DOI: 10.7554/elife.00461. Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles

Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles

10.7554/elife.00461

Crossref journal-article

eLife Sciences Publications, Ltd

eLife (4374)

Abstract

Although electron cryo-microscopy (cryo-EM) single-particle analysis has become an important tool for structural biology of large and flexible macro-molecular assemblies, the technique has not yet reached its full potential. Besides fundamental limits imposed by radiation damage, poor detectors and beam-induced sample movement have been shown to degrade attainable resolutions. A new generation of direct electron detectors may ameliorate both effects. Apart from exhibiting improved signal-to-noise performance, these cameras are also fast enough to follow particle movements during electron irradiation. Here, we assess the potentials of this technology for cryo-EM structure determination. Using a newly developed statistical movie processing approach to compensate for beam-induced movement, we show that ribosome reconstructions with unprecedented resolutions may be calculated from almost two orders of magnitude fewer particles than used previously. Therefore, this methodology may expand the scope of high-resolution cryo-EM to a broad range of biological specimens.

Bibliography

Bai, X., Fernandez, I. S., McMullan, G., & Scheres, S. H. (2013). Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles. ELife, 2. CLOCKSS.

Authors 4

Xiao-chen Bai (first)
Israel S Fernandez (additional)
Greg McMullan (additional)
Sjors HW Scheres (additional)

References 32 Referenced 370

10.1073/pnas.1009999107 / Proc Natl Acad Sci USA / Cryo-EM structure and rRNA model of a translating eukaryotic 80S ribosome at 5.5-A resolution by Armache (2010)
10.1016/S0076-6879(10)81015-8 / Methods Enzymol / Radiation damage in electron cryomicroscopy by Baker (2010)
10.1126/science.1212642 / Science / The structure of the eukaryotic ribosome at 3.0 Å resolution by Ben-Shem (2011)
10.1016/j.jsb.2012.02.003 / J Struct Biol / Beam-induced motion of vitrified specimen on holey carbon film by Brilot (2012)
10.1016/j.str.2012.08.026 / Structure / Movies of ice-embedded particles enhance resolution in electron cryo-microscopy by Campbell (2012)
10.1038/nature09206 / Nature / Ribosome dynamics and tRNA movement by time-resolved electron cryomicroscopy by Fischer (2010)
10.1083/jcb.115.3.597 / J Cell Biol / Three-dimensional reconstruction of the 70S Escherichia coli ribosome in ice: the distribution of ribosomal RNA by Frank (1991)
10.1006/jsbi.1999.4172 / J Struct Biol / Review: electron crystallography: present excitement, a nod to the past, anticipating the future by Glaeser (1999)
10.1016/j.jsb.2008.06.001 / J Struct Biol / Retrospective: radiation damage and its associated “information limitations” by Glaeser (2008)
10.1016/j.sbi.2011.01.008 / Curr Opin Struct Biol / Near-atomic resolution reconstructions of icosahedral viruses from electron cryo-microscopy by Grigorieff (2011)
10.1016/S0304-3991(79)90211-0 / Ultramicroscopy / Radiation damage of purple membrane at low temperature by Hayward (1979)
10.1016/0304-3991(92)90003-3 / Ultramicroscopy / Image contrast in high-resolution electron microscopy of biological macromolecules: TMV in ice by Henderson (1992)
10.1017/S003358350000305X / Q Rev Biophys / The potential and limitations of neutrons, electrons and X-rays for atomic resolution microscopy of unstained biological molecules by Henderson (1995)
10.1016/j.jmb.2011.09.008 / J Mol Biol / Tilt-pair analysis of images from a range of different specimens in single-particle electron cryomicroscopy by Henderson (2011)
10.1016/0304-3991(95)00019-W / Ultramicroscopy / Cryo-electron energy loss spectroscopy: observations on vitrified hydrated specimens and radiation damage by Leapman (1995)
10.1016/j.ultramic.2009.04.002 / Ultramicroscopy / Detective quantum efficiency of electron area detectors in electron microscopy by McMullan (2009a)
10.1016/j.ultramic.2009.07.004 / Ultramicroscopy / Enhanced imaging in low dose electron microscopy using electron counting by McMullan (2009b)
10.1016/j.ultramic.2009.05.005 / Ultramicroscopy / Experimental observation of the improvement in MTF from backthinning a CMOS direct electron detector by McMullan (2009c)
10.1016/S1047-8477(03)00069-8 / J Struct Biol / Accurate determination of local defocus and specimen tilt in electron microscopy by Mindell (2003)
10.1093/jmicro/dfr037 / J Electron Microsc / Another 60 years in electron microscopy: development of phase-plate electron microscopy and biological applications by Nagayama (2011)
10.1002/jcc.20084 / J Comput Chem / UCSF Chimera—a visualization system for exploratory research and analysis by Pettersen (2004)
10.1016/S0168-9002(03)01914-4 / Nucl Instrum Methods Phys Res A / A 512×512 CMOS monolithic active pixel sensor with integrated ADCs for space science by Prydderch (2003)
10.1016/j.jmb.2003.07.013 / J Mol Biol / Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy by Rosenthal (2003)
10.1016/j.jmb.2011.11.010 / J Mol Biol / A Bayesian view on cryo-EM structure determination by Scheres (2012a)
10.1016/j.jsb.2012.09.006 / J Struct Biol / RELION: implementation of a Bayesian approach to cryo-EM structure determination by Scheres (2012b)
10.1038/nmeth.2115 / Nat Methods / Prevention of overfitting in cryo-EM structure determination by Scheres (2012)
10.1038/nmeth992 / Nat Methods / Disentangling conformational states of macromolecules in 3D-EM through likelihood optimization by Scheres (2007)
10.1126/science.1177662 / Science / Structural insight into nascent polypeptide chain-mediated translational stalling by Seidelt (2009)
10.1126/science.1131127 / Science / Structure of the 70S ribosome complexed with mRNA and tRNA by Selmer (2006)
10.1016/j.jsb.2006.04.005 / J Struct Biol / Automated cryoEM data acquisition and analysis of 284742 particles of GroEL by Stagg (2006)
10.1016/j.jsb.2006.05.009 / J Struct Biol / EMAN2: an extensible image processing suite for electron microscopy by Tang (2007)
10.1126/science.1164840 / Science / Insights into translational termination from the structure of RF2 bound to the ribosome by Weixlbaumer (2008)

Dates

Type	When
Created	12 years, 6 months ago (Feb. 19, 2013, 12:35 p.m.)
Deposited	1 year, 10 months ago (Oct. 11, 2023, 8:39 p.m.)
Indexed	1 day ago (Aug. 20, 2025, 9:06 a.m.)
Issued	12 years, 6 months ago (Feb. 19, 2013)
Published	12 years, 6 months ago (Feb. 19, 2013)
Published Online	12 years, 6 months ago (Feb. 19, 2013)

Funders 6

UK Medical Research Council 10.13039/501100000265 Medical Research Council
Region: Europe
gov (National government)
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Wellcome Trust
UK Medical Research Council 10.13039/501100000265 Medical Research Council
Region: Europe
gov (National government)
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2. UK Medical Research Council
3. MRC
Awards1
1. U105184332
Medical Research Council 10.13039/501100000265
Region: Europe
gov (National government)
Labels3
1. Medical Research Council (United Kingdom)
2. UK Medical Research Council
3. MRC
Awards1
1. MC_UP_A025_1013
Wellcome Trust 10.13039/100004440 Wellcome
Medical Research Council 10.13039/501100000265
Region: Europe
gov (National government)
Labels3
1. Medical Research Council (United Kingdom)
2. UK Medical Research Council
3. MRC
Awards1
1. U105184332

BibTeX

@article{Bai_2013, title={Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles}, volume={2}, ISSN={2050-084X}, url={http://dx.doi.org/10.7554/elife.00461}, DOI={10.7554/elife.00461}, journal={eLife}, publisher={eLife Sciences Publications, Ltd}, author={Bai, Xiao-chen and Fernandez, Israel S and McMullan, Greg and Scheres, Sjors HW}, year={2013}, month=feb }

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