Testing the Validity of Single-Particle Maps at Low and High Resolution

Methods in Enzymology

Volumn 579, Issue , 2016, Pages 227-253

  Rosenthal, P B ^a  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

Author keywords

Absolute hand; CryoEM; Electron microscopy; Model bias; Over fitting; Resolution; Single particle reconstruction; Tilt pair; Validation

Indexed keywords

CRYOELECTRON MICROSCOPY; MOLECULAR WEIGHT; RELIABILITY; VALIDATION STUDY; VALIDITY; ALGORITHM; DEVICES; IMAGE PROCESSING; MOLECULAR MODEL; PROCEDURES; PROTEIN CONFORMATION; SOFTWARE; STATISTICS AND NUMERICAL DATA; THREE DIMENSIONAL IMAGING; ULTRASTRUCTURE;

BACTERIAL PROTEIN; BETA GALACTOSIDASE; OXIDOREDUCTASE; PYRUVATE DEHYDROGENASE (NADP+);

ALGORITHMS; BACTERIAL PROTEINS; BETA-GALACTOSIDASE; CRYOELECTRON MICROSCOPY; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; KETONE OXIDOREDUCTASES; MODELS, MOLECULAR; PROTEIN CONFORMATION; SOFTWARE;

EID: 85027436761     PISSN: 00766879     EISSN: 15577988     Source Type: Book Series    
DOI: 10.1016/bs.mie.2016.06.004     Document Type: Chapter

References (62)

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, 2, 2013, e00461.
2. Baker, L.A., Watt, I.N., Runswick, M.J., Walker, J.E., Rubinstein, J.L., Arrangement of subunits in intact mammalian mitochondrial ATP synthase determined by cryo-EM. Proceedings of the National Academy of Sciences of the United States of America 109 (2012), 11675–11680.
3. Blow, D.M., Crick, F.H.C., The treatment of errors in the isomorphous replacement method. Acta Crystallographica 12 (1959), 794–802.
4. Bottcher, B., Wynne, S.A., Crowther, R.A., Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature 386 (1997), 88–91.
5. Brilot, A.F., Chen, J.Z., Cheng, A., Pan, J., Harrison, S.C., Potter, C.S., et al. Beam-induced motion of vitrified specimen on holey carbon film. Journal of Structural Biology 177 (2012), 630–637.
6. Brown, A., Long, F., Nicholls, R.A., Toots, J., Emsley, P., Murshudov, G., Tools for macromolecular model building and refinement into electron cryo-microscopy reconstructions. Acta Crystallographica. Section D, Biological Crystallography 71 (2015), 136–153.
7. Brunger, A.T., Free R value: A novel statistical quantity for assessing the accuracy of crystal structures. Nature 355 (1992), 472–475.
8. Brunger, A.T., Free R value: Cross-validation in crystallography. Methods in Enzymology 277 (1997), 366–396.
9. Cardone, G., Heymann, J.B., Steven, A.C., One number does not fit all: Mapping local variations in resolution in cryo-EM reconstructions. Journal of Structural Biology 184 (2013), 226–236.
10. Chen, S., McMullan, G., Faruqi, A.R., Murshudov, G.N., Short, J.M., Scheres, S.H., et al. High-resolution noise substitution to measure overfitting and validate resolution in 3D structure determination by single particle electron cryomicroscopy. Ultramicroscopy 135 (2013), 24–35.
11. Cong, Y., Ludtke, S.J., Single particle analysis at high resolution. Methods in Enzymology 482 (2010), 211–235.
12. Crowther, R.A., DeRosier, D.J., Klug, A., The reconstruction of a three-dimensional structure from projections and its application to electron microscopy. Proceeding of the Royal Society of London 317 (1970), 319–340.
13. DiMaio, F., Zhang, J., Chiu, W., Baker, D., Cryo-EM model validation using independent map reconstructions. Protein Science: A Publication of the Protein Society 22 (2013), 865–868.
14. Falkner, B., Schroder, G.F., Cross-validation in cryo-EM-based structural modeling. Proceedings of the National Academy of Sciences of the United States of America 110 (2013), 8930–8935.
15. Fernandez, J.J., Luque, D., Caston, J.R., Carrascosa, J.L., Sharpening high resolution information in single particle electron cryomicroscopy. Journal of Structural Biology 164 (2008), 170–175.
16. Frank, J., Three-dimensional electron microscopy of macromolecular assemblies: Visualization of biological molecules in their native state. 2nd ed., 2006, Oxford University Press, Oxford/New York.
17. Frank, J., Radermacher, M., Penczek, P., Zhu, J., Li, Y., Ladjadj, M., et al. SPIDER and WEB: Processing and visualization of images in 3D electron microscopy and related fields. Journal of Structural Biology 116 (1996), 190–199.
18. Glaeser, R.M., Review: Electron crystallography: Present excitement, a nod to the past, anticipating the future. Journal of Structural Biology 128 (1999), 3–14.
19. Glaeser, R.M., How good can cryo-EM become?. Nature Methods 13 (2016), 28–32.
20. Grigorieff, N., Resolution measurement in structures derived from single particles. Acta Crystallographica. Section D, Biological Crystallography 56 (2000), 1270–1277.
21. Harris, A., Belnap, D.M., Watts, N.R., Conway, J.F., Cheng, N., Stahl, S.J., et al. Epitope diversity of hepatitis B virus capsids: Quasi-equivalent variations in spike epitopes and binding of different antibodies to the same epitope. Journal of Molecular Biology 355 (2006), 562–576.
22. Henderson, R., The potential and limitations of neutrons, electrons and x-rays for atomic-resolution microscopy of unstained biological molecules. Quarterly Reviews of Biophysics 28 (1995), 171–193.
23. Henderson, R., Avoiding the pitfalls of single particle cryo-electron microscopy: Einstein from noise. Proceedings of the National Academy of Sciences of the United States of America 110 (2013), 18037–18041.
24. Henderson, R., Chen, S., Chen, J.Z., Grigorieff, N., Passmore, L.A., Ciccarelli, L., et al. Tilt-pair analysis of images from a range of different specimens in single-particle electron cryomicroscopy. Journal of Molecular Biology 413 (2011), 1028–1046.
25. Henderson, R., Sali, A., Baker, M.L., Carragher, B., Devkota, B., Downing, K.H., et al. Outcome of the first electron microscopy validation task force meeting. Structure 20 (2012), 205–214.
26. Heymann, J.B., Validation of 3D EM reconstructions: The phantom in the noise. AIMS Biophysics 2 (2015), 21–35.
27. Heymann, J.B., Belnap, D.M., Bsoft: Image processing and molecular modeling for electron microscopy. Journal of Structural Biology 157 (2007), 3–18.
28. Hohn, M., Tang, G., Goodyear, G., Baldwin, P.R., Huang, Z., Penczek, P.A., et al. SPARX, a new environment for cryo-EM image processing. Journal of Structural Biology 157 (2007), 47–55.
29. Huiskonen, J.T., Kivela, H.M., Bamford, D.H., Butcher, S.J., The PM2 virion has a novel organization with an internal membrane and pentameric receptor binding spikes. Nature Structural & Molecular Biology 11 (2004), 850–856.
30. Kishchenko, G.P., Leith, A., Spherical deconvolution improves quality of single particle reconstruction. Journal of Structural Biology 187 (2014), 84–92.
31. Kucukelbir, A., Sparse and steerable representations for 3D electron cryomicroscopy. Ph.D. thesis, 2014, Yale University, New Haven, CT.
32. Kucukelbir, A., Sigworth, F.J., Tagare, H.D., Quantifying the local resolution of cryo-EM density maps. Nature Methods 11 (2014), 63–65.
33. Li, X., Mooney, P., Zheng, S., Booth, C.R., Braunfeld, M.B., Gubbens, S., et al. Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nature Methods 10 (2013), 584–590.
34. Lyumkis, D., Brilot, A.F., Theobald, D.L., Grigorieff, N., Likelihood-based classification of cryo-EM images using FREALIGN. Journal of Structural Biology 183 (2013), 377–388.
35. Mancini, E.J., Clarke, M., Gowen, B.E., Rutten, T., Fuller, S.D., Cryo-electron microscopy reveals the functional organization of an enveloped virus, Semliki Forest virus. Molecular Cell 5 (2000), 255–266.
36. McMullan, G., Faruqi, A.R., Clare, D., Henderson, R., Comparison of optimal performance at 300 keV of three direct electron detectors for use in low dose electron microscopy. Ultramicroscopy 147 (2014), 156–163.
37. Penczek, P.A., Resolution measures in molecular electron microscopy. Methods in Enzymology 482 (2010), 73–100.
38. Penczek, P., Radermacher, M., Frank, J., Three-dimensional reconstruction of single particles embedded in ice. Ultramicroscopy 40 (1992), 33–53.
39. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., et al. UCSF chimera—A visualization system for exploratory research and analysis. Journal of Computational Chemistry 25 (2004), 1605–1612.
40. Read, R.J., Adams, P.D., Arendall, W.B. 3rd., Brunger, A.T., Emsley, P., Joosten, R.P., et al. A new generation of crystallographic validation tools for the protein data bank. Structure 19 (2011), 1395–1412.
41. Rosenthal, P.B., Henderson, R., Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. Journal of Molecular Biology 333 (2003), 721–745.
42. Rosenthal, P.B., Rubinstein, J.L., Validating maps from single particle electron cryomicroscopy. Current Opinion in Structural Biology 34 (2015), 135–144.
43. Rubinstein, J.L., Walker, J.E., Henderson, R., Structure of the mitochondrial ATP synthase by electron cryomicroscopy. The EMBO Journal 22 (2003), 6182–6192.
44. Russo, C.J., Passmore, L.A., Robust evaluation of 3D electron cryomicroscopy data using tilt-pairs. Journal of Structural Biology 187 (2014), 112–118.
45. Saxton, W.O., Baumeister, W., The correlation averaging of a regularly arranged bacterial cell envelope protein. Journal of Microscopy 127 (1982), 127–138.
46. Schatz, M., van Heel, M., Invariant classification of molecular views in electron micrographs. Ultramicroscopy 32 (1990), 255–264.
47. Scheres, S.H., RELION: Implementation of a Bayesian approach to cryo-EM structure determination. Journal of Structural Biology 180 (2012), 519–530.
48. Scheres, S.H., Carazo, J.M., Introducing robustness to maximum-likelihood refinement of electron-microscopy data. Acta Crystallographica. Section D, Biological Crystallography 65 (2009), 672–678.
49. Scheres, S.H., Chen, S., Prevention of overfitting in cryo-EM structure determination. Nature Methods 9 (2012), 853–854.
50. Shaikh, T.R., Hegerl, R., Frank, J., An approach to examining model dependence in EM reconstructions using cross-validation. Journal of Structural Biology 142 (2003), 301–310.
51. Sigworth, F.J., A maximum-likelihood approach to single-particle image refinement. Journal of Structural Biology 122 (1998), 328–339.
52. Smith, J.M., Ximdisp—A visualization tool to aid structure determination from electron microscope images. Journal of Structural Biology 125 (1999), 223–228.
53. Stagg, S.M., Noble, A.J., Spilman, M., Chapman, M.S., ResLog plots as an empirical metric of the quality of cryo-EM reconstructions. Journal of Structural Biology 185 (2014), 418–426.
54. Stewart, A., Grigorieff, N., Noise bias in the refinement of structures derived from single particles. Ultramicroscopy 102 (2004), 67–84.
55. van Heel, M., Finding trimeric HIV-1 envelope glycoproteins in random noise. Proceedings of the National Academy of Sciences of the United States of America 110 (2013), E4175–E4177.
56. van Heel, M., Harauz, G., Resolution criteria for three dimensional reconstruction. Optik 73 (1986), 119–122.
57. van Heel, M., Stoffler-Meilicke, M., Characteristic views of E. coli and B. stearothermophilus 30S ribosomal subunits in the electron microscope. The EMBO Journal 4 (1985), 2389–2395.
58. Vargas, J., Oton, J., Marabini, R., Carazo, J.M., Sorzano, C.O., Particle alignment reliability in single particle electron cryomicroscopy: A general approach. Scientific Reports, 6, 2016, 21626.
59. Vinothkumar, K.R., Zhu, J., Hirst, J., Architecture of mammalian respiratory complex I. Nature 515 (2014), 80–84.
60. Voss, N.R., Yoshioka, C.K., Radermacher, M., Potter, C.S., Carragher, B., DoG Picker and TiltPicker: Software tools to facilitate particle selection in single particle electron microscopy. Journal of Structural Biology 166 (2009), 205–213.
61. Wasilewski, S., Rosenthal, P.B., Web server for tilt-pair validation of single particle maps from electron cryomicroscopy. Journal of Structural Biology 186 (2014), 122–131.
62. Zhao, M., Wu, S., Zhou, Q., Vivona, S., Cipriano, D.J., Cheng, Y., et al. Mechanistic insights into the recycling machine of the SNARE complex. Nature 518 (2015), 61–67.