In Situ Cryo-Electron Tomography: A Post-Reductionist Approach to Structural Biology

Journal of Molecular Biology

Volumn 428, Issue 2, 2016, Pages 332-343

  Asano, Shoh ^a   Engel, Benjamin D ^a   Baumeister, Wolfgang ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

cryo EM; subtomogram averaging; template matching; tomography; visual proteomics

Indexed keywords

BIOLOGICAL FUNCTIONS; CELL STRUCTURE; CHEMICAL STRUCTURE; ELECTRON TOMOGRAPHY; ENDOPLASMIC RETICULUM; FIDUCIAL MARKER; GOLGI COMPLEX; INTRACELLULAR SPACE; MACROMOLECULE; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN MICROARRAY; PROTEOMICS; RADIOSENSITIVITY; REGULATORY MECHANISM; REVIEW; STRUCTURE ANALYSIS; VITRIFICATION; BIOLOGY; CHEMISTRY; CRYOELECTRON MICROSCOPY; IMAGE PROCESSING; PROCEDURES; ULTRASTRUCTURE; WORKFLOW;

MACROMOLECULE;

BIOLOGY; CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; IMAGE PROCESSING, COMPUTER-ASSISTED; MACROMOLECULAR SUBSTANCES; WORKFLOW;

EID: 84957427113     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.09.030     Document Type: Review

References (134)

1. H.J. Berendsen, and S. Hayward Collective protein dynamics in relation to function Curr. Opin. Struct. Biol. 10 2000 165 169
2. H. Frauenfelder, S.G. Sligar, and P.G. Wolynes The energy landscapes and motions of proteins Science 254 1991 1598 1603
3. L.M. Gierasch, and A. Gershenson Post-reductionist protein science, or putting Humpty Dumpty back together again Nat. Chem. Biol. 5 2009 774 777
4. A. Sali, R. Glaeser, T. Earnest, and W. Baumeister From words to literature in structural proteomics Nature 422 2003 216 225
5. S.D. Durbin, and G. Feher Protein crystallization Annu. Rev. Phys. Chem. 47 1996 171 204
6. V. Lucic, A. Rigort, and W. Baumeister Cryo-electron tomography: The challenge of doing structural biology in situ J. Cell Biol. 202 2013 407 419
7. D. Vanhecke, S. Asano, Z. Kochovski, R. Fernandez-Busnadiego, N. Schrod, W. Baumeister, and et al. Cryo-electron tomography: Methodology, developments and biological applications J. Microsc. 242 2011 221 227
8. O. Medalia, I. Weber, A.S. Frangakis, D. Nicastro, G. Gerisch, and W. Baumeister Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography Science 298 2002 1209 1213
9. S. Asano, Y. Fukuda, F. Beck, A. Aufderheide, F. Forster, R. Danev, and et al. Proteasomes. A molecular census of 26S proteasomes in intact neurons Science 347 2015 439 442
10. B.D. Engel, M. Schaffer, Cuellar L. Kuhn, E. Villa, J.M. Plitzko, and W. Baumeister Native architecture of the Chlamydomonas chloroplast revealed by in situ cryo-electron tomography eLife 4 2015 e04889
11. M. Jasnin, S. Asano, E. Gouin, R. Hegerl, J.M. Plitzko, E. Villa, and et al. Three-dimensional architecture of actin filaments in Listeria monocytogenes comet tails Proc. Natl. Acad. Sci. U. S. A. 110 2013 20521 20526
12. F. Brandt, L.A. Carlson, F.U. Hartl, W. Baumeister, and K. Grunewald The three-dimensional organization of polyribosomes in intact human cells Mol. Cell 39 2010 560 569
13. A. Leforestier, N. Lemercier, and F. Livolant Contribution of cryoelectron microscopy of vitreous sections to the understanding of biological membrane structure Proc. Natl. Acad. Sci. U. S. A. 109 2012 8959 8964
14. A. Al-Amoudi, D.C. Diez, M.J. Betts, and A.S. Frangakis The molecular architecture of cadherins in native epidermal desmosomes Nature 450 2007 832 837
15. Y. Fukuda, U. Laugks, V. Lucic, W. Baumeister, and R. Danev Electron cryotomography of vitrified cells with a Volta phase plate J. Struct. Biol. 190 2015 143 154
16. B.D. Engel, M. Schaffer, S. Albert, S. Asano, J.M. Plitzko, and W. Baumeister In situ structural analysis of Golgi intracisternal protein arrays Proc. Natl. Acad. Sci. U. S. A. 112 2015 11264 11269
17. J. Bohm, A.S. Frangakis, R. Hegerl, S. Nickell, D. Typke, and W. Baumeister Toward detecting and identifying macromolecules in a cellular context: Template matching applied to electron tomograms Proc. Natl. Acad. Sci. U. S. A. 97 2000 14245 14250
18. Y.X. Chen, S. Pfeffer, J.J. Fernandez, C.O.S. Sorzano, and F. Forster Autofocused 3D classification of cryoelectron subtomograms Structure 22 2014 1528 1537
19. J.A.G. Briggs Structural biology in situ - The potential of subtomogram averaging Curr. Opin. Struct. Biol. 23 2013 261 267
20. F. Forster, B.G. Han, and M. Beck Visual proteomics Methods Enzymol. 483 2010 215 243
21. C.V. Robinson, A. Sali, and W. Baumeister The molecular sociology of the cell Nature 450 2007 973 982
22. R. Grimm, H. Singh, R. Rachel, D. Typke, W. Zillig, and W. Baumeister Electron tomography of ice-embedded prokaryotic cells Biophys. J. 74 1998 1031 1042
23. G.E. Murphy, J.R. Leadbetter, and G.J. Jensen In situ structure of the complete Treponema primitia flagellar motor Nature 442 2006 1062 1064
24. A. Briegel, D.R. Ortega, E.I. Tocheva, K. Wuichet, Z. Li, S. Chen, and et al. Universal architecture of bacterial chemoreceptor arrays Proc. Natl. Acad. Sci. U. S. A. 106 2009 17181 17186
25. M. Winey, C.L. Mamay, E.T. O'Toole, D.N. Mastronarde, T.H. Giddings Jr., K.L. McDonald, and et al. Three-dimensional ultrastructural analysis of the Saccharomyces cerevisiae mitotic spindle J. Cell Biol. 129 1995 1601 1615
26. B.K. Garvalov, B. Zuber, C. Bouchet-Marquis, M. Kudryashev, M. Gruska, M. Beck, and et al. Luminal particles within cellular microtubules J. Cell Biol. 174 2006 759 765
27. V. Lucic, A.H. Kossel, T. Yang, T. Bonhoeffer, W. Baumeister, and A. Sartori Multiscale imaging of neurons grown in culture: From light microscopy to cryo-electron tomography J. Struct. Biol. 160 2007 146 156
28. I. Patla, T. Volberg, N. Elad, V. Hirschfeld-Warneken, C. Grashoff, R. Fassler, and et al. Dissecting the molecular architecture of integrin adhesion sites by cryo-electron tomography Nat. Cell Biol. 12 2010 909 915
29. J. Dubochet, M. Adrian, J.J. Chang, J.C. Homo, J. Lepault, A.W. McDowall, and et al. Cryo-electron microscopy of vitrified specimens Q. Rev. Biophys. 21 1988 129 228
30. J. Dubochet, J. Lepault, R. Freeman, J.A. Berriman, and J.C. Homo Electron microscopy of frozen water and aqueous solutions J. Microsc. 128 1982 219 237
31. K.A. Taylor, and R.M. Glaeser Electron microscopy of frozen hydrated biological specimens J. Ultrastruct. Res. 55 1976 448 456
32. N. Sartori, K. Richter, and J. Dubochet Vitrification depth can be increased more than 10-fold by high-pressure freezing J. Microsc. 172 1993 55 61
33. D. Studer, W. Graber, A. Al-Amoudi, and P. Eggli A new approach for cryofixation by high-pressure freezing J. Microsc. 203 2001 285 294
34. R. Cole, G. Matuszek, C. See, and C.L. Rieder A simple pneumatic device for plunge-freezing cells grown on electron microscopy grids J. Electron Microsc. Tech. 16 1990 167 173
35. J.R. Bellare, H.T. Davis, L.E. Scriven, and Y. Talmon Controlled environment vitrification system: An improved sample preparation technique J. Electron Microsc. Tech. 10 1988 87 111
36. C.V. Iancu, W.F. Tivol, J.B. Schooler, D.P. Dias, G.P. Henderson, G.E. Murphy, and et al. Electron cryotomography sample preparation using the Vitrobot Nat. Protoc. 1 2006 2813 2819
37. H. Kanno, R.J. Speedy, and C.A. Angell Supercooling of water to - 92° under pressure Science 189 1975 880 881
38. K. McDonald, H. Schwarz, T. Muller-Reichert, R. Webb, C. Buser, and M. Morphew "Tips and tricks" for high-pressure freezing of model systems Methods Cell Biol. 96 2010 671 693
39. A. Al-Amoudi, D. Studer, and J. Dubochet Cutting artefacts and cutting process in vitreous sections for cryo-electron microscopy J. Struct. Biol. 150 2005 109 121
40. J. Dubochet, B. Zuber, M. Eltsov, C. Bouchet-Marquis, A. Al-Amoudi, and F. Livolant How to "read" a vitreous section Methods Cell Biol. 79 2007 385 406
41. H.M. Han, B. Zuber, and J. Dubochet Compression and crevasses in vitreous sections under different cutting conditions J. Microsc. 230 2008 167 171
42. M.F. Hayles, D.A.M. de Winter, C.T.W.M. Schneijdenberg, J.D. Meeldijk, U. Luecken, H. Persoon, and et al. The making of frozen-hydrated, vitreous lamellas from cells for cryo-electron microscopy J. Struct. Biol. 172 2010 180 190
43. C. Hsieh, T. Schmelzer, G. Kishchenko, T. Wagenknecht, and M. Marko Practical workflow for cryo focused-ion-beam milling of tissues and cells for cryo-TEM tomography J. Struct. Biol. 185 2014 32 41
44. J. Mahamid, R. Schampers, H. Persoon, A.A. Hyman, W. Baumeister, and J.M. Plitzko A focused ion beam milling and lift-out approach for site-specific preparation of frozen-hydrated lamellas from multicellular organisms J. Struct. Biol. 2015 In press
45. A. Sartori, R. Gatz, F. Beck, A. Rigort, W. Baumeister, and J.M. Plitzko Correlative microscopy: Bridging the gap between fluorescence light microscopy and cryo-electron tomography J. Struct. Biol. 160 2007 135 145
46. A.V. Agronskaia, J.A. Valentijn, L.F. van Driel, C.T. Schneijdenberg, B.M. Humbel, P.M. van Bergen en Henegouwen, and et al. Integrated fluorescence and transmission electron microscopy J. Struct. Biol. 164 2008 183 189
47. M. Schorb, and J.A.G. Briggs Correlated cryo-fluorescence and cryo-electron microscopy with high spatial precision and improved sensitivity Ultramicroscopy 143 2014 24 32
48. W. Kukulski, M. Schorb, S. Welsch, A. Picco, M. Kaksonen, and J.A.G. Briggs Correlated fluorescence and 3D electron microscopy with high sensitivity and spatial precision J. Cell Biol. 192 2011 111 119
49. L.F. van Driel, J.A. Valentijn, K.M. Valentijn, R.I. Koning, and A.J. Koster Tools for correlative cryo-fluorescence microscopy and cryo-electron tomography applied to whole mitochondria in human endothelial cells Eur. J. Cell Biol. 88 2009 669 684
50. R. Kaufmann, P. Schellenberger, E. Seiradake, I.M. Dobbie, E.Y. Jones, I. Davis, and et al. Super-resolution microscopy using standard fluorescent proteins in intact cells under cryo-conditions Nano Lett. 14 2014 4171 4175
51. O. Medalia, M. Beck, M. Ecke, I. Weber, R. Neujahr, W. Baumeister, and et al. Organization of actin networks in intact filopodia Curr. Biol. 17 2007 79 84
52. M. Marko, C. Hsieh, R. Schalek, J. Frank, and C. Mannella Focused-ion-beam thinning of frozen-hydrated biological specimens for cryo-electron microscopy Nat. Methods 4 2007 215 217
53. A. Rigort, F.J. Bauerlein, E. Villa, M. Eibauer, T. Laugks, W. Baumeister, and et al. Focused ion beam micromachining of eukaryotic cells for cryoelectron tomography Proc. Natl. Acad. Sci. U. S. A. 109 2012 4449 4454
54. E. Villa, M. Schaffer, J.M. Plitzko, and W. Baumeister Opening windows into the cell: Focused-ion-beam milling for cryo-electron tomography Curr. Opin. Struct. Biol. 23 2013 771 777
55. A. Rigort, E. Villa, F.J. Bauerlein, B.D. Engel, and J.M. Plitzko Integrative approaches for cellular cryo-electron tomography: Correlative imaging and focused ion beam micromachining Methods Cell Biol. 111 2012 259 281
56. M. Schaffer, B.D. Engel, T. Laugks, J. Mahamid, J.M. Plitzko, and W. Baumeister Cryo-focused ion beam sample preparation for imaging vitreous cells by cryo-electron tomography Bio-Protocol 5 2015 e1575
57. A.J. Koster, R. Grimm, D. Typke, R. Hegerl, A. Stoschek, J. Walz, and et al. Perspectives of molecular and cellular electron tomography J. Struct. Biol. 120 1997 276 308
58. J.F. Conway, B.L. Trus, F.P. Booy, W.W. Newcomb, J.C. Brown, and A.C. Steven The effects of radiation damage on the structure of frozen-hydrated Hsv-1 capsids J. Struct. Biol. 111 1993 222 233
59. R.M. Glaeser Limitations to significant information in biological electron microscopy as a result of radiation damage J. Ultrastruct. Res. 36 1971 466 482
60. Y. Talmon, M. Adrian, and J. Dubochet Electron beam radiation damage to organic inclusions in vitreous, cubic, and hexagonal ice J. Microsc. 141 1986 375 384
61. L.A. Baker, E.A. Smith, S.A. Bueler, and J.L. Rubinstein The resolution dependence of optimal exposures in liquid nitrogen temperature electron cryomicroscopy of catalase crystals J. Struct. Biol. 169 2010 431 437
62. H. Stark, F. Zemlin, and C. Boettcher Electron radiation damage to protein crystals of bacteriorhodopsin at different temperatures Ultramicroscopy 63 1996 75 79
63. S.A. Fromm, T.A.M. Bharat, A.J. Jakobi, W.J.H. Hagen, and C. Sachse Seeing tobacco mosaic virus through direct electron detectors J. Struct. Biol. 189 2015 87 97
64. X.C. Bai, I.S. Fernandez, G. McMullan, and S.H. Scheres Ribosome structures to near-atomic resolution from thirty thousand cryo-EM particles eLife 2 2013 e00461
65. A.C. Milazzo, A.C. Cheng, A. Moeller, D. Lyumkis, E. Jacovetty, J. Polukas, and et al. Initial evaluation of a direct detection device detector for single particle cryo-electron microscopy J. Struct. Biol. 176 2011 404 408
66. X. Li, P. Mooney, S. Zheng, C.R. Booth, M.B. Braunfeld, S. Gubbens, and et al. Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM Nat. Methods 10 2013 584 590
67. R. Danev, B. Buijsse, M. Khoshouei, J.M. Plitzko, and W. Baumeister Volta potential phase plate for in-focus phase contrast transmission electron microscopy Proc. Natl. Acad. Sci. U. S. A. 111 2014 15635 15640
68. G. McMullan, A.T. Clark, R. Turchetta, and A.R. Faruqi Enhanced imaging in low dose electron microscopy using electron counting Ultramicroscopy 109 2009 1411 1416
69. G. McMullan, A.R. Faruqi, D. Clare, and R. Henderson Comparison of optimal performance at 300 keV of three direct electron detectors for use in low dose electron microscopy Ultramicroscopy 147 2014 156 163
70. R.S. Ruskin, Z.H. Yu, and N. Grigorieff Quantitative characterization of electron detectors for transmission electron microscopy J. Struct. Biol. 184 2013 385 393
71. M.G. Campbell, D. Veesler, A.C. Cheng, C.S. Potter, and B. Carragher 2.8 Angstrom resolution reconstruction of the Thermoplasma acidophilum 20S proteasome using cryo-electron microscopy eLife 4 2015 e06380
72. R.M. Voorhees, I.S. Fernandez, S.H.W. Scheres, and R.S. Hegde Structure of the mammalian ribosome-Sec61 complex to 3.4 angstrom resolution Cell 157 2014 1632 1643
73. E.H. Cao, M.F. Liao, Y.F. Cheng, and D. Julius TRPV1 structures in distinct conformations reveal activation mechanisms Nature 504 2013 113 118
74. A. Aufderheide, F. Beck, F. Stengel, M. Hartwig, A. Schweitzer, G. Pfeifer, and et al. Structural characterization of the interaction of Ubp6 with the 26S proteasome Proc. Natl. Acad. Sci. U. S. A. 112 2015 8626 8631
75. C. Plaschka, L. Lariviere, L. Wenzeck, M. Seizl, M. Hemann, D. Tegunov, and et al. Architecture of the RNA polymerase II-mediator core initiation complex Nature 518 2015 376 380
76. A. Bartesaghi, A. Merk, S. Banerjee, D. Matthies, X. Wu, J.L. Milne, and et al. 2.2 Å Resolution cryo-EM structure of beta-galactosidase in complex with a cell-permeant inhibitor Science 348 2015 1147 1151
77. W. Kuhlbrandt Biochemistry. The resolution revolution Science 343 2014 1443 1444
78. Y. Cheng Single-particle cryo-EM at crystallographic resolution Cell 161 2015 450 457
79. A. Dubrovsky, S. Sorrentino, J. Harapin, K.T. Sapra, and O. Medalia Developments in cryo-electron tomography for in situ structural analysis Arch. Biochem. Biophys. 581 2015 78 85
80. V.A. Gold, R. Ieva, A. Walter, N. Pfanner, M. van der Laan, and W. Kuhlbrandt Visualizing active membrane protein complexes by electron cryotomography Nat. Commun. 5 2014 4129
81. B. Hu, D.R. Morado, W. Margolin, J.R. Rohde, O. Arizmendi, W.L. Picking, and et al. Visualization of the type III secretion sorting platform of Shigella flexneri Proc. Natl. Acad. Sci. U. S. A. 112 2015 1047 1052
82. C.L. Woodward, L.M. Mendonca, and G.J. Jensen Direct visualization of vaults within intact cells by electron cryo-tomography Cell. Mol. Life Sci. 72 2015 3401 3409
83. Q.R. Xiong, M.K. Morphew, C.L. Schwartz, A.H. Hoenger, and D.N. Mastronarde CTF determination and correction for low dose tomographic tilt series J. Struct. Biol. 168 2009 378 387
84. Z.F. Yang, and P.A. Penczek Cryo-EM image alignment based on nonuniform fast Fourier transform Ultramicroscopy 108 2008 959 969
85. A.S. Frangakis, and R. Hegerl Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion J. Struct. Biol. 135 2001 239 250
86. A. Stoschek, T.P.Y. Yu, and R. Hegerl Denoising of electron tomographic reconstructions from biological specimens using multidimensional multiscale transforms 1997 IEEE International Conference on Acoustics, Speech, and Signal Processing I-V 1997 2793 2796
87. A. Buades, B. Coll, and J.M. Morel A review of image denoising algorithms, with a new one Multiscale Model. Simul. 4 2005 490 530
88. J.J. Fernandez, and S. Li An improved algorithm for anisotropic nonlinear diffusion for denoising cryo-tomograms J. Struct. Biol. 144 2003 152 161
89. P. Gilbert Iterative methods for three-dimensional reconstruction of an object from projections J. Theor. Biol. 36 1972 105 117
90. K.J. Batenburg, S. Bals, J. Sijbers, C. Kubel, P.A. Midgley, J.C. Hernandez, and et al. 3D imaging of nanomaterials by discrete tomography Ultramicroscopy 109 2009 730 740
91. R.A. Crowther, D.J. Derosier, and A. Klug Reconstruction of three-dimensional structure from projections and its application to electron microscopy Proc. R. Soc. A 317 1970 319 340
92. A. Rigort, D. Gunther, R. Hegerl, D. Baum, B. Weber, S. Prohaska, and et al. Automated segmentation of electron tomograms for a quantitative description of actin filament networks J. Struct. Biol. 177 2012 135 144
93. A. Martinez-Sanchez, I. Garcia, and J.J. Fernandez A ridge-based framework for segmentation of 3D electron microscopy datasets J. Struct. Biol. 181 2013 61 70
94. R. Fernandez-Busnadiego, S. Asano, A.M. Oprisoreanu, E. Sakata, M. Doengi, Z. Kochovski, and et al. Cryo-electron tomography reveals a critical role of RIM1alpha in synaptic vesicle tethering J. Cell Biol. 201 2013 725 740
95. Y.X. Zhu, B. Carragher, R.M. Glaeser, D. Fellmann, C. Bajaj, M. Bern, and et al. Automatic particle selection: Results of a comparative study J. Struct. Biol. 145 2004 3 14
96. J.O. Ortiz, F. Forster, J. Kurner, A.A. Linaroudis, and W. Baumeister Mapping 70S ribosomes in intact cells by cryoelectron tomography and pattern recognition J. Struct. Biol. 156 2006 334 341
97. Y.X. Chen, T. Hrabe, S. Pfeffer, O. Pauly, D. Mateus, N. Navab, and et al. Detection and identification of macromolecular complexes in cryo-electron tomograms using support vector machines 2012 9th IEEE International Symposium on Biomedical Imaging (ISBI) 2012 1373 1376
98. J.J. Fernandez Computational methods for electron tomography Micron 43 2012 1010 1030
99. A. Martinez-Sanchez, I. Garcia, S. Asano, V. Lucic, and J.J. Fernandez Robust membrane detection based on tensor voting for electron tomography J. Struct. Biol. 186 2014 49 61
100. N. Volkmann Putting structure into context: Fitting of atomic models into electron microscopic and electron tomographic reconstructions Curr. Opin. Cell Biol. 24 2012 141 147
101. F. Forster, and R. Hegerl Structure determination in situ by averaging of tomograms Methods Cell Biol. 79 2007 741 767
102. A.S. Frangakis, J. Bohm, F. Forster, S. Nickell, D. Nicastro, D. Typke, and et al. Identification of macromolecular complexes in cryoelectron tomograms of phantom cells Proc. Natl. Acad. Sci. U. S. A. 99 2002 14153 14158
103. S. Nickell, O. Mihalache, F. Beck, R. Hegerl, A. Korinek, and W. Baumeister Structural analysis of the 26S proteasome by cryoelectron tomography Biochem. Biophys. Res. Commun. 353 2007 115 120
104. T. Hrabe, Y.X. Chen, S. Pfeffer, L.K. Cuellar, A.V. Mangold, and F. Forster PyTom: A python-based toolbox for localization of macromolecules in cryo-electron tomograms and subtomogram analysis J. Struct. Biol. 178 2012 177 188
105. Y.X. Chen, S. Pfeffer, T. Hrabe, J.M. Schuller, and F. Forster Fast and accurate reference-free alignment of subtomograms J. Struct. Biol. 182 2013 235 245
106. J. Walz, D. Typke, M. Nitsch, A.J. Koster, R. Hegerl, and W. Baumeister Electron tomography of single ice-embedded macromolecules: Three-dimensional alignment and classification J. Struct. Biol. 120 1997 387 395
107. S. Pfeffer, M.W. Woellhaf, J.M. Herrmann, and F. Forster Organization of the mitochondrial translation machinery studied in situ by cryoelectron tomography Nat. Commun. 6 2015 6019
108. M. Stolken, F. Beck, T. Haller, R. Hegerl, I. Gutsche, J.M. Carazo, and et al. Maximum likelihood based classification of electron tomographic data J. Struct. Biol. 173 2011 77 85
109. M.G. Rossmann Fitting atomic models into electron microscopy maps Acta Crystallogr. D Biol. Crystallogr. 56 2000 1341 1349
110. L.G. Trabuco, E. Villa, K. Mitra, J. Frank, and K. Schulten Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics Structure 16 2008 673 683
111. E. Villa, and K. Lasker Finding the right fit: Chiseling structures out of cryo-electron microscopy maps Curr. Opin. Struct. Biol. 25 2014 118 125
112. P. Unverdorben, F. Beck, P. Sledz, A. Schweitzer, G. Pfeifer, J.M. Plitzko, and et al. Deep classification of a large cryo-EM dataset defines the conformational landscape of the 26S proteasome Proc. Natl. Acad. Sci. U. S. A. 111 2014 5544 5549
113. B. Kastner, N. Fischer, M.M. Golas, B. Sander, P. Dube, D. Boehringer, and et al. GraFix: Sample preparation for single-particle electron cryomicroscopy Nat. Methods 5 2008 53 55
114. Y. Cheng, N. Grigorieff, P.A. Penczek, and T. Walz A primer to single-particle cryo-electron microscopy Cell 161 2015 438 449
115. J. Cohen Is high-tech view of HIV too good to be true? Science 341 2013 443 444
116. M. Shatsky, R.J. Hall, S.E. Brenner, and R.M. Glaeser A method for the alignment of heterogeneous macromolecules from electron microscopy J. Struct. Biol. 166 2009 67 78
117. R. Henderson Avoiding the pitfalls of single particle cryo-electron microscopy: Einstein from noise Proc. Natl. Acad. Sci. U. S. A. 110 2013 18037 18041
118. S. Nickell, C. Kofler, A.P. Leis, and W. Baumeister A visual approach to proteomics Nat. Rev. Mol. Cell Biol. 7 2006 225 230
119. D. Voges, P. Zwickl, and W. Baumeister The 26S proteasome: A molecular machine designed for controlled proteolysis Annu. Rev. Biochem. 68 1999 1015 1068
120. W. Baumeister, J. Walz, F. Zuhl, and E. Seemuller The proteasome: Paradigm of a self-compartmentalizing protease Cell 92 1998 367 380
121. D. Finley Recognition and processing of ubiquitin-protein conjugates by the proteasome Annu. Rev. Biochem. 78 2009 477 513
122. F. Beck, P. Unverdorben, S. Bohn, A. Schweitzer, G. Pfeifer, E. Sakata, and et al. Near-atomic resolution structural model of the yeast 26S proteasome Proc. Natl. Acad. Sci. U. S. A. 109 2012 14870 14875
123. H.C. Tai, H. Besche, A.L. Goldberg, and E.M. Schuman Characterization of the brain 26S proteasome and its interacting proteins Front. Mol. Neurosci. 3 2010 12
124. M.E. Matyskiela, G.C. Lander, and A. Martin Conformational switching of the 26S proteasome enables substrate degradation Nat. Struct. Mol. Biol. 20 2013 781 788
125. C.G. Pack, H. Yukii, A. Toh-e, T. Kudo, H. Tsuchiya, A. Kaiho, and et al. Quantitative live-cell imaging reveals spatio-temporal dynamics and cytoplasmic assembly of the 26S proteasome Nat. Commun. 5 2014 3396
126. A.M. Hamilton, and K. Zito Breaking it down: The ubiquitin proteasome system in neuronal morphogenesis Neural Plast. 2013 2013 196848
127. A.H.P. Jansen, E.A.J. Reits, and E.M. Hol The ubiquitin proteasome system in glia and its role in neurodegenerative diseases Front. Mol. Neurosci. 7 2014 73
128. K. Sasai, Y. Ikeda, T. Tsuda, H. Ihara, H. Korekane, K. Shiota, and et al. The critical role of the stem region as a functional domain responsible for the oligomerization and Golgi localization of N-acetylglucosaminyltransferase V - The involvement of a domain homophilic interaction J. Biol. Chem. 276 2001 759 765
129. C. McCormick, G. Duncan, K.T. Goutsos, and F. Tufaro The putative tumor suppressors EXT1 and EXT2 form a stable complex that accumulates in the Golgi apparatus and catalyzes the synthesis of heparan sulfate Proc. Natl. Acad. Sci. U. S. A. 97 2000 668 673
130. Y.H. Chou, G. Pogorelko, Z.T. Young, and O.A. Zabotina Protein-protein interactions among xyloglucan-synthesizing enzymes and formation of Golgi-localized multiprotein complexes Plant Cell Physiol. 56 2015 255 267
131. A. Hassinen, and S. Kellokumpu Organizational interplay of Golgi N-glycosyltransferases involves organelle microenvironment-dependent transitions between enzyme homo- and heteromers J. Biol. Chem. 289 2014 26937 26948
132. M. Klann, and H. Koeppl Spatial simulations in systems biology: From molecules to cells Int. J. Mol. Sci. 13 2012 7798 7827
133. M. Feig, and Y. Sugita Reaching new levels of realism in modeling biological macromolecules in cellular environments J. Mol. Graph. Model. 45 2013 144 156
134. J. Schoneberg, A. Ullrich, and F. Noe Simulation tools for particle-based reaction-diffusion dynamics in continuous space BMC Biophys. 7 2014 11