Automatically Fixing Errors in Glycoprotein Structures with Rosetta

Structure

Volumn 27, Issue 1, 2019, Pages 134-139.e3

  Frenz, Brandon ^a   Rämisch, Sebastian ^b   Borst, Andrew J ^a   Walls, Alexandra C ^a   Adolf Bryfogle, Jared ^b   Schief, William R ^b   Veesler, David ^a   DiMaio, Frank ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

cryoEM; glycans; glycoproteins; refinement

Indexed keywords

GLYCAN; IMMUNOGLOBULIN G1; VIRUS GLYCOPROTEIN; VIRUS SPIKE PROTEIN; GLYCOPROTEIN; VIRAL PROTEIN;

ARTICLE; AUTOMATION; CARBOHYDRATE ANALYSIS; COMPARATIVE STUDY; CONFORMATIONAL TRANSITION; CONJUGATE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; DATA ANALYSIS SOFTWARE; HUMAN; HUMAN CORONAVIRUS NL63; HUMORAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DETERMINATION; PROTEIN STRUCTURE; ROSETTA BASED APPROACH; VIRUS ENVELOPE; X RAY CRYSTALLOGRAPHY; CHEMISTRY; HUMAN IMMUNODEFICIENCY VIRUS; MOLECULAR DYNAMICS; PROCEDURES; SOFTWARE;

CORONAVIRUS NL63, HUMAN; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; GLYCOPROTEINS; HIV; MOLECULAR DYNAMICS SIMULATION; SOFTWARE; VIRAL PROTEINS;

EID: 85059499661     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2018.09.006     Document Type: Article

References (38)

1. Agirre, J., Strategies for carbohydrate model building, refinement and validation. Acta Crystallogr. D Struct. Biol. 73 (2017), 171–186.
2. Agirre, J., Davies, G., Wilson, K., Cowtan, K., Carbohydrate anomalies in the PDB. Nat. Chem. Biol., 11, 2015, 303.
3. Agirre, J., Iglesias-Fernández, J., Rovira, C., Davies, G.J., Wilson, K.S., Cowtan, K.D., Privateer: software for the conformational validation of carbohydrate structures. Nat. Struct. Mol. Biol. 22 (2015), 833–834.
4. Agirre, J., Davies, G.J., Wilson, K.S., Cowtan, K.D., Carbohydrate structure: the rocky road to automation. Curr. Opin. Struct. Biol. 44 (2017), 39–47.
5. Astronomo, R.D., Burton, D.R., Carbohydrate vaccines: developing sweet solutions to sticky situations?. Nat. Rev. Drug Discov. 9 (2010), 308–324.
6. Cingolani, G., Panella, A., Perrone, M.G., Vitale, P., Di Mauro, G., Fortuna, C.G., Armen, R.S., Ferorelli, S., Smith, W.L., Scilimati, A., Structural basis for selective inhibition of Cyclooxygenase-1 (COX-1) by diarylisoxazoles mofezolac and 3-(5-chlorofuran-2-yl)-5-methyl-4-phenylisoxazole (P6). Eur. J. Med. Chem. 138 (2017), 661–668.
7. Conway, P., Tyka, M.D., DiMaio, F., Konerding, D.E., Baker, D., Relaxation of backbone bond geometry improves protein energy landscape modeling. Protein Sci. 23 (2014), 47–55.
8. Derewenda, Z., The use of recombinant methods and molecular engineering in protein crystallization. Methods 34 (2004), 354–363.
9. DiMaio, F., Echols, N., Headd, J.J., Terwilliger, T.C., Adams, P.D., Baker, D., Improved low-resolution crystallographic refinement with Phenix and Rosetta. Nat. Methods 10 (2013), 1102–1104.
10. DiMaio, F., Song, Y., Li, X., Brunner, M.J., Xu, C., Conticello, V., Egelman, E., Marlovits, T., Cheng, Y., Baker, D., Atomic-accuracy models from 4.5-Å cryo-electron microscopy data with density-guided iterative local refinement. Nat. Methods 12 (2015), 361–365.
11. Emsley, P., Cowtan, K., Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004), 2126–2132.
12. Favuzza, P., Guffart, E., Tamborrini, M., Scherer, B., Dreyer, A.M., Rufer, A.C., Erny, J., Hoernschemeyer, J., Thoma, R., Schmid, G., et al. Structure of the malaria vaccine candidate antigen CyRPA and its complex with a parasite invasion inhibitory antibody. Elife, 6, 2017, 10.7554/eLife.20383.
13. Fleishman, S.J., Leaver-Fay, A., Corn, J.E., Strauch, E.-M., Khare, S.D., Koga, N., Ashworth, J., Murphy, P., Richter, F., Lemmon, G., et al. RosettaScripts: a scripting language interface to the Rosetta macromolecular modeling suite. PLoS One, 6, 2011, e20161.
14. French, A.D., Dowd, M.K., Analysis of the ring-form tautomers of psicose with MM3(92). J. Comput. Chem. 15 (1994), 561–570.
15. Frenz, B., Walls, A.C., Egelman, E.H., Veesler, D., DiMaio, F., RosettaES: a sampling strategy enabling automated interpretation of difficult cryo-EM maps. Nat. Methods 14 (2017), 797–800.
16. Goepfert, A., Lehmann, S., Wirth, E., Rondeau, J.-M., The human IL-17A/F heterodimer: a two-faced cytokine with unique receptor recognition properties. Sci. Rep., 7, 2017, 8906.
17. Gorelik, A., Randriamihaja, A., Illes, K., Nagar, B., A key tyrosine substitution restricts nucleotide hydrolysis by the ectoenzyme NPP5. FEBS J. 284 (2017), 3718–3726.
18. Gristick, H.B., Wang, H., Bjorkman, P.J., X-ray and EM structures of a natively glycosylated HIV-1 envelope trimer. Acta Crystallogr. D Struct. Biol. 73 (2017), 822–828.
19. Joosten, R.P., te Beek, T.A.H., Krieger, E., Hekkelman, M.L., Hooft, R.W.W., Schneider, R., Sander, C., Vriend, G., A series of PDB related databases for everyday needs. Nucleic Acids Res. 39 (2011), D411–D419.
20. Kanai, R., Kar, K., Anthony, K., Gould, L.H., Ledizet, M., Fikrig, E., Marasco, W.A., Koski, R.A., Modis, Y., Crystal structure of West Nile virus envelope glycoprotein reveals viral surface epitopes. J. Virol. 80 (2006), 11000–11008.
21. Labonte, J.W., Adolf-Bryfogle, J., Schief, W.R., Gray, J.J., Residue-centric modeling and design of saccharide and glycoconjugate structures. J. Comput. Chem. 38 (2017), 276–287.
22. Liebschner, D., Afonine, P.V., Moriarty, N.W., Poon, B.K., Sobolev, O.V., Terwilliger, T.C., Adams, P.D., Polder maps: improving OMIT maps by excluding bulk solvent. Acta Crystallogr. D Struct. Biol. 73 (2017), 148–157.
23. Lin, C.C., Wu, B.S., Wu, W.G., 5GZ5: crystal structure of snake venom phosphodiesterase (PDE) from Taiwan cobra (Naja atra atra) in complex with AMP. https://www.ncbi.nlm.nih.gov/Structure/pdb/5GZ5, 2017.
24. Lobner, E., Humm, A.-S., Mlynek, G., Kubinger, K., Kitzmüller, M., Traxlmayr, M.W., Djinović-Carugo, K., Obinger, C., Two-faced Fcab prevents polymerization with VEGF and reveals thermodynamics and the 2.15 Å crystal structure of the complex. MAbs 9 (2017), 1088–1104.
25. Lyumkis, D., Julien, J.-P., de Val, N., Cupo, A., Potter, C.S., Klasse, P.-J., Burton, D.R., Sanders, R.W., Moore, J.P., Carragher, B., et al. Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer. Science 342 (2013), 1484–1490.
26. Modis, Y., Ogata, S., Clements, D., Harrison, S.C., Variable surface epitopes in the crystal structure of dengue virus type 3 envelope glycoprotein. J. Virol. 79 (2005), 1223–1231.
27. Moriarty, N.W., Grosse-Kunstleve, R.W., Adams, P.D., electronic Ligand Builder and Optimization Workbench (eLBOW): a tool for ligand coordinate and restraint generation. Acta Crystallogr. D Biol. Crystallogr. 65 (2009), 1074–1080.
28. De Nardis, C., Hendriks, L.J.A., Poirier, E., Arvinte, T., Gros, P., Bakker, A.B.H., de Kruif, J., A new approach for generating bispecific antibodies based on a common light chain format and the stable architecture of human immunoglobulin G. J. Biol. Chem. 292 (2017), 14706–14717.
29. Qin, Z., Yang, D., You, X., Liu, Y., Hu, S., Yan, Q., Yang, S., Jiang, Z., The recognition mechanism of triple-helical β-1,3-glucan by a β-1,3-glucanase. Chem. Commun. (Camb.) 53 (2017), 9368–9371.
30. Schwarzenbacher, R., Zeth, K., Diederichs, K., Gries, A., Kostner, G.M., Laggner, P., Prassl, R., Crystal structure of human beta2-glycoprotein I: implications for phospholipid binding and the antiphospholipid syndrome. EMBO J. 18 (1999), 6228–6239.
31. Song, Y., DiMaio, F., Wang, R.Y.-R., Kim, D., Miles, C., Brunette, T., Thompson, J., Baker, D., High-resolution comparative modeling with RosettaCM. Structure 21 (2013), 1735–1742.
32. Terwilliger, T.C., Dimaio, F., Read, R.J., Baker, D., Bunkóczi, G., Adams, P.D., Grosse-Kunstleve, R.W., Afonine, P.V., Echols, N., phenix.mr_rosetta: molecular replacement and model rebuilding with Phenix and Rosetta. J. Struct. Funct. Genomics 13 (2012), 81–90.
33. Tyka, M.D., Keedy, D.A., André I., Dimaio, F., Song, Y., Richardson, D.C., Richardson, J.S., Baker, D., Alternate states of proteins revealed by detailed energy landscape mapping. J. Mol. Biol. 405 (2011), 607–618.
34. Walls, A.C., Tortorici, M.A., Bosch, B.-J., Frenz, B., Rottier, P.J.M., DiMaio, F., Rey, F.A., Veesler, D., Cryo-electron microscopy structure of a coronavirus spike glycoprotein trimer. Nature 531 (2016), 114–117.
35. Walls, A.C., Tortorici, M.A., Frenz, B., Snijder, J., Li, W., Rey, F.A., DiMaio, F., Bosch, B.-J., Veesler, D., Glycan shield and epitope masking of a coronavirus spike protein observed by cryo-electron microscopy. Nat. Struct. Mol. Biol. 23 (2016), 899–905.
36. Wang, R.Y.-R., Kudryashev, M., Li, X., Egelman, E.H., Basler, M., Cheng, Y., Baker, D., DiMaio, F., De novo protein structure determination from near-atomic-resolution cryo-EM maps. Nat. Methods 12 (2015), 335–338.
37. Wang, R.Y.-R., Song, Y., Barad, B.A., Cheng, Y., Fraser, J.S., DiMaio, F., Automated structure refinement of macromolecular assemblies from cryo-EM maps using Rosetta. Elife, 5, 2016, 10.7554/eLife.17219.
38. Wu, L., Jiang, J., Jin, Y., Kallemeijn, W.W., Kuo, C.-L., Artola, M., Dai, W., van Elk, C., van Eijk, M., van der Marel, G.A., et al. Activity-based probes for functional interrogation of retaining β-glucuronidases. Nat. Chem. Biol. 13 (2017), 867–873.