Seeing tobacco mosaic virus through direct electron detectors

Journal of Structural Biology

Volumn 189, Issue 2, 2015, Pages 87-97

  Fromm, Simon A ^a   Bharat, Tanmay A M ^b   Jakobi, Arjen J ^a,c   Hagen, Wim J H ^a   Sachse, Carsten ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Direct electron detectors; High resolution electron cryo microscopy; Radiation damage; Single particle helical reconstruction; Tobacco mosaic virus

Indexed keywords

CARBOXYL GROUP; CAPSID PROTEIN;

ARTICLE; DIRECT ELECTRON DETECTOR; ELECTRON MICROSCOPE; ELECTRON MICROSCOPY; IMAGE PROCESSING; IMAGE QUALITY; IMAGE RECONSTRUCTION; NONHUMAN; PERFORMANCE; PRIORITY JOURNAL; RADIATION INJURY; TOBACCO MOSAIC VIRUS; CHEMICAL STRUCTURE; CRYOELECTRON MICROSCOPY; DEVICES; PROTEIN QUATERNARY STRUCTURE; ULTRASTRUCTURE;

FALCONIDAE; TOBACCO MOSAIC VIRUS;

CAPSID PROTEINS; CRYOELECTRON MICROSCOPY; MODELS, MOLECULAR; PROTEIN STRUCTURE, QUATERNARY; TOBACCO MOSAIC VIRUS;

EID: 84922595259     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2014.12.002     Document Type: Article

References (51)

1. Adams P.D., Afonine P.V., Bunkoczi G., Chen V.B., Davis I.W., Echols N., Headd J.J., Hung L.W., Kapral G.J., Grosse-Kunstleve R.W., et al. PHENIX: a comprehensive python-based system for macromolecular structure solution. Acta Crystallogr. 2010, D66(2010):213-221.
2. Adrian M., Dubochet J., Lepault J., McDowall A. Cryo-electron microscopy of viruses. Nature 1984, 308:32-36.
3. Allegretti M., Mills D.J., McMullan G., Kühlbrandt W., Vonck J. Atomic model of the F420-reducing [NiFe] hydrogenase by electron cryo-microscopy using a direct electron detector. eLife 2014, 3:e01963.
4. Amunts A., Brown A., Bai X.C., Llacer J.L., Hussain T., Emsley P., Long F., Murshudov G., Scheres S.H.W., Ramakrishnan V. Structure of the yeast mitochondrial large ribosomal subunit. Science 2014, 343:1485-1489.
5. Bai X.-C., Fernandez I.S., McMullan G., Scheres S.H. Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles. eLife 2013, 2:e00461.
6. Bartesaghi A., Matthies D., Banerjee S., Merk A., Subramaniam S. Structure of β-galactosidase at 3.2-Å resolution obtained by cryo-electron microscopy. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:11709-11714.
7. Bernal J.D., Fankuchen I. X-ray and crystallographic studies of plant virus preparations. III. J. Gen. Physiol. 1941, 25:147-165.
8. Brilot A.F., Chen J.Z., Cheng A., Pan J., Harrison S.C., Potter C.S., Carragher B., Henderson R., Grigorieff N. Beam-induced motion of vitrified specimen on holey carbon film. J. Struct. Biol. 2012, 177:630-637.
9. Campbell M.G., Cheng A., Brilot A.F., Moeller A., Lyumkis D., Veesler D., Pan J., Harrison S.C., Potter C.S., Carragher B., et al. Movies of ice-embedded particles enhance resolution in electron cryo-microscopy. Structure 2012, 20:1823-1828.
10. Chen S., McMullan G., Faruqi A.R., Murshudov G.N., Short J.M., Scheres S.H.W., Henderson R. Ultramicroscopy 2013, 135:24-35.
11. Clare D.K., Orlova E.V. 4.6Å Cryo-EM reconstruction of tobacco mosaic virus from images recorded at 300keV on a 4k×4k CCD camera. J. Struct. Biol. 2009, 171:303-308.
12. Cyrklaff M., Kühlbrandt W. High-resolution electron microscopy of biological specimens in cubic ice. Ultramicroscopy 1994, 55:141-153.
13. Desfosses A., Ciuffa R., Gutsche I., Sachse C. SPRING - an image processing package for single-particle based helical reconstruction from electron cryomicrographs. J. Struct. Biol. 2014, 185:15-26.
14. Egelman E.H. A robust algorithm for the reconstruction of helical filaments using single-particle methods. Ultramicroscopy 2000, 85:225-234.
15. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2126-2132.
16. Faruqi A.R., Henderson R. Electronic detectors for electron microscopy. Curr. Opin. Struct. Biol. 2007, 17:549-555.
17. Fernandez I.S., Bai X.-C., Hussain T., Kelley A.C., Lorsch J.R., Ramakrishnan V., Scheres S.H.W. Molecular architecture of a eukaryotic translational initiation complex. Science 2013, 342:1240585.
18. Ge P., Zhou Z.H. Hydrogen-bonding networks and RNA bases revealed by cryo electron microscopy suggest a triggering mechanism for calcium switches. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:9637-9642.
19. Grigorieff N. Direct detection pays off for electron cryo-microscopy. eLife 2013, 2:e00573.
20. Grigorieff N., Ceska T., Downing K., Baldwin J., Henderson R. Electron-crystallographic refinement of the structure of bacteriorhodopsin. J. Mol. Biol. 1996, 259:393-421.
21. Henderson R. Cryo-protection of protein crystals against radiation damage in electron and X-ray diffraction. Proc. R. Soc. Lond. B Biol. Sci. 1990, 241:6-8.
22. Henderson R., Baldwin J.M., Ceska T.A., Zemlin F., Beckmann E., Downing K.H. Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J. Mol. Biol. 1990, 213:899-929.
23. ICRU (1984). Stopping Powers for Electrons and Positrons (Report 37) (Bethesda, Maryland, USA).
24. Karuppasamy M., Karimi Nejadasl F., Vulovic M., Koster A.J., Ravelli R.B.G. Radiation damage. J. Synchrotron Radiat. 2011, 18:398-412.
25. Kucukelbir A., Sigworth F.J., Tagare H.D. Quantifying the local resolution of cryo-EM density maps. Nat. Methods 2014, 11:63-65.
26. Li X., Mooney P., Zheng S., Booth C.R., Braunfeld M.B., Gubbens S., Agard D.A., Cheng Y. Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat. Methods 2013, 10:584-590.
27. Li X., Zheng S.Q., Egami K., Agard D.A., Cheng Y. J. Struct. Biol. 2013, 184:251-260.
28. Liao M., Cao E., Julius D., Cheng Y. Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 2013, 504:107-112.
29. Lu P., Bai X.-C., Ma D., Xie T., Yan C., Sun L., Yang G., Zhao Y., Zhou R., Scheres S.H.W., et al. Three-dimensional structure of human γ-secretase. Nature 2014, 512:166-170.
30. Mastronarde D.N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 2005, 152:36-51.
31. McMullan G., Faruqi A.R., Clare D., Henderson R. Comparison of optimal performance at 300keV of three direct electron detectors for use in low dose electron microscopy. Ultramicroscopy 2014, 147:156-163.
32. Mindell J.A., Grigorieff N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 2003, 142:334-347.
33. Owen R.L., Rudiño-Piñera E., Garman E.F. Experimental determination of the radiation dose limit for cryocooled protein crystals. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:4912-4917.
34. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., Ferrin T.E. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
35. Ravelli R., Garman E. Radiation damage in macromolecular cryocrystallography. Curr. Opin. Struct. Biol. 2006, 16:624-629.
36. 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.
37. Ruskin R.S., Yu Z., Grigorieff N. Quantitative characterization of electron detectors for transmission electron microscopy. J. Struct. Biol. 2013, 184:385-393.
38. Sachse C., Chen J.Z., Coureux P.-D., Stroupe M.E., Fändrich M., Grigorieff N. High-resolution electron microscopy of helical specimens: a fresh look at tobacco mosaic virus. J. Mol. Biol. 2007, 371:812-835.
39. Scheres S.H. Beam-induced motion correction for sub-megadalton cryo-EM particles. eLife 2014, 3:e03665.
40. Scheres S.H.W., Chen S. Prevention of overfitting in cryo-EM structure determination. Nat. Methods 2012, 9:853-854.
41. Shigematsu H., Sigworth F.J. Noise models and cryo-EM drift correction with a direct-electron camera. Ultramicroscopy 2013, 131:61-69.
42. Tang G., Peng L., Baldwin P.R., Mann D.S., Jiang W., Rees I., Ludtke S.J. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 2007, 157:38-46.
43. Unwin N. Refined structure of the nicotinic acetylcholine receptor at 4A resolution. J. Mol. Biol. 2005, 346:967-989.
44. Vinothkumar K.R., McMullan G., Henderson R. Molecular mechanism of antibody-mediated activation of β-galactosidase. Structure 2014, 22:621-627.
45. Voorhees R.M., Fernandez I.S., Scheres S.H.W., Hegde R.S. Structure of the Mammalian ribosome-sec61 complex to 3.4Å resolution. Cell 2014, 157:1632-1643.
46. Wang Z., Hryc C.F., Bammes B., Afonine P.V., Jakana J., Chen D.-H., Liu X., Baker M.L., Kao C., Ludtke S.J., et al. An atomic model of brome mosaic virus using direct electron detection and real-space optimization. Nat. Commun. 2014, 5:4808.
47. Weik M., Ravelli R.B., Kryger G., McSweeney S., Raves M.L., Harel M., Gros P., Silman I., Kroon J., Sussman J.L. Specific chemical and structural damage to proteins produced by synchrotron radiation. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:623-628.
48. Winn M.D., Ballard C.C., Cowtan K.D., Dodson E.J., Emsley P., Evans P.R., Keegan R.M., Krissinel E.B., Leslie A.G.W., McCoy A., et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 2011, 67:235-242.
49. Yu X., Jin L., Zhou Z.H. 3.88A structure of cytoplasmic polyhedrosis virus by cryo-electron microscopy. Nature 2008, 453:415-419.
50. Zhang X., Zhou Z.H. Limiting factors in atomic resolution cryo electron microscopy: no simple tricks. J. Struct. Biol. 2011, 175:253-263.
51. 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.