Efficient Estimation of Three-Dimensional Covariance and its Application in the Analysis of Heterogeneous Samples in Cryo-Electron Microscopy

Bai, 2013, Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles, Elife, 2, e00461, 10.7554/eLife.00461 Baird, 2012, Eukaryotic initiation factor 2 phosphorylation and translational control in metabolism, Adv. Nutr., 3, 307, 10.3945/an.112.002113 Baxter, 2009, Determination of signal-to-noise ratios and spectral SNRs in cryo-EM low-dose imaging of molecules, J. Struct. Biol., 166, 126, 10.1016/j.jsb.2009.02.012 Campbell, 2012, Movies of ice-embedded particles enhance resolution in electron cryo-microscopy, Structure, 20, 1823, 10.1016/j.str.2012.08.026 Censor, 1997 Dashti, 2014, Trajectories of the ribosome as a Brownian nanomachine, Proc. Natl. Acad. Sci. USA, 111, 17492, 10.1073/pnas.1419276111 Dubochet, 1988, Cryo-electron microscopy of vitrified specimens, Q. Rev. Biophys., 21, 129, 10.1017/S0033583500004297 Elmlund, 2013, PRIME: probabilistic initial 3D model generation for single-particle cryo-electron microscopy, Structure, 21, 1299, 10.1016/j.str.2013.07.002 Frank, 2006 Grassucci, 2007, Preparation of macromolecular complexes for cryo-electron microscopy, Nat. Protoc., 2, 3239, 10.1038/nprot.2007.452 Hashem, 2013, Structure of the mammalian ribosomal 43S preinitiation complex bound to the scanning factor DHX29, Cell, 153, 1108, 10.1016/j.cell.2013.04.036 Henderson, 2012, Outcome of the first electron microscopy validation task force meeting, Structure, 20, 205, 10.1016/j.str.2011.12.014 Herman, 1970, Algebraic reconstruction techniques (ART) for three-dimensional electron microscopy and X-ray photography, J. Theor. Biol., 29, 471, 10.1016/0022-5193(70)90109-8 Herman, 2008, Classification of heterogeneous electron microscopic projections into homogeneous subsets, Ultramicroscopy, 108, 327, 10.1016/j.ultramic.2007.05.005 Jin, 2014, HEMNMA: hybrid electron microscopy normal mode analysis to fully explore macromolecular dynamics, Structure, 22, 496, 10.1016/j.str.2014.01.004 Katsevich, 2015, Covariance matrix estimation for the cryo-EM heterogeneity problem, SIAM J. Imaging Sci., 8, 126, 10.1137/130935434 Langlois, 2014, Automated particle picking for low-contrast macromolecules in cryo-electron microscopy, J. Struct. Biol., 186, 1, 10.1016/j.jsb.2014.03.001 Lee, 2011, Multiclass maximum-likelihood symmetry determination and motif reconstruction of 3-D helical objects from projection images for electron microscopy, IEEE Trans. Image Process., 20, 1962, 10.1109/TIP.2011.2107329 Leith, 2012, Use of SPIDER and SPIRE in image reconstruction, 620, 10.1107/97809553602060000874 Li, 2013, Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM, Nat. Methods, 10, 584, 10.1038/nmeth.2472 Liao, 2010 Liu, 1995, Estimation of variance distribution in three-dimensional reconstruction. I. Theory, J. Opt. Soc. Am. A Opt. Image Sci. Vis., 12, 2615, 10.1364/JOSAA.12.002615 Lyumkis, 2013, Likelihood-based classification of cryo-EM images using FREALIGN, J. Struct. Biol., 183, 377, 10.1016/j.jsb.2013.07.005 Meyer, 1998, The effects of electron and photon scattering on signal and noise transfer properties of scintillators in CCD cameras used for electron detection, Ultramicroscopy, 75, 23, 10.1016/S0304-3991(98)00051-5 Meyuhas, 2008, Physiological roles of ribosomal protein S6: one of its kind, Int. Rev. Cell Mol. Biol., 268, 1, 10.1016/S1937-6448(08)00801-0 Penczek, 2011, Identifying conformational states of macromolecules by eigen-analysis of resampled cryo-EM images, Structure, 19, 1582, 10.1016/j.str.2011.10.003 Scheres, 2010, Classification of structural heterogeneity by maximum-likelihood methods, Methods Enzymol., 482, 295, 10.1016/S0076-6879(10)82012-9 Scheres, 2012, A Bayesian view on cryo-EM structure determination, J. Mol. Biol., 415, 406, 10.1016/j.jmb.2011.11.010 Shaikh, 2008, SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs, Nat. Protoc., 3, 1941, 10.1038/nprot.2008.156 Shatsky, 2010, Automated multi-model reconstruction from single-particle electron microscopy data, J. Struct. Biol., 170, 98, 10.1016/j.jsb.2010.01.007 Shigematsu, 2013, Noise models and cryo-EM drift correction with a direct-electron camera, Ultramicroscopy, 131, 61, 10.1016/j.ultramic.2013.04.001 Sigworth, 2010, An introduction to maximum-likelihood methods in cryo-EM, Methods Enzymol., 482, 263, 10.1016/S0076-6879(10)82011-7 Simonetti, 2008, Structure of the 30S translation initiation, Nature, 455, 416, 10.1038/nature07192 Sorzano, 2004, Normalizing projection images: a study of image normalizing procedures for single particle three-dimensional electron microscopy, Ultramicroscopy, 101, 129, 10.1016/j.ultramic.2004.04.004 Spahn, 2009, Exploring conformational modes of macromolecular assemblies by multi-particle cryo-EM, Curr. Opin. Struct. Biol., 19, 623, 10.1016/j.sbi.2009.08.001 Suloway, 2005, Automated molecular microscopy: the new Leginon system, J. Struct. Biol., 151, 41, 10.1016/j.jsb.2005.03.010 Tang, 2007, EMAN2: an extensible image processing suite for electron microscopy, J. Struct. Biol., 157, 38, 10.1016/j.jsb.2006.05.009 Van Heel, 1981, Use of multivariate statistics in analyzing the images of biological macromolecules, Ultramicroscopy, 6, 187 Wagenknecht, 1988, Direct localization of the tRNA-anticodon interaction site on the Escherichia coli 30 S ribosomal subunit by electron microscopy and computerized image averaging, J. Mol. Biol., 203, 753, 10.1016/0022-2836(88)90207-0 Wang, 2013, Dynamics in cryo EM reconstructions visualized with maximum-likelihood derived variance maps, J. Struct. Biol., 181, 195, 10.1016/j.jsb.2012.11.005