Quantifying resolution limiting factors in subtomogram averaged cryo-electron tomography using simulations

Journal of Structural Biology

Volumn 187, Issue 2, 2014, Pages 103-111

  Voortman, Lenard M ^a   Vulović, Miloš ^a,b   Maletta, Massimiliano ^c   Voigt, Andreas ^d   Franken, Erik M ^d   Simonetti, Angelita ^e   Peters, Peter J ^b,c   van Vliet, Lucas J ^a   Rieger, Bernd ^a  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c ANTONI VAN LEEUWENHOEK HOSPITAL   (Netherlands)

^d Thermo Fisher Scientific   (United States)

^e UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Acquisition protocol; Cryo EM; Ribosome; Subtomogram averaging; TEM image simulation; Tilted CTF correction; Tomography

Indexed keywords

ALGORITHM; ARTICLE; ELECTRON TOMOGRAPHY; IMAGE RECONSTRUCTION; INFORMATION PROCESSING; PREDICTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RIBOSOME; SIMULATION; SIMULATOR; SUBTOMOGRAM AVERAGING; TRANSMISSION ELECTRON MICROSCOPY; CRYOELECTRON MICROSCOPY; IMAGE PROCESSING; MACROMOLECULE; PROCEDURES; ULTRASTRUCTURE;

MACROMOLECULE;

CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; IMAGE PROCESSING, COMPUTER-ASSISTED; MACROMOLECULAR SUBSTANCES; RIBOSOMES;

EID: 84905221054     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2014.06.007     Document Type: Article

References (35)

1. 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.
2. Bartesaghi A., Lecumberry F., Sapiro G., Subramaniam S. Protein secondary structure determination by constrained single-particle cryo-electron tomography. Structure 2012, 20:2003-2013. 10.1016/j.str.2012.10.016.
3. Briggs J.A.G., Riches J.D., Glass B., Bartonova V., Zanetti G., Kräusslich H.G. Structure and assembly of immature HIV. Proc. Natl. Acad. Sci. 2009, 106:11090-11095.
4. 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. 10.1016/j.jsb.2012.02.003.
5. 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.
6. Chen Y., Pfeffer S., Hrabe T., Schuller J.M., Förster F. Fast and accurate reference-free alignment of subtomograms. J. Struct. Biol. 2013, 182:235-245. 10.1016/j.jsb.2013.03.002.
7. Dümmler A., Lawrence A.M., De Marco A. Simplified screening for the detection of soluble fusion constructs expressed in E. coli using a modular set of vectors. Microb. Cell Factories 2005, 4:34.
8. Eibauer M., Hoffmann C., Plitzko J.M., Baumeister W., Nickell S., Engelhardt H. Unraveling the structure of membrane proteins in situ by transfer function corrected cryo-electron tomography. J. Struct. Biol. 2012, 180:488-496.
9. Elmlund H., Elmlund D., Bengio S. PRIME: Probabilistic initial 3D model generation for single-particle cryo-electron microscopy. Structure 2013, 21:1299-1306. 10.1016/j.str.2013.07.002.
10. Fechter P., Chevalier C., Yusupova G., Yusupov M., Romby P., Marzi S. Ribosomal initiation complexes probed by toeprinting and effect of trans-acting translational regulators in bacteria. Riboswitches, Methods in Molecular Biology 2009, vol. 540:247-263. Humana Press.
11. Fernández J.J., Li S., Crowther R.A. CTF determination and correction in electron cryotomography. Ultramicroscopy 2006, 106:587-596.
12. Jensen G.J., Kornberg R.D. Defocus-gradient corrected back-projection. Ultramicroscopy 2000, 84:57-64.
13. Kazantsev I.G., Klukowska J., Herman G.T., Cernetic L. Fully three-dimensional defocus-gradient corrected backprojection in cryoelectron microscopy. Ultramicroscopy 2010, 110:1128-1142.
14. Kremer J.R., Mastronarde D.N., McIntosh J.R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 1996, 116:71-76.
15. J.J. Kuffner, Effective sampling and distance metrics for 3D rigid body path planning, in: Proceedings of the IEEE International Conference on Robotics and Automation (ICRA 2004), 2009, pp. 3993-3998.
16. 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.
17. Li X., Zheng S.Q., Egami K., Agard D.A., Cheng Y. Influence of electron dose rate on electron counting images recorded with the K2 camera. J. Struct. Biol. 2013, 184:251-260.
18. Mastronarde D.N. Dual-axis tomography: an approach with alignment methods that preserve resolution. J. Struct. Biol. 1997, 120:343-352. 10.1006/jsbi.1997.3919.
19. McMullan G., Chen S., Henderson R., Faruqi A.R. Detective quantum efficiency of electron area detectors in electron microscopy. Ultramicroscopy 2009, 109:1126-1143.
20. Nicastro D., Schwartz C., Pierson J., Gaudette R., Porter M.E., McIntosh J.R. The molecular architecture of axonemes revealed by cryoelectron tomography 2006, Science.
21. 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.
22. Philippsen A., Engel H.A., Engel A. The contrast-imaging function for tilted specimens. Ultramicroscopy 2007, 107:202-212. 10.1016/j.ultramic.2006.07.010.
23. 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.
24. Scheres S.H.W., Chen S. Prevention of overfitting in cryo-EM structure determination. Nat. Methods 2012, 9:853-854.
25. Schur F.K.M., Hagen W., de Marco A., Briggs J.A.G. Determination of protein structure at 8. 5Å resolution using cryo-electron tomography and sub-tomogram averaging. J. Struct. Biol. 2013, 184:394-400. 10.1016/j.jsb.2013.10.015.
26. Voortman L.M., Franken E.M., van Vliet L.J., Rieger B. Fast, spatially varying CTF correction in TEM. Ultramicroscopy 2012, 118:26-34.
27. Voortman L.M., Stallinga S., Schoenmakers R.H.M., van Vliet L.J., Rieger B. A fast algorithm for computing and correcting the CTF for tilted, thick specimens in TEM. Ultramicroscopy 2011, 111:1029-1036.
28. Vulović M., Franken E., Ravelli R.B.G., van Vliet L.J., Rieger B. Precise and unbiased estimation of astigmatism and defocus in transmission electron microscopy. Ultramicroscopy 2012, 116s:115-134. 10.1016/j.ultramic.2012.03.004.
29. Vulović M., Ravelli R.B., van Vliet L.J., Koster A.J., Lazić I., Lücken U., Rullgård H., Öktem O., Rieger B. Image formation modeling in cryo-electron microscopy. J. Struct. Biol. 2013, 183:19-32.
30. Vulović M., Rieger B., van Vliet L.J., Koster A.J., Ravelli R.B.G. A toolkit for the characterization of CCD cameras for transmission electron microscopy. Acta Crystallogr. Sect. D 2010, 66:97-109.
31. Vulović M., Voortman L.M., van Vliet L.J., Rieger B. When to use the projection assumption and the weak-phase object approximation in phase contrast cryo-EM. Ultramicroscopy 2014, 136:61-66.
32. Winkler H., Taylor K.A. Focus gradient correction applied to tilt series image data used in electron tomography. J. Struct. Biol. 2003, 143:24-32.
33. Xiong Q., Morphew M.K., Schwartz C.L., Hoenger A.H., Mastronarde D.N. CTF determination and correction for low dose tomographic tilt series. J. Struct. Biol. 2009, 168:378-387.
34. Zanetti G., Riches J.D., Fuller S.D., Briggs J.A.G. Contrast transfer function correction applied to cryo-electron tomography and sub-tomogram averaging. J. Struct. Biol. 2009, 168:305-312.
35. Zhang L., Ren G. IPET and FETR: Experimental approach for studying molecular structure dynamics by cryo-electron tomography of a single-molecule structure. PLoS ONE 2012, 7:e30249. 10.1371/journal.pone.0030249.