Reaching the information limit in cryo-EM of biological macromolecules: Experimental aspects

Biophysical Journal

Volumn 100, Issue 10, 2011, Pages 2331-2337

  Glaeser, Robert M ^a   Hall, Richard J ^b  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 79959668319     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.04.018     Document Type: Review

References (64)

1. Glaeser, R. M. 2008. Cryo-electron microscopy of biological nanostructures. Phys. Today. 61:48-54.
2. Mulder, A. M., C. Yoshioka,..., J. R. Williamson. 2010. Visualizing ribosome biogenesis: parallel assembly pathways for the 30S subunit. Science. 330:673-677.
3. Fischer, N., A. L. Konevega,..., H. Stark. 2010. Ribosome dynamics and tRNA movement by time-resolved electron cryomicroscopy. Nature. 466:329-333.
4. Leis, A., B. Rockel,..., W. Baumeister. 2009. Visualizing cells at the nanoscale. Trends Biochem. Sci. 34:60-70.
5. Glaeser, R. M. 2008. Retrospective: radiation damage and its associated "information limitations". J. Struct. Biol. 163:271-276.
6. Baker, L. A., E. A. Smith,..., J. L. Rubinstein. 2010. The resolution dependence of optimal exposures in liquid nitrogen temperature electron cryomicroscopy of catalase crystals. J. Struct. Biol. 169:431-437.
7. Harrison, S. C. 2010. Virology. Looking inside adenovirus. Science. 329:1026-1027.
8. Frank, J. 2006. Three-Dimensional Electron Microscopy of Macromolecular Assemblies-Visualization of Biological Molecules in their Native State. Oxford University Press, New York.
9. Glaeser, R. M., K. Downing,..., J. Frank. 2007. Electron Crystallography of Biological Macromolecules. Oxford University Press, New York.
10. Zernike, F. 1955. How I discovered phase contrast. Science. 121:345-349.
11. Wang, L. G., P. S. Bose, and F. J. Sigworth. 2006. Using cryo-EM to measure the dipole potential of a lipid membrane. Proc. Natl. Acad. Sci. USA. 103:18528-18533. (Pubitemid 44913444)
12. Bammes, B. E., J. Jakana,..., W. Chiu. 2010. Radiation damage effects at four specimen temperatures from 4 to 100 K. J. Struct. Biol. 169:331-341.
13. McMullan, G., S. Chen,..., A. R. Faruqi. 2009. Detective quantum efficiency of electron area detectors in electron microscopy. Ultramicroscopy. 109:1126-1143.
14. McEwen, B. F., K. H. Downing, and R. M. Glaeser. 1995. The relevance of dose-fractionation in tomography of radiation-sensitive specimens. Ultramicroscopy. 60:357-373.
15. Hoppe, W., and R. Hegerl. 1981. Some remarks concerning the influence of electron noise on 3D reconstruction. Ultramicroscopy. 6:205-206. (Pubitemid 12511113)
16. Saxberg, B. E. H., and W. O. Saxton. 1981. Quantum noise in 2D projections and 3D reconstructions. Ultramicroscopy. 6:85-90.
17. Henderson, R. 1995. The potential and limitations of neutrons, electrons and X-rays for atomic resolution microscopy of unstained biological molecules. Q. Rev. Biophys. 28:171-193.
18. Glaeser, R. M. 1999. Review: electron crystallography: present excitement, a nod to the past, anticipating the future. J. Struct. Biol. 128:3-14. (Pubitemid 30013425)
19. Rosenthal, P. B., and R. Henderson. 2003. Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J. Mol. Biol. 333:721-745. (Pubitemid 37268015)
20. Wolf, M., R. L. Garcea,..., S. C. Harrison. 2010. Subunit interactions in bovine papillomavirus. Proc. Natl. Acad. Sci. USA. 107:6298-6303.
21. Chen, J. Z., E. C. Settembre,..., N. Grigorieff. 2009. Molecular interactions in rotavirus assembly and uncoating seen by high-resolution cryo-EM. Proc. Natl. Acad. Sci. USA. 106:10644-10648.
22. Jiang, W., M. L. Baker,..., W. Chiu. 2008. Backbone structure of the infectious epsilon15 virus capsid revealed by electron cryomicroscopy. Nature. 451:1130-1134. (Pubitemid 351317451)
23. Yu, X. K., L. Jin, and Z. H. Zhou. 2008. 3.88 A structure of cytoplasmic polyhedrosis virus by cryo-electron microscopy. Nature. 453:415-419. (Pubitemid 351693126)
24. Zhang, X., E. Settembre,..., N. Grigorieff. 2008. Near-atomic resolution using electron cryomicroscopy and single-particle reconstruction. Proc. Natl. Acad. Sci. USA. 105:1867-1872. (Pubitemid 351439431)
25. Zhang, X., L. Jin,..., Z. H. Zhou. 2010. 3.3 A cryo-EM structure of a nonenveloped virus reveals a priming mechanism for cell entry. Cell. 141:472-482.
26. Zhou, Z. H. 2008. Towards atomic resolution structural determination by single-particle cryo-electron microscopy. Curr. Opin. Struct. Biol. 18:218-228.
27. Liu, H. R., L. Jin,..., Z. H. Zhou. 2010. Atomic structure of human adenovirus by cryo-EM reveals interactions among protein networks. Science. 329:1038-1043.
28. Chen, D.-H., M. L. Baker,..., W. Chiu. 2011. Structural basis for scaffolding-mediated assembly and maturation of a dsDNA virus. Proc. Natl. Acad. Sci. U. S. A. 108:1355-1360.
29. Löwe, J., H. Li,..., E. Nogales. 2001. Refined structure of αβ-tubulin at 3.5 A resolution. J. Mol. Biol. 313:1045-1057. (Pubitemid 33081900)
30. Gonen, T., Y. F. Cheng,..., T. Walz. 2005. Lipid-protein interactions in double-layered two-dimensional AQP0 crystals. Nature. 438:633-638. (Pubitemid 41740568)
31. Yonekura, K., S. Maki-Yonekura, and K. Namba. 2003. Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature. 424:643-650. (Pubitemid 36987983)
32. Unwin, N. 2005. Refined structure of the nicotinic acetylcholine receptor at 4A resolution. J. Mol. Biol. 346:967-989. (Pubitemid 40215523)
33. Zhang, J. J., M. L. Baker,..., W. Chiu. 2010. Mechanism of folding chamber closure in a group II chaperonin. Nature. 463:379-383.
34. Ludtke, S. J., M. L. Baker,..., W. Chiu. 2008. De novo backbone trace of GroEL from single particle electron cryomicroscopy. Structure. 16:441-448. (Pubitemid 351324126)
35. Cong, Y., M. L. Baker,..., W. Chiu. 2010. 4.0-A resolution cryo-EM structure of the mammalian chaperonin TRiC/CCT reveals its unique subunit arrangement. Proc. Natl. Acad. Sci. USA. 107:4967-4972.
36. Amit, M., S. J. Weisberg,..., A. Horovitz. 2010. Equivalent mutations in the eight subunits of the chaperonin CCT produce dramatically different cellular and gene expression phenotypes. J. Mol. Biol. 401:532-543.
37. Schuette, J. C., F. V. Murphy, 4th,..., C. M. Spahn. 2009. GTPase activation of elongation factor EF-Tu by the ribosome during decoding. EMBO J. 28:755-765.
38. Villa, E., J. Sengupta,..., J. Frank. 2009. Ribosome-induced changes in elongation factor Tu conformation control GTP hydrolysis. Proc. Natl. Acad. Sci. USA. 106:1063-1068.
39. Armache, J. P., A. Jarasch,..., R. Beckmann. 2010. Cryo-EM structure and rRNA model of a translating eukaryotic 80S ribosome at 5.5-A resolution. Proc. Natl. Acad. Sci. USA. 107:19748-19753.
40. Spahn, C. M. T., and P. A. Penczek. 2009. Exploring conformational modes of macromolecular assemblies by multiparticle cryo-EM. Curr. Opin. Struct. Biol. 19:623-631.
41. Battaglia, M., D. Contarato,..., V. Radmilovic. 2010. Characterisation of a CMOS active pixel sensor for use in the TEAM microscope. Nucl. Instrum. Methods Phys. Res. A. 622:669-677.
42. Li, S. D., H. S. Matis,..., S. Kleinfelder. 2009. Modeling and analysis of charged-particle CMOS image sensor arrays. IEEE Trans. Nucl. Sci. 56:1062-1068.
43. Chang, W. H., M. T. K. Chiu,..., I. P. Tu. 2010. Zernike phase plate cryoelectron microscopy facilitates single particle analysis of unstained asymmetric protein complexes. Structure. 18:17-27.
44. Boersch, H. 1947. Uber die Kontraste von Atomen im Electronenmikroskop. Z. Naturforschg. 2 a: 615-633.
45. Nagayama, K. 2008. Development of phase plates for electron microscopes and their biological application. Eur. Biophys. J. 37:345-358.
46. Nagayama, K., and R. Danev. 2008. Phase contrast electron microscopy: development of thin-film phase plates and biological applications. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363:2153-2162. (Pubitemid 351693527)
47. Danev, R., R. M. Glaeser, and K. Nagayama. 2009. Practical factors affecting the performance of a thin-film phase plate for transmission electron microscopy. Ultramicroscopy. 109:312-325.
48. Murata, K., X. A. Liu,..., W. Chiu. 2010. Zernike phase contrast cryoelectron microscopy and tomography for structure determination at nanometer and subnanometer resolutions. Structure. 18:903-912.
49. Danev, R., and K. Nagayama. 2008. Single particle analysis based on Zernike phase contrast transmission electron microscopy. J. Struct. Biol. 161:211-218.
50. Danev, R., S. Kanamaru,..., K. Nagayama. 2010. Zernike phase contrast cryo-electron tomography. J. Struct. Biol. 171:174-181.
51. Danev, R., and K. Nagayama. 2001. Transmission electron microscopy with Zernike phase plate. Ultramicroscopy. 88:243-252. (Pubitemid 32737552)
52. Schultheiss, K., F. Perez-Willard,..., R. R. Schroder. 2006. Fabrication of a Boersch phase plate for phase contrast imaging in a transmission electron microscope. Rev. Sci. Instrum. 77:033701-033704.
53. Cambie, R., K. H. Downing,..., J. Jin. 2007. Design of a microfabricated, two-electrode phase-contrast element suitable for electron microscopy. Ultramicroscopy. 107:329-339. (Pubitemid 46136725)
54. Majorovits, E., B. Barton,..., R. R. Schröder. 2007. Optimizing phase contrast in transmission electron microscopy with an electrostatic (Boersch) phase plate. Ultramicroscopy. 107:213-226. (Pubitemid 44959451)
55. Mueller, H., J. A. Jin,..., R. M. Glaeser. 2010. Design of an electron microscope phase plate using a focused continuous-wave laser. N. J. Phys. 12:073011.
56. Henderson, R., and R. M. Glaeser. 1985. Quantitative analysis of image contrast in electron micrographs of beam-sensitive crystals. Ultramicroscopy. 16:139-150. (Pubitemid 15509886)
57. Sander, B., M. M. Golas, and H. Stark. 2003. Automatic CTF correction for single particles based upon multivariate statistical analysis of individual power spectra. J. Struct. Biol. 142:392-401. (Pubitemid 36644152)
58. Downing, K. H. 1991. Spot-scan imaging in transmission electron microscopy. Science. 251:53-59. (Pubitemid 21916850)
59. Bullough, P., and R. Henderson. 1987. Use of spot-scan procedure for recording low-dose micrographs of beam-sensitive specimens. Ultramicroscopy. 21:223-229. (Pubitemid 17606354)
60. Typke, D., K. H. Downing, and R. M. Glaeser. 2004. Electron microscopy of biological macromolecules: bridging the gap between what physics allows and what we currently can get. Microsc. Microanal. 10:21-27. (Pubitemid 38272163)
61. Yoshioka, C., B. Carragher, and C. S. Potter. 2010. Cryomesh: a new substrate for cryo-electron microscopy. Microsc. Microanal. 16:43-53.
62. Glaeser, R. M., G. McMullan,..., R. Henderson. 2011. Images of paraffin monolayer crystals with perfect contrast: minimization of beam-induced specimen motion. Ultramicroscopy. 111:90-100.
63. Toyoshima, C., and N. Unwin. 1988. Contrast transfer for frozenhydrated specimens: determination from pairs of defocused images. Ultramicroscopy. 25:279-291.
64. Yonekura, K., M. B. Braunfeld,..., D. A. Agard. 2006. Electron energy filtering significantly improves amplitude contrast of frozen-hydrated protein at 300kV. J. Struct. Biol. 156:524-536. (Pubitemid 44751474)