173
Views
2
CrossRef citations to date
0
Altmetric
Research Article

Molecular modeling and dynamic simulations of agglutinin-like family members from Candida albicans: New insights into potential targets for the treatment of candidiasis

, , , &
Pages 4352-4365 | Received 23 Feb 2017, Accepted 30 Nov 2017, Published online: 04 Jan 2018

References

  • Ahmad, M. F., Yadav, B., Kumar, P., Puri, A., Mazumder, M., Ali, A., … Komath, S. S. (2012). The GPI anchor signal sequence dictates the folding and functionality of the Als5 adhesin from Candida albicans. PLoS One, 7(4), e35305.10.1371/journal.pone.0035305
  • Almeida, R. S., Brunke, S., Albrecht, A., Thewes, S., Laue, M., Edwards, J. E., … Hube, B. (2008). The hyphal-associated adhesin and invasin Als3 of Candida albicans mediates iron acquisition from host ferritin. PLoS Pathogens, 4(11), e1000217.10.1371/journal.ppat.1000217
  • Alsteens, D., Beaussart, A., Derclaye, S., El-Kirat-Chatel, S., Park, H. R., Lipke, P. N., & Dufrêne, Y. F. (2013). Single-cell force spectroscopy of Als-mediated fungal adhesion. Analytical Methods, 5(15), 3657–3662.10.1039/c3ay40473 k
  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.10.1016/S0022-2836(05)80360-2
  • Alves, C. T., Wei, X. Q., Silva, S., Azeredo, J., Henriques, M., & Williams, D. W. (2014). Candida albicans promotes invasion and colonisation of Candida glabrata in a reconstituted human vaginal epithelium. Journal of Infection, 69(4), 396–407.10.1016/j.jinf.2014.06.002
  • Arfken, G. (1985). The Method of Steepest Descents. In Mathematical Methods for Physicists (3rd ed., pp. 428–436). Orlando, FL: Academic Press.
  • Bamford, C. V., Nobbs, A. H., Barbour, M. E., Lamont, R. J., & Jenkinson, H. F. (2015). Functional regions of Candida albicans hyphal cell wall protein Als3 that determine interaction with the oral bacterium Streptococcus gordonii. Microbiology, 161(1), 18–29.10.1099/mic.0.083378-0
  • Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., & Haak, J. R. (1984). Molecular dynamics with coupling to an external bath. The Journal of Chemical Physics, 81, 3684.10.1063/1.448118
  • Bois, M., Singh, S., Samlalsingh, A., Lipke, P. N., & Garcia, M. C. (2013). Does Candida albicans Als5p amyloid play a role in commensalism in Caenorhabditis elegans? Eukaryotic Cell, 12(5), 703–711.10.1128/EC.00020-13
  • Chan, C. X. J., & Lipke, P. N. (2014). Role of force-sensitive amyloid-like interactions in fungal catch bonding and biofilms. Eukaryotic Cell, 13(9), 1136–1142.10.1128/EC.00068-14
  • Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T. J., Higgins, D. G., & Thompson, J. D. (2003). Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Research, 31, 3497–3500.10.1093/nar/gkg500
  • Coleman, D. A., Oh, S.-H., Zhao, X., Zhao, H., Hutchins, J. T., Vernachio, J. H., … Hoyer, L. L. (2009). Monoclonal antibodies specific for Candida albicans Als3 that immunolabel fungal cells in vitro and in vivo and block adhesion to host surfaces. Journal of Microbiological Methods, 78(1), 71–78.10.1016/j.mimet.2009.05.002
  • Cota, E., & Hoyer, L. L. (2015). The Candida albicans agglutinin-like sequence family of adhesins: Functional insights gained from structural analysis. Future Microbiology, 10, 1635–1548.10.2217/fmb.15.79
  • Darden, T., York, D., & Pedersen, L. (1993). Particle Mesh Ewald: An N log(N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98, 10089–10092.10.1063/1.464397
  • De Bernardis, F., Arancia, S., Sandini, S., Graziani, S., & Norelli, S. (2015). Studies of Immune Responses in Candida vaginitis. Pathogens, 4(4), 697–707.10.3390/pathogens4040697
  • Dominguez, C., Boelens, R., & Bonvin, A. (2003). HADDOCK: A protein-protein docking approach based on biochemical and/or biophysical information. Journal of the American Chemical Society, 125, 1731–1737.10.1021/ja026939x
  • Donohue, D. S., Ielasi, F. S., Goossens, K. V., & Willaert, R. G. (2011). The N-terminal part of Als1 protein from Candida albicans specifically binds fucose-containing glycans. Molecular Microbiology, 80(6), 1667–1679.10.1111/mmi.2011.80.issue-6
  • Dranginis, A. M., Rauceo, J. M., Coronado, J. E., & Lipke, P. N. (2007). A biochemical guide to yeast adhesins: Glycoproteins for social and antisocial occasions. Microbiology and Molecular Biology Reviews, 71(2), 282–294.10.1128/MMBR.00037-06
  • Ewald, P. P. (1921). Die Berechnung Optischer und Elektrostatischer Gitterpotentiale [Evaluation of optical and electrostatic lattice potentials]. Annalen der Physik, 369, 253–287.10.1002/(ISSN)1521-3889
  • Fiser, A., Do, R. K., & Šali, A. (2000). Modeling of loops in protein structures. Protein Science, 9, 1753–1773.10.1110/(ISSN)1469-896X
  • Frank, A., Ramsook, C., Otoo, H., Tan, C., Soybelman, G., Rauceo, J., … Lipke, P. (2010). Structure and function of glycosylated tandem repeats from Candida albicans Als Adhesins. Eukaryotic Cell, 9(3), 405–414.10.1128/EC.00235-09
  • Garcia, M., Lipke, P., & Klotz, S. (2013). Pathogenic microbial amyloids: Their function and the host response. OA Microbiol, 1(1), 2.
  • Garcia-Sherman, M. C., Lysak, N., Filonenko, A., Richards, H., Sobonya, R. E., Klotz, S. A., & Lipke, P. N. (2014). Peptide detection of fungal functional amyloids in infected tissue. PLoS One, 9(1), e86067. 10.1371/journal.pone.0086067
  • Gaur, N. K., Klotz, S. A., & Henderson, R. L. (1999). Overexpression of the Candida albicans ALA1 gene in Saccharomyces cerevisiae results in aggregation following attachment of yeast cells to extracellular matrix proteins, adherence properties similar to those of Candida albicans. Infect. Immun, 67, 6040–6047.
  • Gaur, N. K., Smith, R. L., & Klotz, S. A. (2002). Candida albicans and Saccharomyces cerevisiae Expressing ALA1/ALS5 Adhere to Accessible Threonine, Serine, or Alanine Patches. Cell Communication & Adhesion, 9(1), 45–57.10.1080/15419060212187
  • Guex, N., Peitsch, M. C., & Schwede, T. (2009). Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: A historical perspective. Electrophoresis, 30, S162–S173.10.1002/elps.v30.10s
  • Hatters, D. M., MacRaild, C. A., Daniels, R., Gosal, W. S., Thomson, N. H., Jones, J. A., … Howlett, G. J. (2003). The circularization of amyloid fibrils formed by apolipoprotein C-II. Biophysical Journal, 85(6), 3979–3990.10.1016/S0006-3495(03)74812-7
  • Hoyer, L. L., & Hecht, J. E. (2001). TheALS5 gene of Candida albicans and analysis of the Als5p N-terminal domain. Yeast, 18(1), 49–60.10.1002/(ISSN)1097-0061
  • Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38.10.1016/0263-7855(96)00018-5
  • Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of simple potential functions for simulating liquid water. The Journal of Chemical Physics, 79, 926–935.10.1063/1.445869
  • Klotz, S. A., Gaur, N. K., De Armond, R., Sheppard, D., Khardori, N., Edwards, J. E., … El-Azizi, M. (2007). Candida albicans Als proteins mediate aggregation with bacteria and yeasts. Medical Mycology, 45(4), 363–370.10.1080/13693780701299333
  • Klotz, S. A., Gaur, N. K., Lake, D. F., Chan, V., Rauceo, J., & Lipke, P. N. (2004). Degenerate peptide recognition by Candida albicans adhesins Als5p and Als1p. Infection and Immunity, 72(4), 2029–2034.10.1128/IAI.72.4.2029-2034.2004
  • Klotz, S. A., & Smith, R. L. (1991). A fibronectin receptor on Candida albicans mediates adherence of the fungus to extracellular matrix. Journal of Infectious Diseases, 163(3), 604–610.10.1093/infdis/163.3.604
  • Klotz, S. A., Smith, R. L., & Stewart, B. W. (1992). Effect of an arginine-glycine-aspartic acid-containing peptide on hematogenous candidal infections in rabbits. Antimicrobial Agents and Chemotherapy, 36(1), 132–136.10.1128/AAC.36.1.132
  • Kravchuk, V. O., Savytskyi, O. V., Odynets, K. O., Mykuliak, V. V., & Kornelyuk, A. I. (2016). Computational modeling and molecular dynamics simulations of mammalian cytoplasmic tyrosyl-tRNA synthetase and its complexes with substrates. Journal of Biomolecular Structure and Dynamics, 28, 1–17.
  • Kumar, R., Saraswat, D., Tati, S., & Edgerton, M. (2015). Novel aggregation properties of Candida albicans secreted aspartyl proteinase Sap6 mediate virulence in oral candidiasis. Infection and Immunity, 83(7), 2614–2626.10.1128/IAI.00282-15
  • Laskowski, R. A., MacArthur, M. W., Moss, D. S., & Thornton, J. M. (1993). PROCHECK: A program to check the stereochemical quality of protein structures. Journal of Applied Crystallography, 26, 283–291.10.1107/S0021889892009944
  • Le Guilloux, V., Schmidtke, P., & Tuffery, P. (2009). Fpocket: An open source platform for ligand pocket detection. BMC Bioinformatics, 10, 168.10.1186/1471-2105-10-168
  • Lin, J., Oh, S.-H., Jones, R., Garnett, J. A., Salgado, P. S., Rusnakova, S., … Cota, E. (2014). The peptide-binding cavity is essential for Als3-mediated adhesion of Candida albicans to human cells. Journal of Biological Chemistry, 289(26), 18401–18412.10.1074/jbc.M114.547877
  • Lipke, P. N., Garcia, M. C., Alsteens, D., Ramsook, C. B., Klotz, S. A., & Dufrêne, Y. F. (2012). Strengthening relationships: Amyloids create adhesion nanodomains in yeasts. Trends in Microbiology, 20(2), 59–65.10.1016/j.tim.2011.10.002
  • Liu, Y., & Filler, S. G. (2011). Candida albicans Als3, a multifunctional adhesin and invasin. Eukaryotic Cell, 10(2), 168–173.10.1128/EC.00279-10
  • Lugo, M. R., & Merrill, A. R. (2015). Pocket analysis of the full-length cholix toxin. An assessment of the structure-dynamics of the apo catalytic domain. Journal of Biomolecular Structure and Dynamics, 33(11), 2452–2468.10.1080/07391102.2014.1000972
  • Magrane, M. (2011). UniProt knowledgebase: A hub of integrated protein data. Database (Oxford), 29(2011), bar009.
  • Marques, J. V., Oliveira, A., Raggi, L. R., Young, M. C., & Kato, J. (2010). Antifungal activity of natural and synthetic amides from Piper species. Journal of the Brazilian Chemical Society, 21(10), 1807–1813.10.1590/S0103-50532010001000003
  • Murciano, C., Moyes, D. L., Runglall, M., Tobouti, P., & Islam, A. (2012). Evaluation of the role of Candida albicans agglutinin-like sequence (Als) proteins in human oral epithelial cell interactions. PLoS One, 7(3), e33362.10.1371/journal.pone.0033362
  • Nobbs, A. H., Vickerman, M. M., & Jenkinson, H. F. (2010). Heterologous expression of Candida albicans cell wall-associated adhesins in Saccharomyces cerevisiae Reveals differential specificities in adherence and biofilm formation and in binding oral Streptococcus gordonii. Eukaryotic Cell, 9(10), 1622–1634.10.1128/EC.00103-10
  • Otoo, H. N., Lee, K. G., Qiu, W., & Lipke, P. N. (2008). Candida albicans Als adhesins have conserved amyloid-forming sequences. Eukaryotic Cell, 7(5), 776–782.10.1128/EC.00309-07
  • Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera–A visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612.10.1002/(ISSN)1096-987X
  • Phan, Q. T., Myers, C. L., Fu, Y., Sheppard, D. C., Yeaman, M. R., Welch, W. H., … Filler, S. G. (2007). Als3 Is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biology, 5(3), e64.10.1371/journal.pbio.0050064
  • Ramachandran, G. N., Ramakrishnan, C., & Sasisekharan, V. (1963). Stereochemistry of polypeptide chain configurations. Journal of Molecular Biology, 7, 95–99.10.1016/S0022-2836(63)80023-6
  • Ramsook, C. B., Tan, C., Garcia, M. C., Fung, R., Soybelman, G., Henry, R., … Lipke, P. N. (2010). Yeast cell adhesion molecules have functional amyloid-forming sequences. Eukaryotic Cell, 9(3), 393–404.10.1128/EC.00068-09
  • Rauceo, J., Armond, R., Otoo, H., Kahn, P., Klotz, S., Gaur, N., & Lipke, P. (2006). Threonine-rich repeats increase fibronectin binding in the Candida albicans Adhesin Als5p. Eukaryotic Cell, 5(10), 1664–1673.10.1128/EC.00120-06
  • Ruhnke, M. (2014). Antifungal stewardship in invasive Candida infections. Clinical Microbiology and Infection, 20, 11–18.10.1111/1469-0691.12622
  • Salgado, P. S., Yan, R., Taylor, J. D., Burchell, L., Jones, R., Hoyer, L. L., … Cota, E. (2011). Structural basis for the broad specificity to host-cell ligands by the pathogenic fungus Candida albicans. Proceedings of the National Academy of Sciences, 108(38), 15775–15779.10.1073/pnas.1103496108
  • Šali, A., & Blundell, T. L. (1993). Comparative protein modelling by satisfaction of spatial restraints. Journal of Molecular Biology, 234, 779–815.10.1006/jmbi.1993.1626
  • Sawyer, R. T., Garner, R. E., & Hudson, J. A. (1992). Arg-Gly-Asp (RGD) peptides alter hepatic killing of Candida albicans in the isolated perfused mouse liver model. Infect Immun, 60(1), 213–218.
  • Schmidtke, P., Bidon-Chanal, A., Luque, F. J., & Barril, X. (2011). MDpocket: Open-source cavity detection and characterization on molecular dynamics trajectories. Bioinformatics, 27(23), 3276–3285.10.1093/bioinformatics/btr550
  • Schmidtke, P., Le Guilloux, V., Maupetit, J., & Tufféry, P. (2010). Fpocket: Online tools for protein ensemble pocket detection and tracking. Nucleic Acids Research, 38(Suppl_2), W582–W589.10.1093/nar/gkq383
  • Shao, J., Wang, T., Yan, Y., Shi, G., Cheng, H., Wu, D., & Wang, C. (2014). Matrine reduces yeast-to-hypha transition and resistance of a fluconazole-resistant strain of Candida albicans. Journal of Applied Microbiology, 117(3), 618–626.10.1111/jam.2014.117.issue-3
  • Sheppard, D. C., Yeaman, M. R., Welch, W. H., Phan, Q. T., Fu, Y.; Ibrahim, A. S., … Edwards, J. E. (2004). Functional and structural diversity in the Als protein family of Candida albicans. Journal of Biological Chemistry, 279; (29), 30480–30489.10.1074/jbc.M401929200
  • Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680.10.1093/nar/22.22.4673
  • Tripathi, H., Luqman, S., Meena, A., & Khan, F. (2014). Genomic identification of potential targets unique to Candida albicans for the discovery of antifungal agents. Current Drug Targets, 15(1), 136–149.10.2174/138945011501140115112242
  • Uniprot Consortium. (2015). UniProt: A hub for protein information. Nucleic Acids Research, 43(D1), D204–D212
  • Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. (2005). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 26(16), 1701–1718.10.1002/(ISSN)1096-987X
  • van Zundert, G. C. P., Rodrigues, J., Trellet, M., Schmitz, C., Kastritis, P., Karaca, E., … Bonvin, A. (2016). The HADDOCK2.2 webserver: User-friendly integrative modeling of biomolecular complexes. Journal of Molecular Biology, 428, 720–725.10.1016/j.jmb.2015.09.014
  • Wu, H., Downs, D., Ghosh, K., Ghosh, A. K., Staib, P., Monod, M., & Tang, J. (2013). Candida albicans secreted aspartic proteases 4-6 induce apoptosis of epithelial cells by a novel Trojan horse mechanism. The FASEB Journal, 27(6), 2132–2144.10.1096/fj.12-214353
  • Zhao, X., Oh, S.-H., Jajko, R., Diekema, D. J., Pfaller, M. A., Pujol, C., … Hoyer, L. L. (2007). Analysis of ALS5 and ALS6 allelic variability in a geographically diverse collection of Candida albicans isolates. Fungal Genetics and Biology, 44(12), 1298–1309.10.1016/j.fgb.2007.05.004
  • Zhao, X., Pujol, C., Soll, D. R., & Hoyer, L. L. (2003). Allelic variation in the contiguous loci encoding Candida albicans ALS5, ALS1 and ALS9. Microbiology, 149(10), 2947–2960.10.1099/mic.0.26495-0
  • Zhu, W., Phan, Q. T., Boontheung, P., Solis, N. V., Loo, J. A., & Filler, S. J. (2012). EGFR and HER2 receptor kinase signaling mediate epithelial cell invasion by Candida albicans during oropharyngeal infection. Proceedings of the National Academy of Sciences, 109(35), 14194–14199.10.1073/pnas.1117676109

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.