Single versus dual-axis cryo-electron tomography of microtubules assembled in vitro: Limits and perspectives

Journal of Structural Biology

Volumn 181, Issue 2, 2013, Pages 169-178

  Guesdon, Audrey ^a   Blestel, Sophie ^a,b   Kervrann, Charles ^b   Chrétien, Denis ^a,c  

^a UNIVERSITÉ DE RENNES 1   (France)

^b INRIA   (France)

^c UNIVERSITÉ DE RENNES 1   (France)

Author keywords

3D Fourier transforms; Cryo electron microscopy; Dual axis cryo electron tomography; Microtubules; Radiation damage; Single axis cryo electron tomography

Indexed keywords

TUBULIN;

ANIMAL TISSUE; ANISOTROPY; ARTICLE; DOUBLE AXIS CRYOELECTRON TOMOGRAPHY; ELECTRON BEAM; ELECTRON TOMOGRAPHY; FOURIER TRANSFORMATION; IMAGE ANALYSIS; IMAGE RECONSTRUCTION; IN VITRO STUDY; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; RADIATION INJURY; SINGLE AXIS CRYOELECTRON TOMOGRAPHY;

CRYOELECTRON MICROSCOPY; FOURIER ANALYSIS; GUANOSINE TRIPHOSPHATE; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; MICROTUBULES; TOMOGRAPHY, X-RAY COMPUTED;

EID: 84873198809     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2012.11.004     Document Type: Article

References (45)

1. Abramoff M.D., Magalhaes P.J., Ram S.J. Image processing with ImageJ. Biophoton. Int. 2004, 11:36-42.
2. Arnal I., Chrétien D., Malleter M. Vitrification of Dynamic Microtubules. Handbook of Cryo-Preparation Methods for Electron Microscopy 2008, CRC Press, pp. 237-258.
3. Arslan I., Tong J.R., Midgley P.A. Reducing the missing wedge: high-resolution dual axis tomography of inorganic materials. Ultramicroscopy 2006, 106:994-1000.
4. Ashford A.J., Hyman A.A. Chapter 22 - Preparation of tubulin from porcine brain. Cell Biology 2006, 155-160. Academic Press, Burlington. Third ed. E.C. Julio (Ed.).
5. Ben-Harush K., Maimon T., Patla I., Villa E., Medalia O. Visualizing cellular processes at the molecular level by cryo-electron tomography. J. Cell Sci. 2010, 123:7-12.
6. Benjamin J., Ganser-Pornillos B.K., Tivol W.F., Sundquist W.I., Jensen G.J. Three-dimensional structure of HIV-1 virus-like particles by electron cryotomography. J. Mol. Biol. 2005, 346:577-588.
7. Blestel, S., Kervrann, C., Chrétien, D., 2009. A Fourier-based method for detecting curved microtubule centers: application to straightening of cryo-electron microscope images. In: IEEE, New York.
8. Briegel A., Dias D.P., Li Z., Jensen R.B., Frangakis A.S., et al. Multiple large filament bundles observed in Caulobacter crescentus by electron cryotomography. Mol. Microbiol. 2006, 62:5-14.
9. Chrétien D., Wade R.H. New data on the microtubule surface lattice. Biol. Cell 1991, 71:161-174.
10. Chrétien D., Metoz F., Verde F., Karsenti E., Wade R.H. Lattice defects in microtubules: protofilament numbers vary within individual microtubules. J. Cell Biol. 1992, 117:1031-1040.
11. Cope J., Gilbert S., Rayment I., Mastronarde D., Hoenger A. Cryo-electron tomography of microtubule-kinesin motor complexes. J. Struct. Biol. 2010, 170:257-265.
12. Coquelle F.M., Blestel S., Heichette C., Arnal I., Kervrann C., et al. Cryo-electron tomography of microtubules assembled in vitro from purified components. Microtubule Dynamics: Methods and Protocols 2011, 193-208. Humana Press Inc., Totowa. A. Straube (Ed.).
13. Davies K.M., Anselmi C., Wittig I., Faraldo-Gomez J.D., Kuhlbrandt W. Structure of the yeast F1Fo-ATP synthase dimer and its role in shaping the mitochondrial cristae. Proc. Natl. Acad. Sci. USA 2012, 109:13602-13607.
14. Dierksen K., Typke D., Hegerl R., Walz J., Sackmann E., et al. Three-dimensional structure of lipid vesicles embedded in vitreous ice and investigated by automated electron tomography. Biophys. J. 1995, 68:1416-1422.
15. Dudkina N.V., Oostergetel G.T., Lewejohann D., Braun H.P., Boekema E.J. Row-like organization of ATP synthase in intact mitochondria determined by cryo-electron tomography. Biochim. Biophys. Acta 2010, 1797:272-277.
16. Fernandez-Busnadiego R., Schrod N., Kochovski Z., Asano S., Vanhecke D., et al. Insights into the molecular organization of the neuron by cryo-electron tomography. J. Electron. Microsc. (Tokyo) 2011, 60(Suppl. 1):S137-148.
17. Frank J. Approaches to large-scale structures. Curr. Opin. Struct. Biol. 1995, 5:194-201.
18. He Y., Jensen G.J., Bjorkman P.J. Cryo-electron tomography of homophilic adhesion mediated by the neural cell adhesion molecule L1. Structure 2009, 17:460-471.
19. Henderson G.P., Jensen G.J. Three-dimensional structure of Mycoplasma pneumoniae's attachment organelle and a model for its role in gliding motility. Mol. Microbiol. 2006, 60:376-385.
20. Henderson G.P., Gan L., Jensen G.J. 3-D ultrastructure of O. tauri: electron cryotomography of an entire eukaryotic cell. PLoS ONE 2007, 2:e749.
21. Hyman A.A., Chrétien D., Arnal I., Wade R.H. Structural changes accompanying GTP hydrolysis in microtubules: information from a slowly hydrolyzable analogue guanylyl-(alpha,beta)-methylene-diphosphonate. J. Cell Biol. 1995, 128:117-125.
22. Iancu C.V., Ding H.J., Morris D.M., Dias D.P., Gonzales A.D., et al. The structure of isolated Synechococcus strain WH8102 carboxysomes as revealed by electron cryotomography. J. Mol. Biol. 2007, 372:764-773.
23. Iancu C.V., Wright E.R., Benjamin J., Tivol W.F., Dias D.P., et al. A " flip-flop" rotation stage for routine dual-axis electron cryotomography. J. Struct. Biol. 2005, 151:288-297.
24. Komeili A., Li Z., Newman D.K., Jensen G.J. Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 2006, 311:242-245.
25. Kremer J.R., Mastronarde D.N., McIntosh J.R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 1996, 116:71-76.
26. Li Z., Jensen G.J. Electron cryotomography: a new view into microbial ultrastructure. Curr. Opin. Microbiol. 2009, 12:333-340.
27. Mader A., Elad N., Medalia O. Cryoelectron tomography of eukaryotic cells. Methods Enzymol. 2010, 483:245-265.
28. Mastronarde D.N. Dual-axis tomography: an approach with alignment methods that preserve resolution. J. Struct. Biol. 1997, 120:343-352.
29. Mastronarde D.N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 2005, 152:36-51.
30. McEwen B.F., Renken C., Marko M., Mannella C. Chapter 6: Principles and practice in electron tomography. Methods Cell Biol. 2008, 89:129-168.
31. McIntosh R., Nicastro D., Mastronarde D. New views of cells in 3D: an introduction to electron tomography. Trends Cell Biol. 2005, 15:43-51.
32. Milazzo A.C., Cheng A., Moeller A., Lyumkis D., Jacovetty E., et al. Initial evaluation of a direct detection device detector for single particle cryo-electron microscopy. J. Struct. Biol. 2011, 176:404-408.
33. Milne J.L., Subramaniam S. Cryo-electron tomography of bacteria: progress, challenges and future prospects. Nat. Rev. Microbiol. 2009, 7:666-675.
34. Mitchison T., Kirschner M. Dynamic instability of microtubule growth. Nature 1984, 312:237-242.
35. Murphy G.E., Jensen G.J. Electron cryotomography of the E. coli pyruvate and 2-oxoglutarate dehydrogenase complexes. Structure 2005, 13:1765-1773.
36. Nicastro D. Cryo-electron microscope tomography to study axonemal organization. Methods Cell Biol. 2009, 91:1-39.
37. Nicastro D., Frangakis A.S., Typke D., Baumeister W. Cryo-electron tomography of neurospora mitochondria. J. Struct. Biol. 2000, 129:48-56.
38. Nickell S., Hegerl R., Baumeister W., Rachel R. Pyrodictium cannulae enter the periplasmic space but do not enter the cytoplasm, as revealed by cryo-electron tomography. J. Struct. Biol. 2003, 141:34-42.
39. Penczek P., Marko M., Buttle K., Frank J. Double-tilt electron tomography. Ultramicroscopy 1995, 60:393-410.
40. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., et al. UCSF chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25:1605-1612.
41. Plitzko J.M., Rigort A., Leis A. Correlative cryo-light microscopy and cryo-electron tomography: from cellular territories to molecular landscapes. Curr. Opin. Biotechnol. 2009, 20:83-89.
42. Saxton W.O., Baumeister W., Hahn M. Three-dimensional reconstruction of imperfect two-dimensional crystals. Ultramicroscopy 1984, 13:57-70.
43. Shetty A., Chen S., Tocheva E.I., Jensen G.J., Hickey W.J. Nanopods: a new bacterial structure and mechanism for deployment of outer membrane vesicles. PLoS ONE 2011, 6:e20725.
44. Vanhecke D., Asano S., Kochovski Z., Fernandez-Busnadiego R., Schrod N., et al. Cryo-electron tomography: methodology, developments and biological applications. J. Microsc. 2011, 242:221-227.
45. Wade R.H., Chrétien D. Cryoelectron microscopy of microtubules. J. Struct. Biol. 1993, 110:1-27.