All-atom ensemble modeling to analyze small-angle X-ray scattering of glycosylated proteins

Structure

Volumn 21, Issue 3, 2013, Pages 321-331

  Guttman, Miklos ^a   Weinkam, Patrick ^b   Sali, Andrej ^b   Lee, Kelly K ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA1 GLYCOPROTEIN; BROMELAIN; BROMELAIN RELEASED INFLUENZA HEMAGGLUTININ; FC RECEPTOR; FETUIN; GLYCAN; GLYCOSYLATED PROTEIN; HEMAGGLUTININ; LYSOZYME; RIBONUCLEASE; RIBONUCLEASE A; UNCLASSIFIED DRUG;

ARTICLE; HUMAN; MOLECULAR WEIGHT; NONHUMAN; PRACTICE GUIDELINE; PRIORITY JOURNAL; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY;

ANIMALS; CATTLE; COMPUTER SIMULATION; GLYCOPROTEINS; GLYCOSYLATION; HUMANS; INTERNET; MODELS, MOLECULAR; POLYSACCHARIDES; SCATTERING, SMALL ANGLE; SOFTWARE; X-RAY DIFFRACTION;

EID: 84874855471     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.02.004     Document Type: Article

References (72)

1. T. Araki, Y. Yoshioka, and K. Schmid The position of the disulfide bonds in human plasma alpha 2 HS-glycoprotein and the repeating double disulfide bonds in the domain structure Biochim. Biophys. Acta 994 1989 195 199
2. P. Bernadó Effect of interdomain dynamics on the structure determination of modular proteins by small-angle scattering Eur. Biophys. J. 39 2010 769 780
3. S. Bernocco, B.M. Steiglitz, D.I. Svergun, M.V. Petoukhov, F. Ruggiero, S. Ricard-Blum, C. Ebel, C. Geourjon, G. Deleage, and B. Font Low resolution structure determination shows procollagen C-proteinase enhancer to be an elongated multidomain glycoprotein J. Biol. Chem. 278 2003 7199 7205
4. A. Bohne-Lang, and C.W. von der Lieth GlyProt: in silico glycosylation of proteins Nucleic Acids Res. 33 Web Server issue 2005 W214 W219
5. S.A. Brooks Strategies for analysis of the glycosylation of proteins: current status and future perspectives Mol. Biotechnol. 43 2009 76 88
6. R.W. Compans, H.D. Klenk, L.A. Caliguiri, and P.W. Choppin Influenza virus proteins. I. Analysis of polypeptides of the virion and identification of spike glycoproteins Virology 42 1970 880 889
7. J. Deisenhofer Crystallographic refinement and atomic models of a human Fc fragment and its complex with fragment B of protein A from Staphylococcus aureus at 2.9- and 2.8-A resolution Biochemistry 20 1981 2361 2370
8. W.L. DeLano The PyMOL Molecular Graphics System 2002 DeLano Scientific San Carlos, CA, USA
9. A.S. Edge, and R.G. Spiro Presence of an O-glycosidically linked hexasaccharide in fetuin J. Biol. Chem. 262 1987 16135 16141
10. H. Fischer, M. de Oliveira Neto, H.B. Napolitano, I. Polikarpov, and A.F. Craievich Determination of the molecular weight of proteins in solution from a single small-angle X-ray scattering measurement on a relative scale J. Appl. Crystallogr. 43 2010 101 109
11. M. Frank, and S. Schloissnig Bioinformatics and molecular modeling in glycobiology Cell. Mol. Life Sci. 67 2010 2749 2772
12. M.L. Friedman, J.R. Wermeling, and H.B. Halsall The influence of N-acetylneuraminic acid on the properties of human orosomucoid Biochem. J. 236 1986 149 153
13. A. Guttman Multistructure sequencing of N-linked fetuin glycans by capillary gel electrophoresis and enzyme matrix digestion Electrophoresis 18 1997 1136 1141
14. M. Guttman, M. Kahn, N.K. Garcia, S.L. Hu, and K.K. Lee Solution structure, conformational dynamics, and CD4-induced activation in full-length, glycosylated, monomeric HIV gp120 J. Virol. 86 2012 8750 8764
15. O. Guvench, S.N. Greene, G. Kamath, J.W. Brady, R.M. Venable, R.W. Pastor, and A.D. Mackerell Jr. Additive empirical force field for hexopyranose monosaccharides J. Comput. Chem. 29 2008 2543 2564
16. O. Guvench, E.R. Hatcher, R.M. Venable, R.W. Pastor, and A.D. Mackerell CHARMM Additive All-Atom Force Field for Glycosidic Linkages between Hexopyranoses J. Chem. Theory Comput. 5 2009 2353 2370
17. M. Hammel Validation of macromolecular flexibility in solution by small-angle X-ray scattering (SAXS) Eur. Biophys. J. 41 2012 789 799
18. M. Hammel, M. Kriechbaum, A. Gries, G.M. Kostner, P. Laggner, and R. Prassl Solution structure of human and bovine beta(2)-glycoprotein I revealed by small-angle X-ray scattering J. Mol. Biol. 321 2002 85 97
19. G.L. Hura, A.L. Menon, M. Hammel, R.P. Rambo, F.L. Poole 2nd, S.E. Tsutakawa, F.E. Jenney Jr., S. Classen, K.A. Frankel, and R.C. Hopkins Robust, high-throughput solution structural analyses by small angle X-ray scattering (SAXS) Nat. Methods 6 2009 606 612
20. A. Imberty, and S. Pérez Structure, conformation, and dynamics of bioactive oligosaccharides: theoretical approaches and experimental validations Chem. Rev. 100 2000 4567 4588
21. T. Imre, G. Schlosser, G. Pocsfalvi, R. Siciliano, E. Molnár-Szöllosi, T. Kremmer, A. Malorni, and K. Vékey Glycosylation site analysis of human alpha-1-acid glycoprotein (AGP) by capillary liquid chromatography-electrospray mass spectrometry J. Mass Spectrom. 40 2005 1472 1483
22. T. Ishida, and K. Kinoshita PrDOS: prediction of disordered protein regions from amino acid sequence Nucleic Acids Res. 35 Web Server issue 2007 W460 W464
23. D.A. Jacques, and J. Trewhella Small-angle scattering for structural biology - expanding the frontier while avoiding the pitfalls Protein Sci. 19 2010 642 657
24. K.N. Kirschner, A.B. Yongye, S.M. Tschampel, J. González- Outeiriño, C.R. Daniels, B.L. Foley, and R.J. Woods GLYCAM06: a generalizable biomolecular force field. Carbohydrates J. Comput. Chem. 29 2008 622 655
25. P.V. Konarev, V.V. Volkov, A.V. Sokolova, M.H.J. Koch, and D.I. Svergun PRIMUS: a Windows PC-based system for small-angle scattering data analysis J. Appl. Crystallogr. 36 2003 1277 1282
26. M.B. Kozin, and D.I. Svergun Automated matching of high- and low-resolution structural models J. Appl. Crystallogr. 34 2001 33 41
27. T.M. Laue, B.D. Shah, T.M. Ridgeway, and S.L. Pelletier Analytical Ultracentrifugation in Biochemistry and Polymer Science 1992 Royal Society of Chemistry Cambridge, UK
28. M.S. Lewis, and R.P. Junghans Ultracentrifugal analysis of molecular mass of glycoproteins of unknown or ill-defined carbohydrate composition Methods Enzymol. 321 2000 136 149
29. R. Linding, L.J. Jensen, F. Diella, P. Bork, T.J. Gibson, and R.B. Russell Protein disorder prediction: implications for structural proteomics Structure 11 2003 1453 1459
30. T. Lütteke, M. Frank, and C.W. von der Lieth Carbohydrate Structure Suite (CSS): analysis of carbohydrate 3D structures derived from the PDB Nucleic Acids Res. 33 Database issue 2005 D242 D246
31. G.W. Lynn, W.T. Heller, A. Mayasundari, K.H. Minor, and C.B. Peterson A model for the three-dimensional structure of human plasma vitronectin from small-angle scattering measurements Biochemistry 44 2005 565 574
32. A. McPherson, M.L. Friedman, and H.B. Halsall Crystallization of alpha 1-acid glycoprotein Biochem. Biophys. Res. Commun. 124 1984 619 624
33. H.D. Mertens, and D.I. Svergun Structural characterization of proteins and complexes using small-angle X-ray solution scattering J. Struct. Biol. 172 2010 128 141
34. S.Y. Mir-Shekari, D.A. Ashford, D.J. Harvey, R.A. Dwek, and I.T. Schulze The glycosylation of the influenza A virus hemagglutinin by mammalian cells. A site-specific study J. Biol. Chem. 272 1997 4027 4036
35. E. Mylonas, and D.I. Svergun Accuracy of molecular mass determination of proteins in solution by small-angle X-ray scattering J. Appl. Crystallogr. 40 2007 s245 s249
36. P. Nawratil, S. Lenzen, J. Kellermann, H. Haupt, T. Schinke, W. Müller-Esterl, and W. Jahnen-Dechent Limited proteolysis of human alpha2-HS glycoprotein/fetuin. Evidence that a chymotryptic activity can release the connecting peptide J. Biol. Chem. 271 1996 31735 31741
37. M. Pelikan, G.L. Hura, and M. Hammel Structure and flexibility within proteins as identified through small angle X-ray scattering Gen. Physiol. Biophys. 28 2009 174 189
38. M.V. Petoukhov, and D.I. Svergun Analysis of X-ray and neutron scattering from biomacromolecular solutions Curr. Opin. Struct. Biol. 17 2007 562 571
39. M.V. Petoukhov, P.V. Konarev, A.G. Kikhney, and D.I. Svergun ATSAS 2.1 - towards automated and web-supported small-angle scattering data analysis J. Appl. Crystallogr. 40 2007 s223 s228
40. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
41. G. Porod General Theory O. Kratky, O. Gladder, Small-Angle X-ray Scattering 1982 Academic Press London 17 51
42. C.D. Putnam, M. Hammel, G.L. Hura, and J.A. Tainer X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution Q. Rev. Biophys. 40 2007 191 285
43. R.P. Rambo, and J.A. Tainer Bridging the solution divide: comprehensive structural analyses of dynamic RNA, DNA, and protein assemblies by small-angle X-ray scattering Curr. Opin. Struct. Biol. 20 2010 128 137
44. D.V. Renouf, and E.F. Hounsell Molecular modelling of glycoproteins by homology with non-glycosylated protein domains, computer simulated glycosylation and molecular dynamics Adv. Exp. Med. Biol. 376 1995 37 45
45. A. Roy, A. Kucukural, and Y. Zhang I-TASSER: a unified platform for automated protein structure and function prediction Nat. Protoc. 5 2010 725 738
46. L. Royle, T.S. Mattu, E. Hart, J.I. Langridge, A.H. Merry, N. Murphy, D.J. Harvey, R.A. Dwek, and P.M. Rudd An analytical and structural database provides a strategy for sequencing O-glycans from microgram quantities of glycoproteins Anal. Biochem. 304 2002 70 90
47. A. Sali, and T.L. Blundell Comparative protein modelling by satisfaction of spatial restraints J. Mol. Biol. 234 1993 779 815
48. J. Santoro, C. González, M. Bruix, J.L. Neira, J.L. Nieto, J. Herranz, and M. Rico High-resolution three-dimensional structure of ribonuclease A in solution by nuclear magnetic resonance spectroscopy J. Mol. Biol. 229 1993 722 734
49. D. Schneidman-Duhovny, M. Hammel, and A. Sali FoXS: a web server for rapid computation and fitting of SAXS profiles Nucleic Acids Res. 38 Web Server issue 2010 W540 W544
50. D. Schneidman-Duhovny, S.J. Kim, and A. Sali Integrative structural modeling with small angle X-ray scattering profiles BMC Struct. Biol. 12 2012 17
51. D.L. Schönfeld, R.B. Ravelli, U. Mueller, and A. Skerra The 1.8-A crystal structure of alpha1-acid glycoprotein (Orosomucoid) solved by UV RIP reveals the broad drug-binding activity of this human plasma lipocalin J. Mol. Biol. 384 2008 393 405
52. D. Shental-Bechor, and Y. Levy Effect of glycosylation on protein folding: a close look at thermodynamic stabilization Proc. Natl. Acad. Sci. USA 105 2008 8256 8261
53. M. Sickmeier, J.A. Hamilton, T. LeGall, V. Vacic, M.S. Cortese, A. Tantos, B. Szabo, P. Tompa, J. Chen, and V.N. Uversky DisProt: the Database of Disordered Proteins Nucleic Acids Res. 35 Database issue 2007 D786 D793
54. V. Slynko, M. Schubert, S. Numao, M. Kowarik, M. Aebi, and F.H. Allain NMR structure determination of a segmentally labeled glycoprotein using in vitro glycosylation J. Am. Chem. Soc. 131 2009 1274 1281
55. I.L. Smolsky, P. Liu, M. Niebuhr, K. Ito, T.M. Weiss, and H. Tsuruta Biological small-angle X-ray scattering facility at the Stanford Synchrotron Radiation Laboratory J. Appl. Crystallogr. 40 2007 s453 s458
56. D.I. Svergun Mathematical Methods in Small-Angle Scattering Data Analysis J. Appl. Crystallogr. 24 1991 485 492
57. D.I. Svergun Determination of the regularization parameter in indirect-transform methods using perceptual criteria J. Appl. Crystallogr. 25 1992 495 503
58. D.I. Svergun Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing Biophys. J. 76 1999 2879 2886
59. D. Svergun, C. Barberato, and M.H.J. Koch CRYSOL- a Program to Evaluate X-ray Solution Scattering of Biological Macromolecules from Atomic Coordinates J. Appl. Crystallogr. 28 1995 768 773
60. D.I. Svergun, M.V. Petoukhov, and M.H. Koch Determination of domain structure of proteins from X-ray solution scattering Biophys. J. 80 2001 2946 2953
61. M.J. Treuheit, C.E. Costello, and H.B. Halsall Analysis of the five glycosylation sites of human alpha 1-acid glycoprotein Biochem. J. 283 1992 105 112
62. V.V. Volkov, and D.I. Svergun Uniqueness of ab-initio shape determination in small-angle scattering J. Appl. Crystallogr. 36 2003 860 864
63. G. Walsh Biopharmaceutical benchmarks 2010 Nat. Biotechnol. 28 2010 917 924
64. P. Weinkam, J. Pons, and A. Sali Structure-based model of allostery predicts coupling between distant sites Proc. Natl. Acad. Sci. USA 109 2012 4875 4880
65. J. Wen, T. Arakawa, and J.S. Philo Size-exclusion chromatography with on-line light-scattering, absorbance, and refractive index detectors for studying proteins and their interactions Anal. Biochem. 240 1996 155 166
66. A.E. Whitten, and J. Trewhella Small-angle scattering and neutron contrast variation for studying bio-molecular complexes Methods Mol. Biol. 544 2009 307 323
67. R.L. Williams, S.M. Greene, and A. McPherson The crystal structure of ribonuclease B at 2.5-A resolution J. Biol. Chem. 262 1987 16020 16031
68. I.A. Wilson, J.J. Skehel, and D.C. Wiley Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution Nature 289 1981 366 373
69. V. Wittmann Glycopeptides and Glycoprotein; Synthesis, Structure, and Application Volume 267 2007 Springer Berlin, Heidelberg, New York
70. R.J. Woods, A. Pathiaseril, M.R. Wormald, C.J. Edge, and R.A. Dwek The high degree of internal flexibility observed for an oligomannose oligosaccharide does not alter the overall topology of the molecule Eur. J. Biochem. 258 1998 372 386
71. W. Wriggers, and S. Birmanns Using situs for flexible and rigid-body fitting of multiresolution single-molecule data J. Struct. Biol. 133 2001 193 202
72. Y. Zhang I-TASSER server for protein 3D structure prediction BMC Bioinformatics 9 2008 40