Image formation modeling in cryo-electron microscopy

Journal of Structural Biology

Volumn 183, Issue 1, 2013, Pages 19-32

  Vulović, Miloš ^a,b   Ravelli, Raimond B G ^b   van Vliet, Lucas J ^a   Koster, Abraham J ^b   Lazić, Ivan ^c   Lücken, Uwe ^c   Rullgård, Hans ^d   Öktem, Ozan ^e   Rieger, Bernd ^a  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c Thermo Fisher Scientific   (United States)

^d Technical Sales Engineer Comsol Multiphysics GmbH   (Sweden)

^e ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

Author keywords

Amplitude contrast; Cryo electron microscopy; Image simulation; InSilicoTEM; Interaction potential; Phase contrast

Indexed keywords

CHAPERONIN 60; HEMOGLOBIN; PROTEASOME; SOLVENT;

ARTICLE; CAMERA; CRYOELECTRON MICROSCOPY; ELECTRIC POTENTIAL; ELECTRON MICROSCOPE; ELECTRON TRANSPORT; MICROSCOPE IMAGE; MOLECULAR INTERACTION; OPTICS; PHASE CONTRAST MICROSCOPY; POISSON DISTRIBUTION; PRIORITY JOURNAL; QUANTUM MECHANICS; SIGNAL NOISE RATIO; SIMULATION; THEORETICAL MODEL; TRANSMISSION ELECTRON MICROSCOPY;

AMPLITUDE CONTRAST; CRYO-ELECTRON MICROSCOPY; IMAGE SIMULATION; INSILICOTEM; INTERACTION POTENTIAL; PHASE CONTRAST;

CHAPERONIN 60; CRYOELECTRON MICROSCOPY; HEMOGLOBINS; IMAGE PROCESSING, COMPUTER-ASSISTED; MODELS, MOLECULAR; POISSON DISTRIBUTION; PROTEASOME ENDOPEPTIDASE COMPLEX; SOFTWARE; STATIC ELECTRICITY;

EID: 84879890758     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2013.05.008     Document Type: Article

References (83)

1. Agostinelli S., Allison J., Amako K., Apostolakis J., Zschiesche D., et al. Geant4 - a simulation toolkit. Nucl. Instrum. Methods Phys. Res. 2003, 506:250-303.
2. Alcorn T., Juers D.H. Progress in rational methods of cryoprotection in macromolecular crystallography. Acta Crystallogr. Sect. D 2010, 66:366-373.
3. Allen F.H., Kennard O., Watson D.G., Brammer L., Orpen A.G., Taylor R. Tables of bond lengths determined by X-ray and neutron diffraction. Part 1. Bond lengths in organic compounds. J. Chem. Soc., Perkin Trans. 1987, 2(12):1-19.
4. Bai X., Fernandez I.S., McMullan G., Scheres S.H.W. Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles. eLife Sciences 2013, 2.
5. Bajaj C., Chen S., Rand A. An efficient higher-order fast multipole boundary element solution for Poisson Boltzmann-based molecular electrostatics. SIAM J. Sci. Comput. 2011, 33:826-848.
6. Baker N.A., Sept D., Joseph S., Holst M.J., McCammon J.A. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:10037-10041.
7. Bilbao-Castro J.R., Sorzano C.O.S., García I., Fernáandez J.J. Phan3D: Design of biological phantoms in 3D electron microscopy. Bioinformatics 2004, 20:3286-3288.
8. Boothroyd, C.B., Dunin-Borkowski, R.E., Stobbs, W.M., Humphreys, C.J., 1995. Quantifying the effects of amorphous layers on image contrast using energy filtered transmission electron microscopy. In: MRS Proceedings, vol. 354, pp. 495-500.
9. Brilot A.F., Chen J.Z., Cheng A., Pan J., Harrison S.C., Potter C., Carragher B., Henderson R., Grigorieff N. Beam-induced motion of vitrified specimen on holey carbon film. J. Struct. Biol. 2012, 177:630-637.
10. Bullough P., Henderson R. Use of spot-scan procedure for recording low-dose micrographs of beam-sensitive specimens. Ultramicroscopy 1987, 21:223-230.
11. Campbell M.G., Cheng A., Brilot A., Moeller A., Lyumkis D., Veesler D., Pan J., Harrison S., Potter C., Carragher B., Grigorieff N. Movies of ice-embedded particles enhance resolution in electron cryo-microscopy. Structure 2012, 20:1823-1828.
12. Colliex C., Jeanguillaume C., Mory C. Unconventional modes for stem imaging of biological structures. J. Ultrastruct. Res. 1984, 88:177-206.
13. Cowley J.M., Moodie A.F. The scattering of electrons by atoms and crystals. I. A new theoretical approach. Acta Crystallogr. 1957, 10:609-613.
14. DeRosier D.J. Correction of high-resolution data for curvature of the Ewald sphere. Ultramicroscopy 2000, 81:83-98.
15. Dinges C., Rose H. Simulation of filtered and unfiltered TEM images and diffraction patterns. Phys. Stat. Sol. A. Appl. Mater. Sci. 1995, 150:23-29.
16. Dolinsky T.J., Nielsen J.E., McCammon J.A., Baker N.A. Pdb2pqr: an automated pipeline for the setup of poisson boltzmann electrostatics calculations. Nucleic Acids Res. 2004, 32:665-667.
17. Egerton, R., 1992. A data base for energy-loss cross sections and mean free paths. In: Proc. 50th Ann. Meet. Elec. Microsc, vol. 136, pp. 1248-1249.
18. Egerton R.F. Electron Energy-Loss Spectroscopy in the Electron Microscope 1996, Springer. second ed.
19. Feja B., Aebi U. Determination of inelastic mean free path of electrons in vitrified ice layers for on-line thickness measurments by zero-loss imaging. J. Microsc. 1999, 193:15-19.
20. Frank J. Three-Dimensional Electron Microscopy of Macromolecular Assemblies: Visualization of Biological Molecules in Their Native State 2006, Oxford University Press. 2nd ed.
21. Frank J., Shimkin B. A new image processing software for structural analysis and constrast enhancement. Papers Presented at the Ninth International Congress on Electron Microscopy, Toronto 1978, vol. 1:210-211. Microscopical Society of Canada, Toronto. J.M. Sturgess (Ed.).
22. Glaeser R.M. Retrospective: Radiation damage and its associated "information limitations". J. Struct. Biol. 2008, 163:271-276.
23. Glaeser R.M., Downing K.H. Specimen charging on thin films with one conducting layer: discussion of physical principles. Microsc. Microanal. 2004, 10:790-796.
24. Glaeser R.M., Downing K.H., DeRozier D., Chu W., Frank J. Electron Crystallography of Biological Macromolecules 2006, Oxford University Press.
25. Glaeser R.M., Taylor K.A. Radiation damage relative to transmission electron microscopy of biological specimens at low temperature: a review. J. Microsc. 1978, 112:127-138.
26. Gómez-Rodríguez A., Beltrán-del Río L.M., Herrera-Becerra R. SimulaTEM: Multislice simulations for general objects. Ultramicroscopy 2009, 110:95-104.
27. Grimm R., Typke D., Bärmann M., Baumeister W. Determination of the inelastic mean free path in ice by examination of tilted vesicles and automated most probable loss imaging. Ultramicroscopy 1996, 63:169-179.
28. Hall R.J., Nogales E., Glaeser R.M. Accurate modeling of single-particle cryo-EM images quantitates the benefits expected from using Zernike phase contrast. J. Struct. Biol. 2011, 174:468-475.
29. van Heel M., Harauz G., Orlova E.V., Schmidt R., Schatz M. A new generation of the IMAGIC image processing system. J. Struct. Biol. 1996, 116:17-24.
30. Henderson R. Image contrast in high-resolution electron microscopy of biological macromolecules: TMV in ice. Ultramicroscopy 1992, 46:1-18.
31. Henderson R. Realizing the potential of electron cryo-microscopy. Q. Rev. Biophys. 2004, 37:3-13.
32. Henderson R., Glaeser R.M. Quantitative analysis of image contrast in electron micrographs of beam-sensitive crystals. Ultramicroscopy 1985, 16:139-150.
33. Hess B., Kutzner C., van der Spoel D., Lindahl E. GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 2008, 4:435-447.
34. Heymann J.B., Belnap D.M. Bsoft: image processing and molecular modeling for electron microscopy. J. Struct. Biol. 2007, 157:3-18.
35. Hytch M.J., Stobbs W.M. Quantitative comparison of high resolution TEM images with image simulations. Ultramicroscopy 1994, 53:191-203.
36. Jensen G.J. Alignment error envelopes for single particle analysis. J. Struct. Biol. 2001, 133:143-155.
37. Karimi Nejadasl F., Karuppasamy M., Newman E.R., McGeehan J.E., Ravelli R.B.G. Non-rigid image registration to reduce beam-induced blurring of cryo-electron microscopy images. J. Synchrotron Radiat. 2013, 20:58-66.
38. Karuppasamy M., Karimi Nejadasl F., Vulović M., Koster A.J., Ravelli R.B.G. Radiation damage in single-particle cryo-electron microscopy: effects of dose and dose rate. J. Synchrotron Radiat. 2011, 18:398-412.
39. Kieft E., Bosch E. Refinement of monte carlo simulations of electron-specimen interaction in low-voltage SEM. J. Phys. D: Appl. Phys. 2008, 41:215310.
40. Kirkland A.I., Chang L.-Y.S., Hutchison J.L. Atomic resolution transmission electron microscopy. Science of Microscopy 2008, 3-64. Springer Verlag, chapter 1. P.W. Hawkes, J.C.H. Spence (Eds.).
41. Kirkland E.J. Advanced Computing in Electron Microscopy 2010, Springer Verlag. second ed.
42. Langmore J.P., Smith M.F. Quantitative energy-filtered electron microscopy of biological molecules in ice. Ultramicroscopy 1992, 46:349-373.
43. Leis A., Rockel B., Andrees L., Baumeister W. Visualizing cells at the nanoscale. Trends Biochem. Sci. 2009, 34:60-70.
44. 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, 10.1038/nmeth.2472.
45. Lucić V., Förster F., Baumeister W. Structural studies by electron tomography: from cells to molecules. Ann. Rev. Biochem. 2005, 74:833-865.
46. Lücken U., Tiemeijer P., Barfels M., Mooney P., Bailey B., Agard D. Image information transfer through a post-column energy filter with detection by a lens-coupled transmission-scintillator CCD camera. Microsc. Microanal. 2008, 14:1322-1323.
47. Marabini R., Herman G.T., Carazo J.-M. 3D reconstruction in electron microscopy using ART with smooth spherically symmetric volume elements (blobs). Ultramicroscopy 1998, 72:53-65.
48. Marabini R., Rietzel E., Schröder R., Herman G.T., Carazo J.-M. Three-dimensional reconstruction from reduced sets of very noisy images acquired following a single-axis tilt scheme: application of a new three-dimensional reconstruction algorithm and objective comparison with weighted backprojection. J. Struct. Biol. 1997, 120:363-371.
49. McIntosh R., Nicastro D., Mastronarde D. New views of cells in 3D: an introduction to electron tomography. Trends Cell Biol. 2005, 15:43-51.
50. Meyer R.R., Kirkland A. The effects of electron and photon scattering on signal and noise transfer properties of scintillators in CCD cameras used for electron detection. Ultramicroscopy 1998, 75:23-33.
51. Mobus G., Schweinfest R., Gemming T., Wagner T., Rühle M. Iterative structure retrieval techniques in HREM: a comparative study and a modular program package. J. Microsc. 1998, 190:109-130.
52. Müller H., Rose H., Schorsch P. A coherence function approach to image simulation. J. Microsc. 1998, 190:73-88.
53. Nickell S., Förster F., Linaroudis A., Del Net W., Beck F., Hegerl R., Baumeister W., Plitzko J.M. TOM software toolbox: acquisition and analysis for electron tomography. J. Struct. Biol. 2005, 149:227-234.
54. Peng L.-M., Dudarev S.L., Whelan M.J. Electron scattering factors of ions and dynamical RHEED from surfaces of ionic crystals. Phys. Rev. B 1998, 57:7259-7265.
55. Peng L.-M., Dudarev S.L., Whelan M.J. High-energy electron diffraction and microscopy. vol. 61 2004, Oxford University Press.
56. Peng L.-M., Ren G., Dudarev S.L., Whelan M.J. Robust parameterization of elastic and absorptive electron atomic scattering factors. Acta Crystallogr. A 1996, 52:257-276.
57. Philippsen A., Engel H., Engel A. The contrast-imaging function for tilted specimens. Ultramicroscopy 2007, 107:202-212.
58. Reichelt R., Engel A. Monte carlo calculations of elastic and inelastic electron scattering in biological and plastic materials. Ultramicroscopy 1984, 13:279-293.
59. Reimer L., Kohl H. Transmission electron microscopy. Springer Series in Optical Sciences 2008, vol. 36. Springer-Verlag. fifth ed.
60. Rullgård H., Öfverstedt L.-G., Masich S., Daneholt B., Öktem O. Simulation of transmission electron microscope images of biological specimens. J. Microsc. 2011, 242:234-256.
61. Sali A., Glaeser R.M., Earnest T., Baumeister W. From words to literature in structural proteomics. Nature 2003, 422:216-225.
62. Saxton O. Quantitative comparison of images and transforms. J. Microsc. 1997, 190:52-60.
63. Shaikh T.R., Gao H., Baxter W.T., Asturias F.J., Boisset N., Leith A., Frank F. SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs. Nat. Protoc. 2008, 3:1941-1974.
64. Shang Z., Sigworth F.J. Hydration-layer models for cryo-EM image simulation. J. Struct. Biol. 2012, 180:10-16.
65. Sorzano C.O.S., Marabini R., Boisset N., Rietzel E., Schröder R., Herman G.T., Carazo J.-M. The effect of overabundant projection directions on 3D reconstruction algorithms. J. Struct. Biol. 2001, 133:108-118.
66. Sorzano C.O.S., Marabini R., Velázquez-Muriel J., Bilbao-Castro J., Scheres S.H.W., Carazo J.M., Pascual-Montano A. XMIPP: a new generation of an open-source image processing package for electron microscopy. J. Struct. Biol. 2004, 148:194-204.
67. Sun S., Shi S., Leapman R. Water distributions of hydrated biological specimens by valence electron energy loss spectroscopy. Ultramicroscopy 1993, 50:127-139.
68. Tang D., Kirkland A., Jefferson D. Optimisation of high-resolution image simulations: I.Image selection in real space. Ultramicroscopy 1993, 48:321-331.
69. Tang D., Kirkland A., Jefferson D. Optimisation of high-resolution image simulations: II. Image selection in reciprocal space. Ultramicroscopy 1994, 53:137-146.
70. Tang G., Peng L., Baldwin P.R., Mann D.S., Jiang W., Rees I., Ludtke S.J. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 2007, 157:38-46.
71. Teeter M.M. Water structure of a hydrophobic protein at atomic resolution: pentagon rings of water molecules in crystals of crambin. Proc. Natl. Acad. Sci. 1984, 81:6014-6018.
72. Thust A. High-resolution transmission electron microscopy on an absolute contrast scale. Phys. Rev. Lett. 2009, 102:2208011-2208014.
73. Vinogradov S.N., Sharma P.K. Preparation and characterization of invertebrate globin complexes. Hemoglobins Part B: Biochemical and Analytical Methods 1994, 112-124. Academic Press, (Chapter 8). J. Everse, K.D. Vandegriff, R.M. Winslow (Eds.).
74. Voortman L.M., Franken E.M., van Vliet L.J., Rieger B. Fast, spatially varying CTF correction in TEM. Ultramicroscopy 2012, 118:26-34.
75. 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.
76. Vriend G. WHAT IF: a molecular modeling and drug design program. J. Mol. Graph. 1990, 8:52-56.
77. 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, 116:115-134.
78. Vulovic 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. D 2010, 66:97-109.
79. Vulović, M., Voortman, L.M., van Vliet, L.J., Rieger, B., 2013. When to use the projection assumption and weak-phase object approximation in phase contrast cryo-EM (submitted for publication).
80. Wall J., Isaacson M., Langmore J.P. Collection of scattered electrons in dark field electron microscopy - 2. Inelastic scattering. Optik 1974, 39:359-374.
81. Wan, Y., Chiu, W., Zhou, Z.H., 2004. Full contrast transfer function correction in 3D cryo-EM reconstruction. In: IEEE Proceedings of ICCCAS 2004, vol. 2, pp. 960-964.
82. Wang Y., Chiu J., He Q. Proteomics in computer-aided drug design. Curr. Computer-Aided Drug Des. 2005, 1:43-52.
83. 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.