Near-atomic resolution reconstructions of icosahedral viruses from electron cryo-microscopy

Current Opinion in Structural Biology

Volumn 21, Issue 2, 2011, Pages 265-273

  Grigorieff, Nikolaus ^a,c   Harrison, Stephen C ^b,c  

^a BRANDEIS UNIVERSITY   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; DOUBLE STRANDED RNA;

ADENOVIRUS; BACTERIOPHAGE; CRYOELECTRON MICROSCOPY; ELECTRON BEAM; IMAGE ENHANCEMENT; IMAGE PROCESSING; IMAGE QUALITY; IMAGE RECONSTRUCTION; IMAGING SYSTEM; NONHUMAN; PAPILLOMA VIRUS; PRIORITY JOURNAL; RADIATION SCATTERING; RADIOLYSIS; REVIEW; ROTAVIRUS; THREE DIMENSIONAL IMAGING; VIRUS CAPSID; VIRUS GENOME; VIRUS MORPHOLOGY; X RAY CRYSTALLOGRAPHY;

COMPUTER SIMULATION; CRYOELECTRON MICROSCOPY; IMAGE PROCESSING, COMPUTER-ASSISTED; MODELS, MOLECULAR; VIRUS ASSEMBLY; VIRUSES;

EID: 79953108462     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2011.01.008     Document Type: Review

References (73)

1. Zhang X., Settembre E., Xu C., Dormitzer P.R., Bellamy R., Harrison S.C., Grigorieff N. Near-atomic resolution using electron cryomicroscopy and single-particle reconstruction. Proc Natl Acad Sci U S A 2008, 105:1867-1872.
2. Jiang W., Baker M.L., Jakana J., Weigele P.R., King J., Chiu W. Backbone structure of the infectious epsilon15 virus capsid revealed by electron cryomicroscopy. Nature 2008, 451:1130-1134.
3. Yu X., Jin L., Zhou Z.H. 3.88 A structure of cytoplasmic polyhedrosis virus by cryo-electron microscopy. Nature 2008, 453:415-419.
4. Chen J.Z., Settembre E.C., Aoki S.T., Zhang X., Bellamy A.R., Dormitzer P.R., Harrison S.C., Grigorieff N. Molecular interactions in rotavirus assembly and uncoating seen by high-resolution cryo-EM. Proc Natl Acad Sci U S A 2009, 106:10644-10648.
5. Wolf M., Garcea R.L., Grigorieff N., Harrison S.C. Subunit interactions in bovine papillomavirus. Proc Natl Acad Sci U S A 2010, 107:6298-6303.
6. Zhang X., Jin L., Fang Q., Hui W.H., Zhou Z.H. 3.3 A cryo-EM structure of a nonenveloped virus reveals a priming mechanism for cell entry. Cell 2010, 141:472-482.
7. Liu X., Zhang Q., Murata K., Baker M.L., Sullivan M.B., Fu C., Dougherty M.T., Schmid M.F., Osburne M.S., Chisholm S.W., et al. Structural changes in a marine podovirus associated with release of its genome into Prochlorococcus. Nat Struct Mol Biol 2010, 17:830-836.
8. Liu H., Jin L., Koh S.B., Atanasov I., Schein S., Wu L., Zhou Z.H. Atomic structure of human adenovirus by cryo-EM reveals interactions among protein networks. Science 2010, 329:1038-1043.
9. Settembre E.C., Chen J.Z., Dormitzer P.R., Grigorieff N., Harrison S.C. Atomic model of an infectious rotavirus particle. Embo J 2011, 30:408-416.
10. Henderson R. The potential and limitations of neutrons, electrons and X-rays for atomic resolution microscopy of unstained biological molecules. Q Rev Biophys 1995, 28:171-193.
11. Glaeser R.M. Review: electron crystallography: present excitement, a nod to the past, anticipating the future. J Struct Biol 1999, 128:3-14.
12. Böttcher B., Wynne S.A., Crowther R.A. Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature 1997, 386:88-91.
13. Conway J.F., Cheng N., Zlotnick A., Wingfield P.T., Stahl S.J., Steven A.C. Visualization of a 4-helix bundle in the hepatitis B virus capsid by cryo-electron microscopy. Nature 1997, 386:91-94.
14. Armache J.P., Jarasch A., Anger A.M., Villa E., Becker T., Bhushan S., Jossinet F., Habeck M., Dindar G., Franckenberg S., et al. Localization of eukaryote-specific ribosomal proteins in a 5.5-A cryo-EM map of the 80S eukaryotic ribosome. Proc Natl Acad Sci U S A 2010, 107:19754-19759.
15. Henderson R. Image contrast in high-resolution electron microscopy of biological macromolecules: TMV in ice. Ultramicroscopy 1992, 46:1-18.
16. Glaeser R.M. Retrospective: radiation damage and its associated " information limitations" J Struct Biol 2008, 163:271-276.
17. Chen J.Z., Sachse C., Xu C., Mielke T., Spahn C.M., Grigorieff N. A dose-rate effect in single-particle electron microscopy. J Struct Biol 2008, 161:92-100.
18. Rhinow D., Kuhlbrandt W. Electron cryo-microscopy of biological specimens on conductive titanium-silicon metal glass films. Ultramicroscopy 2008, 108:698-705.
19. Yoshioka C., Carragher B., Potter C.S. Cryomesh: a new substrate for cryo-electron microscopy. Microsc Microanal 2010, 16:43-53.
20. Ermantraut E., Wohlfart K., Tichelaar W. Perforated support foils with pre-defined hole size, shape and arrangement. Ultramicroscopy 1998, 74:75-81.
21. Quispe J., Damiano J., Mick S.E., Nackashi D.P., Fellmann D., Ajero T.G., Carragher B., Potter C.S. An improved holey carbon film for cryo-electron microscopy. Microsc Microanal 2007, 13:365-371.
22. Bullough P., Henderson R. Use of spot-scan procedure for recording low-dose micrographs of beam-sensitive specimens. Ultramicroscopy 1987, 21:223-230.
23. Fujiyoshi Y. The structural study of membrane proteins by electron crystallography. Adv Biophys 1998, 35:25-80.
24. Stark H., Zemlin F., Boettcher C. Electron radiation damage to protein crystals of bacteriorhodopsin at different temperatures. Ultramicroscopy 1996, 63:75-79.
25. Bammes B.E., Jakana J., Schmid M.F., Chiu W. Radiation damage effects at four specimen temperatures from 4 to 100K. J Struct Biol 2010, 169:331-341.
26. Wright E.R., Iancu C.V., Tivol W.F., Jensen G.J. Observations on the behavior of vitreous ice at approximately 82 and approximately 12K. J Struct Biol 2006, 153:241-252.
27. McMullan G., Chen S., Henderson R., Faruqi A.R. Detective quantum efficiency of electron area detectors in electron microscopy. Ultramicroscopy 2009, 109:1126-1143.
28. Milazzo A.C., Leblanc P., Duttweiler F., Jin L., Bouwer J.C., Peltier S., Ellisman M., Bieser F., Matis H.S., Wieman H., et al. Active pixel sensor array as a detector for electron microscopy. Ultramicroscopy 2005, 104:152-159.
29. Cambie R., Downing K.H., Typke D., Glaeser R.M., Jin J. Design of a microfabricated, two-electrode phase-contrast element suitable for electron microscopy. Ultramicroscopy 2007, 107:329-339.
30. Danev R., Nagayama K. Transmission electron microscopy with Zernike phase plate. Ultramicroscopy 2001, 88:243-252.
31. Majorovits E., Barton B., Schultheiss K., Perez-Willard F., Gerthsen D., Schroder R.R. Optimizing phase contrast in transmission electron microscopy with an electrostatic (Boersch) phase plate. Ultramicroscopy 2007, 107:213-226.
32. Muller H., Jin J., Danev R., Spence J., Padmore H., Glaeser R.M. Design of an electron microscope phase plate using a focused continuous-wave laser. New J Phys 2010, 12.
33. Rosenthal P.B., Henderson R. Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J Mol Biol 2003, 333:721-745.
34. Stewart A., Grigorieff N. Noise bias in the refinement of structures derived from single particles. Ultramicroscopy 2004, 102:67-84.
35. Liu H., Cheng L., Zeng S., Cai C., Zhou Z.H., Yang Q. Symmetry-adapted spherical harmonics method for high-resolution 3D single-particle reconstructions. J Struct Biol 2008, 161:64-73.
36. Navaza J. On the three-dimensional reconstruction of icosahedral particles. J Struct Biol 2003, 144:13-23.
37. Scheres S.H.W., Valle M., Carazo J.M. Fast maximum likelihood refinement of electron microscopy images. Bioinformatics 2005, 21(Suppl. 2):ii243-ii244.
38. Sigworth F.J. A maximum-likelihood approach to single-particle image refinement. J Struct Biol 1998, 122:328-339.
39. Aldroubi A., Trus B.L., Unser M., Booy F.P., Steven A.C. Magnification mismatches between micrographs: corrective procedures and implications for structural analysis. Ultramicroscopy 1992, 46:175-188.
40. Thon F. Zur Defokussierungsabhängigkeit des Phasenkontrastes bei der elektronenmikroskopischen Abbildung. Zeitschrift für Naturforschung 1966, 21a:476-478.
41. Mindell J.A., Grigorieff N. Accurate determination of local defocus and specimen tilt in electron microscopy. J Struct Biol 2003, 142:334-347.
42. Zemlin F., Weiss K., Schiske P., Kunath W., Herrmann K.-H. Coma-free alignment of high resolution electron microscopes with the aid of optical diffractograms. Ultramicroscopy 1978, 3:49-60.
43. Smith D.J., Saxton W.O., O'Keefe M.A., Wood G.J., Stobbs W.M. The importance of beam alignment and crystal tilt in high resolution electron microscopy. Ultramicroscopy 1983, 11.
44. Henderson R., Baldwin J.M., Downing K.H., Lepault J., Zemlin F. Structure of purple membrane from halobacterium halobium: recording, measurement and evaluation of electron micrographs at 3.5Å resolution. Ultramicroscopy 1986, 19:147-178.
45. Grigorieff N. FREALIGN: high-resolution refinement of single particle structures. J Struct Biol 2007, 157:117-125.
46. DeRosier D.J. Correction of high-resolution data for curvature of the Ewald sphere. Ultramicroscopy 2000, 81:83-98.
47. Wolf M., DeRosier D.J., Grigorieff N. Ewald sphere correction for single-particle electron microscopy. Ultramicroscopy 2006, 106:376-382.
48. Crowther R.A., Amos L.A., Finch J.T., De Rosier D.J., Klug A. Three dimensional reconstructions of spherical viruses by fourier synthesis from electron micrographs. Nature 1970, 226:421-425.
49. 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 1971, 261:221-230.
50. Estrozi L.F., Navaza J. Ab initio high-resolution single-particle 3D reconstructions: the symmetry adapted functions way. J Struct Biol 2010, 172:253-260.
51. Liang Y., Ke E.Y., Zhou Z.H. IMIRS: a high-resolution 3D reconstruction package integrated with a relational image database. J Struct Biol 2002, 137:292-304.
52. Ludtke S.J., Baldwin P.R., Chiu W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 1999, 128:82-97.
53. Penczek P.A. Fundamentals of three-dimensional reconstruction from projections. Methods Enzymol 2010, 482:1-33.
54. Schmid M.F., Sherman M.B., Matsudaira P., Tsuruta H., Chiu W. Scaling structure factor amplitudes in electron cryomicroscopy using X-ray solution scattering. J Struct Biol 1999, 128:51-57.
55. Harauz G., van Heel M. Exact filters for general geometry three dimensional reconstruction. Optik 1986, 73:146-156.
56. Grigorieff N. Resolution measurement in structures derived from single particles. Acta Crystallogr D Biol Crystallogr 2000, 56:1270-1277.
57. Huang Z., Baldwin P.R., Mullapudi S., Penczek P.A. Automated determination of parameters describing power spectra of micrograph images in electron microscopy. J Struct Biol 2003, 144:79-94.
58. Wikoff W.R., Liljas L., Duda R.L., Tsuruta H., Hendrix R.W., Johnson J.E. Topologically linked protein rings in the bacteriophage HK97 capsid. Science 2000, 289:2129-2133.
59. McClain B., Settembre E., Temple B.R., Bellamy A.R., Harrison S.C. X-ray crystal structure of the rotavirus inner capsid particle at 3.8 A resolution. J Mol Biol 2010, 397:587-599.
60. Trask S.D., Dormitzer P.R. Assembly of highly infectious rotavirus particles recoated with recombinant outer capsid proteins. J Virol 2006, 80:11293-11304.
61. Reinisch K.M., Nibert M.L., Harrison S.C. Structure of the reovirus core at 3.6 A resolution. Nature 2000, 404:960-967.
62. Grimes J.M., Burroughs J.N., Gouet P., Diprose J.M., Malby R., Zientara S., Mertens P.P., Stuart D.I. The atomic structure of the bluetongue virus core. Nature 1998, 395:470-478.
63. Dryden K.A., Wang G., Yeager M., Nibert M.L., Coombs K.M., Furlong D.B., Fields B.N., Baker T.S. Early steps in reovirus infection are associated with dramatic changes in supramolecular structure and protein conformation: analysis of virions and subviral particles by cryoelectron microscopy and image reconstruction. J Cell Biol 1993, 122:1023-1041.
64. Liemann S., Chandran K., Baker T.S., Nibert M.L., Harrison S.C. Structure of the reovirus membrane-penetration protein, Mu1, in a complex with is protector protein, Sigma3. Cell 2002, 108:283-295.
65. Zhang X., Ji Y., Zhang L., Harrison S.C., Marinescu D.C., Nibert M.L., Baker T.S. Features of reovirus outer capsid protein mu1 revealed by electron cryomicroscopy and image reconstruction of the virion at 7.0 Angstrom resolution. Structure 2005, 13:1545-1557.
66. Chen X.S., Garcea R.L., Goldberg I., Casini G., Harrison S.C. Structure of small virus-like particles assembled from the L1 protein of human papillomavirus 16. Mol Cell 2000, 5:557-567.
67. Modis Y., Trus B.L., Harrison S.C. Atomic model of the papillomavirus capsid. EMBO J 2002, 21:4754-4762.
68. Harrison S.C. Protein interfaces and intersubunit bonding. The case of tomato bushy stunt virus. Biophys J 1980, 32:139-153.
69. Harrison S.C. Looking inside adenovirus. Science 2010, 329:1026-1027.
70. Chen J.Z., Grigorieff N. SIGNATURE: a single-particle selection system for molecular electron microscopy. J Struct Biol 2007, 157:168-173.
71. Jones T.A. Molecular Replacement 1992, Science and Engineering Research Council, Daresbury Laboratory. E.J. Dodson, S. Gover, Wolf W: (Eds.).
72. Kleywegt G.J., Zou J.Y., Kjeldgaard M., Jones T.A. International Tables for Crystallography 2001, Kluwer Academic. M.G. Rossmann, Arnold E: (Eds.).
73. Liu X., Jiang W., Jakana J., Chiu W. Averaging tens to hundreds of icosahedral particle images to resolve protein secondary structure elements using a Multi-Path Simulated Annealing optimization algorithm. J Struct Biol 2007, 160:11-27.