The combination of chemical fixation procedures with high pressure freezing and freeze substitution preserves highly labile tissue ultrastructure for electron tomography applications

Al-Amoudi, 2005, Nanostructure of the epidermal extracellular space as observed by cryo-electron microscopy of vitreous sections of human skin, J. Invest. Dermatol., 124, 764, 10.1111/j.0022-202X.2005.23630.x Belichenko, 1995, Studies on the 3-dimensional architecture of dendritic spines and varicosities in human cortex by confocal laser scanning microscopy and Lucifer yellow microinjections, J. Neurosci. Methods, 57, 55, 10.1016/0165-0270(94)00125-Z Buhl, 1993, Intracellular injection in fixed slices in combination with neuroanatomical tracing techniques and electron microscopy to determine multisynaptic pathways in the brain, Microsc. Res. Tech., 24, 15, 10.1002/jemt.1070240104 Bushong, 2002, Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains, J. Neurosci., 22, 183, 10.1523/JNEUROSCI.22-01-00183.2002 Calle, 2005, Evidence that urocortin I acts as a neurohormone to stimulate alpha MSH release in the toad Xenopus laevis, Brain Res., 1040, 14, 10.1016/j.brainres.2004.12.056 Capani, 2001, Phalloidin-eosin followed by photo-oxidation: a novel method for localizing F-actin at the light and electron microscopic levels, J. Histochem. Cytochem., 49, 1351, 10.1177/002215540104901103 Chan, 1992, Localization of heparan sulfate proteoglycan in basement membrane by side chain staining with cuprolinic blue as compared with core protein labeling with immunogold, J. Histochem. Cytochem., 40, 1559, 10.1177/40.10.1527375 Chan, 1993, The basement membranes of cryofixed or aldehyde-fixed, freeze-substituted tissues are composed of a lamina densa and do not contain a lamina lucida, Cell Tissue Res., 273, 41, 10.1007/BF00304610 Dahl, 1989, High-pressure freezing for the preservation of biological structure: theory and practice, J. Electron Microsc. Tech., 13, 165, 10.1002/jemt.1060130305 Deerinck, 1994, Fluorescence photooxidation with eosin: a method for high resolution immunolocalization and in situ hybridization detect for light and electron microscopy, J. Cell Biol., 126, 910, 10.1083/jcb.126.4.901 Donohoe, 2007, Identification and characterization of COPIa- and COPIb-type vesicle classes associated with plant and algal Golgi, Proc. Natl. Acad. Sci. USA, 104, 163, 10.1073/pnas.0609818104 Epperlein, 2000, Immunohistochemical demonstration of hyaluronan and its possible involvement in axolotl neural crest cell migration, J. Struct. Biol., 132, 19, 10.1006/jsbi.2000.4298 Epperlein, 1997, Improved preservation of the subepidermal extracellular matrix in axolotl embryos using electron microscopical techniques based on cryoimmobilization, J. Struct. Biol., 118, 43, 10.1006/jsbi.1996.3838 Friesen, 1981, Synthesis of black beetle virus proteins in cultured drosophila cells: differential expression of RNAs 1 and 2, J. Virol., 37, 876, 10.1128/JVI.37.3.876-886.1981 Frotscher, 2007, New ways of looking at synapses, Histochem. Cell Biol., 128, 91, 10.1007/s00418-007-0305-7 Gaietta, 2002, Multicolor and electron microscopic imaging of connexin trafficking, Science, 296, 503, 10.1126/science.1068793 Gaietta, 2006, Golgi twins in late mitosis revealed by genetically encoded tags for live cell imaging and correlated electron microscopy, Proc. Natl. Acad. Sci. USA, 103, 17777, 10.1073/pnas.0608509103 Galvan, 2004, Differential subcellular and subsynaptic distribution of GABA(A) and GABA(B) receptors in the monkey subthalamic nucleus, Neuroscience, 127, 709, 10.1016/j.neuroscience.2004.05.014 Giepmans, 2005, Correlated light and electron microscopic imaging of multiple endogenous proteins using Quantum dots, Nat. Methods, 2, 743, 10.1038/nmeth791 Hawes, 2007, Rapid freeze-substitution preserves membranes in high-pressure frozen tissue culture cells, J. Microsc., 226, 182, 10.1111/j.1365-2818.2007.01767.x Hayat, 1982 Hohenberg, 1996, High-pressure freezing of tissue obtained by fine-needle biopsy, J. Microsc., 183, 133, 10.1046/j.1365-2818.1996.820642.x Hsieh, 2006, Towards high-resolution three-dimensional imaging of native mammalian tissue: electron tomography of frozen-hydrated rat liver sections, J. Struct. Biol., 153, 1, 10.1016/j.jsb.2005.10.004 Kieval, 2001, Subcellular and subsynaptic localization of presynaptic and postsynaptic kainate receptor subunits in the monkey striatum, J. Neurosci., 21, 8746, 10.1523/JNEUROSCI.21-22-08746.2001 Kirschning, 1998, High-pressure freezing and freeze-substitution of native rat brain: suitability for preservation and immunoelectron microscopic localization of myelin glycolipids, J. Neurosci. Res., 53, 465, 10.1002/(SICI)1097-4547(19980815)53:4<465::AID-JNR8>3.0.CO;2-4 Konig, 2005, Use of surface affinity enrichment and cryo-embedding to prepare in vitro reconstituted mitotic chromosomes for EM tomography, Ultramicroscopy, 103, 261, 10.1016/j.ultramic.2004.12.008 Kremer, 1996, Computer visualization of three-dimensional image data using IMOD, J. Struct. Biol., 116, 71, 10.1006/jsbi.1996.0013 Lanman, J., Crum, J., Deerinck, T.J., Gaietta, G.M., Schneemann, A., Sosinsky, G.E., Ellisman, M.H., Johnson, J.E. 2008. Visualizing flock house virus infection in Drosophila cells with correlated fluorescence and electron microscopy. J. Struct. Biol. in press, doi:10.1016/j.jsb.2007.09.009. Lawrence, 2006, Transform-based backprojection for volume reconstruction of large format electron microscope tilt series, J. Struct. Biol., 154, 144, 10.1016/j.jsb.2005.12.012 Marsh, 2004, Direct continuities between cisternae at different levels of the Golgi complex in glucose-stimulated mouse islet beta cells, Proc. Natl. Acad. Sci. USA, 101, 5565, 10.1073/pnas.0401242101 Martone, 2002, A cell-centered database for electron tomographic data, J. Struct. Biol., 138, 145, 10.1016/S1047-8477(02)00006-0 Martone, 1992, Ultrastructural examination of enkephalin and substance P input to cholinergic neurons within the rat neostriatum, Brain Res., 594, 253, 10.1016/0006-8993(92)91132-X Martone, 2003, The cell-centered database: a database for multiscale structural and protein localization data from light and electron microscopy, Neuroinformatics, 1, 379, 10.1385/NI:1:4:379 Masich, 2006, A procedure to deposit fiducial markers on vitreous cryo-sections for cellular tomography, J. Struct. Biol., 156, 461, 10.1016/j.jsb.2006.05.010 Mastronarde, 1997, Dual-axis tomography: an approach with alignment methods that preserve resolution, J. Struct. Biol., 120, 343, 10.1006/jsbi.1997.3919 McDonald, 1999, High-pressure freezing for preservation of high resolution fine structure and antigenicity for immunolabeling, Methods Mol. Biol., 117, 77 McDonald, K.L., Auer, M., 2006. High-pressure freezing, cellular tomography, and structural cell biology. Biotechniques. 41:137, 139, 141 passim. Miller, 2001, Flock house virus RNA replicates on outer mitochondrial membranes in Drosophila cells, J. Virol., 75, 11664, 10.1128/JVI.75.23.11664-11676.2001 Mobius, 2002, Immunoelectron microscopic localization of cholesterol using biotinylated and non-cytolytic perfringolysin O, J. Histochem. Cytochem., 50, 43, 10.1177/002215540205000105 Monaghan, 1998, High-pressure freezing for immunocytochemistry, J. Microsc., 192, 248, 10.1046/j.1365-2818.1998.00387.x Moor, H., 1987. Theory and practice of high pressure freezing. In: R.A.Z. Steinbrecht, K., (Ed.), Springer-Verlag, Berlin. pp. 175–191. Moor, 1980, The influence of high pressure freezing on mammalian nerve tissue, Cell Tissue Res., 209, 201, 10.1007/BF00237626 Murk, 2003, Influence of aldehyde fixation on the morphology of endosomes and lysosomes: quantitative analysis and electron tomography, J. Microsc., 212, 81, 10.1046/j.1365-2818.2003.01238.x Nicolas, 1997, In situ localization of two fibrillar collagens in two compact connective tissues by immunoelectron microscopy after cryotechnical processing, J. Histochem. Cytochem., 45, 119, 10.1177/002215549704500115 Peters, 1991 Potrebic, 2003, Peptidergic nociceptors of both trigeminal and dorsal root ganglia express serotonin 1D receptors: implications for the selective antimigraine action of triptans, J. Neurosci., 23, 10988, 10.1523/JNEUROSCI.23-34-10988.2003 Reipert, 2004, High-pressure cryoimmobilization of murine skin reveals novel structural features and prevents extraction artifacts, Exp Dermatol., 13, 419, 10.1111/j.0906-6705.2004.00180.x Rostaing, 2006, Analysis of synaptic ultrastructure without fixative using high-pressure freezing and tomography, Eur. J. Neurosci., 24, 3463, 10.1111/j.1460-9568.2006.05234.x Schwab, 1997, The distribution of normal brain water content in Wistar rats and its increase due to ischemia, Brain Res., 749, 82, 10.1016/S0006-8993(96)01165-1 Senda, 2005, Visualization of the nuclear lamina in mouse anterior pituitary cells and immunocytochemical detection of lamin A/C by quick-freeze freeze-substitution electron microscopy, J. Histochem. Cytochem., 53, 497, 10.1369/jhc.4A6478.2005 Shimoni, 1998, On optimizing high-pressure freezing: from heat transfer theory to a new microbiopsy device, J. Microsc., 192, 236, 10.1046/j.1365-2818.1998.00389.x Siksou, 2007, Three-dimensional architecture of presynaptic terminal cytomatrix, J. Neurosci., 27, 6868, 10.1523/JNEUROSCI.1773-07.2007 Small, 1981, Organization of actin in the leading edge of cultured cells: influence of osmium tetroxide and dehydration on the ultrastructure of actin meshworks, J. Cell Biol., 91, 695, 10.1083/jcb.91.3.695 Sosinsky, 2005, Development of a model for microphysiological simulations: small nodes of Ranvier from peripheral nerves of mice reconstructed by electron tomography, Neuroinformatics, 3, 133, 10.1385/NI:3:2:133 Sosinsky, 2007, Markers for correlated light and electron microscopy, vol. 79, 573 Studer, 1995, Vitrification of articular cartilage by high-pressure freezing, J. Microsc., 179, 321, 10.1111/j.1365-2818.1995.tb03648.x Van Harreveld, 1964, Electron microscopy after rapid freezing on a metal surface and substitution fixation, Anat. Rec., 149, 381, 10.1002/ar.1091490307 Van Harreveld, 1965, A study of extracellular space in central nervous tissue by freeze-substitution, J Cell Biol., 25, 117, 10.1083/jcb.25.1.117 Vanhecke, 2006, A new microbiopsy system enables rapid preparation of tissue for high-pressure freezing, Methods Mol. Biol., 319, 463, 10.1007/978-1-59259-993-6_21 Vanhecke, 2003, A rapid microbiopsy system to improve the preservation of biological samples prior to high-pressure freezing, J. Microsc., 212, 3, 10.1046/j.1365-2818.2003.01226.x Wang, 2004, Activity-dependent dynamics of coexisting brain-derived neurotrophic factor, pro-opiomelanocortin and alpha-melanophore-stimulating hormone in melanotrope cells of Xenopus laevis, J. Neuroendocrinol., 16, 19, 10.1111/j.1365-2826.2004.01110.x Zechmann, 2007, Membrane associated qualitative differences in cell ultrastructure of chemically and high pressure cryofixed plant cells, J. Struct. Biol., 158, 370, 10.1016/j.jsb.2006.12.003 Zuber, 2005, The mammalian central nervous synaptic cleft contains a high density of periodically organized complexes, Proc. Natl. Acad. Sci. USA, 102, 19192, 10.1073/pnas.0509527102