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      The 2018 correlative microscopy techniques roadmap

      review-article
      1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 , 9 , 10 , 4 , 11 , 12 , 13 , 4 , 14 , 15 , 16 , 17 , 18 , 19 , 10 , 20 , 10 , 17 , 18 , 21 , 22 , 23 , 24 , 22 , 23 , 25 , 26 , 23 , 27 , 28 , 29 , 30 , 31 , 23 , 2 , 2 , 10 , 32
      Journal of Physics D
      IOP Publishing
      correlative microscopy, fluorescence microscopy, x-ray microscopy, electron microscopy, magnetic resonance imaging, atomic force microscopy, super-resolution microscopy

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          Abstract

          Developments in microscopy have been instrumental to progress in the life sciences, and many new techniques have been introduced and led to new discoveries throughout the last century. A wide and diverse range of methodologies is now available, including electron microscopy, atomic force microscopy, magnetic resonance imaging, small-angle x-ray scattering and multiple super-resolution fluorescence techniques, and each of these methods provides valuable read-outs to meet the demands set by the samples under study. Yet, the investigation of cell development requires a multi-parametric approach to address both the structure and spatio-temporal organization of organelles, and also the transduction of chemical signals and forces involved in cell–cell interactions. Although the microscopy technologies for observing each of these characteristics are well developed, none of them can offer read-out of all characteristics simultaneously, which limits the information content of a measurement. For example, while electron microscopy is able to disclose the structural layout of cells and the macromolecular arrangement of proteins, it cannot directly follow dynamics in living cells. The latter can be achieved with fluorescence microscopy which, however, requires labelling and lacks spatial resolution. A remedy is to combine and correlate different readouts from the same specimen, which opens new avenues to understand structure–function relations in biomedical research. At the same time, such correlative approaches pose new challenges concerning sample preparation, instrument stability, region of interest retrieval, and data analysis. Because the field of correlative microscopy is relatively young, the capabilities of the various approaches have yet to be fully explored, and uncertainties remain when considering the best choice of strategy and workflow for the correlative experiment. With this in mind, the Journal of Physics D: Applied Physics presents a special roadmap on the correlative microscopy techniques, giving a comprehensive overview from various leading scientists in this field, via a collection of multiple short viewpoints.

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          Most cited references132

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          Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion.

          The morphology and cytoskeletal structure of fibroblasts, endothelial cells, and neutrophils are documented for cells cultured on surfaces with stiffness ranging from 2 to 55,000 Pa that have been laminated with fibronectin or collagen as adhesive ligand. When grown in sparse culture with no cell-cell contacts, fibroblasts and endothelial cells show an abrupt change in spread area that occurs at a stiffness range around 3,000 Pa. No actin stress fibers are seen in fibroblasts on soft surfaces, and the appearance of stress fibers is abrupt and complete at a stiffness range coincident with that at which they spread. Upregulation of alpha5 integrin also occurs in the same stiffness range, but exogenous expression of alpha5 integrin is not sufficient to cause cell spreading on soft surfaces. Neutrophils, in contrast, show no dependence of either resting shape or ability to spread after activation when cultured on surfaces as soft as 2 Pa compared to glass. The shape and cytoskeletal differences evident in single cells on soft compared to hard substrates are eliminated when fibroblasts or endothelial cells make cell-cell contact. These results support the hypothesis that mechanical factors impact different cell types in fundamentally different ways, and can trigger specific changes similar to those stimulated by soluble ligands. Copyright 2004 Wiley-Liss, Inc.
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            Nanometer resolution imaging and tracking of fluorescent molecules with minimal photon fluxes

            We introduce MINFLUX, a concept for localizing photon emitters in space. By probing the emitter with a local intensity minimum of excitation light, MINFLUX minimizes the fluorescence photons needed for high localization precision. In our experiments, 22 times fewer fluorescence photons are required as compared to popular centroid localization. In superresolution microscopy, MINFLUX attained ~1-nm precision, resolving molecules only 6 nanometers apart. MINFLUX tracking of single fluorescent proteins increased the temporal resolution and the number of localizations per trace by a factor of 100, as demonstrated with diffusing 30S ribosomal subunits in living Escherichia coli As conceptual limits have not been reached, we expect this localization modality to break new ground for observing the dynamics, distribution, and structure of macromolecules in living cells and beyond.
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              Fluorescence spectroscopy of single biomolecules.

              S. Weiss (1999)
              Recent advances in single-molecule detection and single-molecule spectroscopy at room temperature by laser-induced fluorescence offer new tools for the study of individual macromolecules under physiological conditions. These tools relay conformational states, conformational dynamics, and activity of single biological molecules to physical observables, unmasked by ensemble averaging. Distributions and time trajectories of these observables can therefore be measured during a reaction without the impossible need to synchronize all the molecules in the ensemble. The progress in applying these tools to biological studies with the use of fluorophores that are site-specifically attached to macromolecules is reviewed.
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                Author and article information

                Journal
                J Phys D Appl Phys
                J Phys D Appl Phys
                d
                JPAPBE
                Journal of Physics D
                IOP Publishing
                0022-3727
                7 November 2018
                31 August 2018
                : 51
                : 44
                : 443001
                Affiliations
                [1 ]Nano Life Science Institute (WPI-NanoLSI), Kanazawa University , Kanazawa, Japan
                [2 ]Department of Life Sciences & Chemistry, Jacobs University , Bremen, Germany
                [3 ]Ionovation GmbH , Osnabrück, Germany
                [4 ]MRC Human Immunology Unit, Weatherall Institute of Molecular Medicine, University of Oxford , Headley Way, OX3 9DS Oxford, United Kingdom
                [5 ]Francis Crick Institute , London, United Kingdom
                [6 ]INM—Leibniz Institute for New Materials , 66123 Saarbrücken, Germany
                [7 ]Saarland University , 66123 Saarbrücken, Germany
                [8 ]Dpto. Física de la Materia Condensada Universidad Autónoma de Madrid 28049, Madrid, Spain
                [9 ]Instituto de Física de la Materia Condensada IFIMAC , Universidad Autónoma de Madrid 28049, Madrid, Spain
                [10 ]KU Leuven , Department of Chemistry, B-3001 Heverlee, Belgium
                [11 ]Institute of Applied Optics, Friedrich-Schiller University , Jena, Germany
                [12 ]Leibniz Institute of Photonic Technology (IPHT) , Jena, Germany
                [13 ]Department of Mechanical Engineering, University of Wisconsin-Madison , 1513 University Ave, Madison, WI 53706, United States of America
                [14 ]Kennedy Institute for Rheumatology, University of Oxford , Oxford, United Kingdom
                [15 ]Debye Institute, Utrecht University , Utrecht, Netherlands
                [16 ]Department of Cell Biology, University of Groningen, University Medical Center Groningen , Groningen, Netherlands
                [17 ]Division of Structural Biology, Wellcome Trust Centre for Human Genetics, University of Oxford , Oxford, United Kingdom
                [18 ]Centre of Structural Systems Biology Hamburg and University of Hamburg , Hamburg, Germany
                [19 ]Heinrich-Pette-Institute, Leibniz Institute of Virology , Hamburg, Germany
                [20 ]Imaging Physics, Delft University of Technology , Delft, Netherlands
                [21 ]Department of Biochemistry, University of Oxford , Oxford, United Kingdom
                [22 ]Section Cell Biology, Center for Molecular Medicine, University Medical Center Utrecht, Utrecht University , Heidelberglaan 100, 3584CX Utrecht, Netherlands
                [23 ]Centre for Advanced Imaging, The University of Queensland , Brisbane, QLD 4072, Australia
                [24 ]University Hospital Jena , Jena, Germany
                [25 ]Faculty of Medicine, Saarland University , 66421 Homburg, Germany
                [26 ]University of Göttingen , Third Institute of Physics—Biophysics, 37077 Göttingen, Germany
                [27 ]KU Leuven , Department of Bioscience Engineering, B-3001 Heverlee, Belgium
                [28 ]University of Göttingen , Institute for X-Ray Physics, 37077 Göttingen, Germany
                [29 ]SmarAct GmbH , Schütte-Lanz-Str. 9, D-26135 Oldenburg, Germany
                [30 ]Institute for Theoretical Physics and BioQuant, Heidelberg University , Heidelberg, Germany
                [31 ]School of Biochemistry, University of Bristol , Bristol, United Kingdom
                [32 ]Department of Physiology, Anatomy and Genetics, University of Oxford , Oxford, United Kingdom
                christian.eggeling@ 123456rdm.ox.ac.uk
                J.P.Hoogenboom@ 123456tudelft.nl
                Schaap@ 123456smaract.com
                Author notes
                [33]

                Authors to whom any correspondence should be addressed.

                Author information
                http://orcid.org/0000-0001-8819-154X
                http://orcid.org/0000-0002-6585-3237
                http://orcid.org/0000-0003-2386-3186
                http://orcid.org/0000-0002-3698-5599
                http://orcid.org/0000-0003-4539-8772
                http://orcid.org/0000-0002-2181-9635
                http://orcid.org/0000-0003-4835-6228
                http://orcid.org/0000-0003-2654-9117
                http://orcid.org/0000-0001-9086-3835
                http://orcid.org/0000-0001-6665-5104
                Article
                daad055 aad055 JPhysD-116140.R1
                10.1088/1361-6463/aad055
                6372154
                30799880
                4e293e33-5b59-4b19-b226-a7b7c111927d
                © 2018 IOP Publishing Ltd

                Original content from this work may be used under the terms of the Creative Commons Attribution 3.0 licence. Any further distribution of this work must maintain attribution to the author(s) and the title of the work, journal citation and DOI.

                History
                : 9 February 2018
                : 14 June 2018
                : 1 July 2018
                : 19 June 2018
                : 31 August 2018
                Page count
                Pages: 42
                Funding
                Funded by: KU Leuven https://doi.org/10.13039/501100004040
                Award ID: C14/15/053
                Funded by: Nederlandse Organisatie voor Wetenschappelijk Onderzoek https://doi.org/10.13039/501100003246
                Award ID: ZonMW 91111.006
                Award ID: STW Microscopy Valley 12718
                Award ID: TTW1
                Award ID: projects 12713
                Award ID: 12714
                Award ID: 12715
                Funded by: Medical Research Council https://doi.org/10.13039/501100000265
                Award ID: FC001999
                Award ID: MC_UU_12010
                Award ID: MC_UU_12025
                Award ID: MR/K01577X/1
                Funded by: Fonds Wetenschappelijk Onderzoek https://doi.org/10.13039/501100003130
                Award ID: G.0197.11
                Award ID: G.0962.13
                Award ID: G0B39.15
                Award ID: ZW15_09 GOH6
                Funded by: Cancer Research UK https://doi.org/10.13039/501100000289
                Award ID: A17721 to E. Yvonne Jones
                Award ID: FC001999
                Funded by: H2020 European Research Council https://doi.org/10.13039/100010663
                Award ID: GA-307523
                Funded by: Wellcome Trust https://doi.org/10.13039/100004440
                Award ID: 104924/14/Z/14
                Award ID: 107806/Z/15/Z to KG
                Award ID: 107457/Z/15/Z to Micron Ox
                Funded by: Niedersachsen Israel framework
                Award ID: MWK-VWZN2722
                Funded by: Hercules foundation
                Award ID: HER/11/14
                Funded by: Marie Curie Cancer Care https://doi.org/10.13039/501100000654
                Award ID: GA-642196
                Funded by: Deutsche Forschungsgemeinschaft https://doi.org/10.13039/501100001659
                Award ID: BMBF project 05K16MG2
                Award ID: SFB 755 project B08
                Award ID: SFB 755 project C10
                Award ID: SFB 937 project A11
                Award ID: SFB 937 project A13
                Award ID: SFB1027
                Award ID: TRR 166 project B7
                Funded by: Flemish government
                Award ID: CASAS2
                Award ID: Meth/15/04
                Categories
                Topical Review
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                1361-6463/18/443001+42$33.00
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                correlative microscopy,fluorescence microscopy,x-ray microscopy,electron microscopy,magnetic resonance imaging,atomic force microscopy,super-resolution microscopy

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