DOI: 10.1083/jcb.201304193. Cryo-electron tomography: The challenge of doing structural biology in situ

Cryo-electron tomography: The challenge of doing structural biology in situ

10.1083/jcb.201304193

Crossref journal-article

Rockefeller University Press

Journal of Cell Biology (291)

Abstract

Electron microscopy played a key role in establishing cell biology as a discipline, by producing fundamental insights into cellular organization and ultrastructure. Many seminal discoveries were made possible by the development of new sample preparation methods and imaging modalities. Recent technical advances include sample vitrification that faithfully preserves molecular structures, three-dimensional imaging by electron tomography, and improved image-processing methods. These new techniques have enabled the extraction of high fidelity structural information and are beginning to reveal the macromolecular organization of unperturbed cellular environments.

Bibliography

LuÄiÄ, V., Rigort, A., & Baumeister, W. (2013). Cryo-electron tomography: The challenge of doing structural biology in situ. Journal of Cell Biology, 202(3), 407â419.

Authors 3

Vladan Lučić (first)
Alexander Rigort (additional)
Wolfgang Baumeister (additional)

References 130 Referenced 345

10.1016/j.tice.2003.11.001 / Tissue Cell. / Biological ultrastructure research; the first 50 years by Afzelius (2004)
10.1016/j.jsb.2004.03.010 / J. Struct. Biol. / Cryo-electron microscopy of vitreous sections of native biological cells and tissues by Al-Amoudi (2004)
10.1016/j.jsb.2005.01.003 / J. Struct. Biol. / Cutting artefacts and cutting process in vitreous sections for cryo-electron microscopy by Al-Amoudi (2005)
10.1038/nature05994 / Nature. / The molecular architecture of cadherins in native epidermal desmosomes by Al-Amoudi (2007)
10.1016/S0092-8674(00)80922-8 / Cell. / The cell as a collection of protein machines: preparing the next generation of molecular biologists by Alberts (1998)
10.1038/nbt1018 / Nat. Biotechnol. / Ten thousand interactions for the molecular biologist by Aloy (2004)
10.1038/nature01404 / Nature. / Portrait of a molecule by Ball (2003)
10.1091/mbc.E11-08-0692 / Mol. Biol. Cell. / Three-dimensional structure of the radial spokes reveals heterogeneity and interactions with dyneins in Chlamydomonas flagella by Barber (2012)
10.1038/nature06170 / Nature. / Snapshots of nuclear pore complexes in action captured by cryo-electron tomography by Beck (2007)
10.1038/nmeth.1390 / Nat. Methods. / Visual proteomics of the human pathogen Leptospira interrogans by Beck (2009)
10.1002/jemt.20408 / Microsc. Res. Tech. / Contribution of high-resolution correlative imaging techniques in the study of the liver sieve in three-dimensions by Braet (2007)
10.1016/j.molcel.2010.08.003 / Mol. Cell. / The three-dimensional organization of polyribosomes in intact human cells by Brandt (2010)
10.1098/rstb.1971.0043 / Philos. Trans. R. Soc. Lond. B Biol. Sci. / Freeze-etching studies of membrane structure by Branton (1971)
10.1111/j.1365-2958.2008.06219.x / Mol. Microbiol. / Location and architecture of the Caulobacter crescentus chemoreceptor array by Briegel (2008)
10.1073/pnas.1115719109 / Proc. Natl. Acad. Sci. USA. / Bacterial chemoreceptor arrays are hexagonally packed trimers of receptor dimers networked by rings of kinase and coupling proteins by Briegel (2012)
10.1016/j.sbi.2013.02.003 / Curr. Opin. Struct. Biol. / Structural biology in situ-the potential of subtomogram averaging by Briggs (2013)
10.1038/288569a0 / Nature. / Complete vitrification in pure liquid water and dilute aqueous solutions by Bruggeller (1980)
10.1083/jcb.200903082 / J. Cell Biol. / Asymmetry of inner dynein arms and inter-doublet links in Chlamydomonas flagella by Bui (2009)
{'key': '2023072307282095600_bib19', 'article-title': 'La biologie cellulaire: étude comparée de la cellule dans les deux règnes', 'author': 'Carnoy', 'year': '1884'} / La biologie cellulaire: étude comparée de la cellule dans les deux règnes by Carnoy (1884)
10.1098/rspa.1970.0119 / Proc. R. Soc. Lond. A Math. Phys. Sci. / The reconstruction of a three-dimensional structure from projections and its application to electron microscopy by Crowther (1970)
10.1371/journal.pone.0000420 / PLoS ONE. / Whole cell cryo-electron tomography reveals distinct disassembly intermediates of vaccinia virus by Cyrklaff (2007)
10.1126/science.1213775 / Science. / Hemoglobins S and C interfere with actin remodeling in Plasmodium falciparum-infected erythrocytes by Cyrklaff (2011)
10.1016/j.pt.2012.08.003 / Trends Parasitol. / Host actin remodeling and protection from malaria by hemoglobinopathies by Cyrklaff (2012)
10.1016/S0076-6879(10)81014-6 / Methods Enzymol. / Phase plates for transmission electron microscopy by Danev (2010)
10.1371/journal.pbio.0020329 / PLoS Biol. / Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure by Denk (2004)
10.1016/0304-3991(92)90235-C / Ultramicroscopy. / Towards automatic electron tomography by Dierksen (1992)
10.1016/j.jsb.2008.11.009 / J. Struct. Biol. / Visualization of proteins in intact cells with a clonable tag for electron microscopy by Diestra (2009)
10.1017/S0033583500004297 / Q. Rev. Biophys. / Cryo-electron microscopy of vitrified specimens by Dubochet (1988)
10.1073/pnas.0810057105 / Proc. Natl. Acad. Sci. USA. / Analysis of cryo-electron microscopy images does not support the existence of 30-nm chromatin fibers in mitotic chromosomes in situ by Eltsov (2008)
10.1016/j.jsb.2012.12.004 / J. Struct. Biol. / Localization of fluorescently labeled structures in frozen-hydrated samples using integrated light electron microscopy by Faas (2013)
10.1016/j.micron.2012.05.003 / Micron. / Computational methods for electron tomography by Fernandez (2012)
10.1016/j.jsb.2003.09.010 / J. Struct. Biol. / An improved algorithm for anisotropic nonlinear diffusion for denoising cryo-tomograms by Fernández (2003)
10.1016/j.ultramic.2006.02.004 / Ultramicroscopy. / CTF determination and correction in electron cryotomography by Fernández (2006)
10.1083/jcb.200908082 / J. Cell Biol. / Quantitative analysis of the native presynaptic cytomatrix by cryoelectron tomography by Fernández-Busnadiego (2010)
10.1083/jcb.201206063 / J. Cell Biol. / Cryo-electron tomography reveals a critical role of RIM1α in synaptic vesicle tethering by Fernández-Busnadiego (2013)
10.1016/0014-4827(53)90112-8 / Exp. Cell Res. / A diamond knife for ultrathin sectioning by Fernandez-Moran (1953)
10.1073/pnas.0409178102 / Proc. Natl. Acad. Sci. USA. / Retrovirus envelope protein complex structure in situ studied by cryo-electron tomography by Förster (2005)
10.1016/j.jsb.2007.07.006 / J. Struct. Biol. / Classification of cryo-electron sub-tomograms using constrained correlation by Förster (2008)
10.1006/jsbi.2001.4406 / J. Struct. Biol. / Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion by Frangakis (2001)
10.1146/annurev.biophys.31.082901.134202 / Annu. Rev. Biophys. Biomol. Struct. / Single-particle imaging of macromolecules by cryo-electron microscopy by Frank (2002)
10.1093/jmicro/dfr033 / J. Electron Microsc. (Tokyo). / Electron crystallography for structural and functional studies of membrane proteins by Fujiyoshi (2011)
10.1017/S0033583511000102 / Q. Rev. Biophys. / Electron tomography of cells by Gan (2012)
10.1083/jcb.200606074 / J. Cell Biol. / Luminal particles within cellular microtubules by Garvalov (2006)
10.1038/415141a / Nature. / Functional organization of the yeast proteome by systematic analysis of protein complexes by Gavin (2002)
10.1016/S0962-8924(98)01493-7 / Trends Cell Biol. / A future for electron microscopy in cell biology? by Geuze (1999)
10.1016/j.jsb.2008.06.001 / J. Struct. Biol. / Retrospective: radiation damage and its associated “information limitations” by Glaeser (2008)
10.1093/oso/9780195088717.001.0001 / Electron Crystallography of Biological Macromolecules by Glaeser (2007)
10.1126/science.1222789 / Science. / Cartwheel architecture of Trichonympha basal body by Guichard (2012)
10.1038/35011540 / Nature. / From molecular to modular cell biology by Hartwell (1999)
10.1016/j.jsb.2010.07.004 / J. Struct. Biol. / The making of frozen-hydrated, vitreous lamellas from cells for cryo-electron microscopy by Hayles (2010)
10.1017/S0033583504003920 / Q. Rev. Biophys. / Realizing the potential of electron cryo-microscopy by Henderson (2004)
10.1016/S0248-4900(02)00013-8 / Biol. Cell. / Whatever happened to the ‘microtrabecular concept’? by Heuser (2002)
10.1083/jcb.81.2.275 / J. Cell Biol. / Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release by Heuser (1979)
10.1083/jcb.200908067 / J. Cell Biol. / The dynein regulatory complex is the nexin link and a major regulatory node in cilia and flagella by Heuser (2009)
10.1073/pnas.0709530105 / Proc. Natl. Acad. Sci. USA. / Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure by Hoffmann (2008)
10.1016/j.jsb.2005.10.004 / J. Struct. Biol. / Towards high-resolution three-dimensional imaging of native mammalian tissue: electron tomography of frozen-hydrated rat liver sections by Hsieh (2006)
10.1002/(SICI)1097-0029(19980701)42:1<43::AID-JEMT6>3.0.CO;2-S / Microsc. Res. Tech. / Pre-embedding immunolabeling for electron microscopy: an evaluation of permeabilization methods and markers by Humbel (1998)
10.1042/BC20110015 / Biol. Cell. / The future is cold: cryo-preparation methods for transmission electron microscopy of cells by Hurbain (2011)
10.1038/ncb2087 / Nat. Cell Biol. / The metabolic enzyme CTP synthase forms cytoskeletal filaments by Ingerson-Mahar (2010)
10.1073/pnas.0806401105 / Proc. Natl. Acad. Sci. USA. / Role of HAMP domains in chemotaxis signaling by bacterial chemoreceptors by Khursigara (2008)
10.1038/emboj.2011.77 / EMBO J. / Lateral density of receptor arrays in the membrane plane influences sensitivity of the E. coli chemotaxis response by Khursigara (2011)
10.1016/j.jsb.2007.08.011 / J. Struct. Biol. / Cryo electron tomography of vitrified fibroblasts: microtubule plus ends in situ by Koning (2008)
{'issue': 'Suppl', 'key': '2023072307282095600_bib63', 'first-page': 'SS6', 'article-title': 'Electron microscopy in cell biology: integrating structure and function', 'volume': '4', 'author': 'Koster', 'year': '2003', 'journal-title': 'Nat. Rev. Mol. Cell Biol.'} / Nat. Rev. Mol. Cell Biol. / Electron microscopy in cell biology: integrating structure and function by Koster (2003)
10.1016/0304-3991(92)90016-D / Ultramicroscopy. / Automated microscopy for electron tomography by Koster (1992)
10.1006/jsbi.1997.3933 / J. Struct. Biol. / Perspectives of molecular and cellular electron tomography by Koster (1997)
10.1111/j.1365-2958.2009.06613.x / Mol. Microbiol. / Comparative cryo-electron tomography of pathogenic Lyme disease spirochetes by Kudryashev (2009)
10.1016/j.jsb.2009.08.008 / J. Struct. Biol. / Distinct in situ structures of the Borrelia flagellar motor by Kudryashev (2010)
10.1111/j.1462-5822.2009.01399.x / Cell. Microbiol. / Positioning of large organelles by a membrane- associated cytoskeleton in Plasmodium sporozoites by Kudryashev (2010)
10.3181/00379727-74-17931 / Proc. Soc. Exp. Biol. Med. / Use of a glass edge in thin sectioning for electron microscopy by Latta (1950)
10.1111/j.1365-2818.2009.03184.x / J. Microsc. / High-aperture cryogenic light microscopy by Le Gros (2009)
10.1038/sj.emboj.7601895 / EMBO J. / The structure of FtsZ filaments in vivo suggests a force-generating role in cell division by Li (2007)
10.1038/emboj.2011.460 / EMBO J. / Three-dimensional structure of basal body triplet revealed by electron cryo-tomography by Li (2012)
10.1074/jbc.M111.241760 / J. Biol. Chem. / Building blocks of the nexin-dynein regulatory complex in Chlamydomonas flagella by Lin (2011)
10.1128/JB.00340-09 / J. Bacteriol. / Intact flagellar motor of Borrelia burgdorferi revealed by cryo-electron tomography: evidence for stator ring curvature and rotor/C-ring assembly flexion by Liu (2009)
10.1073/pnas.1200781109 / Proc. Natl. Acad. Sci. USA. / Molecular architecture of chemoreceptor arrays revealed by cryoelectron tomography of Escherichia coli minicells by Liu (2012)
10.1146/annurev.biochem.73.011303.074112 / Annu. Rev. Biochem. / Structural studies by electron tomography: from cells to molecules by Lucić (2005)
10.1016/j.str.2005.02.005 / Structure. / Morphological characterization of molecular complexes present in the synaptic cleft by Lucić (2005)
10.1016/j.jsb.2007.08.014 / J. Struct. Biol. / Multiscale imaging of neurons grown in culture: from light microscopy to cryo-electron tomography by Lucić (2007)
{'key': '2023072307282095600_bib79', 'first-page': '45', 'article-title': 'Cryo-electron tomography: the realization of a vision', 'volume': '26', 'author': 'Mahamid', 'year': '2012', 'journal-title': 'Microscopy and Analysis.'} / Microscopy and Analysis. / Cryo-electron tomography: the realization of a vision by Mahamid (2012)
10.1016/j.str.2012.03.025 / Structure. / The human nuclear pore complex as revealed by cryo-electron tomography by Maimon (2012)
10.1111/j.1365-2818.2006.01567.x / J. Microsc. / Focused ion beam milling of vitreous water: prospects for an alternative to cryo-ultramicrotomy of frozen-hydrated biological samples by Marko (2006)
10.1038/nmeth1014 / Nat. Methods. / Focused-ion-beam thinning of frozen-hydrated biological specimens for cryo-electron microscopy by Marko (2007)
10.1073/pnas.051631998 / Proc. Natl. Acad. Sci. USA. / Organellar relationships in the Golgi region of the pancreatic beta cell line, HIT-T15, visualized by high resolution electron tomography by Marsh (2001)
10.1016/j.jsb.2011.05.010 / J. Struct. Biol. / A differential structure approach to membrane segmentation in electron tomography by Martinez-Sanchez (2011)
10.1126/science.177.4045.268 / Science. / Electron diffraction of wet proteins: catalase by Matricardi (1972)
{'key': '2023072307282095600_bib86', 'article-title': 'Biomedical Electron Microscopy', 'author': 'Maunsbach', 'year': '1999'} / Biomedical Electron Microscopy by Maunsbach (1999)
10.1111/j.1365-2818.1983.tb04225.x / J. Microsc. / Electron microscopy of frozen hydrated sections of vitreous ice and vitrified biological samples by McDowall (1983)
10.1016/j.ultramic.2009.04.002 / Ultramicroscopy. / Detective quantum efficiency of electron area detectors in electron microscopy by McMullan (2009)
10.1126/science.1076184 / Science. / Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography by Medalia (2002)
10.1016/j.jsb.2007.06.010 / J. Struct. Biol. / Concatenated metallothionein as a clonable gold label for electron microscopy by Mercogliano (2007)
10.1016/j.jsb.2011.09.002 / J. Struct. Biol. / Initial evaluation of a direct detection device detector for single particle cryo-electron microscopy by Milazzo (2011)
10.1083/jcb.10.1.1 / J. Biophys. Biochem. Cytol. / A new freezing-ultramicrotome by Moor (1961)
10.1016/j.jsb.2009.12.015 / J. Struct. Biol. / 3D segmentation of cell boundaries from whole cell cryogenic electron tomography volumes by Moussavi (2010)
10.1038/nsmb.1832 / Nat. Struct. Mol. Biol. / Nucleotide-induced global conformational changes of flagellar dynein arms revealed by in situ analysis by Movassagh (2010)
10.1016/S0022-5320(57)80001-X / J. Ultrastruct. Res. / [Freeze-drying as a fixation technic for plant cells] by Müller (1957)
10.1126/science.110.2846.66 / Science. / New sectioning techniques for light and electron microscopy by Newman (1949)
10.1073/pnas.1106178108 / Proc. Natl. Acad. Sci. USA. / Cryo-electron tomography reveals conserved features of doublet microtubules in flagella by Nicastro (2011)
10.1038/nrm1861 / Nat. Rev. Mol. Cell Biol. / A visual approach to proteomics by Nickell (2006)
10.1093/jmicro/dfm008 / J. Electron Microsc. (Tokyo). / A genetically encoded metallothionein tag enabling efficient protein detection by electron microscopy by Nishino (2007)
10.1016/j.jsb.2006.04.014 / J. Struct. Biol. / Mapping 70S ribosomes in intact cells by cryoelectron tomography and pattern recognition by Ortiz (2006)
10.1083/jcb.201005007 / J. Cell Biol. / Structure of hibernating ribosomes studied by cryoelectron tomography in vitro and in situ by Ortiz (2010)
10.1016/j.str.2012.06.010 / Structure. / Structure and 3D arrangement of endoplasmic reticulum membrane-associated ribosomes by Pfeffer (2012)
10.1016/j.jsb.2010.09.017 / J. Struct. Biol. / Exploring vitreous cryo-section-induced compression at the macromolecular level using electron cryo-tomography; 80S yeast ribosomes appear unaffected by Pierson (2011)
10.1083/jcb.201106125 / J. Cell Biol. / Cryoelectron tomography of radial spokes in cilia and flagella by Pigino (2011)
10.1016/j.ceb.2012.10.019 / Curr. Opin. Cell Biol. / The bacterial cytoskeleton: more than twisted filaments by Pilhofer (2013)
10.1083/jcb.91.3.vii / J. Cell Biol. / Introduction: recollections on the beginnings of the journal of cell biology by Porter (1981)
10.1002/ar.1091170403 / Anat. Rec. / A study in microtomy for electron microscopy by Porter (1953)
{'key': '2023072307282095600_bib108', 'article-title': 'Transmission Electron Microscopy. Optical Sciences', 'author': 'Reimer', 'year': '2008'} / Transmission Electron Microscopy. Optical Sciences by Reimer (2008)
10.1016/j.jsb.2010.02.011 / J. Struct. Biol. / Micromachining tools and correlative approaches for cellular cryo-electron tomography by Rigort (2010)
10.1073/pnas.1201333109 / Proc. Natl. Acad. Sci. USA. / Focused ion beam micromachining of eukaryotic cells for cryoelectron tomography by Rigort (2012)
10.1016/j.jsb.2011.08.012 / J. Struct. Biol. / Automated segmentation of electron tomograms for a quantitative description of actin filament networks by Rigort (2012)
10.1016/B978-0-12-416026-2.00014-5 / Methods Cell Biol. / Integrative approaches for cellular cryo-electron tomography: correlative imaging and focused ion beam micromachining by Rigort (2012)
10.1038/nature06523 / Nature. / The molecular sociology of the cell by Robinson (2007)
{'key': '2023072307282095600_bib114', 'article-title': 'Die fruhe Entwicklung der Elektronenlinsen und der Elektronmikroskopie, In Acta historica leopoldina, Vol. 12', 'author': 'Ruska', 'year': '1979'} / Die fruhe Entwicklung der Elektronenlinsen und der Elektronmikroskopie, In Acta historica leopoldina, Vol. 12 by Ruska (1979)
10.1126/science.1164346 / Science. / Electron cryomicroscopy of E. coli reveals filament bundles involved in plasmid DNA segregation by Salje (2009)
10.1016/j.jsb.2007.07.011 / J. Struct. Biol. / Correlative microscopy: bridging the gap between light- and cryo-electron microscopy by Sartori (2007)
10.1016/0304-3991(84)90057-3 / Ultramicroscopy. / Three-dimensional reconstruction of imperfect two-dimensional crystals by Saxton (1984)
10.1111/j.1365-2818.2007.01794.x / J. Microsc. / Cryo-fluorescence microscopy facilitates correlations between light and cryo-electron microscopy and reduces the rate of photobleaching by Schwartz (2007)
10.1002/jcp.1030420104 / J. Cell. Physiol. / The ultrastructure of the innersegments of the retinal rods of the guinea pig eye as revealed by electron microscopy by Sjostrand (1953)
10.1083/jcb.3.1.45 / J. Biophys. Biochem. Cytol. / Electron microscopy of structural detail in frozen biological specimens by Steere (1957)
10.1007/s00418-008-0500-1 / Histochem. Cell Biol. / Electron microscopy of high pressure frozen samples: bridging the gap between cellular ultrastructure and atomic resolution by Studer (2008)
10.1126/science.186.4168.1036 / Science. / Electron diffraction of frozen, hydrated protein crystals by Taylor (1974)
10.1126/science.1091317 / Science. / Global mapping of the yeast genetic interaction network by Tong (2004)
10.1016/j.ejcb.2009.07.002 / Eur. J. Cell Biol. / Tools for correlative cryo-fluorescence microscopy and cryo-electron tomography applied to whole mitochondria in human endothelial cells by van Driel (2009)
10.1111/j.1365-2818.2010.03478.x / J. Microsc. / Cryo-electron tomography: methodology, developments and biological applications by Vanhecke (2011)
10.1016/0304-4157(78)90017-5 / Biochim. Biophys. Acta. / Freeze-fracture morphology of biological membranes by Verkleij (1978)
10.1083/jcb.201004052 / J. Cell Biol. / Mass spectrometry-based proteomics in cell biology by Walther (2010)
10.1016/j.str.2010.12.002 / Structure. / A ferritin-based label for cellular electron cryotomography by Wang (2011)
10.1073/pnas.0610106104 / Proc. Natl. Acad. Sci. USA. / Direct visualization of Escherichia coli chemotaxis receptor arrays using cryo-electron microscopy by Zhang (2007)
10.1128/JB.01919-07 / J. Bacteriol. / Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state by Zuber (2008)

Dates

Type	When
Created	12 years ago (Aug. 5, 2013, 11:34 a.m.)
Deposited	1 year, 3 months ago (May 15, 2024, 9:33 p.m.)
Indexed	2 weeks, 3 days ago (Aug. 3, 2025, 6:58 p.m.)
Issued	12 years ago (Aug. 5, 2013)
Published	12 years ago (Aug. 5, 2013)
Published Online	12 years ago (Aug. 5, 2013)
Published Print	12 years ago (Aug. 5, 2013)

Funders 0

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BibTeX

@article{Lu_i__2013, title={Cryo-electron tomography: The challenge of doing structural biology in situ}, volume={202}, ISSN={0021-9525}, url={http://dx.doi.org/10.1083/jcb.201304193}, DOI={10.1083/jcb.201304193}, number={3}, journal={Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Lučić, Vladan and Rigort, Alexander and Baumeister, Wolfgang}, year={2013}, month=aug, pages={407–419} }

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      "first-page": "291",
      "DOI": "10.1016/S0092-8674(00)80922-8",
      "article-title": "The cell as a collection of protein machines: preparing the next generation of molecular biologists",
      "volume": "92",
      "author": "Alberts",
      "year": "1998",
      "journal-title": "Cell."
    },
    {
      "key": "2023072307282095600_bib6",
      "doi-asserted-by": "publisher",
      "first-page": "1317",
      "DOI": "10.1038/nbt1018",
      "article-title": "Ten thousand interactions for the molecular biologist",
      "volume": "22",
      "author": "Aloy",
      "year": "2004",
      "journal-title": "Nat. Biotechnol."
    },
    {
      "key": "2023072307282095600_bib7",
      "doi-asserted-by": "publisher",
      "first-page": "421",
      "DOI": "10.1038/nature01404",
      "article-title": "Portrait of a molecule",
      "volume": "421",
      "author": "Ball",
      "year": "2003",
      "journal-title": "Nature."
    },
    {
      "key": "2023072307282095600_bib8",
      "doi-asserted-by": "publisher",
      "first-page": "111",
      "DOI": "10.1091/mbc.E11-08-0692",
      "article-title": "Three-dimensional structure of the radial spokes reveals heterogeneity and interactions with dyneins in Chlamydomonas flagella",
      "volume": "23",
      "author": "Barber",
      "year": "2012",
      "journal-title": "Mol. Biol. Cell."
    },
    {
      "key": "2023072307282095600_bib9",
      "doi-asserted-by": "publisher",
      "first-page": "611",
      "DOI": "10.1038/nature06170",
      "article-title": "Snapshots of nuclear pore complexes in action captured by cryo-electron tomography",
      "volume": "449",
      "author": "Beck",
      "year": "2007",
      "journal-title": "Nature."
    },
    {
      "key": "2023072307282095600_bib10",
      "doi-asserted-by": "publisher",
      "first-page": "817",
      "DOI": "10.1038/nmeth.1390",
      "article-title": "Visual proteomics of the human pathogen Leptospira interrogans",
      "volume": "6",
      "author": "Beck",
      "year": "2009",
      "journal-title": "Nat. Methods."
    },
    {
      "key": "2023072307282095600_bib11",
      "doi-asserted-by": "publisher",
      "first-page": "230",
      "DOI": "10.1002/jemt.20408",
      "article-title": "Contribution of high-resolution correlative imaging techniques in the study of the liver sieve in three-dimensions",
      "volume": "70",
      "author": "Braet",
      "year": "2007",
      "journal-title": "Microsc. Res. Tech."
    },
    {
      "key": "2023072307282095600_bib12",
      "doi-asserted-by": "publisher",
      "first-page": "560",
      "DOI": "10.1016/j.molcel.2010.08.003",
      "article-title": "The three-dimensional organization of polyribosomes in intact human cells",
      "volume": "39",
      "author": "Brandt",
      "year": "2010",
      "journal-title": "Mol. Cell."
    },
    {
      "key": "2023072307282095600_bib13",
      "doi-asserted-by": "publisher",
      "first-page": "133",
      "DOI": "10.1098/rstb.1971.0043",
      "article-title": "Freeze-etching studies of membrane structure",
      "volume": "261",
      "author": "Branton",
      "year": "1971",
      "journal-title": "Philos. Trans. R. Soc. Lond. B Biol. Sci."
    },
    {
      "key": "2023072307282095600_bib14",
      "doi-asserted-by": "publisher",
      "first-page": "30",
      "DOI": "10.1111/j.1365-2958.2008.06219.x",
      "article-title": "Location and architecture of the Caulobacter crescentus chemoreceptor array",
      "volume": "69",
      "author": "Briegel",
      "year": "2008",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "2023072307282095600_bib15",
      "doi-asserted-by": "publisher",
      "first-page": "3766",
      "DOI": "10.1073/pnas.1115719109",
      "article-title": "Bacterial chemoreceptor arrays are hexagonally packed trimers of receptor dimers networked by rings of kinase and coupling proteins",
      "volume": "109",
      "author": "Briegel",
      "year": "2012",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072307282095600_bib16",
      "doi-asserted-by": "publisher",
      "first-page": "261",
      "DOI": "10.1016/j.sbi.2013.02.003",
      "article-title": "Structural biology in situ-the potential of subtomogram averaging",
      "volume": "23",
      "author": "Briggs",
      "year": "2013",
      "journal-title": "Curr. Opin. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib17",
      "doi-asserted-by": "publisher",
      "first-page": "569",
      "DOI": "10.1038/288569a0",
      "article-title": "Complete vitrification in pure liquid water and dilute aqueous solutions",
      "volume": "288",
      "author": "Bruggeller",
      "year": "1980",
      "journal-title": "Nature."
    },
    {
      "key": "2023072307282095600_bib18",
      "doi-asserted-by": "publisher",
      "first-page": "437",
      "DOI": "10.1083/jcb.200903082",
      "article-title": "Asymmetry of inner dynein arms and inter-doublet links in Chlamydomonas flagella",
      "volume": "186",
      "author": "Bui",
      "year": "2009",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072307282095600_bib19",
      "article-title": "La biologie cellulaire: \u00e9tude compar\u00e9e de la cellule dans les deux r\u00e8gnes",
      "author": "Carnoy",
      "year": "1884"
    },
    {
      "key": "2023072307282095600_bib20",
      "doi-asserted-by": "publisher",
      "first-page": "319",
      "DOI": "10.1098/rspa.1970.0119",
      "article-title": "The reconstruction of a three-dimensional structure from projections and its application to electron microscopy",
      "volume": "317",
      "author": "Crowther",
      "year": "1970",
      "journal-title": "Proc. R. Soc. Lond. A Math. Phys. Sci."
    },
    {
      "key": "2023072307282095600_bib21",
      "doi-asserted-by": "publisher",
      "first-page": "e420",
      "DOI": "10.1371/journal.pone.0000420",
      "article-title": "Whole cell cryo-electron tomography reveals distinct disassembly intermediates of vaccinia virus",
      "volume": "2",
      "author": "Cyrklaff",
      "year": "2007",
      "journal-title": "PLoS ONE."
    },
    {
      "key": "2023072307282095600_bib22",
      "doi-asserted-by": "publisher",
      "first-page": "1283",
      "DOI": "10.1126/science.1213775",
      "article-title": "Hemoglobins S and C interfere with actin remodeling in Plasmodium falciparum-infected erythrocytes",
      "volume": "334",
      "author": "Cyrklaff",
      "year": "2011",
      "journal-title": "Science."
    },
    {
      "key": "2023072307282095600_bib23",
      "doi-asserted-by": "publisher",
      "first-page": "479",
      "DOI": "10.1016/j.pt.2012.08.003",
      "article-title": "Host actin remodeling and protection from malaria by hemoglobinopathies",
      "volume": "28",
      "author": "Cyrklaff",
      "year": "2012",
      "journal-title": "Trends Parasitol."
    },
    {
      "key": "2023072307282095600_bib24",
      "doi-asserted-by": "publisher",
      "first-page": "343",
      "DOI": "10.1016/S0076-6879(10)81014-6",
      "article-title": "Phase plates for transmission electron microscopy",
      "volume": "481",
      "author": "Danev",
      "year": "2010",
      "journal-title": "Methods Enzymol."
    },
    {
      "key": "2023072307282095600_bib25",
      "doi-asserted-by": "publisher",
      "first-page": "e329",
      "DOI": "10.1371/journal.pbio.0020329",
      "article-title": "Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure",
      "volume": "2",
      "author": "Denk",
      "year": "2004",
      "journal-title": "PLoS Biol."
    },
    {
      "key": "2023072307282095600_bib26",
      "doi-asserted-by": "publisher",
      "first-page": "71",
      "DOI": "10.1016/0304-3991(92)90235-C",
      "article-title": "Towards automatic electron tomography",
      "volume": "40",
      "author": "Dierksen",
      "year": "1992",
      "journal-title": "Ultramicroscopy."
    },
    {
      "key": "2023072307282095600_bib27",
      "doi-asserted-by": "publisher",
      "first-page": "157",
      "DOI": "10.1016/j.jsb.2008.11.009",
      "article-title": "Visualization of proteins in intact cells with a clonable tag for electron microscopy",
      "volume": "165",
      "author": "Diestra",
      "year": "2009",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib28",
      "doi-asserted-by": "publisher",
      "first-page": "129",
      "DOI": "10.1017/S0033583500004297",
      "article-title": "Cryo-electron microscopy of vitrified specimens",
      "volume": "21",
      "author": "Dubochet",
      "year": "1988",
      "journal-title": "Q. Rev. Biophys."
    },
    {
      "key": "2023072307282095600_bib29",
      "doi-asserted-by": "publisher",
      "first-page": "19732",
      "DOI": "10.1073/pnas.0810057105",
      "article-title": "Analysis of cryo-electron microscopy images does not support the existence of 30-nm chromatin fibers in mitotic chromosomes in situ",
      "volume": "105",
      "author": "Eltsov",
      "year": "2008",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072307282095600_bib30",
      "doi-asserted-by": "publisher",
      "first-page": "283",
      "DOI": "10.1016/j.jsb.2012.12.004",
      "article-title": "Localization of fluorescently labeled structures in frozen-hydrated samples using integrated light electron microscopy",
      "volume": "181",
      "author": "Faas",
      "year": "2013",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib31",
      "doi-asserted-by": "publisher",
      "first-page": "1010",
      "DOI": "10.1016/j.micron.2012.05.003",
      "article-title": "Computational methods for electron tomography",
      "volume": "43",
      "author": "Fernandez",
      "year": "2012",
      "journal-title": "Micron."
    },
    {
      "key": "2023072307282095600_bib32",
      "doi-asserted-by": "publisher",
      "first-page": "152",
      "DOI": "10.1016/j.jsb.2003.09.010",
      "article-title": "An improved algorithm for anisotropic nonlinear diffusion for denoising cryo-tomograms",
      "volume": "144",
      "author": "Fern\u00e1ndez",
      "year": "2003",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib33",
      "doi-asserted-by": "publisher",
      "first-page": "587",
      "DOI": "10.1016/j.ultramic.2006.02.004",
      "article-title": "CTF determination and correction in electron cryotomography",
      "volume": "106",
      "author": "Fern\u00e1ndez",
      "year": "2006",
      "journal-title": "Ultramicroscopy."
    },
    {
      "key": "2023072307282095600_bib34",
      "doi-asserted-by": "publisher",
      "first-page": "145",
      "DOI": "10.1083/jcb.200908082",
      "article-title": "Quantitative analysis of the native presynaptic cytomatrix by cryoelectron tomography",
      "volume": "188",
      "author": "Fern\u00e1ndez-Busnadiego",
      "year": "2010",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072307282095600_bib35",
      "doi-asserted-by": "publisher",
      "first-page": "725",
      "DOI": "10.1083/jcb.201206063",
      "article-title": "Cryo-electron tomography reveals a critical role of RIM1\u03b1 in synaptic vesicle tethering",
      "volume": "201",
      "author": "Fern\u00e1ndez-Busnadiego",
      "year": "2013",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072307282095600_bib36",
      "doi-asserted-by": "publisher",
      "first-page": "255",
      "DOI": "10.1016/0014-4827(53)90112-8",
      "article-title": "A diamond knife for ultrathin sectioning",
      "volume": "5",
      "author": "Fernandez-Moran",
      "year": "1953",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "2023072307282095600_bib37",
      "doi-asserted-by": "publisher",
      "first-page": "4729",
      "DOI": "10.1073/pnas.0409178102",
      "article-title": "Retrovirus envelope protein complex structure in situ studied by cryo-electron tomography",
      "volume": "102",
      "author": "F\u00f6rster",
      "year": "2005",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072307282095600_bib38",
      "doi-asserted-by": "publisher",
      "first-page": "276",
      "DOI": "10.1016/j.jsb.2007.07.006",
      "article-title": "Classification of cryo-electron sub-tomograms using constrained correlation",
      "volume": "161",
      "author": "F\u00f6rster",
      "year": "2008",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib39",
      "doi-asserted-by": "publisher",
      "first-page": "239",
      "DOI": "10.1006/jsbi.2001.4406",
      "article-title": "Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion",
      "volume": "135",
      "author": "Frangakis",
      "year": "2001",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib40",
      "doi-asserted-by": "publisher",
      "first-page": "303",
      "DOI": "10.1146/annurev.biophys.31.082901.134202",
      "article-title": "Single-particle imaging of macromolecules by cryo-electron microscopy",
      "volume": "31",
      "author": "Frank",
      "year": "2002",
      "journal-title": "Annu. Rev. Biophys. Biomol. Struct."
    },
    {
      "issue": "Suppl 1",
      "key": "2023072307282095600_bib41",
      "doi-asserted-by": "publisher",
      "first-page": "S149",
      "DOI": "10.1093/jmicro/dfr033",
      "article-title": "Electron crystallography for structural and functional studies of membrane proteins",
      "volume": "60",
      "author": "Fujiyoshi",
      "year": "2011",
      "journal-title": "J. Electron Microsc. (Tokyo)."
    },
    {
      "key": "2023072307282095600_bib42",
      "doi-asserted-by": "publisher",
      "first-page": "27",
      "DOI": "10.1017/S0033583511000102",
      "article-title": "Electron tomography of cells",
      "volume": "45",
      "author": "Gan",
      "year": "2012",
      "journal-title": "Q. Rev. Biophys."
    },
    {
      "key": "2023072307282095600_bib43",
      "doi-asserted-by": "publisher",
      "first-page": "759",
      "DOI": "10.1083/jcb.200606074",
      "article-title": "Luminal particles within cellular microtubules",
      "volume": "174",
      "author": "Garvalov",
      "year": "2006",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072307282095600_bib44",
      "doi-asserted-by": "publisher",
      "first-page": "141",
      "DOI": "10.1038/415141a",
      "article-title": "Functional organization of the yeast proteome by systematic analysis of protein complexes",
      "volume": "415",
      "author": "Gavin",
      "year": "2002",
      "journal-title": "Nature."
    },
    {
      "key": "2023072307282095600_bib45",
      "doi-asserted-by": "publisher",
      "first-page": "92",
      "DOI": "10.1016/S0962-8924(98)01493-7",
      "article-title": "A future for electron microscopy in cell biology?",
      "volume": "9",
      "author": "Geuze",
      "year": "1999",
      "journal-title": "Trends Cell Biol."
    },
    {
      "key": "2023072307282095600_bib46",
      "doi-asserted-by": "publisher",
      "first-page": "271",
      "DOI": "10.1016/j.jsb.2008.06.001",
      "article-title": "Retrospective: radiation damage and its associated \u201cinformation limitations\u201d",
      "volume": "163",
      "author": "Glaeser",
      "year": "2008",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib47",
      "doi-asserted-by": "crossref",
      "DOI": "10.1093/oso/9780195088717.001.0001",
      "article-title": "Electron Crystallography of Biological Macromolecules",
      "author": "Glaeser",
      "year": "2007"
    },
    {
      "key": "2023072307282095600_bib48",
      "doi-asserted-by": "publisher",
      "first-page": "553",
      "DOI": "10.1126/science.1222789",
      "article-title": "Cartwheel architecture of Trichonympha basal body",
      "volume": "337",
      "author": "Guichard",
      "year": "2012",
      "journal-title": "Science."
    },
    {
      "key": "2023072307282095600_bib49",
      "doi-asserted-by": "publisher",
      "first-page": "C47",
      "DOI": "10.1038/35011540",
      "article-title": "From molecular to modular cell biology",
      "volume": "402",
      "author": "Hartwell",
      "year": "1999",
      "journal-title": "Nature."
    },
    {
      "key": "2023072307282095600_bib50",
      "doi-asserted-by": "publisher",
      "first-page": "180",
      "DOI": "10.1016/j.jsb.2010.07.004",
      "article-title": "The making of frozen-hydrated, vitreous lamellas from cells for cryo-electron microscopy",
      "volume": "172",
      "author": "Hayles",
      "year": "2010",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib51",
      "doi-asserted-by": "publisher",
      "first-page": "3",
      "DOI": "10.1017/S0033583504003920",
      "article-title": "Realizing the potential of electron cryo-microscopy",
      "volume": "37",
      "author": "Henderson",
      "year": "2004",
      "journal-title": "Q. Rev. Biophys."
    },
    {
      "key": "2023072307282095600_bib52",
      "doi-asserted-by": "publisher",
      "first-page": "561",
      "DOI": "10.1016/S0248-4900(02)00013-8",
      "article-title": "Whatever happened to the \u2018microtrabecular concept\u2019?",
      "volume": "94",
      "author": "Heuser",
      "year": "2002",
      "journal-title": "Biol. Cell."
    },
    {
      "key": "2023072307282095600_bib53",
      "doi-asserted-by": "publisher",
      "first-page": "275",
      "DOI": "10.1083/jcb.81.2.275",
      "article-title": "Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release",
      "volume": "81",
      "author": "Heuser",
      "year": "1979",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072307282095600_bib54",
      "doi-asserted-by": "publisher",
      "first-page": "921",
      "DOI": "10.1083/jcb.200908067",
      "article-title": "The dynein regulatory complex is the nexin link and a major regulatory node in cilia and flagella",
      "volume": "187",
      "author": "Heuser",
      "year": "2009",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072307282095600_bib55",
      "doi-asserted-by": "publisher",
      "first-page": "3963",
      "DOI": "10.1073/pnas.0709530105",
      "article-title": "Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure",
      "volume": "105",
      "author": "Hoffmann",
      "year": "2008",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072307282095600_bib56",
      "doi-asserted-by": "publisher",
      "first-page": "1",
      "DOI": "10.1016/j.jsb.2005.10.004",
      "article-title": "Towards high-resolution three-dimensional imaging of native mammalian tissue: electron tomography of frozen-hydrated rat liver sections",
      "volume": "153",
      "author": "Hsieh",
      "year": "2006",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib57",
      "doi-asserted-by": "publisher",
      "first-page": "43",
      "DOI": "10.1002/(SICI)1097-0029(19980701)42:1&lt;43::AID-JEMT6&gt;3.0.CO;2-S",
      "article-title": "Pre-embedding immunolabeling for electron microscopy: an evaluation of permeabilization methods and markers",
      "volume": "42",
      "author": "Humbel",
      "year": "1998",
      "journal-title": "Microsc. Res. Tech."
    },
    {
      "key": "2023072307282095600_bib58",
      "doi-asserted-by": "publisher",
      "first-page": "405",
      "DOI": "10.1042/BC20110015",
      "article-title": "The future is cold: cryo-preparation methods for transmission electron microscopy of cells",
      "volume": "103",
      "author": "Hurbain",
      "year": "2011",
      "journal-title": "Biol. Cell."
    },
    {
      "key": "2023072307282095600_bib59",
      "doi-asserted-by": "publisher",
      "first-page": "739",
      "DOI": "10.1038/ncb2087",
      "article-title": "The metabolic enzyme CTP synthase forms cytoskeletal filaments",
      "volume": "12",
      "author": "Ingerson-Mahar",
      "year": "2010",
      "journal-title": "Nat. Cell Biol."
    },
    {
      "key": "2023072307282095600_bib60",
      "doi-asserted-by": "publisher",
      "first-page": "16555",
      "DOI": "10.1073/pnas.0806401105",
      "article-title": "Role of HAMP domains in chemotaxis signaling by bacterial chemoreceptors",
      "volume": "105",
      "author": "Khursigara",
      "year": "2008",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072307282095600_bib61",
      "doi-asserted-by": "publisher",
      "first-page": "1719",
      "DOI": "10.1038/emboj.2011.77",
      "article-title": "Lateral density of receptor arrays in the membrane plane influences sensitivity of the E. coli chemotaxis response",
      "volume": "30",
      "author": "Khursigara",
      "year": "2011",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023072307282095600_bib62",
      "doi-asserted-by": "publisher",
      "first-page": "459",
      "DOI": "10.1016/j.jsb.2007.08.011",
      "article-title": "Cryo electron tomography of vitrified fibroblasts: microtubule plus ends in situ",
      "volume": "161",
      "author": "Koning",
      "year": "2008",
      "journal-title": "J. Struct. Biol."
    },
    {
      "issue": "Suppl",
      "key": "2023072307282095600_bib63",
      "first-page": "SS6",
      "article-title": "Electron microscopy in cell biology: integrating structure and function",
      "volume": "4",
      "author": "Koster",
      "year": "2003",
      "journal-title": "Nat. Rev. Mol. Cell Biol."
    },
    {
      "key": "2023072307282095600_bib64",
      "doi-asserted-by": "publisher",
      "first-page": "207",
      "DOI": "10.1016/0304-3991(92)90016-D",
      "article-title": "Automated microscopy for electron tomography",
      "volume": "46",
      "author": "Koster",
      "year": "1992",
      "journal-title": "Ultramicroscopy."
    },
    {
      "key": "2023072307282095600_bib65",
      "doi-asserted-by": "publisher",
      "first-page": "276",
      "DOI": "10.1006/jsbi.1997.3933",
      "article-title": "Perspectives of molecular and cellular electron tomography",
      "volume": "120",
      "author": "Koster",
      "year": "1997",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib66",
      "doi-asserted-by": "publisher",
      "first-page": "1415",
      "DOI": "10.1111/j.1365-2958.2009.06613.x",
      "article-title": "Comparative cryo-electron tomography of pathogenic Lyme disease spirochetes",
      "volume": "71",
      "author": "Kudryashev",
      "year": "2009",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "2023072307282095600_bib67",
      "doi-asserted-by": "publisher",
      "first-page": "54",
      "DOI": "10.1016/j.jsb.2009.08.008",
      "article-title": "Distinct in situ structures of the Borrelia flagellar motor",
      "volume": "169",
      "author": "Kudryashev",
      "year": "2010",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib68",
      "doi-asserted-by": "publisher",
      "first-page": "362",
      "DOI": "10.1111/j.1462-5822.2009.01399.x",
      "article-title": "Positioning of large organelles by a membrane- associated cytoskeleton in Plasmodium sporozoites",
      "volume": "12",
      "author": "Kudryashev",
      "year": "2010",
      "journal-title": "Cell. Microbiol."
    },
    {
      "key": "2023072307282095600_bib69",
      "doi-asserted-by": "publisher",
      "first-page": "436",
      "DOI": "10.3181/00379727-74-17931",
      "article-title": "Use of a glass edge in thin sectioning for electron microscopy",
      "volume": "74",
      "author": "Latta",
      "year": "1950",
      "journal-title": "Proc. Soc. Exp. Biol. Med."
    },
    {
      "key": "2023072307282095600_bib70",
      "doi-asserted-by": "publisher",
      "first-page": "1",
      "DOI": "10.1111/j.1365-2818.2009.03184.x",
      "article-title": "High-aperture cryogenic light microscopy",
      "volume": "235",
      "author": "Le Gros",
      "year": "2009",
      "journal-title": "J. Microsc."
    },
    {
      "key": "2023072307282095600_bib71",
      "doi-asserted-by": "publisher",
      "first-page": "4694",
      "DOI": "10.1038/sj.emboj.7601895",
      "article-title": "The structure of FtsZ filaments in vivo suggests a force-generating role in cell division",
      "volume": "26",
      "author": "Li",
      "year": "2007",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023072307282095600_bib72",
      "doi-asserted-by": "publisher",
      "first-page": "552",
      "DOI": "10.1038/emboj.2011.460",
      "article-title": "Three-dimensional structure of basal body triplet revealed by electron cryo-tomography",
      "volume": "31",
      "author": "Li",
      "year": "2012",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023072307282095600_bib73",
      "doi-asserted-by": "publisher",
      "first-page": "29175",
      "DOI": "10.1074/jbc.M111.241760",
      "article-title": "Building blocks of the nexin-dynein regulatory complex in Chlamydomonas flagella",
      "volume": "286",
      "author": "Lin",
      "year": "2011",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072307282095600_bib74",
      "doi-asserted-by": "publisher",
      "first-page": "5026",
      "DOI": "10.1128/JB.00340-09",
      "article-title": "Intact flagellar motor of Borrelia burgdorferi revealed by cryo-electron tomography: evidence for stator ring curvature and rotor/C-ring assembly flexion",
      "volume": "191",
      "author": "Liu",
      "year": "2009",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "2023072307282095600_bib75",
      "doi-asserted-by": "publisher",
      "first-page": "E1481",
      "DOI": "10.1073/pnas.1200781109",
      "article-title": "Molecular architecture of chemoreceptor arrays revealed by cryoelectron tomography of Escherichia coli minicells",
      "volume": "109",
      "author": "Liu",
      "year": "2012",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072307282095600_bib76",
      "doi-asserted-by": "publisher",
      "first-page": "833",
      "DOI": "10.1146/annurev.biochem.73.011303.074112",
      "article-title": "Structural studies by electron tomography: from cells to molecules",
      "volume": "74",
      "author": "Luci\u0107",
      "year": "2005",
      "journal-title": "Annu. Rev. Biochem."
    },
    {
      "key": "2023072307282095600_bib77",
      "doi-asserted-by": "publisher",
      "first-page": "423",
      "DOI": "10.1016/j.str.2005.02.005",
      "article-title": "Morphological characterization of molecular complexes present in the synaptic cleft",
      "volume": "13",
      "author": "Luci\u0107",
      "year": "2005",
      "journal-title": "Structure."
    },
    {
      "key": "2023072307282095600_bib78",
      "doi-asserted-by": "publisher",
      "first-page": "146",
      "DOI": "10.1016/j.jsb.2007.08.014",
      "article-title": "Multiscale imaging of neurons grown in culture: from light microscopy to cryo-electron tomography",
      "volume": "160",
      "author": "Luci\u0107",
      "year": "2007",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib79",
      "first-page": "45",
      "article-title": "Cryo-electron tomography: the realization of a vision",
      "volume": "26",
      "author": "Mahamid",
      "year": "2012",
      "journal-title": "Microscopy and Analysis."
    },
    {
      "key": "2023072307282095600_bib80",
      "doi-asserted-by": "publisher",
      "first-page": "998",
      "DOI": "10.1016/j.str.2012.03.025",
      "article-title": "The human nuclear pore complex as revealed by cryo-electron tomography",
      "volume": "20",
      "author": "Maimon",
      "year": "2012",
      "journal-title": "Structure."
    },
    {
      "key": "2023072307282095600_bib81",
      "doi-asserted-by": "publisher",
      "first-page": "42",
      "DOI": "10.1111/j.1365-2818.2006.01567.x",
      "article-title": "Focused ion beam milling of vitreous water: prospects for an alternative to cryo-ultramicrotomy of frozen-hydrated biological samples",
      "volume": "222",
      "author": "Marko",
      "year": "2006",
      "journal-title": "J. Microsc."
    },
    {
      "key": "2023072307282095600_bib82",
      "doi-asserted-by": "publisher",
      "first-page": "215",
      "DOI": "10.1038/nmeth1014",
      "article-title": "Focused-ion-beam thinning of frozen-hydrated biological specimens for cryo-electron microscopy",
      "volume": "4",
      "author": "Marko",
      "year": "2007",
      "journal-title": "Nat. Methods."
    },
    {
      "key": "2023072307282095600_bib83",
      "doi-asserted-by": "publisher",
      "first-page": "2399",
      "DOI": "10.1073/pnas.051631998",
      "article-title": "Organellar relationships in the Golgi region of the pancreatic beta cell line, HIT-T15, visualized by high resolution electron tomography",
      "volume": "98",
      "author": "Marsh",
      "year": "2001",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072307282095600_bib84",
      "doi-asserted-by": "publisher",
      "first-page": "372",
      "DOI": "10.1016/j.jsb.2011.05.010",
      "article-title": "A differential structure approach to membrane segmentation in electron tomography",
      "volume": "175",
      "author": "Martinez-Sanchez",
      "year": "2011",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib85",
      "doi-asserted-by": "publisher",
      "first-page": "268",
      "DOI": "10.1126/science.177.4045.268",
      "article-title": "Electron diffraction of wet proteins: catalase",
      "volume": "177",
      "author": "Matricardi",
      "year": "1972",
      "journal-title": "Science."
    },
    {
      "key": "2023072307282095600_bib86",
      "article-title": "Biomedical Electron Microscopy",
      "author": "Maunsbach",
      "year": "1999"
    },
    {
      "key": "2023072307282095600_bib87",
      "doi-asserted-by": "publisher",
      "first-page": "1",
      "DOI": "10.1111/j.1365-2818.1983.tb04225.x",
      "article-title": "Electron microscopy of frozen hydrated sections of vitreous ice and vitrified biological samples",
      "volume": "131",
      "author": "McDowall",
      "year": "1983",
      "journal-title": "J. Microsc."
    },
    {
      "key": "2023072307282095600_bib88",
      "doi-asserted-by": "publisher",
      "first-page": "1126",
      "DOI": "10.1016/j.ultramic.2009.04.002",
      "article-title": "Detective quantum efficiency of electron area detectors in electron microscopy",
      "volume": "109",
      "author": "McMullan",
      "year": "2009",
      "journal-title": "Ultramicroscopy."
    },
    {
      "key": "2023072307282095600_bib89",
      "doi-asserted-by": "publisher",
      "first-page": "1209",
      "DOI": "10.1126/science.1076184",
      "article-title": "Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography",
      "volume": "298",
      "author": "Medalia",
      "year": "2002",
      "journal-title": "Science."
    },
    {
      "key": "2023072307282095600_bib90",
      "doi-asserted-by": "publisher",
      "first-page": "70",
      "DOI": "10.1016/j.jsb.2007.06.010",
      "article-title": "Concatenated metallothionein as a clonable gold label for electron microscopy",
      "volume": "160",
      "author": "Mercogliano",
      "year": "2007",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib91",
      "doi-asserted-by": "publisher",
      "first-page": "404",
      "DOI": "10.1016/j.jsb.2011.09.002",
      "article-title": "Initial evaluation of a direct detection device detector for single particle cryo-electron microscopy",
      "volume": "176",
      "author": "Milazzo",
      "year": "2011",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib92",
      "doi-asserted-by": "publisher",
      "first-page": "1",
      "DOI": "10.1083/jcb.10.1.1",
      "article-title": "A new freezing-ultramicrotome",
      "volume": "10",
      "author": "Moor",
      "year": "1961",
      "journal-title": "J. Biophys. Biochem. Cytol."
    },
    {
      "key": "2023072307282095600_bib93",
      "doi-asserted-by": "publisher",
      "first-page": "134",
      "DOI": "10.1016/j.jsb.2009.12.015",
      "article-title": "3D segmentation of cell boundaries from whole cell cryogenic electron tomography volumes",
      "volume": "170",
      "author": "Moussavi",
      "year": "2010",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib94",
      "doi-asserted-by": "publisher",
      "first-page": "761",
      "DOI": "10.1038/nsmb.1832",
      "article-title": "Nucleotide-induced global conformational changes of flagellar dynein arms revealed by in situ analysis",
      "volume": "17",
      "author": "Movassagh",
      "year": "2010",
      "journal-title": "Nat. Struct. Mol. Biol."
    },
    {
      "key": "2023072307282095600_bib95",
      "doi-asserted-by": "publisher",
      "first-page": "109",
      "DOI": "10.1016/S0022-5320(57)80001-X",
      "article-title": "[Freeze-drying as a fixation technic for plant cells]",
      "volume": "1",
      "author": "M\u00fcller",
      "year": "1957",
      "journal-title": "J. Ultrastruct. Res."
    },
    {
      "key": "2023072307282095600_bib96",
      "doi-asserted-by": "publisher",
      "first-page": "66",
      "DOI": "10.1126/science.110.2846.66",
      "article-title": "New sectioning techniques for light and electron microscopy",
      "volume": "110",
      "author": "Newman",
      "year": "1949",
      "journal-title": "Science."
    },
    {
      "key": "2023072307282095600_bib97",
      "doi-asserted-by": "publisher",
      "first-page": "E845",
      "DOI": "10.1073/pnas.1106178108",
      "article-title": "Cryo-electron tomography reveals conserved features of doublet microtubules in flagella",
      "volume": "108",
      "author": "Nicastro",
      "year": "2011",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072307282095600_bib98",
      "doi-asserted-by": "publisher",
      "first-page": "225",
      "DOI": "10.1038/nrm1861",
      "article-title": "A visual approach to proteomics",
      "volume": "7",
      "author": "Nickell",
      "year": "2006",
      "journal-title": "Nat. Rev. Mol. Cell Biol."
    },
    {
      "key": "2023072307282095600_bib99",
      "doi-asserted-by": "publisher",
      "first-page": "93",
      "DOI": "10.1093/jmicro/dfm008",
      "article-title": "A genetically encoded metallothionein tag enabling efficient protein detection by electron microscopy",
      "volume": "56",
      "author": "Nishino",
      "year": "2007",
      "journal-title": "J. Electron Microsc. (Tokyo)."
    },
    {
      "key": "2023072307282095600_bib100",
      "doi-asserted-by": "publisher",
      "first-page": "334",
      "DOI": "10.1016/j.jsb.2006.04.014",
      "article-title": "Mapping 70S ribosomes in intact cells by cryoelectron tomography and pattern recognition",
      "volume": "156",
      "author": "Ortiz",
      "year": "2006",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib101",
      "doi-asserted-by": "publisher",
      "first-page": "613",
      "DOI": "10.1083/jcb.201005007",
      "article-title": "Structure of hibernating ribosomes studied by cryoelectron tomography in vitro and in situ",
      "volume": "190",
      "author": "Ortiz",
      "year": "2010",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072307282095600_bib102",
      "doi-asserted-by": "publisher",
      "first-page": "1508",
      "DOI": "10.1016/j.str.2012.06.010",
      "article-title": "Structure and 3D arrangement of endoplasmic reticulum membrane-associated ribosomes",
      "volume": "20",
      "author": "Pfeffer",
      "year": "2012",
      "journal-title": "Structure."
    },
    {
      "key": "2023072307282095600_bib103",
      "doi-asserted-by": "publisher",
      "first-page": "345",
      "DOI": "10.1016/j.jsb.2010.09.017",
      "article-title": "Exploring vitreous cryo-section-induced compression at the macromolecular level using electron cryo-tomography; 80S yeast ribosomes appear unaffected",
      "volume": "173",
      "author": "Pierson",
      "year": "2011",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib104",
      "doi-asserted-by": "publisher",
      "first-page": "673",
      "DOI": "10.1083/jcb.201106125",
      "article-title": "Cryoelectron tomography of radial spokes in cilia and flagella",
      "volume": "195",
      "author": "Pigino",
      "year": "2011",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072307282095600_bib105",
      "doi-asserted-by": "publisher",
      "first-page": "125",
      "DOI": "10.1016/j.ceb.2012.10.019",
      "article-title": "The bacterial cytoskeleton: more than twisted filaments",
      "volume": "25",
      "author": "Pilhofer",
      "year": "2013",
      "journal-title": "Curr. Opin. Cell Biol."
    },
    {
      "key": "2023072307282095600_bib106",
      "doi-asserted-by": "crossref",
      "first-page": "IX",
      "DOI": "10.1083/jcb.91.3.vii",
      "article-title": "Introduction: recollections on the beginnings of the journal of cell biology",
      "volume": "91",
      "author": "Porter",
      "year": "1981",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072307282095600_bib107",
      "doi-asserted-by": "publisher",
      "first-page": "685",
      "DOI": "10.1002/ar.1091170403",
      "article-title": "A study in microtomy for electron microscopy",
      "volume": "117",
      "author": "Porter",
      "year": "1953",
      "journal-title": "Anat. Rec."
    },
    {
      "key": "2023072307282095600_bib108",
      "article-title": "Transmission Electron Microscopy. Optical Sciences",
      "author": "Reimer",
      "year": "2008"
    },
    {
      "key": "2023072307282095600_bib109",
      "doi-asserted-by": "publisher",
      "first-page": "169",
      "DOI": "10.1016/j.jsb.2010.02.011",
      "article-title": "Micromachining tools and correlative approaches for cellular cryo-electron tomography",
      "volume": "172",
      "author": "Rigort",
      "year": "2010",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib110",
      "doi-asserted-by": "publisher",
      "first-page": "4449",
      "DOI": "10.1073/pnas.1201333109",
      "article-title": "Focused ion beam micromachining of eukaryotic cells for cryoelectron tomography",
      "volume": "109",
      "author": "Rigort",
      "year": "2012",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072307282095600_bib111",
      "doi-asserted-by": "publisher",
      "first-page": "135",
      "DOI": "10.1016/j.jsb.2011.08.012",
      "article-title": "Automated segmentation of electron tomograms for a quantitative description of actin filament networks",
      "volume": "177",
      "author": "Rigort",
      "year": "2012",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib112",
      "doi-asserted-by": "publisher",
      "first-page": "259",
      "DOI": "10.1016/B978-0-12-416026-2.00014-5",
      "article-title": "Integrative approaches for cellular cryo-electron tomography: correlative imaging and focused ion beam micromachining",
      "volume": "111",
      "author": "Rigort",
      "year": "2012",
      "journal-title": "Methods Cell Biol."
    },
    {
      "key": "2023072307282095600_bib113",
      "doi-asserted-by": "publisher",
      "first-page": "973",
      "DOI": "10.1038/nature06523",
      "article-title": "The molecular sociology of the cell",
      "volume": "450",
      "author": "Robinson",
      "year": "2007",
      "journal-title": "Nature."
    },
    {
      "key": "2023072307282095600_bib114",
      "article-title": "Die fruhe Entwicklung der Elektronenlinsen und der Elektronmikroskopie, In Acta historica leopoldina, Vol. 12",
      "author": "Ruska",
      "year": "1979"
    },
    {
      "key": "2023072307282095600_bib115",
      "doi-asserted-by": "publisher",
      "first-page": "509",
      "DOI": "10.1126/science.1164346",
      "article-title": "Electron cryomicroscopy of E. coli reveals filament bundles involved in plasmid DNA segregation",
      "volume": "323",
      "author": "Salje",
      "year": "2009",
      "journal-title": "Science."
    },
    {
      "key": "2023072307282095600_bib116",
      "doi-asserted-by": "publisher",
      "first-page": "135",
      "DOI": "10.1016/j.jsb.2007.07.011",
      "article-title": "Correlative microscopy: bridging the gap between light- and cryo-electron microscopy",
      "volume": "160",
      "author": "Sartori",
      "year": "2007",
      "journal-title": "J. Struct. Biol."
    },
    {
      "key": "2023072307282095600_bib117",
      "doi-asserted-by": "publisher",
      "first-page": "57",
      "DOI": "10.1016/0304-3991(84)90057-3",
      "article-title": "Three-dimensional reconstruction of imperfect two-dimensional crystals",
      "volume": "13",
      "author": "Saxton",
      "year": "1984",
      "journal-title": "Ultramicroscopy."
    },
    {
      "key": "2023072307282095600_bib118",
      "doi-asserted-by": "publisher",
      "first-page": "98",
      "DOI": "10.1111/j.1365-2818.2007.01794.x",
      "article-title": "Cryo-fluorescence microscopy facilitates correlations between light and cryo-electron microscopy and reduces the rate of photobleaching",
      "volume": "227",
      "author": "Schwartz",
      "year": "2007",
      "journal-title": "J. Microsc."
    },
    {
      "key": "2023072307282095600_bib119",
      "doi-asserted-by": "publisher",
      "first-page": "45",
      "DOI": "10.1002/jcp.1030420104",
      "article-title": "The ultrastructure of the innersegments of the retinal rods of the guinea pig eye as revealed by electron microscopy",
      "volume": "42",
      "author": "Sjostrand",
      "year": "1953",
      "journal-title": "J. Cell. Physiol."
    },
    {
      "key": "2023072307282095600_bib120",
      "doi-asserted-by": "publisher",
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      "article-title": "Electron microscopy of structural detail in frozen biological specimens",
      "volume": "3",
      "author": "Steere",
      "year": "1957",
      "journal-title": "J. Biophys. Biochem. Cytol."
    },
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      "key": "2023072307282095600_bib121",
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      "first-page": "877",
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      "article-title": "Electron microscopy of high pressure frozen samples: bridging the gap between cellular ultrastructure and atomic resolution",
      "volume": "130",
      "author": "Studer",
      "year": "2008",
      "journal-title": "Histochem. Cell Biol."
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      "article-title": "Electron diffraction of frozen, hydrated protein crystals",
      "volume": "186",
      "author": "Taylor",
      "year": "1974",
      "journal-title": "Science."
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      "doi-asserted-by": "publisher",
      "first-page": "808",
      "DOI": "10.1126/science.1091317",
      "article-title": "Global mapping of the yeast genetic interaction network",
      "volume": "303",
      "author": "Tong",
      "year": "2004",
      "journal-title": "Science."
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      "key": "2023072307282095600_bib124",
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      "first-page": "669",
      "DOI": "10.1016/j.ejcb.2009.07.002",
      "article-title": "Tools for correlative cryo-fluorescence microscopy and cryo-electron tomography applied to whole mitochondria in human endothelial cells",
      "volume": "88",
      "author": "van Driel",
      "year": "2009",
      "journal-title": "Eur. J. Cell Biol."
    },
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      "key": "2023072307282095600_bib125",
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      "first-page": "221",
      "DOI": "10.1111/j.1365-2818.2010.03478.x",
      "article-title": "Cryo-electron tomography: methodology, developments and biological applications",
      "volume": "242",
      "author": "Vanhecke",
      "year": "2011",
      "journal-title": "J. Microsc."
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      "volume": "515",
      "author": "Verkleij",
      "year": "1978",
      "journal-title": "Biochim. Biophys. Acta."
    },
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      "key": "2023072307282095600_bib127",
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      "first-page": "491",
      "DOI": "10.1083/jcb.201004052",
      "article-title": "Mass spectrometry-based proteomics in cell biology",
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      "author": "Walther",
      "year": "2010",
      "journal-title": "J. Cell Biol."
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      "first-page": "147",
      "DOI": "10.1016/j.str.2010.12.002",
      "article-title": "A ferritin-based label for cellular electron cryotomography",
      "volume": "19",
      "author": "Wang",
      "year": "2011",
      "journal-title": "Structure."
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      "article-title": "Direct visualization of Escherichia coli chemotaxis receptor arrays using cryo-electron microscopy",
      "volume": "104",
      "author": "Zhang",
      "year": "2007",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
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      "article-title": "Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state",
      "volume": "190",
      "author": "Zuber",
      "year": "2008",
      "journal-title": "J. Bacteriol."
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