Cryoelectron Tomography of Eukaryotic Cells

Methods in Enzymology

Volumn 483, Issue C, 2010, Pages 245-265

  Mader, Asaf ^a   Elad, Nadav ^a   Medalia, Ohad ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Actin; Correlated microscopy; Cryoelectron tomography; Cytoskeleton; Microtubule; Nuclear pore complex

Indexed keywords

CADMIUM SELENIDE; CARBON; COPPER; F ACTIN; GOLD; PLATINUM; PROTEOME; QUANTUM DOT; SCLEROPROTEIN;

BOOK; CELL ADHESION; CELL NUCLEUS MEMBRANE; CELL ORGANELLE; CELL STRUCTURE; CHEMICAL STRUCTURE; CYTOKINESIS; CYTOSKELETON; DICTYOSTELIUM DISCOIDEUM; ELECTRON TOMOGRAPHY; EUKARYOTIC CELL; EXTRACELLULAR MATRIX; FLUORESCENCE MICROSCOPY; FREEZING; FUSION GENE; MACROMOLECULE; MICROSCOPY; MIDBODY; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR PORE COMPLEX; OPTICAL RESOLUTION; PHOTOACTIVATED LOCALIZATION MICROSCOPY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; STAINING; STIMULATED EMISSION DEPLETION MICROSCOPY; STOCHASTIC OPTICAL RECONSTRUCTION MICROSCOPY; STRUCTURE ANALYSIS; THREE DIMENSIONAL IMAGING; ULTRAMICROTOMY; VITRIFICATION;

EUKARYOTA;

EID: 77957252774     PISSN: 00766879     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0076-6879(10)83012-5     Document Type: Chapter

References (115)

1. Adrian M., et al. Cryo-electron microscopy of viruses. Nature 1984, 308:32-36.
2. Akerman M.E., et al. Nanocrystal targeting in vivo. Proc. Natl. Acad. Sci. USA 2002, 99:12617-12621.
3. Akey C.W., Radermacher M. Architecture of the Xenopus nuclear pore complex revealed by three-dimensional cryo-electron microscopy. J. Cell Biol. 1993, 122:1-19.
4. Al-Amoudi A., et al. Cryo-electron microscopy of vitreous sections. EMBO J. 2004, 23:3583-3588.
5. Barr F.A., Gruneberg U. Cytokinesis: Placing and making the final cut. Cell 2007, 131:847-860.
6. Beck M., Medalia O. Structural and functional insights into nucleocytoplasmic transport. Histol. Histopathol. 2008, 23:1025-1033.
7. Beck M., et al. Nuclear pore complex structure and dynamics revealed by cryoelectron tomography. Science 2004, 306:1387-1390.
8. Beck M., et al. Snapshots of nuclear pore complexes in action captured by cryo-electron tomography. Nature 2007, 449:611-615.
9. Beck M., et al. Visual proteomics in Leptospira interrogans. Methods Enzymol. 2010, 1. Cryo-EM. Part 2 Lessons learned from specific examples chapter.
10. Ben-Harush K., et al. The supramolecular organization of the C. elegans nuclear lamin filament. J. Mol. Biol. 2009, 386:1392-1402.
11. Ben-Harush K., et al. Visualizing cellular processes at the molecular level by cryo-electron tomography. J. Cell Sci. 2010, 123:7-12.
12. Betzig E., et al. Imaging intracellular fluorescent proteins at nanometer resolution. Science 2006, 313:1642-1645.
13. Brown S., et al. Cytoskeletal elements of chick embryo fibroblasts revealed by detergent extraction. J. Supramol. Struct. 1976, 5:119-130.
14. Byers B., Abramson D.H. Cytokinesis in HeLa: Post-telophase delay and microtubule-associated motility. Protoplasma 1968, 66:413-435.
15. Callan H.G., Tomlin S.G. Experimental studies on amphibian oocyte nuclei. 1. Investigation of the structure of the nuclear membrane by means of the electron microscope. Proc. R. Soc. Lond. B Biol. Sci. 1950, 137:367-378.
16. Campbell I.D. The Croonian lecture 2006. Structure of the living cell. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2008, 363:2379-2391.
17. Chalfie M., et al. Green fluorescent protein as a marker for gene expression. Science 1994, 263:802-805.
18. Chen S., Briegel A. Correlative cryo-light and -electron microscopy. Methods Enzymol. 2010, 1. Cryo-EM. Part 1 Data collection chapter.
19. Connell J.W., et al. Spastin couples microtubule severing to membrane traffic in completion of cytokinesis and secretion. Traffic 2009, 10:42-56.
20. Cronshaw J.M., et al. Proteomic analysis of the mammalian nuclear pore complex. J. Cell Biol. 2002, 158:915-927.
21. Deerinck T.J., et al. Light and electron microscopic localization of multiple proteins using quantum dots. Methods Mol. Biol. 2007, 374:43-53.
22. Dierksen K., et al. Towards automatic electron tomography. Ultramicroscopy 1992, 40:71-87.
23. Dierksen K., et al. Towards automatic electron tomography. 2. Implementation of autofocus and low-dose procedures. Ultramicroscopy 1993, 49:109-120.
24. Dubochet J., et al. Electron-microscopy of frozen water and aqueous-solutions. J. Microsc. Oxf. 1982, 128:219-237.
25. Echard A., et al. Terminal cytokinesis events uncovered after an RNAi screen. Curr. Biol. 2004, 14:1685-1693.
26. Eggert U.S., et al. Animal cytokinesis: From parts list to mechanisms. Annu. Rev. Biochem. 2006, 75:543-566.
27. Elad N., et al. Structural analysis of the nuclear pore complex by integrated approaches. Curr. Opin. Struct. Biol. 2009, 19:226-232.
28. Euteneuer U., McIntosh J.R. Polarity of midbody and phragmoplast microtubules. J. Cell Biol. 1980, 87:509-515.
29. Forster F., et al. Retrovirus envelope protein complex structure in situ studied by cryo-electron tomography. Proc. Natl. Acad. Sci. USA 2005, 102:4729-4734.
30. Frangakis A.S., et al. Identification of macromolecular complexes in cryoelectron tomograms of phantom cells. Proc. Natl. Acad. Sci. USA 2002, 99:14153-14158.
31. Frenkiel-Krispin D., et al. Structural analysis of a metazoan nuclear pore complex reveals a fused concentric ring architecture. J. Mol. Biol. 2010, 395:578-586.
32. Gan L., et al. Molecular organization of Gram-negative peptidoglycan. Proc. Natl. Acad. Sci. USA 2008, 105:18953-18957.
33. Garvalov B.K., et al. Luminal particles within cellular microtubules. J. Cell Biol. 2006, 174:759-765.
34. Giepmans B.N., et al. Correlated light and electron microscopic imaging of multiple endogenous proteins using Quantum dots. Nat. Methods 2005, 2:743-749.
35. Glotzer M. The molecular requirements for cytokinesis. Science 2005, 307:1735-1739.
36. Gorlich D., Kutay U. Transport between the cell nucleus and the cytoplasm. Annu. Rev. Cell Dev. Biol. 1999, 15:607-660.
37. Grassucci R.A., et al. Preparation of macromolecular complexes for cryo-electron microscopy. Nat. Protoc. 2007, 2:3239-3246.
38. Grimm R., et al. 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.
39. Gromley A., et al. Centriolin anchoring of exocyst and SNARE complexes at the midbody is required for secretory-vesicle-mediated abscission. Cell 2005, 123:75-87.
40. Heim R., et al. Improved green fluorescence. Nature 1995, 373:663-664.
41. Hell S.W. Toward fluorescence nanoscopy. Nat. Biotechnol. 2003, 21:1347-1355.
42. Henderson G.P., et al. 3-D ultrastructure of O. tauri: Electron cryotomography of an entire eukaryotic cell. PLoS ONE 2007, 2:e749.
43. Heuser J.E., Kirschner M.W. Filament organization revealed in platinum replicas of freeze-dried cytoskeletons. J. Cell Biol. 1980, 86:212-234.
44. Hoshino A., et al. Quantum dots targeted to the assigned organelle in living cells. Microbiol. Immunol. 2004, 48:985-994.
45. Howarth M., et al. Monovalent, reduced-size quantum dots for imaging receptors on living cells. Nat. Methods 2008, 5:397-399.
46. Hsieh C.E., et al. Towards high-resolution three-dimensional imaging of native mammalian tissue: Electron tomography of frozen-hydrated rat liver sections. J. Struct. Biol. 2006, 153:1-13.
47. Iancu C.V., et al. Organization, structure, and assembly of alpha-carboxysomes determined by electron cryotomography of intact cells. J. Mol. Biol. 2010, 396:105-117.
48. Komeili A., et al. Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 2006, 311:242-245.
49. Koning R.I., Koster A.J. Cryo-electron tomography in biology and medicine. Ann. Anat. 2009, 191:427-445.
50. Konorty M., et al. Structural analysis of photosynthetic membranes by cryo-electron tomography of intact Rhodopseudomonas viridis cells. J. Struct. Biol. 2008, 161:393-400.
51. Kürner J., Baumeister W. Cryo-Electron Tomography Reveals the Architecture of a Bacterial Cytoskeleton. Complex Intracellular Structures in Prokaryotes 2006, 313-318. Springer-Verlag, Berlin-Heidelberg.
52. Kurner J., et al. New insights into the structural organization of eukaryotic and prokaryotic cytoskeletons using cryo-electron tomography. Exp. Cell Res. 2004, 301:38-42.
53. Ladinski M., et al. High-pressure freezing and cryosectioning thick samples. Methods Enzymol. 2010, 1. Cryo-EM. Part 1 Sample preparation chapter.
54. Li Z., Jensen G.J. Electron cryotomography: A new view into microbial ultrastructure. Curr. Opin. Microbiol. 2009, 12:333-340.
55. Lim R.Y., et al. Towards reconciling structure and function in the nuclear pore complex. Histochem. Cell Biol. 2008, 129:105-116.
56. Liu T., et al. The fluorescence bioassay platforms on quantum dots nanoparticles. J. Fluoresc. 2005, 15:729-733.
57. Lucic V., et al. Structural studies by electron tomography: From cells to molecules. Annu. Rev. Biochem. 2005, 74:833-865.
58. Lucic V., et al. Multiscale imaging of neurons grown in culture: From light microscopy to cryo-electron tomography. J. Struct. Biol. 2007, 160:146-156.
59. Lucic V., et al. Cryo-electron tomography of cells: Connecting structure and function. Histochem. Cell Biol. 2008, 130:185-196.
60. Marko M., et al. Focused-ion-beam thinning of frozen-hydrated biological specimens for cryo-electron microscopy. Nat. Methods 2007, 4:215-217.
61. Mastronarde D.N., et al. Interpolar spindle microtubules in PTK cells. J. Cell Biol. 1993, 123:1475-1489.
62. McDonald K.L., et al. Cross-sectional structure of the central mitotic spindle of Diatoma vulgare. Evidence for specific interactions between antiparallel microtubules. J. Cell Biol. 1979, 83:443-461.
63. McDowall A.W., et al. Electron microscopy of frozen hydrated sections of vitreous ice and vitrified biological samples. J. Microsc. 1983, 131:1-9.
64. McDowall A.W., et al. Plunge-freezing isolated macomolecular complexes, viruses, and small cells. Methods Enzymol. 2010, 1. Cryo-EM. Part 1 Sample preparation chapter.
65. McIntosh J.R., et al. Structure and physiology of the mammalian mitotic spindle. Soc. Gen. Physiol. Ser. 1975, 30:31-76.
66. Medalia O., et al. Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography. Science 2002, 298:1209-1213.
67. Medalia O., et al. Organization of actin networks in intact filopodia. Curr. Biol. 2007, 17:79-84.
68. Mercogliano C.P., DeRosier D.J. Gold nanocluster formation using metallothionein: Mass spectrometry and electron microscopy. J. Mol. Biol. 2006, 355:211-223.
69. Milne J.L., Subramaniam S. Cryo-electron tomography of bacteria: Progress, challenges and future prospects. Nat. Rev. Microbiol. 2009, 7:666-675.
70. Mollinari C., et al. PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone. J. Cell Biol. 2002, 157:1175-1186.
71. Moor H. Theory and practice of high-pressure freezing. Cryotechniques in Biological Electron Microscopy 1987, 175-191. Springer-Verlag, Berlin. R.A. Steinbrecht, K. Zierold (Eds.).
72. Muller-Taubenberger A., et al. Calreticulin and calnexin in the endoplasmic reticulum are important for phagocytosis. EMBO J. 2001, 20:6772-6782.
73. Mullins J.M., Biesele J.J. Terminal phase of cytokinesis in D-98s cells. J. Cell Biol. 1977, 73:672-684.
74. Mullins J.M., McIntosh J.R. Isolation and initial characterization of the mammalian midbody. J. Cell Biol. 1982, 94:654-661.
75. Myster S.H., et al. The Chlamydomonas Dhc1 gene encodes a dynein heavy chain subunit required for assembly of the I1 inner arm complex. Mol. Biol. Cell 1997, 8:607-620.
76. Nemethova M., et al. Building the actin cytoskeleton: Filopodia contribute to the construction of contractile bundles in the lamella. J. Cell Biol. 2008, 180:1233-1244.
77. Nicastro D., et al. 3D structure of eukaryotic flagella in a quiescent state revealed by cryo-electron tomography. Proc. Natl. Acad. Sci. USA 2005, 102:15889-15894.
78. Nicastro D., et al. The molecular architecture of axonemes revealed by cryoelectron tomography. Science 2006, 313:944-948.
79. Nickell S., et al. A visual approach to proteomics. Nat. Rev. Mol. Cell Biol. 2006, 7:225-230.
80. Nisman R., et al. Application of quantum dots as probes for correlative fluorescence, conventional, and energy-filtered transmission electron microscopy. J. Histochem. Cytochem. 2004, 52:13-18.
81. Otegui M.S., et al. Midbodies and phragmoplasts: Analogous structures involved in cytokinesis. Trends Cell Biol. 2005, 15:404-413.
82. Paweletz N. On the function of the "Flemming body" during division of animal cells. Naturwissenschaften 1967, 54:533-535.
83. Plitzko J.M., et al. Correlative cryo-light microscopy and cryo-electron tomography: From cellular territories to molecular landscapes. Curr. Opin. Biotechnol. 2009, 20:83-89.
84. Rigort A., et al. Micromachining tools and correlative approaches for cellular cryo-electron tomography. J. Struct. Biol. 2010, (In press).
85. Robinson J.M., et al. Correlative fluorescence and electron microscopy on ultrathin cryosections: Bridging the resolution gap. J. Histochem. Cytochem. 2001, 49:803-808.
86. Rout M.P., et al. The yeast nuclear pore complex: Composition, architecture, and transport mechanism. J. Cell Biol. 2000, 148:635-651.
87. Rual J.F., et al. Towards a proteome-scale map of the human protein-protein interaction network. Nature 2005, 437:1173-1178.
88. Rust M.J., et al. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods 2006, 3:793-795.
89. Saibil H.R. Conformational changes studied by cryo-electron microscopy. Nat. Struct. Biol. 2000, 7:711-714.
90. Sali A., et al. From words to literature in structural proteomics. Nature 2003, 422:216-225.
91. Sartori A., et al. Correlative microscopy: Bridging the gap between fluorescence light microscopy and cryo-electron tomography. J. Struct. Biol. 2007, 160:135-145.
92. Schermelleh L., et al. Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science 2008, 320:1332-1336.
93. Schwartz C.L., et al. Cryo-fluorescence microscopy facilitates correlations between light and cryo-electron microscopy and reduces the rate of photobleaching. J. Microsc. 2007, 227:98-109.
94. Sellitto C., Kuriyama R. Distribution of a matrix component of the midbody during the cell cycle in Chinese hamster ovary cells. J. Cell Biol. 1988, 106:431-439.
95. Seybert A., et al. Structural analysis of Mycoplasma pneumoniae by cryo-electron tomography. J. Struct. Biol. 2006, 156:342-354.
96. Shimomura O., et al. Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J. Cell. Comp. Physiol. 1962, 59:223-239.
97. Skop A.R., et al. Dissection of the mammalian midbody proteome reveals conserved cytokinesis mechanisms. Science 2004, 305:61-66.
98. Slot J.W., Geuze H.J. A new method of preparing gold probes for multiple-labeling cytochemistry. Eur. J. Cell Biol. 1985, 38:87-93.
99. Small J.V., et al. Visualization of actin filaments in keratocyte lamellipodia: Negative staining compared with freeze-drying. J. Struct. Biol. 1994, 113:135-141.
100. Steigemann P., Gerlich D.W. Cytokinetic abscission: Cellular dynamics at the midbody. Trends Cell Biol. 2009, 19:606-616.
101. Stewart M. Molecular mechanism of the nuclear protein import cycle. Nat. Rev. Mol. Cell Biol. 2007, 8:195-208.
102. Stoffler D., et al. Cryo-electron tomography provides novel insights into nuclear pore architecture: Implications for nucleocytoplasmic transport. J. Mol. Biol. 2003, 328:119-130.
103. Studer D., et al. Electron microscopy of high pressure frozen samples: Bridging the gap between cellular ultrastructure and atomic resolution. Histochem. Cell Biol. 2008, 130:877-889.
104. Suntharalingam M., Wente S.R. Peering through the pore: Nuclear pore complex structure, assembly, and function. Dev. Cell 2003, 4:775-789.
105. Svitkina T.M., et al. Analysis of the actin-myosin II system in fish epidermal keratocytes: Mechanism of cell body translocation. J. Cell Biol. 1997, 139:397-415.
106. Terry L.J., et al. Crossing the nuclear envelope: Hierarchical regulation of nucleocytoplasmic transport. Science 2007, 318:1412-1416.
107. Tippit D.H., et al. Organization of spindle microtubules in Ochromonas danica. J. Cell Biol. 1980, 87:531-545.
108. Urban E., et al. Electron tomography reveals unbranched networks of actin filaments in lamellipodia. Nat. Cell Biol. 2010, 12:429-435.
109. van Driel L.F., et al. Tools for correlative cryo-fluorescence microscopy and cryo-electron tomography applied to whole mitochondria in human endothelial cells. Eur. J. Cell Biol. 2009, 88:669-684.
110. Vicidomini G., et al. A novel approach for correlative light electron microscopy analysis. Microsc. Res. Tech. 2010, 73:215-224.
111. Weston A.E., et al. Towards native-state imaging in biological context in the electron microscope. J. Chem. Biol. 2010, 3:101-112.
112. Xue F.L., et al. Enhancement of intracellular delivery of CdTe quantum dots (QDs) to living cells by Tat conjugation. J. Fluoresc. 2007, 17:149-154.
113. Yang Q., et al. Three-dimensional architecture of the isolated yeast nuclear pore complex: Functional and evolutionary implications. Mol. Cell 1998, 1:223-234.
114. Yuste R. Fluorescence microscopy today. Nat. Methods 2005, 2:902-904.
115. Zhang P., et al. Direct visualization of Escherichia coli chemotaxis receptor arrays using cryo-electron microscopy. Proc. Natl. Acad. Sci. USA 2007, 104:3777-3781.