Combining electron microscopy and comparative protein structure modeling

Current Opinion in Structural Biology

Volumn 15, Issue 5, 2005, Pages 578-585

  Topf, Maya ^a   Sali, Andrej ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; ANALYTIC METHOD; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; HUMAN; INTERMETHOD COMPARISON; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN STRUCTURE; REVIEW; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS;

CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; PROTEIN CONFORMATION;

EID: 25844459522     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2005.08.001     Document Type: Review

References (79)

1. B. Alberts The cell as a collection of protein machines: preparing the next generation of molecular biologists Cell 92 1998 291 294
2. A. Sali, R. Glaeser, T. Earnest, and W. Baumeister From words to literature in structural proteomics Nature 422 2003 216 225
3. R.B. Russell, F. Alber, P. Aloy, F.P. Davis, D. Korkin, M. Pichaud, M. Topf, and A. Sali A structural perspective on protein-protein interactions Curr Opin Struct Biol 14 2004 313 324
4. S. Dutta, and H.M. Berman Large macromolecular complexes in the Protein Data Bank: a status report Structure 13 2005 381 388
5. J. Frank Single-particle imaging of macromolecules by cryo-electron microscopy Annu Rev Biophys Biomol Struct 31 2002 303 319
6. R. Henderson, J.M. Baldwin, T.A. Ceska, F. Zemlin, E. Beckmann, and K.H. Downing Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy J Mol Biol 213 1990 899 929
7. E. Nogales, S.G. Wolf, and K.H. Downing Structure of the alpha beta tubulin dimer by electron crystallography Nature 391 1998 199 203
8. K. Yonekura, S. Maki-Yonekura, and K. Namba Building the atomic model for the bacterial flagellar filament by electron cryomicroscopy and image analysis Structure 13 2005 407 412
9. M. van Heel, B. Gowen, R. Matadeen, E.V. Orlova, R. Finn, T. Pape, D. Cohen, H. Stark, R. Schmidt, and M. Schatz Single-particle electron cryo-microscopy: towards atomic resolution Q Rev Biophys 33 2000 307 369
10. N.A. Ranson, G.W. Farr, A.M. Roseman, B. Gowen, W.A. Fenton, A.L. Horwich, and H.R. Saibil ATP-bound states of GroEL captured by cryo-electron microscopy Cell 107 2001 869 879
11. R. Henderson Realizing the potential of electron cryo-microscopy Q Rev Biophys 37 2004 3 13
12. W. Chiu, M.L. Baker, W. Jiang, M. Dougherty, and M.F. Schmid Electron cryomicroscopy of biological machines at subnanometer resolution Structure 13 2005 363 372
13. M.G. Rossmann, M.C. Morais, P.G. Leiman, and W. Zhang Combining X-ray crystallography and electron microscopy Structure 13 2005 355 362
14. J.A. Davis, Y. Takagi, R.D. Kornberg, and F.A. Asturias Structure of the yeast RNA polymerase II holoenzyme: mediator conformation and polymerase interaction Mol Cell 10 2002 409 415
15. H. Gao, J. Sengupta, M. Valle, A. Korostelev, N. Eswar, S.M. Stagg, P.V. Roey, R.K. Agrawal, S.C. Harvey, and A. Sali Study of the structural dynamics of the E. coli 70S ribosome using real-space refinement Cell 113 2003 789 801
16. K.C. Holmes, I. Angert, F.J. Kull, W. Jahn, and R.R. Schroder Electron cryo-microscopy shows how strong binding of myosin to actin releases nucleotide Nature 425 2003 423 427
17. S.J. Ludtke, D.H. Chen, J.L. Song, D.T. Chuang, and W. Chiu Seeing GroEL at 6 Å resolution by single particle electron cryomicroscopy Structure 12 2004 1129 1136
18. A.M. Roseman Docking structures of domains into maps from cryo-electron microscopy using local correlation Acta Crystallogr D Biol Crystallogr 56 2000 1332 1340
19. W. Jiang, M.L. Baker, S.J. Ludtke, and W. Chiu Bridging the information gap: computational tools for intermediate resolution structure interpretation J Mol Biol 308 2001 1033 1044
20. P. Chacon, and W. Wriggers Multi-resolution contour-based fitting of macromolecular structures J Mol Biol 317 2002 375 384
21. J. Navaza, J. Lepault, F.A. Rey, C. Alvarez-Rua, and J. Borge On the fitting of model electron densities into EM reconstructions: a reciprocal-space formulation Acta Crystallogr D Biol Crystallogr 58 2002 1820 1825
22. N. Volkmann, and D. Hanein Docking of atomic models into reconstructions from electron microscopy Methods Enzymol 374 2003 204 225
23. M. Topf, M.L. Baker, B. John, W. Chiu, and A. Sali Structural characterization of components of protein assemblies by comparative modeling and electron cryo-microscopy J Struct Biol 149 2005 191 203 A new method for fitting comparative models into intermediate-resolution cryo-EM density maps (Mod-EM, a module in MODELLER) is used to demonstrate how such maps can be helpful in improving the accuracy of models. It is shown that one of the most accurate models among alternative comparative models can be identified by the quality of its fit into the density.
24. F. Tama, W. Wriggers, and C.L. Brooks III Exploring global distortions of biological macromolecules and assemblies from low-resolution structural information and elastic network theory J Mol Biol 321 2002 297 305
25. O. Keskin, S.R. Durell, I. Bahar, R.L. Jernigan, and D.G. Covell Relating molecular flexibility to function: a case study of tubulin Biophys J 83 2002 663 680
26. Y. Kong, D. Ming, Y. Wu, J.K. Stoops, Z.H. Zhou, and J. Ma Conformational flexibility of pyruvate dehydrogenase complexes: a computational analysis by quantized elastic deformational model J Mol Biol 330 2003 129 135
27. P. Chacon, F. Tama, and W. Wriggers Mega-Dalton biomolecular motion captured from electron microscopy reconstructions J Mol Biol 326 2003 485 492
28. J. Ma Usefulness and limitations of normal mode analysis in modeling dynamics of biomolecular complexes Structure 13 2005 373 380
29. H. Gao, and J. Frank Molding atomic structures into intermediate- resolution cryo-EM density maps of ribosomal complexes using real-space refinement Structure 13 2005 401 406
30. F. Fabiola, and M.S. Chapman Fitting of high-resolution structures into electron microscopy reconstruction images Structure 13 2005 389 400
31. W. Wriggers Spanning the length scales of biomolecular simulation Structure 12 2004 1 2
32. T.L. Blundell, B.L. Sibanda, M.J. Sternberg, and J.M. Thornton Knowledge-based prediction of protein structures and the design of novel molecules Nature 326 1987 347 352
33. A. Sali, and T.L. Blundell Comparative protein modelling by satisfaction of spatial restraints J Mol Biol 234 1993 779 815
34. M.S. Madhusudhan, M.A. Marti-Renom, N. Eswar, B. John, U. Pieper, R. Karchin, M. Shen, and A. Sali Comparative protein structure modeling J.M. Walker The Proteomics Protocols Handbook 2005 Humana Press Inc 831 860
35. K. Ginalski, N.V. Grishin, A. Godzik, and L. Rychlewski Practical lessons from protein structure prediction Nucleic Acids Res 33 2005 1874 1891
36. A. Bairoch, R. Apweiler, C.H. Wu, W.C. Barker, B. Boeckmann, S. Ferro, E. Gasteiger, H. Huang, R. Lopez, and M. Magrane The Universal Protein Resource (UniProt) Nucleic Acids Res 33 2005 D154 D159
37. U. Pieper, N. Eswar, H. Braberg, M.S. Madhusudhan, F.P. Davis, A.C. Stuart, N. Mirkovic, A. Rossi, M.A. Marti-Renom, and A. Fiser MODBASE, a database of annotated comparative protein structure models, and associated resources Nucleic Acids Res 32 2004 D217 D222
38. A. Sali, and J. Kuriyan Challenges at the frontiers of structural biology Trends Cell Biol 9 1999 M20 M24
39. D. Baker, and A. Sali Protein structure prediction and structural genomics Science 294 2001 93 96
40. B. Wallner, and A. Elofsson All are not equal: a benchmark of different homology modeling programs Protein Sci 14 2005 1315 1327
41. N. Volkmann, D. DeRosier, P. Matsudaira, and D. Hanein An atomic model of actin filaments cross-linked by fimbrin and its implications for bundle assembly and function J Cell Biol 153 2001 947 956
42. S. Stoilova-McPhie, B.O. Villoutreix, K. Mertens, G. Kemball-Cook, and A. Holzenburg 3-dimensional structure of membrane-bound coagulation factor VIII: modeling of the factor VIII heterodimer within a 3-dimensional density map derived by electron crystallography Blood 99 2002 1215 1223
43. 2+ release channel has an oxidoreductase-like domain Proc Natl Acad Sci USA 99 2002 12155 12160
44. P. Aloy, F.D. Ciccarelli, C. Leutwein, A.C. Gavin, G. Superti-Furga, P. Bork, B. Boettcher, and R.B. Russell A complex prediction: three-dimensional model of the yeast exosome EMBO Rep 3 2002 628 635
45. J. Liu, D.W. Taylor, and K.A. Taylor A 3-D reconstruction of smooth muscle alpha-actinin by cryoEM reveals two different conformations at the actin-binding region J Mol Biol 338 2004 115 125
46. J. Martin-Benito, S. Bertrand, T. Hu, P.J. Ludtke, J.N. McLaughlin, B.M. Willardson, J.L. Carrascosa, and J.M. Valpuesta Structure of the complex between the cytosolic chaperonin CCT and phosducin-like protein Proc Natl Acad Sci USA 101 2004 17410 17415
47. C. Petosa, G. Schoehn, P. Askjaer, U. Bauer, M. Moulin, U. Steuerwald, M. Soler-Lopez, F. Baudin, I.W. Mattaj, and C.W. Muller Architecture of CRM1/Exportin1 suggests how cooperativity is achieved during formation of a nuclear export complex Mol Cell 16 2004 761 775 A structural model of the human karyopherin CRM1 is suggested based on a combination of X-ray crystallography, EM and comparative modeling. The architecture of CRM1 resembles that of the import receptor transportin1, with 19 HEAT repeats and a large loop implicated in the binding of the small GTPase Ran. The integrated structural information provides insights into karyopherin-mediated nuclear export signal recognition.
48. W. Wriggers, and P. Chacon Modeling tricks and fitting techniques for multiresolution structures Structure 9 2001 779 788
49. M.P. Rout, J.D. Aitchison, A. Suprapto, K. Hjertaas, Y. Zhao, and B.T. Chait The yeast nuclear pore complex: composition, architecture, and transport mechanism J Cell Biol 148 2000 635 651
50. F. Alber, M.F. Kim, and A. Sali Structural characterization of assemblies from overall shape and subcomplex compositions Structure 13 2005 435 445
51. R. Beckmann, C.M. Spahn, N. Eswar, J. Helmers, P.A. Penczek, A. Sali, J. Frank, and G. Blobel Architecture of the protein-conducting channel associated with the translating 80S ribosome Cell 107 2001 361 372
52. C.S. Tung, S. Joseph, and K.Y. Sanbonmatsu All-atom homology model of the Escherichia coli 30S ribosomal subunit Nat Struct Biol 9 2002 750 755
53. M. Halic, T. Becker, M.R. Pool, C.M. Spahn, R.A. Grassucci, J. Frank, and R. Beckmann Structure of the signal recognition particle interacting with the elongation-arrested ribosome Nature 427 2004 808 814
54. K. Wild, M. Halic, I. Sinning, and R. Beckmann SRP meets the ribosome Nat Struct Mol Biol 11 2004 1049 1053
55. J. Sengupta, J. Nilsson, R. Gursky, C.M. Spahn, P. Nissen, and J. Frank Identification of the versatile scaffold protein RACK1 on the eukaryotic ribosome by cryo-EM Nat Struct Mol Biol 11 2004 957 962 Using an 11.7 Å resolution cryo-EM map of the S. cerevisiae 80S ribosome, the RACK1 protein was localized to the head region of the 40S subunit in the immediate vicinity of the mRNA exit channel. A detailed analysis of the fit of the RACK1 comparative model into the density reveals how the protein interacts with rRNA and how it can recruit proteins to the ribosome via its WD-repeat platform.
56. A. Fotin, Y. Cheng, P. Sliz, N. Grigorieff, S.C. Harrison, T. Kirchhausen, and T. Walz Molecular model for a complete clathrin lattice from electron cryomicroscopy Nature 432 2004 573 579 The architecture of a complete clathrin lattice is resolved by fitting X-ray structures and comparative models into its subnanometer-resolution cryo-EM density map (1675 residues). The structure explains how clathrin-coated vesicles adapt to cargos of different shapes and sizes.
57. Z.H. Zhou, and W. Chiu Determination of icosahedral virus structures by electron cryomicroscopy at subnanometer resolution Adv Protein Chem 64 2003 93 124
58. H. Stahlberg, A. Engel, and A. Philippsen Assessing the structure of membrane proteins: combining different methods gives the full picture Biochem Cell Biol 80 2002 563 568
59. W. Chiu, M.L. Baker, W. Jiang, and Z.H. Zhou Deriving folds of macromolecular complexes through electron cryomicroscopy and bioinformatics approaches Curr Opin Struct Biol 12 2002 263 269
60. A. Enosh, S.J. Fleishman, N. Ben-Tal, and D. Halperin Assigning transmembrane segments to helices in intermediate-resolution structures Bioinformatics 20 suppl 1 2004 I122 I129
61. Y. Kong, and J. Ma A structural-informatics approach for mining beta-sheets: locating sheets in intermediate-resolution density maps J Mol Biol 332 2003 399 413
62. Y. Kong, X. Zhang, T.S. Baker, and J. Ma A Structural-informatics approach for tracing beta-sheets: building pseudo-C(alpha) traces for beta-strands in intermediate-resolution density maps J Mol Biol 339 2004 117 130
63. Y. Wu, M. Chen, M. Lu, Q. Wang, and J. Ma Determining protein topology from skeletons of secondary structures J Mol Biol 350 2005 571 586 A new method for determining protein topology by defining loop connectivity based on skeletons of secondary structure segments obtained from intermediate-resolution cryo-EM density maps. The method involves a knowledge-based geometry filter and an energy-based evaluation. It is tested successfully on a wide range of protein architectures.
64. B. Rost, C. Sander, and R. Schneider PHD-an automatic mail server for protein secondary structure prediction Comput Appl Biosci 10 1994 53 60
65. P. Baldi, S. Brunak, P. Frasconi, G. Soda, and G. Pollastri Exploiting the past and the future in protein secondary structure prediction Bioinformatics 15 1999 937 946
66. L.J. McGuffin, K. Bryson, and D.T. Jones The PSIPRED protein structure prediction server Bioinformatics 16 2000 404 405
67. Z.H. Zhou, M.L. Baker, W. Jiang, M. Dougherty, J. Jakana, G. Dong, G. Lu, and W. Chiu Electron cryomicroscopy and bioinformatics suggest protein fold models for rice dwarf virus Nat Struct Biol 8 2001 868 873
68. W. Jiang, Z. Li, Z. Zhang, M.L. Baker, P.E. Prevelige Jr., and W. Chiu Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions Nat Struct Biol 10 2003 131 135
69. M.L. Baker, W. Jiang, B.R. Bowman, Z.H. Zhou, F.A. Quiocho, F.J. Rixon, and W. Chiu Architecture of the herpes simplex virus major capsid protein derived from structural bioinformatics J Mol Biol 331 2003 447 456 Structural analysis of the 8.5 Å resolution cryo-EM map of the major capsid protein (VP5) of herpes simplex virus type 1 is combined with sequence-based informatics to give its architectural model. The model provides insights into the strategies used to achieve viral capsid stability.
70. W. Zhang, P.R. Chipman, J. Corver, P.R. Johnson, Y. Zhang, S. Mukhopadhyay, T.S. Baker, J.H. Strauss, M.G. Rossmann, and R.J. Kuhn Visualization of membrane protein domains by cryo-electron microscopy of dengue virus Nat Struct Biol 10 2003 907 912
71. G.J. Kleywegt, and T.A. Jones Detecting folding motifs and similarities in protein structures W. Charles J. Carter R.M. Sweet Methods in Enzymology vol 277 1997 Academic Press 525 545
72. K. Kinoshita, A. Kidera, and N. Go Diversity of functions of proteins with internal symmetry in spatial arrangement of secondary structural elements Protein Sci 8 1999 1210 1217
73. K. Mizuguchi, and N. Go Comparison of spatial arrangements of secondary structural elements in proteins Protein Eng 8 1995 353 362
74. J.A. Velazquez-Muriel, C.O. Sorzano, S.H. Scheres, and J.M. Carazo SPI-EM: towards a tool for predicting CATH superfamilies in 3D-EM maps J Mol Biol 345 2005 759 771 SPI-EM is a new method for determining the fold of a protein domain using its EM density map at intermediate resolution. This aim is achieved by fitting protein structural domains representative of the Protein Data Bank into an EM map of the specimen, followed by a probabilistic analysis of the results. The approach is demonstrated with the aid of simulated and experimental multidomain density maps.
75. C.A. Orengo, F.M. Pearl, and J.M. Thornton The CATH domain structure database Methods Biochem Anal 44 2003 249 271
76. M.J. Sippl Recognition of errors in three-dimensional structures of proteins Proteins 17 1993 355 362
77. F. Melo, R. Sanchez, and A. Sali Statistical potentials for fold assessment Protein Sci 11 2002 430 448
78. B. John, and A. Sali Comparative protein structure modeling by iterative alignment, model building and model assessment Nucleic Acids Res 31 2003 3982 3992
79. C.M. Spahn, M.G. Gomez-Lorenzo, R.A. Grassucci, R. Jorgensen, G.R. Andersen, R. Beckmann, P.A. Penczek, J.P. Ballesta, and J. Frank Domain movements of elongation factor eEF2 and the eukaryotic 80S ribosome facilitate tRNA translocation EMBO J 23 2004 1008 1019