Cryo-electron Microscopy as a Functional Instrument for Systems Biology, Structural Analysis and Experimental Manipulations with Living Cells. A Comprehensive Analytical Review of the Current Works
DOI:
https://doi.org/10.15407/cryo24.03.193Keywords:
cryo-electron microscopy, cryo-electron tomography, system biology, localomics, dynamomics, micromachining, structural analysis, in silico, molecular machinesAbstract
The aim of this paper is to give an introductory review of the cryo-electron microscopy as a complex data source for most of the system biology branches, including the most perspective non-local approaches known as localomics and dynamomics.
A brief summary of various cryo-electron microscopy methods and corresponding system biological approaches is given in the text. The above classification can be considered as a useful framework for the primary comprehensions about cryo-electron microscopy aims and instrumental tools. We do not discuss any of these concepts in details, but merely point out that their methodological complexity follows only from the structure-functional complexity of biological systems which are investigated in this manner. We also postulate that one can employ some of the cryo-electron microscopic techniques not only for observation, but also for modification and structural refunctionalization of some biological and similar soft matter objects and microscopic samples. In other worlds, we start
with the cryoelectron microscopy as a tool for the system biology and progress to its applying as an instrument for system biology and functional biomimetics. All these conclusions can be deduced from the most recent works of the latest years.
Probl Cryobiol Cryomed 2014; 24(3):193-211.
References
Abreu F., Sousa A.A., Aronova M.A. et al. Cryo-electron tomography of the magnetotactic vibrio Magnetovibrio blakemorei: insights into the biomineralization of prismatic magnetosomes. Journ Struct Biol 2013; 181(2): 162–168. CrossRef PubMed
Agirre J., Goret G., LeGoff M. et al. Cryo-electron microscopy reconstructions of triatoma virus particles: a clue to unravel genome delivery and capsid disassembly. Journ Gen Virol 2013; 94: 1058–1068. CrossRef PubMed
Ahmed A., Whitford P.C., Sanbonmatsu K.Y., Tama F. Consensus among flexible fitting approaches improves the interpretation of cryo-EM data. Journ Struct Biol 2012; 177(2): 561–570. CrossRef PubMed
Allen G.S., Stokes D.L. Modeling, docking, and fitting of atomic structures to 3D maps from cryo-electron microscopy. Meth Mol Biol 2013; 955: 229–241. CrossRef PubMed
Azuaje F. Bioinformatics and Biomarker Discovery: "Omic" Data Analysis for Personalized Medicine. Hoboken, New Jersey; 2010.
Bai X.C., Martin T.G., Scheres S.H., Dietz H. Cryo-EM structure of a 3D DNA-origami object. Proc Nat Acad Sci USA 2012; 109(49): 20012–20017. CrossRef PubMed
Bajaj C., Goswami S., Zhang Q. Detection of secondary and supersecondary structures of proteins from cryo-electron microscopy. Journ Struc Biol 2012; 177(2): 367–381. CrossRef PubMed
Balfour B.M., Goscicka T., MacKenzie J.L. et al. Combined time-lapse cinematography and immuno-electron microscopy. Anat Rec 1990; 226(4): 509–514. CrossRef PubMed
Bartesaghi A., Lecumberry F., Sapiro G., Subramaniam S. Protein secondary structure determination by constrained single-particle cryo-electron tomography. Structure 2012; 20(12): 2003–2013. CrossRef PubMed
Barton B., Rhinow D., Walter A. et al. In-focus electron microscopy of frozen-hydrated biological samples with a Boersch phase plate. Ultramicroscopy 2011; 111(12): 1696–1705. CrossRef PubMed
Bergstrцm L.M., Skoglund S., Edwards K. et al. Self-assembly in mixtures of an anionic and a cationic surfactant: a comparison between small-angle neutron scattering and cryo-transmission electron microscopy. Langmuir 2013; 29(38): 11834–11848. CrossRef PubMed
Bharat T.A., Davey N.E., Ulbrich P. et al. Structure of the immature retroviral capsid at 8A resolution by cryo-electron microscopy. Nature 2012; 487(7407): 385–389. CrossRef PubMed
Bouchet-Marquis C., Pagratis M., Kirmse R., Hoenger A. Metallothionein as a clonable high-density marker for cryo-electron microscopy. Journ Struc Biol 2012; 177(1): 119–127. CrossRef PubMed
Briegel A., Chen S., Koster A.J. et al. Correlated light and electron cryo-microscopy. Meth Enzymol 2010; 481: 317–341. CrossRef
Briggs J.A. Structural biology in situ – the potential of subtomogram averaging. Curr Opin Struct Biol 2013; 23(2): 261–267. CrossRef PubMed
Brusic V. From immunoinformatics to immunomics. Journ Bioinform Comput Biol 2003; 1: 179–181. CrossRef
Bui K.H., Ishikawa T. 3D structural analysis of flagella/cilia by cryo-electron tomography. Meth Enzymol 2013; 524: 305–323. CrossRef PubMed
Campbell M.G., Cheng A., Brilot A.F. et al. Movies of ice-embedded particles enhance resolution in electron cryomicroscopy. Structure 2012; 20(11): 1823–1828. CrossRef PubMed
Cao C., Dong X., Wu X. et al. Conserved fiber-penton base interaction revealed by nearly atomic resolution cryo-electron microscopy of the structure of adenovirus provides insight into receptor interaction. Journ Virol 2012; 86(22): 12322–12329. CrossRef PubMed
Cardone G., Heymann J.B., Steven A.C. One number does not fit all: Mapping local variations in resolution in cryo-EM reconstructions. Journ Struc Biol 2013; 184(2): 226–236. CrossRef PubMed
Carlson D.B., Gelb J., Palshin V., Evans J.E. Laboratory-based cryogenic soft X-ray tomography with correlative cryo-light and electron microscopy. Micros Microanal 2013; 19(1): 22–29. CrossRef PubMed
Caston J.R. Conventional electron microscopy, cryo-electron microscopy and cryo-electron tomography of viruses. Subcell Biochem 2013; 68: 79–115. CrossRef PubMed
Chan K.Y., Trabuco L.G., Schreiner E., Schulten K. Cryo-electron microscopy modeling by the molecular dynamics flexible fitting method. Biopolymers 2012; 97(9): 678–686. CrossRef PubMed
Comolli L.R., Duarte R., Baum D. et al. A portable cryo-plunger for on-site intact cryogenic microscopy sample preparation in natural environments. Micros Res Tech 2012; 75(6): 829–836. CrossRef PubMed
Cong Y., Schröder G.F., Meyer A.S. et al. Symmetry-free cryo-EM structures of the chaperonin TRiC along its ATPase-driven conformational cycle. EMBO Journ 2012; 31(3): 720–730. CrossRef PubMed
Crauste-Manciet S., Larquet E., Khawand K. et al. Lipidic spherulites: Formulation optimisation by paired optical and cryo-electron microscopy. Eur Journ Pharm Biopharm 2013; 85(3): 1088–1094. CrossRef PubMed
De Vries S.J., Zacharias M. ATTRACT-EM: a new method for the computational assembly of large molecular machines using cryo-EM maps. PLoS One 2012; 7(12): e49733.
De Winter D.A., Mesman R.J., Hayles M.F. et al. In-situ integrity control of frozen-hydrated, vitreous lamellas prepared by the cryo-focused ion beam scanning electron microscope. Journ Struc Biol 2013; 183(1): 11–18. CrossRef PubMed
Diebolder C.A., Koster A.J., Koning R.I. Pushing the resolution limits in cryoelectron tomography of biological structures. Journ Microsc 2012; 248(1): 1–5. CrossRef PubMed
DiMaio F., Zhang J., Chiu W., Baker D. Cryo-EM model validation using independent map reconstructions. Prot Sci 2013; 22(6): 865–868. CrossRef PubMed
Dubochet J. Cryo-EM – the first thirty years. Journ Microsc 2012; 245(3): 221–224. CrossRef
Duke E.M., Razi M., Weston A. et al. Imaging endosomes and autophagosomes in whole mammalian cells using correlative cryo-fluorescence and cryo-soft X-ray microscopy (cryo-CLXM). Ultramicroscopy 2014; 143: 77–87. CrossRef PubMed
Eibauer M., Hoffmann C., Plitzko J.M. et al. Unraveling the structure of membrane proteins in situ by transfer function corrected cryo-electron tomography. Journ Struct Biol 2012; 180(3): 488–496. CrossRef PubMed
Elber R. Watching biomolecular machines in action. Structure 2010; 18(4): 415–416. CrossRef PubMed
Elmlund H., Elmlund D., Bengio S. PRIME: probabilistic initial 3D model generation for single-particle cryo-electron microscopy. Structure 2013; 21(8): 1299–1306. CrossRef PubMed
Falkner B., Schroder G.F. Cross-validation in cryo-EM-based structural modeling. Proc Nat Acad Sci USA 2013; 110(22): 8930–8935. CrossRef PubMed
Fitzpatrick A.W., Lorenz U.J., Vanacore G.M., Zewail A.H. 4D cryo-electron microscopy of proteins. Journ Am Chem Soc 2013; 135(51): 19123–19126. CrossRef PubMed
Forrester J.S., Milne S.B., Ivanova P.T., Brown H.A. Computational lipidomics: a multi-plexed analysis of dynamic changes in membrane lipid composition during signal transduc-tion. Mol Pharmacol 2004; 65(4): 813–821. CrossRef PubMed
Frank J. Story in a sample – the potential (and limitations) of cryo-electron microscopy applied to molecular machines. Biopolymers 2013; 99(11): 832–836. CrossRef PubMed
Fujiyoshi Y. Low dose techniques and cryo-electron microscopy. Meth Mol Biol 2013; 955: 103–118. CrossRef PubMed
Fukuda Y., Nagayama K. Zernike phase contrast cryo-electron tomography of whole mounted frozen cells. Journ Struc Biol 2012; 177(2): 484–489. CrossRef PubMed
Garewal M., Zhang L., Ren G. Optimized negative-staining protocol for examining lipid-protein interactions by electron microscopy. Meth Mol Biol 2013; 974: 111–118. CrossRef PubMed
Gopalakrishnan G., Yam P.T., Madwar C. et al. Label-free visualization of ultrastructural features of artificial synapses via cryo-EM. ACS Chem Neurosci 2011; 2(12): 700–704. CrossRef PubMed
Grélard A., Guichard P., Bonnafous P. et al. Hepatitis B subvirus particles display both a fluid bilayer membrane and a strong resistance to freeze drying: a study by solid-state NMR, light scattering, and cryo-electron microscopy/tomography. FASEB Journ 2013; 27(10): 4316–4326. CrossRef PubMed
Greunz T., Strauß B., Schausberger S.E. et al. Cryo ultra-low-angle microtomy for XPS-depth profiling of organic coatings. Anal Bioanal Chem 2013; 405(22): 7153–7160. CrossRef PubMed
Grigorieff N. Direct detection pays off for electron cryo-microscopy. ELIFE 2013; 2: e00573.
Guesdon A., Blestel S., Kervrann C., Chrétien D. Single versus dual-axis cryo-electron tomography of microtubules assembled in vitro: limits and perspectives. Journ Struc Biol 2013; 181(2): 169–178. CrossRef PubMed
Gyobu N. Grid preparation for cryo-electron microscopy. Meth Mol Biol 2013; 955: 119–128. CrossRef PubMed
Han H.M., Bouchet-Marquis C., Huebinger J., Grabenbauer M. Golgi apparatus analyzed by cryo-electron microscopy. Histochem Cell Biol 2013; 140(4): 369–381. CrossRef PubMed
Han H.M., Huebinger J., Grabenbauer M. Self-pressurized rapid freezing (SPRF) as a simple fixation method for cryo-electron microscopy of vitreous sections. Journ Struc Biol 2012; 178(2): 84–87. CrossRef PubMed
Heymann J.B., Winkler D.C., Yim Y.I. et al. Clathrin-coated vesicles from brain have small payloads: a cryo-electron tomographic study. Journ Struc Biol 2013; 184(1): 43–51. CrossRef PubMed
Hoang T.V., Cavin X., Schultz P., Ritchie D.W. gEMpicker: A highly parallel GPU-accelerated particle picking tool for cryo-electron microscopy. BMC Struct Biol 2013; 13(25): 1–10. CrossRef
Hoofnagle A.N., Heinecke J.W. Lipoproteomics: using mass spectrometry-based proteomics to explore the assembly, structure, and function of lipoproteins. Journ Lipid Res 2009; 50(10): 1967–1975. CrossRef PubMed
Hrabe T., Chen Y., Pfeffer S. et al. PyTom: a python-based toolbox for localization of macromolecules in cryo-electron tomograms and subtomogram analysis. Journ Struct Biol 2012; 178(2): 177–188. CrossRef PubMed
Hsieh C., Schmelzer T., Kishchenko G. et al. Practical workflow for cryo focused-ion-beam milling of tissues and cells for cryo-TEM tomography. Journ Struc Biol 2014; 185(1): 32–41. CrossRef PubMed
Huisken J., Stainier D.Y. Selective plane illumination microscopy techniques in developmental biology. Development 2009; 136(12): 1963–1975. CrossRef PubMed
Iijima H., Fukuda Y., Arai Y. et al. Hybrid fluorescence and electron cryo-microscopy for simultaneous electron and photon imaging. Journ Struc Biol 2014; 185(1): 107–115. CrossRef PubMed
Johnson M.C., Schmidt-Krey I. Two-dimensional crystallization by dialysis for structural studies of membrane proteins by the cryo-EM method electron crystallography. Meth Cell Biol 2013; 113: 325–337. CrossRef PubMed
Jun S., Zhao G., Ning J. et al. Correlative microscopy for 3D structural analysis of dynamic interactions. Journ Vis Exp 2013; 76: e50386.
Kim J.J. Using viral genomics to develop viral gene products as a novel class of drugs to treat human ailments. Biotech Lett 2001; 23(13): 1015–1020. CrossRef
Kiss G., Chen X., Brindley M.A. et al. Capturing enveloped viruses on affinity grids for downstream cryo-electron microscopy applications. Microsc Microanal 2014; 20(1): 164–174. CrossRef PubMed
Knoops K., Schoehn G., Schaffitzel C. Cryo-electron microscopy of ribosomal complexes in cotranslational folding, targeting, and translocation. Wil Interdisc Rev RNA 2012; 3(3): 429–441. CrossRef PubMed
Koning R.I., Koster A.J. Cellular nanoimaging by cryo electron tomography. Meth Mol Biol 2013; 950: 227–251.
Kucukelbir A., Sigworth F.J., Tagare H.D. Quantifying the local resolution of cryo-EM density maps. Nat Meth 2014; 11(1): 63–65. CrossRef PubMed
Kudryashev M., Stahlberg H., CastaÑo-Dнez D. Assessing the benefits of focal pair cryo-electron tomography. Journ Struct Biol 2012; 178(2): 88–97. CrossRef PubMed
Kwon S., Choi S.B., Park M.G. et al. Extraction of three-dimensional information of biological membranous tissue with scanning confocalinfrared laser microscope tomography. Micros Microanal 2013; 19 (Suppl 5): 194–197.
Kymionis G.D., Grentzelos M.A., Plaka A.D. et al. Correlation of the corneal collagen cross-linking demarcation line using confocal microscopy and anterior segment optical coherence tomography in keratoconic patients. Am Journ Ophthalmol 2014; 157(1): 110–115. CrossRef PubMed
Lagarde M., Géloën A., Record M. et al. Lipidomics is emerging. Biochim Biophys Acta 2003; 1634(3): 61. CrossRef PubMed
Lee J., Saha A., Pancera S.M. et al. Shear free and blotless cryo-TEM imaging: a new method for probing early evolution of nanostructures. Langmuir 2012; 28(9): 4043–4046. CrossRef PubMed
Leforestier A., Lemercier N., Livolant F. Contribution of cryoelectron microscopy of vitreous sections to the understanding of biological membrane structure. Proc Nat Acad Sci USA 2012; 109(23): 8959–8964. CrossRef PubMed
Lerch T.F., O'Donnell J.K., Meyer N.L. et al. Structure of AAV-DJ, a retargeted gene therapy vector: cryo-electron microscopy at 4.5Е resolution. Structure 2012; 20(8): 1310–1320. CrossRef PubMed
Li M., Zheng W. All-atom structural investigation of kinesin-microtubule complex constrained by high-quality cryo-electron-microscopy maps. Biochemistry 2012; 51(25): 5022–5032. CrossRef PubMed
Li X., Mooney P., Zheng S. et al. Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat Meth 2013; 10(6): 584–590. CrossRef PubMed
Lin J., Cheng N., Hogle J.M. et al. Conformational shift of a major poliovirus antigen confirmed by immuno-cryogenic electron microscopy. Journ Immunol 2013; 191(2): 884–891. CrossRef PubMed
LuÄiÄ V., Rigort A., Baumeister W. Cryo-electron tomography: the challenge of doing structural biology in situ. Journ Cell Biol 2013; 202(3): 407–419. CrossRef PubMed
Ludtke S.J., Lawson C.L., Kleywegt G.J. et al. The 2010 cryo-EM modeling challenge. Biopolymers 2012; 97(9): 651–654. CrossRef PubMed
Martinez J.M., Swan B.K., Wilson W.H. Marine viruses, a genetic reservoir revealed by targeted viromics. ISME Journ 2014; 8(5): 1079–1088. CrossRef PubMed
McCully M., Canny M. Quantitative cryo-analytical scanning electron microscopy (CEDX): an important technique useful for cell-specific localization of salt. Meth Mol Biol 2012; 913: 137–148.
Milne J.L., Borgnia M.J., Bartesaghi A. et al. Cryo-electron microscopy – a primer for the non-microscopist. FEBS Journ 2013; 280(1): 28–45. CrossRef PubMed
Miyazaki N., Nakagawa A., Iwasaki K. Life cycle of phyto-reoviruses visualized by electron microscopy and tomo-graphy. Front Microb 2013; 4(306): 1–9.
Müllertz A., Fatouros D.G., Smith J.R. et al. Insights into intermediate phases of human intestinal fluids visualized by atomic force microscopy and cryo-transmission electron microscopy ex vivo. Mol Pharm 2012; 9(2): 237–247. CrossRef PubMed
Nederlof I., Li Y.W., van Heel M., Abrahams J.P. Imaging protein three-dimensional nano-crystals with cryo-EM. Acta Crystallogr D: Biol. Crystallogr 2013; 69: 852–859. CrossRef PubMed
Nejadasl F.K., Karuppasamy M., Newman E.R. et al. Non-rigid image registration to reduce beam-induced blurring of cryo-electron microscopy images. Journ Synchrotron Radiat 2013; 20: 58–66. CrossRef PubMed
Noble A.J., Zhang Q., O'Donnell J. et al. A pseudoatomic model of the COPII cage obtained from cryo-electron microscopy and mass spectrometry. Nat Struct Mol Biol 2013; 20(2): 167–173. CrossRef PubMed
Norousi R., Wickles S., Leidig C. et al. Automatic post-picking using MAPPOS improves particle image detection from cryo-EM micrographs. Journ Struct Biol 2013; 182(2): 59–66. CrossRef PubMed
Nyuta K., Yoshimura T., Tsuchiya K. et al. Zwitterionic heterogemini surfactants containing ammonium and carboxylate headgroups 2: aggregation behavior studied by SANS, DLS, and cryo-TEM. Journ Colloid Interface Sci 2012; 370(1): 80–85. CrossRef PubMed
Oda T., Kikkawa M. Novel structural labeling method using cryo-electron tomography and biotin-streptavidin system. Journ Struc Biol 2013; 183(3): 305–311. CrossRef PubMed
Ounjai P., Kim K.D., Lishko P.V., Downing K.H. Three-dimensional structure of the bovine sperm connecting piece revealed by electron cryotomography. Biol Reprod 2012; 87(3): 1–9. CrossRef PubMed
Paessens L.C., Fluitsma D.M., van Kooyk Y. Haematopoietic antigen-presenting cells in the human thymic cortex: evidence for a role in selection and removal of apoptotic thymocytes. Journ Pathol 2008; 214(1): 96–103. CrossRef PubMed
Pandurangan A.P., Topf M. RIBFIND: a web server for identifying rigid bodies in protein structures and to aid flexible fitting into cryo EM maps. Bioinformatics 2012; 28(18): 2391–2393. CrossRef PubMed
Pigino G., Cantele F., Vannuccini E. et al. Electron tomography of IFT particles. Meth Enzymol 2013; 524: 325–342. CrossRef PubMed
Quan B.D., Sone E.D. Cryo-TEM analysis of collagen fibrillar structure. Meth Enzymol 2013; 532: 189–205. CrossRef PubMed
Rigort A., Bäuerlein F.J., Villa E. et al. Focused ion beam micro-machining of eukaryotic cells for cryoelectron tomography. Proc Nat Acad Sci USA 2012; 109(12): 4449–4454. CrossRef PubMed
Rigort A., Villa E., Bäuerlein F.J. et al. Integrative approaches for cellular cryo-electron tomography: correlative imaging and focused ion beam micromachining. Meth Cell Biol 2012; 111: 259–281. CrossRef PubMed
Rusu M., Wriggers W. Evolutionary bidirectional expansion for the tracing of alpha helices in cryo-electron microscopy reconstructions. Journ Struc Biol 2012; 177(2): 410–419. CrossRef PubMed
Schellenberger P., Kaufmann R., Siebert C.A. et al. High-precision correlative fluorescence and electron cryo-microscopy using two independent alignment markers. Ultramicroscopy 2014; 143: 41–51. CrossRef PubMed
Scheres S.H. A Bayesian view on cryo-EM structure determination. Journ Mol Biol 2012; 415(2): 406–418. CrossRef PubMed
Schertel A., Snaidero N., Han H.M. et al. Cryo FIB-SEM: Volume imaging of cellular ultra-structure in native frozen specimens. Journ Struc Biol 2013; 184(2): 355–360. CrossRef PubMed
Schorb M., Briggs J.A. Correlated cryo-fluorescence and cryo-electron microscopy with high spatial precision and improved sensitivity. Ultramicroscopy 2014; 143: 24–32. CrossRef PubMed
Shang Z., Sigworth F.J. Hydration-layer models for cryo-EM image simulation. Journ Struct Biol 2012; 180(1): 10–16. CrossRef PubMed
Sharp T.H., Bruning M., Mantell J. et al. Cryo-transmission electron microscopy structure of a gigadalton peptide fiber of de novo design. Proc Nat Acad Sci USA 2012; 109(33): 13266–13271. CrossRef PubMed
Shigematsu H., Sigworth F.J. Noise models and cryo-EM drift correction with a direct-electron camera. Ultramicroscopy 2013; 131: 61–69. CrossRef PubMed
Shimanouchi T., Oyama E., Ishii H. et al. Membranomics research on interactions between liposome membranes with membrane chip analysis. Membrane 2009; 34(6): 342–350. CrossRef
Shrum D.C., Woodruff B.W., Stagg S.M. Creating an infra-structure for high-throughput high-resolution cryogenic electron microscopy. Journ Struc Biol 2012; 180(1): 254–258. CrossRef PubMed
Si D., Ji S., Nasr K.A., He J. A machine learning approach for the identification of protein secondary structure elements from electron cryo-microscopy density maps. Biopolymers 2012; 97(9): 698–708. CrossRef PubMed
Singer A., Zhao Z., Shkolnisky Y., Hadani R. Viewing angle classification of cryo-electron microscopy images using eigenvectors. SIAM Journ Imaging Sci 2011; 4(2): 723–759. CrossRef PubMed
Song K., Comolli L.R., Horowitz M. Removing high contrast artifacts via digital inpainting in cryo-electron tomography: an application of compressed sensing. Journ Struc Biol 2012; 178(2): 108–120. CrossRef PubMed
Strunk K.M., Wang K., Ke D. et al. Thinning of large mammalian cells for cryo-TEM characterization by cryo-FIB milling. Journ Microsc 2012; 247(3): 220–227. CrossRef PubMed
Sun J., Kawakami H., Zech J. et al. Cdc6-induced conformational changes in ORC bound to origin DNA revealed by cryo-electron microscopy. Structure 2012; 20(3): 534–544. CrossRef PubMed
Tatischeff I., Larquet E., Falcón-Pérez J.M. et al. Fast characterisation of cell-derived extracellular vesicles by nanoparticles tracking analysis, cryo-electron microscopy, and Raman tweezers microspectroscopy. Journ Extracell Vesicles 2012: 1–11.
Taylor K.A., Glaeser R.M. Retrospective on the early development of cryoelectron microscopy of macromolecules and a prospective on opportunities for the future. Journ Struc Biol 2008; 163(3): 214–223. CrossRef PubMed
Tremoulet A.H., Albani S. Immunomics in clinical development: bridging the gap. Exp Rev Clin Immunol 2005; 1(1): 3–6. CrossRef PubMed
Vahedi-Faridi A., Jastrzebska B., Palczewski K., Engel A. 3D imaging and quantitative analysis of small solubilized membrane proteins and their complexes by transmission electron microscopy. Microscopy 2013; 62(1): 95–107. CrossRef PubMed
Vargas J., Otуn J., Marabini R. et al. FASTDEF: fast defocus and astigmatism estimation for high-throughput transmission electron microscopy. Journ Struc Biol 2013; 181(2): 136–148. CrossRef PubMed
Vonesch C., Wang L., Shkolnisky Y., Singer A. Fast wavelet-based single-particle reconstruction in cryo-EM. Proceedings of the 8th IEEE Int Symp on Biomed. Imaging: From Nano to Macro; 2011; Chicago, Illinois. p. 1950–1953.
VuloviÄ M., Ravelli R.B., van Vliet L.J. et al. Image formation modeling in cryo-electron microscopy. Journ Struct Biol 2013; 183(1): 19–32. CrossRef PubMed
Walter A., Muzik H., Vieker H. et al. Practical aspects of Boersch phase contrast electron microscopy of biological specimens. Ultramicroscopy 2012; 116: 62–72. CrossRef PubMed
Wang J., Yin C. A Zernike-moment-based non-local denoising filter for cryo-EM images. Sci Ch Life Sci 2013; 56(4): 384–390. CrossRef PubMed
Wang K., Strunk K., Zhao G. et al. 3D structure determination of native mammalian cells using cryo-FIB and cryo-electron tomography. Journ Struc Biol 2012; 180(2): 318–326. CrossRef PubMed
Wang Q., Matsui T., Domitrovic T. et al. Dynamics in cryo EM reconstructions visualized with maximum-likelihood derived variance maps. Journ Struc Biol 2013; 181(3): 195–206. CrossRef PubMed
Wang Z., Gao K., Chen J. et al. Advantages of intermediate X-ray energies in Zernike phase contrast X-ray microscopy. Biotech Adv 2013; 31(3): 387–392. CrossRef PubMed
Weber M., Huisken J. Omnidirectional microscopy. Nat Meth 2012; 9: 656–657. CrossRef PubMed
Weiner A., Kapishnikov S., Shimoni E. et al. Vitrification of thick samples for soft X-ray cryo-tomography by high pressure freezing. Journ Struc Biol 2013; 181(1): 77–81. CrossRef PubMed
Willmann J., Leibfritz D., Thiele H. Hyphenated tools for phospholipidomics. Journ Biomol Tech 2008; 19(3): 211–216.
Yajima H., Ogura T., Nitta R. et al. Conformational changes in tubulin in GMPCPP and GDP-taxol microtubules observed by cryoelectron microscopy. Journ Cell Biol 2012; 198(3): 315–322. CrossRef PubMed
Yang F., Abe K., Tani K., Fujiyoshi Y. Carbon sandwich preparation preserves quality of two-dimensional crystals for cryo-electron microscopy. Microscopy 2013; 62(6): 597–606. CrossRefPubMed
Yoder J.D., Cifuente J.O., Pan J. et al. The crystal structure of a coxsackievirus B3–RD variant and a refined 9-angstrom cryo-electron microscopy reconstruction of the virus com-plexed with decay-accelerating factor (DAF) provide a new footprint of DAF on the virus surface. Journ Virol 2012; 86(23): 12571–12581. CrossRef PubMed
Zhang L., Tong H., Garewal M., Ren G. Optimized negative-staining electron microscopy for lipoprotein studies. Biochim Biophys Acta 2013; 1830(1): 2150–2159. CrossRef PubMed
Zhang P. Correlative cryo-electron tomography and optical microscopy of cells. Curr Opin Struc Biol 2013; 23(5): 763–770. CrossRef PubMed
Zhang X., Ge P., Yu X. et al. Cryo-EM structure of the mature dengue virus at 3.5–A resolution. Nat Struc Mol Biol 2013; 20(1): 105–110. CrossRef PubMed
Zhao G., Perilla J.R., Yufenyuy E.L. et al. Mature HIV-1 capsid structure by cryo-electron microscopy and all-atom molecular dynamics. Nature 2013; 497(7451): 643–646. CrossRef PubMed
Zou X., Hovmöller S., Oleynikov P. Phase contrast, contrast transfer function (CTF) and high-resolution electron microscopy (HRTEM). In: Electron Crystallography: Electron Microscopy and Electron Diffraction. Oxford, New York 2011: 131–155.
Zuckerkandl E., Pauling L. Molecules as documents of evolutionary history. Journ Theor Biol 1965; 8(2): 357–366. CrossRef
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