Towards atomic resolution structural determination by single-particle cryo-electron microscopy

Current Opinion in Structural Biology

Volumn 18, Issue 2, 2008, Pages 218-228

  Zhou, Z Hong ^a  

^a CALIFORNIA NANOSYSTEMS INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; POLYHEDRIN; RNA;

BACTERIOPHAGE; CONFORMATION; CRYOELECTRON MICROSCOPY; CYTOPLASM; INSTRUMENTATION; MACROMOLECULE; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE; POLYHEDROSIS VIRUS; PRIORITY JOURNAL; REVIEW; RNA PROCESSING; RNA REPLICATION; STRUCTURE ANALYSIS; VIRUS MORPHOLOGY; X RAY CRYSTALLOGRAPHY;

CRYOELECTRON MICROSCOPY; IMAGE PROCESSING, COMPUTER-ASSISTED; MACROMOLECULAR SUBSTANCES; MODELS, MOLECULAR; MOLECULAR CONFORMATION;

CYPOVIRUS;

EID: 41949099222     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2008.03.004     Document Type: Review

References (82)

1. Subramaniam S., and Henderson R. Molecular mechanism of vectorial proton translocation by bacteriorhodopsin. Nature 406 (2000) 653-657
2. Mitsuoka K., Hirai T., Murata K., Miyazawa A., Kidera A., Kimura Y., and Fujiyoshi Y. The structure of bacteriorhodopsin at 3.0 Å resolution based on electron crystallography: implication of the charge distribution. J Mol Biol 286 (1999) 861-882
3. Murata K., Mitsuoka K., Hirai T., Walz T., Agre P., Heymann J.B., Engel A., and Fujiyoshi Y. Structural determinants of water permeation through aquaporin-1. Nature 407 (2000) 599-605
4. Gonen T., Sliz P., Kistler J., Cheng Y., and Walz T. Aquaporin-0 membrane junctions reveal the structure of a closed water pore. Nature 429 (2004) 193-197
5. Böttcher B., Wynne S.A., and Crowther R.A. Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature 386 (1997) 88-91. The structure of hepatitis B virus core was reconstructed to an unprecedented 7.4 Å resolution, resolving all helices in the viral core protein. The authors documented the first successful identification of a protein fold by single-particle cryoEM.
6. •], this represents the obtainment of the subnanometer resolution by single-particle cryoEM, where helices were resolved.
7. Matadeen R., Patwardhan A., Gowen B., Orlova E.V., Pape T., Cuff M., Mueller F., Brimacombe R., and van Heel M. The Escherichia coli large ribosomal subunit at 7.5 Å resolution. Struct Fold Des 7 (1999) 1575-1583
8. Zhou Z.H., Baker M.L., Jiang W., Dougherty M., Jakana J., Dong G., Lu G., and Chiu W. Electron cryomicroscopy and bioinformatics suggest protein fold models for rice dwarf virus. Nat Struct Biol 8 (2001) 868-873
9. Modis Y., Trus B.L., and Harrison S.C. Atomic model of the papillomavirus capsid. EMBO J 21 (2002) 4754-4762
10. Ludtke S.J., Chen D.H., Song J.L., Chuang D.T., and Chiu W. Seeing GroEL at 6 Å resolution by single particle electron cryomicroscopy. Structure 12 (2004) 1129-1136
11. Zhou Z.H., Dougherty M., Jakana J., He J., Rixon F.J., and Chiu W. Seeing the herpesvirus capsid at 8.5 Å. Science 288 (2000) 877-880
12. Golas M.M., Sander B., Will C.L., Luhrmann R., and Stark H. Molecular architecture of the multiprotein splicing factor SF3b. Science 300 (2003) 980-984
13. Zhou Z.H., Zhang H., Jakana J., Lu X.-Y., and Zhang J.-Q. Cytoplasmic polyhedrosis virus structure at 8 Å by electron cryomicroscopy: structural basis of capsid stability and mRNA processing regulation. Structure 11 (2003) 651-663
14. Saban S.D., Nepomuceno R.R., Gritton L.D., Nemerow G.R., and Stewart P.L. CryoEM structure at 9 Å resolution of an adenovirus vector targeted to hematopoietic cells. J Mol Biol 349 (2005) 526-537
15. Zhang X., Walker S.B., Chipman P.R., Nibert M.L., and Baker T.S. Reovirus polymerase lambda 3 localized by cryo-electron microscopy of virions at a resolution of 7.6 Å. Nat Struct Biol 10 (2003) 1011-1018
16. Jiang W., Li Z., Zhang Z., Baker M.L., Prevelige Jr. P.E., and Chiu W. Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions. Nat Struct Biol 10 (2003) 131-135
17. Jiang W., Baker M.L., Jakana J., Weigele P., King J., and Chiu W. Backbone structure of the infectious epsilon15 virus capsid revealed by electron cryomicroscopy. Nature 451 (2008) 1130-1134. The structure of bacteriophage Epsilon 15 was determined to 4.5 Å resolution. A backbone model was derived for the major capsid protein gp7, which has a similar structure to HK97 bacteriophage. In addition, a cementing protein gp10 was identified by proteomics analysis.
18. Yu X, Jin L, Zhou ZH: 3.88 Å structure of cytoplasmic polyhedrosis virus by cryo-electron microscopy. Nature 2008, 452: doi:10.1038/nature06893, in press. This paper describes the structure of the cytoplasmic polyhedrosis virus determined by single-particle cryoEM reconstruction to 3.88 Å resolution. Cα models were built using O. The authors presented three new findings of functional significance, including a conformational change related to RNA packaging, a coupling mechanism between RNA release and capping, and the structure of a long sought-after polyhedrin-binding domain which might have potentials for nano-biotechnological applications.
19. Zhang X., Settembre E., Xu C., Dormitzer P.R., Bellamy R., Harrison S.C., and Grigorieff N. Near-atomic resolution using electron cryomicroscopy and single-particle reconstruction. Proc Natl Acad Sci U S A 105 (2008) 1867-1872. This paper describes a near-atomic resolution structure of the double-layered rotavirus by single-particle cryoEM. In particular, a systematic evaluation was employed to select the best data included in the reconstruction. Non-icosahedral averaging of 13-fold was further used to improve the map quality to about 3.8 Å resolution, based on direct comparison with the X-ray structure of the same virus.
20. Ludtke SJ, Baker ML, Chen D-H, Song J-L, Chuang DT, Chiu W: De novo backbone trace of GroEL from single particle electron cryomicroscopy. Structure 2008, 16:441-448. This paper describes the 4.2 Å structure of GroEL, a nonicosahedral particle, by cryoEM single-particle reconstruction and demonstrates the exciting potential toward atomic resolution in structural studies of nonicosahedral particles. Liquid helium sample cooling was used in obtaining the cryoEM images and skeletonization was used to assist model building.
21. Jiang W., Baker M.L., Jakana J., Weigele P.R., King J., and Chiu W. Backbone structure of the infectious epsilon15 virus capsid revealed by electron cryomicroscopy. Nature 451 (2008) 1130-1134
22. Zhou Z.H., Liao W., Cheng R.H., Lawson J.E., McCarthy D.B., Reed L.J., and Stoops J.K. Direct evidence for the size and conformational variability of the pyruvate dehydrogenase complex revealed by three-dimensional electron microscopy. J Biol Chem 276 (2001) 21704-21713
23. Stark H., Zemlin F., and Boettcher C. Electron radiation damage to protein crystals of bacteriorhodopsin at different temperatures. Ulramicroscopy 63 (1996) 75-79
24. IES IESG: Cryoprotection in electron microscopy. J Microsc 1986, 141:385-391.
25. Comolli L., and Downing K. Dose tolerance at helium and nitrogen temperatures for whole cell electron tomography. J Struct Biol 152 (2005) 149-156
26. Iancu C.V., Wright E.R., Heymann J.B., and Jensen G.J. A comparison of liquid nitrogen and liquid helium as cryogens for electron cryotomography. J Struct Biol 153 (2006) 231-240
27. Wright E.R., Iancu C.V., Tivol W.F., and Jensen G.J. Observations on the behavior of vitreous ice at approximately 82 and approximately 12 K. J Struct Biol 153 (2006) 241-252
28. Zhou Z.H., and Chiu W. Prospects for using an IVEM with a FEG for imaging macromolecules towards atomic resolution. Ultramicroscopy 49 (1993) 407-416
29. DeRosier D.J. Correction of high-resolution data for curvature of the Ewald sphere. Ultramicroscopy 81 (2000) 83-98
30. Wolf M., DeRosier D.J., and Grigorieff N. Ewald sphere correction for single-particle electron microscopy. Ultramicroscopy 106 (2006) 376-382. This paper demonstrates the benefits of the full correction of transfer function using simulated data.
31. Jensen G.J., and Kornberg R.D. Defocus-gradient corrected back-projection. Ultramicroscopy 84 (2000) 57-64
32. Wan Y, Chiu W, Zhou ZH: Full contrast transfer function correction in 3D cryo-EM reconstruction. In IEEE Proceedings of ICCCAS 2004. Edited by; 2004:960-964. This paper documented the formulation of depth of field/focus gradient in image formation using real-space multi-slice method other than Fourier space/Ewald sphere. The authors demonstrated two possible ways for the full correction of transfer function using simulated data.
33. Crowther R.A. Procedures for three-dimensional reconstruction of spherical viruses by Fourier synthesis from electron micrographs. Philos Trans R Soc Lond B Biol Sci 261 (1971) 221-230
34. Crowther R.A., Amos L.A., Finch J.T., DeRosier D.J., and Klug A. Three dimensional reconstructions of spherical viruses by Fourier synthesis from electron micrographs. Nature 226 (1970) 421-425
35. Sherman M.B., and Chiu W. Reliability of phases retrieved from 400-kV spot-scan images of purple membranes acquired on a slow-scan CCD camera. J Microsc 188 (1997) 285-289
36. Stewart P.L., Cary R.B., Peterson S.R., and Chiu C.Y. Digitally collected cryo-electron micrographs for single particle reconstruction. Microsc Res Technol 49 (2000) 224-232
37. Sander B., Golas M.M., and Stark H. Advantages of CCD detectors for de novo three-dimensional structure determination in single-particle electron microscopy. J Struct Biol 151 (2005) 92-105
38. Zhang P., Borgnia M.J., Mooney P., Shi D., Pan M., O'Herron P., Mao A., Brogan D., Milne J.L., and Subramaniam S. Automated image acquisition and processing using a new generation of 4 K × 4 K CCD cameras for cryo electron microscopic studies of macromolecular assemblies. J Struct Biol 143 (2003) 135-144
39. Booth C.R., Jiang W., Baker M.L., Zhou Z.H., Ludtke S.J., and Chiu W. A 9 angstroms single particle reconstruction from CCD captured images on a 200 kV electron cryomicroscope. J Struct Biol 147 (2004) 116-127. This paper demonstrated that subnanometer resolution cryoEM reconstruction can be obtained using a CCD camera as a recording media.
40. Faruqi A.R., and Subramaniam S. CCD detectors in high-resolution biological electron microscopy. Q Rev Biophys 33 (2000) 1-27
41. Zhou Z.H., Prasad B.V., Jakana J., Rixon F.J., and Chiu W. Protein subunit structures in the herpes simplex virus A-capsid determined from 400 kV spot-scan electron cryomicroscopy. J Mol Biol 242 (1994) 456-469
42. Zhou Z.H., Hardt S., Wang B., Sherman M.B., Jakana J., and Chiu W. CTF determination of images of ice-embedded single particles using a graphics interface. J Struct Biol 116 (1996) 216-222
43. Ludtke S.J., Baldwin P.R., and Chiu W. EMAN: semi-automated software for high resolution single particle reconstructions. J Struct Biol 128 (1999) 82-97
44. Grigorieff N. FREALIGN: high-resolution refinement of single particle structures. J Struct Biol 157 (2007) 117-125
45. Liang Y., Ke E.Y., and Zhou Z.H. IMIRS: a high-resolution 3D reconstruction package integrated with a relational image database. J Struct Biol 137 (2002) 292-304
46. Zhou Z.H., and Chiu W. Determination of icosahedral virus structures by electron cryomicroscopy at subnanometer resolution. Adv Protein Chem 64 (2003) 93-124
47. Baker T.S., and Cheng R.H. A model-based approach for determining orientations of biological macromolecules imaged by cryoelectron microscopy. J Struct Biol 116 (1996) 120-130
48. Liu H., Cheng L., Zeng S., Cai C., Zhou Z.H., and Yang Q. Symmetry-adapted spherical harmonics method for high-resolution 3D single-particle reconstructions. J Struct Biol 161 (2008) 64-73
49. Saxton W.O., and Baumeister W. The correlation averaging of a regularly arranged bacterial cell envelope protein. J Microsc 127 (1982) 127-138
50. Unser M., Trus B.L., and Steven A.C. A new resolution criterion based on spectral signal-to-noise ratios. Ultramicroscopy 23 (1987) 39-51
51. Penczek P.A. Three-dimensional spectral signal-to-noise ratio for a class of reconstruction algorithms. J Struct Biol 138 (2002) 34-46
52. Yang S., Yu X., Galkin V.E., and Egelman E.H. Issues of resolution and polymorphism in single-particle reconstruction. J Struct Biol 144 (2003) 162-171
53. Stewart A., and Grigorieff N. Noise bias in the refinement of structures derived from single particles. Ultramicroscopy 102 (2004) 67-84
54. Fuller S.D., and Argos P. Is Sindbis a simple picornavirus with an envelope?. EMBO J 6 (1987) 1099-1105
55. Inaba K., Murakami S., Suzuki M., Nakagawa A., Yamashita E., Okada K., and Ito K. Crystal structure of the DsbB-DsbA complex reveals a mechanism of disulfide bond generation. Cell 127 (2006) 789-801
56. He J., Schmid M.F., Zhou Z.H., Rixon F., and Chiu W. Finding and using local symmetry in identifying lower domain movements in hexon subunits of the herpes simplex virus type 1 b capsid. J Mol Biol 309 (2001) 903-914
57. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 47 Pt 2 (1991) 110-119
58. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60 (2004) 2126-2132
59. Baker M.L., Ju T., and Chiu W. Identification of secondary structure elements in intermediate-resolution density maps. Structure 15 (2007) 7-19
60. Kinoshita K., Kidera A., and Go N. Diversity of functions of proteins with internal symmetry in spatial arrangement of secondary structural elements. Protein Sci 8 (1999) 1210-1217
61. Kleywegt G.J., and Jones T.A. In: Carter C.W., and Sweet R.M. (Eds). Detecting Folding Motifs and Similarities in Protein Structures vol 277 (1997), Academic Press, London
62. Mizuguchi K., and Go N. Comparison of spatial arrangements of secondary structural elements in proteins. Protein Eng 8 (1995) 353-362
63. Mertens P.P.C., Attoui H., Duncan R., and Dermody T.S. Reoviridae. In: Fauquet C.M., Mayo M.A., Maniloff J., Desselberger U., and Ball L.A. (Eds). Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses (2005), Elsevier/Academic Press 447-454
64. Zhou Z.H. Cypovirus. In: Patton J.T. (Ed). Segmented Double-stranded RNA Viruses: Structure and Molecular Biology (2008), Caister Academic Press 27-43
65. Hill C.L., Booth T.F., Prasad B.V., Grimes J.M., Mertens P.P., Sutton G.C., and Stuart D.I. The structure of a cypovirus and the functional organization of dsRNA viruses. Nat Struct Biol 6 (1999) 565-568
66. Zhang H., Zhang J., Yu X., Lu X., Zhang Q., Jakana J., Chen D.H., Zhang X., and Zhou Z.H. Visualization of protein-RNA interactions in cytoplasmic polyhedrosis virus. J Virol 73 (1999) 1624-1629
67. Xia Q., Jakana J., Zhang J.Q., and Zhou Z.H. Structural comparisons of empty and full cytoplasmic polyhedrosis virus: protein-RNA interactions and implications for endogenous RNA transcription mechanism. J Biol Chem 278 (2003) 1094-1100
68. Reinisch K.M., Nibert M.L., and Harrison S.C. Structure of the reovirus core at 3.6 Å resolution. Nature 404 (2000) 960-967
69. Grimes J.M., Burroughs J.N., Gouet P., Diprose J.M., Malby R., Zientara S., Mertens P.P.C., and Stuart D.I. The atomic structure of the bluetongue virus core. Nature 395 (1998) 470-478. This paper described the first atomic structure of a dsRNA virus particle by X-ray diffraction.
70. Lawton J.A., Estes M.K., and Prasad B.V. Three-dimensional visualization of mRNA release from actively transcribing rotavirus particles. Nat Struct Biol 4 (1997) 118-121
71. Hakansson K., Doherty A.J., Shuman S., and Wigley D.B. X-ray crystallography reveals a large conformational change during guanyl transfer by mRNA capping enzymes. Cell 89 (1997) 545-553
72. Ikeda K., Nakazawa H., Shimo-Oka A., Ishio K., Miyata S., Hosokawa Y., Matsumura S., Masuhara H., Belloncik S., Alain R., et al. Immobilization of diverse foreign proteins in viral polyhedra and potential application for protein microarrays. Proteomics 6 (2006) 54-66. Potential application of polyhedrin-binding domain of the CPV is demonstrated.
73. Coulibaly F., Chiu E., Ikeda K., Gutmann S., Haebel P.W., Schulze-Briese C., Mori H., and Metcalf P. The molecular organization of cypovirus polyhedra. Nature 446 (2007) 97-101. The structure of CPV polyhedrin protein was solved by X-ray diffraction using microcrystals grown inside cells.
74. Ikeda K., Nagaoka S., Winkler S., Kotani K., Yagi H., Nakanishi K., Miyajima S., Kobayashi J., and Mori H. Molecular characterization of Bombyx mori cytoplasmic polyhedrosis virus genome segment 4. J Virol 75 (2001) 988-995
75. Kühlbrandt W., and Wang D.N. Three-dimensional structure of plant light-harvesting complex determined by electron crystallography. Nature 350 (1991) 130-134
76. Nogales E., Wolf S.G., and Downing K.H. Structure of the alpha beta tubulin dimer by electron crystallography. Nature 391 (1998) 199-203
77. Gonen T., Cheng Y., Sliz P., Hiroaki Y., Fujiyoshi Y., Harrison S.C., and Walz T. Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature 438 (2005) 633-638
78. Fotin A., Cheng Y., Sliz P., Grigorieff N., Harrison S.C., Kirchhausen T., and Walz T. Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature 432 (2004) 573-579
79. Baumeister W. Electron tomography: towards visualizing the molecular organization of the cytoplasm. Curr Opin Struct Biol 12 (2002) 679-684
80. Dai W., Jia Q., Bortz E., Shah S., Liu J., Atanasov I., Li X., Taylor K.A., Sun R., and Zhou Z.H. Unique structures of a tumor herpesvirus revealed by cryo-electron tomography and microscopy. J Struct Biol 161 (2008) 428-438
81. Wikoff W.R., Liljas L., Duda R.L., Tsuruta H., Hendrix R.W., and Johnson J.E. Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289 (2000) 2129-2133
82. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera - a visualization system for exploratory research and analysis. J Comput Chem 25 (2004) 1605-1612