Cryo-EM Structure Determination Using Segmented Helical Image Reconstruction

Methods in Enzymology

Volumn 579, Issue , 2016, Pages 307-328

  Fromm, S A ^a   Sachse, C ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Direct electron detectors; Helical assemblies; Helical symmetry; Near atomic resolution; Segmented helical reconstruction; Single particle helical reconstruction; Tobacco mosaic virus

Indexed keywords

ELECTRON TOMOGRAPHY; FOURIER ANALYSIS; IMAGE ANALYSIS; IMAGE PROCESSING; IMAGE QUALITY; IMAGE RECONSTRUCTION; IMAGE SEGMENTATION; NONHUMAN; STRUCTURE ANALYSIS; VALIDATION STUDY; ALGORITHM; ALPHA HELIX; CRYOELECTRON MICROSCOPY; DEVICES; ELECTRON; HUMAN; MOLECULAR MODEL; PROCEDURES; SOFTWARE; STATISTICS AND NUMERICAL DATA; THREE DIMENSIONAL IMAGING; TOBACCO MOSAIC VIRUS; ULTRASTRUCTURE;

ACTIN; ESCHERICHIA COLI PROTEIN; PARM PROTEIN, E COLI; TROPOMYOSIN;

ACTINS; ALGORITHMS; CRYOELECTRON MICROSCOPY; ELECTRONS; ESCHERICHIA COLI PROTEINS; FOURIER ANALYSIS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; MODELS, MOLECULAR; PROTEIN CONFORMATION, ALPHA-HELICAL; SOFTWARE; TOBACCO MOSAIC VIRUS; TROPOMYOSIN;

EID: 84979656046     PISSN: 00766879     EISSN: 15577988     Source Type: Book Series    
DOI: 10.1016/bs.mie.2016.05.034     Document Type: Chapter

References (69)

1. Adrian, M., Dubochet, J., Lepault, J., McDowall, A., Cryo-electron microscopy of viruses. Nature 308 (1984), 32–36.
2. Agirrezabala, X., Méndez-López, E., Lasso, G., Sánchez-Pina, M.A., Aranda, M., Valle, M., The near-atomic cryoEM structure of a flexible filamentous plant virus shows homology of its coat protein with nucleoproteins of animal viruses. eLife, 4, 2015, e11795.
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, 3, 2014, e01963.
4. Bai, X.-C., Fernandez, I.S., McMullan, G., Scheres, S.H.W., Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles. eLife, 2, 2013, e00461.
5. Bai, X.-C., Yan, C., Yang, G., Lu, P., Ma, D., Sun, L. et al., An atomic structure of human γ-secretase. Nature 525 (2015), 212–217.
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. Proceedings of the National Academy of Sciences of the United States of America 111 (2014), 11709–11714.
7. Behrmann, E., Tao, G., Stokes, D.L., Egelman, E.H., Raunser, S., Penczek, P.A., Real-space processing of helical filaments in SPARX. Journal of Structural Biology 177 (2012), 302–313.
8. Beroukhim, R., Unwin, N., Distortion correction of tubular crystals: Improvements in the acetylcholine receptor structure. Ultramicroscopy 70 (1997), 57–81.
9. Bharat, T.A.M., Davey, N.E., Ulbrich, P., Riches, J.D., de Marco, A., Rumlova, M. et al., Structure of the immature retroviral capsid at 8 Å resolution by cryo-electron microscopy. Nature 487 (2012), 385–389.
10. Bharat, T.A.M., Murshudov, G.N., Sachse, C., Löwe, J., Structures of actin-like ParM filaments show architecture of plasmid-segregating spindles. Nature 523 (2015), 106–110.
11. Böttcher, 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.
12. 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.
13. Campbell, M.G., Cheng, A., Brilot, A.F., Moeller, A., Lyumkis, D., Veesler, D. et al., Movies of ice-embedded particles enhance resolution in electron cryo-microscopy. Structure (London, England: 1993) 20 (2012), 1823–1828.
14. Chen, B., Thurber, K.R., Shewmaker, F., Wickner, R.B., Tycko, R., Measurement of amyloid fibril mass-per-length by tilted-beam transmission electron microscopy. Proceedings of the National Academy of Sciences of the United States of America 106 (2009), 14339–14344.
15. Ciuffa, R., Lamark, T., Tarafder, A.K., Guesdon, A., Rybina, S., Hagen, W.J.H. et al., The selective autophagy receptor p62 forms a flexible filamentous helical scaffold. Cell Reports 11 (2015), 748–758.
16. Clare, D.K., Pechnikova, E.V., Skurat, E.V., Makarov, V.V., Sokolova, O.S., Solovyev, A.G. et al., Novel inter-subunit contacts in barley stripe mosaic virus revealed by cryo-electron microscopy. Structure (London, England: 1993) 23 (2015), 1815–1826.
17. Clemens, D.L., Ge, P., Lee, B.-Y., Horwitz, M.A., Zhou, Z.H., Atomic structure of T6SS reveals interlaced array essential to function. Cell 160 (2015), 940–951.
18. DeRosier, D., Klug, A., Reconstruction of three dimensional structures from electron micrographs. Nature 217 (1968), 130–134.
19. Desfosses, A., Ciuffa, R., Gutsche, I., Sachse, C., SPRING—An image processing package for single-particle based helical reconstruction from electron cryomicrographs. Journal of Structural Biology 185 (2014), 15–26.
20. Diaz, R., Rice, W.J., Stokes, D.L., Fourier-Bessel reconstruction of helical assemblies. Methods in Enzymology 482 (2010), 131–165.
21. DiMaio, F., Yu, X., Rensen, E., Krupovic, M., Prangishvili, D., Egelman, E.H., Virology. A virus that infects a hyperthermophile encapsidates A-form DNA. Science (New York, NY) 348 (2015), 914–917.
22. Egelman, E.H., A robust algorithm for the reconstruction of helical filaments using single-particle methods. Ultramicroscopy 85 (2000), 225–234.
23. Egelman, E.H., The iterative helical real space reconstruction method: Surmounting the problems posed by real polymers. Journal of Structural Biology 157 (2007), 83–94.
24. Egelman, E.H., Reconstruction of helical filaments and tubes. Methods in Enzymology 482 (2010), 167–183.
25. Egelman, E.H., Ambiguities in helical reconstruction. eLife, 3, 2014, e04969.
26. Egelman, E.H., Three-dimensional reconstruction of helical polymers. Archives of Biochemistry and Biophysics 581 (2015), 54–58.
27. Faruqi, A.R., Henderson, R., Electronic detectors for electron microscopy. Current Opinion in Structural Biology 17 (2007), 549–555.
28. Fromm, S.A., Bharat, T.A.M., Jakobi, A.J., Hagen, W.J.H., Sachse, C., Seeing tobacco mosaic virus through direct electron detectors. Journal of Structural Biology 189 (2015), 87–97.
29. Fujii, T., Iwane, A.H., Yanagida, T., Namba, K., Direct visualization of secondary structures of F-actin by electron cryomicroscopy. Nature 467 (2010), 724–728.
30. Galkin, V.E., Wu, Y., Zhang, X.-P., Qian, X., He, Y., Yu, X. et al., The Rad51/RadA N-terminal domain activates nucleoprotein filament ATPase activity. Structure/Folding and Design 14 (2006), 983–992.
31. Ge, P., Zhou, Z.H., Hydrogen-bonding networks and RNA bases revealed by cryo electron microscopy suggest a triggering mechanism for calcium switches. Proceedings of the National Academy of Sciences of the United States of America 108 (2011), 9637–9642.
32. Grigorieff, N., Three-dimensional structure of bovine NADH:ubiquinone oxidoreductase (complex I) at 22 A in ice. Journal of Molecular Biology 277 (1998), 1033–1046.
33. Gutsche, I., Desfosses, A., Effantin, G., Ling, W.L., Haupt, M., Ruigrok, R.W.H. et al., Structural virology. Near-atomic cryo-EM structure of the helical measles virus nucleocapsid. Science (New York, NY) 348 (2015), 704–707.
34. 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. Journal of Molecular Biology 213 (1990), 899–929.
35. Henderson, R., Baldwin, J.M., Downing, K.H., Lepault, J., Zemlin, F., Structure of purple membrane from halobacterium halobium: Recording, measurement and evaluation of electron-micrographs at 3.5 Å resolution. Ultramicroscopy 19 (1986), 147–178.
36. Hoffmann, N.A., Jakobi, A.J., Moreno-Morcillo, M., Glatt, S., Kosinski, J., Hagen, W.J.H. et al., Molecular structures of unbound and transcribing RNA polymerase III. Nature 528 (2015), 231–236.
37. Jeng, T., Crowther, R., Stubbs, G., Chiu, W., Visualization of alpha-helices in tobacco mosaic virus by cryo-electron microscopy. Journal of Molecular Biology 205 (1989), 251–257.
38. Jiménez, J.L., Guijarro, J.I., Orlova, E., Zurdo, J., Dobson, C.M., Sunde, M. et al., Cryo-electron microscopy structure of an SH3 amyloid fibril and model of the molecular packing. The EMBO Journal 18 (1999), 815–821.
39. Korkhov, V.M., Sachse, C., Short, J.M., Tate, C.G., Three-dimensional structure of TspO by electron cryomicroscopy of helical crystals. Structure (London, England: 1993) 18 (2010), 677–687.
40. Kudryashev, M., Wang, R.Y.-R., Brackmann, M., Scherer, S., Maier, T., Baker, D. et al., Structure of the type VI secretion system contractile sheath. Cell 160 (2015), 952–962.
41. 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.
42. Low, H.H., Sachse, C., Amos, L.A., Löwe, J., Structure of a bacterial dynamin-like protein lipid tube provides a mechanism for assembly and membrane curving. Cell 139 (2009), 1342–1352.
43. McCullough, J., Clippinger, A.K., Talledge, N., Skowyra, M.L., Saunders, M.G., Naismith, T.V. et al., Structure and membrane remodeling activity of ESCRT-III helical polymers. Science (New York, NY) 350 (2015), 1548–1551.
44. McMullan, G., Chen, S., Henderson, R., Faruqi, A.R., Detective quantum efficiency of electron area detectors in electron microscopy. Ultramicroscopy 109 (2009), 1126–1143.
45. 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.
46. Merk, A., Barthesaghi, A., Banerjee, S., Falconieri, V., Rao, P., Davis, M.I. et al., Breaking cryo-EM resolution barriers to facilitate drug discovery. Cell, 2016 http://dx.doi.org/10.1016/j.cell.2016.05.040.
47. Miyazawa, A., Fujiyoshi, Y., Unwin, N., Structure and gating mechanism of the acetylcholine receptor pore. Nature 423 (2003), 949–955.
48. Moody, M.F., Structural biology using electrons and X-rays. 2011, Academic Press, San Diego, CA.
49. Penczek, P.A., Grassucci, R.A., Frank, J., The ribosome at improved resolution: New techniques for merging and orientation refinement in 3D cryo-electron microscopy of biological particles. Ultramicroscopy 53 (1994), 251–270.
50. Penczek, P., Radermacher, M., Frank, J., Three-dimensional reconstruction of single particles embedded in ice. Ultramicroscopy 40 (1992), 33–53.
51. Rohou, A., Grigorieff, N., Frealix: Model-based refinement of helical filament structures from electron micrographs. Journal of Structural Biology 186 (2014), 234–244.
52. Sachse, C., Single-particle based helical reconstruction—How to make the most of real and Fourier space. AIMS Biophysics 2 (2015), 219–244.
53. 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. Journal of Molecular Biology 371 (2007), 812–835.
54. Scheres, S.H.W., RELION: Implementation of a Bayesian approach to cryo-EM structure determination. Journal of Structural Biology 180 (2012), 519–530.
55. Scheres, S.H., Beam-induced motion correction for sub-megadalton cryo-EM particles. eLife, 3, 2014, e03665.
56. Sindelar, C.V., Downing, K.H., The beginning of kinesin's force-generating cycle visualized at 9-A resolution. The Journal of Cell Biology 177 (2007), 377–385.
57. Skruzny, M., Desfosses, A., Prinz, S., Dodonova, S.O., Gieras, A., Uetrecht, C. et al., An organized co-assembly of clathrin adaptors is essential for endocytosis. Developmental Cell 33 (2015), 150–162.
58. Stewart, M., Computer image processing of electron micrographs of biological structures with helical symmetry. Journal of Electron Microscopy Technique 9 (1988), 325–358.
59. Stewart, A., Grigorieff, N., Noise bias in the refinement of structures derived from single particles. Ultramicroscopy 102 (2004), 67–84.
60. Toyoshima, C., Structure determination of tubular crystals of membrane proteins. I. Indexing of diffraction patterns. Ultramicroscopy 84 (2000), 1–14.
61. Toyoshima, C., Unwin, N., Ion channel of acetylcholine receptor reconstructed from images of postsynaptic membranes. Nature 336 (1988), 247–250.
62. Unwin, N., Refined structure of the nicotinic acetylcholine receptor at 4A resolution. Journal of Molecular Biology 346 (2005), 967–989.
63. von der Ecken, J., Müller, M., Lehman, W., Manstein, D.J., Penczek, P.A., Raunser, S., Structure of the F-actin-tropomyosin complex. Nature 519 (2015), 114–117.
64. Voorhees, R.M., Fernandez, I.S., Scheres, S.H.W., Hegde, R.S., Structure of the Mammalian ribosome-sec61 complex to 3.4 Å resolution. Cell 157 (2014), 1632–1643.
65. Wall, J.S., Hainfeld, J.F., Mass mapping with the scanning transmission electron microscope. Annual Review of Biophysics and Biophysical Chemistry 15 (1986), 355–376.
66. Weik, M., Ravelli, R.B., Kryger, G., McSweeney, S., Raves, M.L., Harel, M. et al., Specific chemical and structural damage to proteins produced by synchrotron radiation. Proceedings of the National Academy of Sciences of the United States of America 97 (2000), 623–628.
67. Wu, B., Peisley, A., Tetrault, D., Li, Z., Egelman, E.H., Magor, K.E. et al., Molecular imprinting as a signal-activation mechanism of the viral RNA sensor RIG-I. Molecular Cell 55 (2014), 511–523.
68. Xu, C., Rice, W.J., He, W., Stokes, D.L., A structural model for the catalytic cycle of Ca(2 +)-ATPase. Journal of Molecular Biology 316 (2002), 201–211.
69. Yonekura, K., Maki-Yonekura, S., Namba, K., Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424 (2003), 643–650.