Intrinsically disordered proteins in human diseases: Introducing the D2 concept. Annual Review of Biophysics, 37, 215–246. doi:10.1146/annurev.biophys.37.032807.125924
   PubMed Web of Science ®Google Scholar
• Vakorina, T. I., Novikova, O. D., Krasikova, I. N., Naberezhnykh, G. N., Solov’eva, T. F., & Ovodov, Y. S. (2003). Interaction of porin from Yersinia pseudotuberculosis with different structural forms of endogenous lipopolysaccharide. Biochemistry (Moscow), 68, 976–983.10.1023/A:1026056411472
   PubMed Web of Science ®Google Scholar
• van den Berg, B. (2012). Structural basis for outer membrane sugar uptake in Pseudomonads. Journal of Biological Chemistry, 287, 41044–41052. doi:10.1074/jbc.M112.408518
   PubMed Web of Science ®Google Scholar
• van der Lee, R., Buljan, M., Lang, B., Weatheritt, R. J., Daughdrill, G. W., Dunker, A. K., … Babu, M. M. (2014). Classification of intrinsically disordered regions and proteins. Chemical Reviews, 114, 6589–6631. doi:10.1021/cr400525m
   PubMed Web of Science ®Google Scholar
• Ward, J. J., Sodhi, J. S., McGuffin, L. J., Buxton, B. F., & Jones, D. T. (2004). Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. Journal of Molecular Biology, 337, 635–645. doi:10.1016/j.jmb.2004.02.002
   PubMed Web of Science ®Google Scholar
• Wright, P. E., & Dyson, H. J. (1999). Intrinsically unstructured proteins: Re-assessing the protein structure-function paradigm. Journal of Molecular Biology, 293, 321–331. doi:10.1006/jmbi.1999.3110
   PubMed Web of Science ®Google Scholar
• Wu, S., & Zhang, Y. (2007). LOMETS: A local meta-threading-server for protein structure prediction. Nucleic Acids Research, 35, 3375–3382. doi:10.1093/nar/gkm251
   PubMed Web of Science ®Google Scholar
• Xu, D., & Zhang, Y. (2011). Improving the physical realism and structural accuracy of protein models by a two-step atomic-level energy minimization. Biophysical Journal, 101, 2525–2534. doi:10.1016/j.bpj.2011.10.024
   PubMed Web of Science ®Google Scholar
• Xue, B., Dunbrack, R. L., Williams, R. W., Dunker, A. K., & Uversky, V. N. (2010). PONDR-FIT: A meta-predictor of intrinsically disordered amino acids. Biochimica et Biophysica Acta (BBA) – Proteins and Proteomics, 1804, 996–1010. doi:10.1016/j.bbapap.2010.01.011
   PubMed Web of Science ®Google Scholar
• Xue, B., Dunker, A. K., & Uversky, V. N. (2012). Orderly order in protein intrinsic disorder distribution: Disorder in 3500 proteomes from viruses and the three domains of life. Journal of Biomolecular Structure & Dynamics, 30, 137–149. doi:10.1080/07391102.2012.675145
   PubMed Web of Science ®Google Scholar
• Xue, B., Li, L., Meroueh, S. O., Uversky, V. N., & Dunker, A. K. (2009). Analysis of structured and intrinsically disordered regions of transmembrane proteins. Molecular BioSystems, 5, 1688–1702. doi:10.1039/B905913J
   PubMed Web of Science ®Google Scholar
• Yang, J., Yan, R., Roy, A., Xu, D., Poisson, J., & Zhang, Y. (2015). The I-TASSER suite: Protein structure and function prediction. Nature Methods, 12, 7–8. doi:10.1038/nmeth.3213
   PubMed Web of Science ®Google Scholar
• Yang, J., & Zhang, Y. (2015a). I-TASSER server: New development for protein structure and function predictions. Nucleic Acids Research, 43, W174–W181. doi:10.1093/nar/gkv342
   PubMed Web of Science ®Google Scholar
• Yang, J., & Zhang, Y. (2015b). Protein structure and function prediction using I-TASSER. Current Protocols in Bioinformatics, 52, 5.8.1–5.8.15. doi:10.1002/0471250953.bi0508s52
   PubMedGoogle Scholar
• Zachariae, U., Klühspies, T., De, S., Engelhardt, H., & Zeth, K. (2006). High resolution crystal structures and molecular dynamics studies reveal substrate binding in the porin Omp32. Journal of Biological Chemistry, 281, 7413–7420. doi:10.1074/jbc.M510939200
   PubMed Web of Science ®Google Scholar
• Zhang, Y. (2008). I-TASSER server for protein 3D structure prediction. BMC Bioinformatics, 9, 40. doi:10.1186/1471-2105-9-40
   PubMed Web of Science ®Google Scholar
• Zhang, J., Liang, Y., & Zhang, Y. (2011). Atomic-level protein structure refinement using fragment-guided molecular dynamics conformation sampling. Structure, 19, 1784–1795. doi:10.1016/j.str.2011.09.022
   PubMed Web of Science ®Google Scholar
• Zhang, Y., & Skolnick, J. (2004). SPICKER: A clustering approach to identify near-native protein folds. Journal of Computational Chemistry, 25, 865–871. doi:10.1002/jcc.20011
   PubMed Web of Science ®Google Scholar