A focused ion beam milling and lift-out approach for site-specific preparation of frozen-hydrated lamellas from multicellular organisms

Journal of Structural Biology

Volumn 192, Issue 2, 2015, Pages 262-269

  Mahamid, Julia ^a   Schampers, Ruud ^b   Persoon, Hans ^b   Hyman, Anthony A ^c   Baumeister, Wolfgang ^a   Plitzko, Jürgen M ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b Thermo Fisher Scientific   (United States)

^c MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

Correlative microscopy; Cryo FIB; Cryo FLM; Cryo planing; Cryo SEM; Cryo TEM; Sample preparation

Indexed keywords

ADULT; ARTICLE; CAENORHABDITIS ELEGANS; CELL VOLUME; CELLULAR DISTRIBUTION; CENTROSOME; CONTROLLED STUDY; CRYO FOCUSED ION BEAM MILLING; CRYOELECTRON MICROSCOPY; ELECTRON TOMOGRAPHY; FEASIBILITY STUDY; FLUORESCENCE MICROSCOPY; FREEZING; FROZEN SECTION; IMAGE ANALYSIS; LAMELLAR BODY; MULTICELLULAR ORGANISM; NONHUMAN; ORGANISM FORMS; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; PROCEDURES; THREE DIMENSIONAL IMAGING; VITRIFICATION;

ANIMALS; CAENORHABDITIS ELEGANS; CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; FROZEN SECTIONS; IMAGING, THREE-DIMENSIONAL; MICROSCOPY, FLUORESCENCE; VITRIFICATION;

EID: 84946482575     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2015.07.012     Document Type: Article

References (46)

1. Al-Amoudi A., Studer D., Dubochet J. Cutting artefacts and cutting process in vitreous sections for cryo-electron microscopy. J. Struct. Biol. 2005, 150:109-121.
2. Al-Amoudi A., Castano-Diez D., Devos D.P., Russell R.B., Johnson G.T., Frangakis A.S. The three-dimensional molecular structure of the desmosomal plaque. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:6480-6485.
3. Arnold, J., Mahamid, J., Lucic, V., de Marko, A., Mayer, T., Fernandez, J.J., Laugks, T., Hyman, A., Baumeister, W., Plitzko, J.M., 2015. Three-dimensional correlative microscopy for targeted cryo-focused ion beam sample preparation. In Preparation.
4. Asano S., Fukuda Y., Beck F., Aufderheide A., Forster F., Danev R., Baumeister W. A molecular census of 26S proteasomes in intact neurons. Science 2015, 347:439-442.
5. Baumeister W. Mapping molecular landscapes inside cells. Biol. Chem. 2004, 385:865-872.
6. Brandt F., Carlson L.A., Hartl F.U., Baumeister W., Grunewald K. The three-dimensional organization of polyribosomes in intact human cells. Mol. Cell 2010, 39:560-569.
7. Brangwynne C.P., Eckmann C.R., Courson D.S., Rybarska A., Hoege C., Gharakhani J., Julicher F., Hyman A.A. Germline P granules are Liquid droplets that localize by controlled dissolution/condensation. Science 2009, 324:1729-1732.
8. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
9. Cowan C.R., Hyman A.A. Centrosomes direct cell polarity independently of microtubule assembly in C. elegans embryos. Nature 2004, 431:92-96.
10. Dai W., Fu C., Raytcheva D., Flanagan J., Khant H.A., Liu X.G., Rochat R.H., Haase-Pettingell C., Piret J., Ludtke S.J., Nagayama K., Schmid M.F., King J.A., Chiu W. Visualizing virus assembly intermediates inside marine cyanobacteria. Nature 2013, 502:707-710.
11. Danev R., Kanamaru S., Marko M., Nagayama K. Zernike phase contrast cryo-electron tomography. J. Struct. Biol. 2010, 171:174-181.
12. Danev R., Buijsse B., Khoshouei M., Plitzko J.M., Baumeister W. Volta potential phase plate for in-focus phase contrast transmission electron microscopy. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:15635-15640.
13. Dubochet J., Mcdowall A.W. Vitrification of pure water for electron-microscopy. J. Microsc. 1981, 124:Rp3-Rp4.
14. Dubochet J., Adrian M., Chang J.J., Homo J.C., Lepault J., McDowall A.W., Schultz P. Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 1988, 21:129-228.
15. Engel B.D., Schaffer M., Cuellar L.K., Villa E., Plitzko J.M., Baumeister W. Native architecture of the Chlamydomonas chloroplast revealed by in situ cryo-electron tomography. Elife 2015, 4:e04889.
16. Fernandez-Busnadiego R., Zuber B., Maurer U.E., Cyrklaff M., Baumeister W., Lucic V. Quantitative analysis of the native presynaptic cytomatrix by cryoelectron tomography. J. Cell Biol. 2010, 188:145-156.
17. Fukuda Y., Laugks U., Lucic V., Baumeister W., Danev R. Electron cryotomography of vitrified cells with a Volta phase plate. J. Struct. Biol. 2015, 190:143-154.
18. Giannuzzi L.A., Drown J.L., Brown S.R., Irwin R.B., Stevie F. Applications of the FIB lift-out technique for TEM specimen preparation. Microsc. Res. Techniq. 1998, 41:285-290.
19. Gruska M., Medalia O., Baumeister W., Leis A. Electron tomography of vitreous sections from cultured mammalian cells. J. Struct. Biol. 2008, 161:384-392.
20. Harapin J., Bormel M., Sapra K.T., Brunner D., Kaech A., Medalia O. Structural analysis of multicellular organisms with cryo-electron tomography. Nat. Methods 2015, 12:634-636.
21. Hayles M.F., Matthijs de Winter D.A., Schneijdenberg C.T., Meeldijk J.D., Luecken U., Persoon H., de Water J., de Jong F., Humbel B.M., Verkleij A.J. The making of frozen-hydrated, vitreous lamellas from cells for cryo-electron microscopy. J. Struct. Biol. 2010, 172:180-190.
22. Hsieh C.E., Leith A., Mannella C.A., Frank J., Marko M. 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.
23. Hsieh C., Schmelzer T., Kishchenko G., Wagenknecht T., Marko M. Practical workflow for cryo focused-ion-beam milling of tissues and cells for cryo-TEM tomography. J. Struct. Biol. 2014, 185:32-41.
24. Mahamid J., Baumeister W. Cryo-electron tomography: the realization of a vision. Microsc. Microanal. 2012, 26:45-48.
25. Marko M., Hsieh C., Moberlychan W., Mannella C.A., Frank J. Focused ion beam milling of vitreous water: prospects for an alternative to cryo-ultramicrotomy of frozen-hydrated biological samples. J. Microsc. 2006, 222:42-47.
26. Marko M., Hsieh C., Schalek R., Frank J., Mannella C. Focused-ion-beam thinning of frozen-hydrated biological specimens for cryo-electron microscopy. Nat. Methods 2007, 4:215-217.
27. McDonald K., Schwarz H., Müller-Reichert T., Webb R., Buser C., Morphew M. "Tips and tricks" for high-pressure freezing of model systems. Methods Cell Biol. 2010, 96:671-693.
28. McDowall A.W., Chang J.J., Freeman R., Lepault J., Walter C.A., Dubochet J. Electron microscopy of frozen hydrated sections of vitreous ice and vitrified biological samples. J. Microsc. 1983, 131:1-9.
29. 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 2014, 147:156-163.
30. Medalia O., Weber I., Frangakis A.S., Nicastro D., Gerisch G., Baumeister W. Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography. Science 2002, 298:1209-1213.
31. Nicastro D., Schwartz C., Pierson J., Gaudette R., Porter M.E., McIntosh J.R. The molecular architecture of axonemes revealed by cryoelectron tomography. Science 2006, 313:944-948.
32. Oegema K., Hyman A.A. Cell division. WormBook 2006, 1-40.
33. Ortiz J.O., Brandt F., Matias V.R., Sennels L., Rappsilber J., Scheres S.H., Eibauer M., Hartl F.U., Baumeister W. Structure of hibernating ribosomes studied by cryoelectron tomography in vitro and in situ. J. Cell Biol. 2010, 190:613-621.
34. Pelletier L., O'Toole E., Schwager A., Hyman A.A., Muller-Reichert T. Centriole assembly in Caenorhabditis elegans. Nature 2006, 444:619-623.
35. Pfeffer S., Woellhaf M.W., Herrmann J.M., Forster F. Organization of the mitochondrial translation machinery studied in situ by cryoelectron tomography. Nat. Commun. 2015, 6:6019.
36. Plitzko J.M., Rigort A., Leis A. Correlative cryo-light microscopy and cryo-electron tomography: from cellular territories to molecular landscapes. Curr. Opin. Biotech. 2009, 20:83-89.
37. Rigort A., Bauerlein F.J.B., Leis A., Gruska M., Hoffmann C., Laugks T., Bohm U., Eibauer M., Gnaegi H., Baumeister W., Plitzko J.M. Micromachining tools and correlative approaches for cellular cryo-electron tomography. J. Struct. Biol. 2010, 172:169-179.
38. Rigort A., Baeuerlein F.J.B., Villa E., Eibauer M., Laugks T., Baumeister W., Plitzko J.M. Focused ion beam micromachining of eukaryotic cells for cryo-electron tomography. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:4449-4454.
39. Rubino S., Akhtar S., Melin P., Searle A., Spellward P., Leifer K. A site-specific focused-ion-beam lift-out method for cryo Transmission Electron Microscopy. J. Struct. Biol. 2012, 180:572-576.
40. Schaffer M., Engel B.D., Laugks T., Mahamid J., Plitzko J.M., Baumeister W. Cryo-focused ion beam sample preparation for imaging vitreous cells by cryo-electron tomography. Bio-protocol 2015.
41. Schur F.K., Hagen W.J., Rumlova M., Ruml T., Muller B., Krausslich H.G., Briggs J.A. Structure of the immature HIV-1 capsid in intact virus particles at 8.8 A resolution. Nature 2015, 517:505-508.
42. Schwartz C.L., Sarbash V.I., Ataullakhanov F.I., Mcintosh J.R., Nicastro D. Cryo-fluorescence microscopy facilitates correlations between light and cryo-electron microscopy and reduces the rate of photobleaching. J. Microsc. 2007, 227:98-109.
43. Strunk K.M., Wang K., Ke D., Gray J.L., Zhang P. Thinning of large mammalian cells for cryo-TEM characterization by cryo-FIB milling. J. Microsc. 2012, 247:220-227.
44. Villa E., Schaffer M., Plitzko J.M., Baumeister W. Opening windows into the cell: focused-ion-beam milling for cryo-electron tomography. Curr. Opin. Struct. Biol. 2013, 23:771-777.
45. Wagner, F.R., Schampers, R., Watanabe, R., Persoon, H., Schaffer, M., Fruhstorfer, P., Villa, E., 2015. Preparing lamellae from whole cells using focused-ion-beam milling for cryo-electron tomography. Submitted.
46. Zuber B., Nikonenko I., Klauser P., Muller D., Dubochet J. The mammalian central nervous synaptic cleft contains a high density of periodically organized complexes. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:19192-19197.