Focused ion beam micromachining of eukaryotic cells for cryoelectron tomography

Cryoelectron tomography provides unprecedented insights into the macromolecular and supramolecular organization of cells in a close-to-living state. However because of the limited thickness range (< 0.5–1 μm) that is accessible with today’s intermediate voltage electron microscopes only small prokaryotic cells or peripheral regions of eukaryotic cells can be examined directly. Key to overcoming this limitation is the ability to prepare sufficiently thin samples. Cryosectioning can be used to prepare thin enough sections but suffers from severe artefacts, such as substantial compression. Here we describe a procedure, based upon focused ion beam (FIB) milling for the preparation of thin (200–500 nm) lamellae from vitrified cells grown on electron microscopy (EM) grids. The self-supporting lamellae are apparently free of distortions or other artefacts and open up large windows into the cell’s interior allowing tomographic studies to be performed on any chosen part of the cell. We illustrate the quality of sample preservation with a structure of the nuclear pore complex obtained from a single tomogram.

[1]  Gregory A Gibson,et al.  Direct visualization of HIV-1 with correlative live-cell microscopy and cryo-electron tomography. , 2011, Structure.

[2]  Florian Beck,et al.  Computer controlled cryo-electron microscopy--TOM² a software package for high-throughput applications. , 2011, Journal of structural biology.

[3]  Felix J. B. Bäuerlein,et al.  Micromachining tools and correlative approaches for cellular cryo-electron tomography. , 2010, Journal of structural biology.

[4]  B. Humbel,et al.  The making of frozen-hydrated, vitreous lamellas from cells for cryo-electron microscopy. , 2010, Journal of structural biology.

[5]  Wolfgang Baumeister,et al.  The three-dimensional organization of polyribosomes in intact human cells. , 2010, Molecular cell.

[6]  Felix J. B. Bäuerlein,et al.  A 360º Rotatable Cryo-FIB Stage for Micromachining Frozen-Hydrated Specimens for Cryo-Electron Tomography , 2010 .

[7]  R. Aebersold,et al.  Visual proteomics of the human pathogen Leptospira interrogans , 2009, Nature Methods.

[8]  Tobias Bonhoeffer,et al.  Multiscale imaging of neurons grown in culture: from light microscopy to cryo-electron tomography. , 2007, Journal of structural biology.

[9]  Friedrich Förster,et al.  Snapshots of nuclear pore complexes in action captured by cryo-electron tomography , 2007, Nature.

[10]  R. Schalek,et al.  Focused-ion-beam thinning of frozen-hydrated biological specimens for cryo-electron microscopy , 2007, Nature Methods.

[11]  J. McIntosh,et al.  The Molecular Architecture of Axonemes Revealed by Cryoelectron Tomography , 2006, Science.

[12]  Wolfgang Baumeister,et al.  A visual approach to proteomics , 2006, Nature Reviews Molecular Cell Biology.

[13]  J. Frank,et al.  Towards high-resolution three-dimensional imaging of native mammalian tissue: electron tomography of frozen-hydrated rat liver sections. , 2006, Journal of structural biology.

[14]  V. Lučić,et al.  Structural studies by electron tomography: from cells to molecules. , 2005, Annual review of biochemistry.

[15]  J. Dubochet,et al.  Cutting artefacts and cutting process in vitreous sections for cryo-electron microscopy. , 2005, Journal of structural biology.

[16]  F. Förster,et al.  Retrovirus envelope protein complex structure in situ studied by cryo-electron tomography. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Friedrich Förster,et al.  TOM software toolbox: acquisition and analysis for electron tomography. , 2005, Journal of structural biology.

[18]  Wolfgang Baumeister,et al.  From proteomic inventory to architecture , 2005, FEBS letters.

[19]  Hans-Christian Hege,et al.  amira: A Highly Interactive System for Visual Data Analysis , 2005, The Visualization Handbook.

[20]  F. Förster,et al.  Nuclear Pore Complex Structure and Dynamics Revealed by Cryoelectron Tomography , 2004, Science.

[21]  Wolfgang Baumeister,et al.  Three-Dimensional Structure of Herpes Simplex Virus from Cryo-Electron Tomography , 2003, Science.

[22]  W. Baumeister,et al.  Macromolecular Architecture in Eukaryotic Cells Visualized by Cryoelectron Tomography , 2002, Science.

[23]  F. Förster,et al.  Identification of macromolecular complexes in cryoelectron tomograms of phantom cells , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[24]  R. Ellis,et al.  Macromolecular crowding: an important but neglected aspect of the intracellular environment. , 2001, Current opinion in structural biology.

[25]  A S Frangakis,et al.  Toward detecting and identifying macromolecules in a cellular context: template matching applied to electron tomograms. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[26]  W. Baumeister,et al.  Perspectives of molecular and cellular electron tomography. , 1997, Journal of structural biology.

[27]  D Typke,et al.  Energy filtered electron tomography of ice-embedded actin and vesicles. , 1997, Biophysical journal.

[28]  Hegerl,et al.  The EM Program Package: A Platform for Image Processing in Biological Electron Microscopy , 1996, Journal of structural biology.

[29]  A. Minton Confinement as a determinant of macromolecular structure and reactivity. II. Effects of weakly attractive interactions between confined macrosolutes and confining structures. , 1995, Biophysical journal.

[30]  C. Bulle-lieuwma,et al.  Novel scheme for the preparation of transmission electron microscopy specimens with a focused ion beam , 1993 .

[31]  A. Minton,et al.  Confinement as a determinant of macromolecular structure and reactivity. , 1992, Biophysical journal.

[32]  C. A. Walter,et al.  Electron microscopy of frozen hydrated sections of vitreous ice and vitrified biological samples , 1983, Journal of microscopy.

[33]  J. Dubochet,et al.  VITRIFICATION OF PURE WATER FOR ELECTRON MICROSCOPY , 1981 .

[34]  J. Ashworth,et al.  Growth of myxameobae of the cellular slime mould Dictyostelium discoideum in axenic culture. , 1970, The Biochemical journal.