Relative merits and limiting factors for x-ray and electron microscopy of thick, hydrated organic materials

Du, Ming; Jacobsen, Chris

doi:10.1016/j.ultramic.2017.10.003

Title: Relative merits and limiting factors for x-ray and electron microscopy of thick, hydrated organic materials

Journal Article · 06 October 2017 · Ultramicroscopy

DOI: https://doi.org/10.1016/j.ultramic.2017.10.003 · OSTI ID:1411044

Du, Ming ^[1]; Jacobsen, Chris ^[2]

Northwestern Univ., Evanston, IL (United States)
Argonne National Lab. (ANL), Argonne, IL (United States); Northwestern Univ., Evanston, IL (United States)

Electron and x-ray microscopes allow one to image the entire, unlabeled structure of hydrated materials at a resolution well beyond what visible light microscopes can achieve. However, both approaches involve ionizing radiation, so that radiation damage must be considered as one of the limits to imaging. Drawing upon earlier work, we describe here a unified approach to estimating the image contrast (and thus the required exposure and corresponding radiation dose) in both x-ray and electron microscopy. This approach accounts for factors such as plural and inelastic scattering, and (in electron microscopy) the use of energy filters to obtain so-called "zero loss" images. As expected, it shows that electron microscopy offers lower dose for specimens thinner than about 1 mu m (such as for studies of macromolecules, viruses, bacteria and archaebacteria, and thin sectioned material), while x-ray microscopy offers superior characteristics for imaging thicker specimen such as whole eukaryotic cells, thick-sectioned tissues, and organs. The required radiation dose scales strongly as a function of the desired spatial resolution, allowing one to understand the limits of live and frozen hydrated specimen imaging. Lastly, we consider the factors limiting x-ray microscopy of thicker materials, suggesting that specimens as thick as a whole mouse brain can be imaged with x-ray microscopes without significant image degradation should appropriate image reconstruction methods be identified.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22), Scientific User Facilities Division

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1411044

Journal Information:: Ultramicroscopy, Journal Name: Ultramicroscopy Journal Issue: PA Vol. 184; ISSN 0304-3991

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (102)

Spiegelsysteme streifenden Einfalls als abbildende Optiken für Röntgenstrahlen Wolter, Hans Annalen der Physik, Vol. 445, Issue 1-2 https://doi.org/10.1002/andp.19524450108	journal	January 1952
Optimum energies for x-ray transmission tomography of small samples Grodzins, L. Nuclear Instruments and Methods in Physics Research, Vol. 206, Issue 3 https://doi.org/10.1016/0167-5087(83)90393-9	journal	March 1983
Some remarks concerning the influence of electron noise on 3D reconstruction Hoppe, W.; Hegerl, R. Ultramicroscopy, Vol. 6, Issue 2 https://doi.org/10.1016/0304-3991(81)90062-0	journal	January 1981
Electron Tomography of Ice-Embedded Prokaryotic Cells Grimm, Rudo; Singh, Hapreet; Rachel, Reinhard Biophysical Journal, Vol. 74, Issue 2 https://doi.org/10.1016/s0006-3495(98)74028-7	journal	February 1998
Phase contrast, a new method for the microscopic observation of transparent objects part II Zernike, F. Physica, Vol. 9, Issue 10 https://doi.org/10.1016/s0031-8914(42)80079-8	journal	December 1942
Transmission microscopy of unmodified biological materials. Comparative radiation dosages with electrons and ultrasoft X-ray photons Sayre, D.; Kirz, J.; Feder, R. Ultramicroscopy, Vol. 2 https://doi.org/10.1016/s0304-3991(76)91997-5	journal	January 1976
Reconstruction of glutamine synthetase using computer averaging Frank, J.; Goldfarb, W.; Eisenberg, D. Ultramicroscopy, Vol. 3 https://doi.org/10.1016/s0304-3991(78)80038-2	journal	January 1978
Tomographic brain imaging with nucleolar detail and automatic cell counting Hieber, Simone E.; Bikis, Christos; Khimchenko, Anna Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep32156	journal	September 2016
Invited Review Article: Methods for imaging weak-phase objects in electron microscopy Glaeser, Robert M. Review of Scientific Instruments, Vol. 84, Issue 11 https://doi.org/10.1063/1.4830355	journal	November 2013
Atomic form factors, incoherent scattering functions, and photon scattering cross sections Hubbell, J. H.; Veigele, Wm. J.; Briggs, E. A. Journal of Physical and Chemical Reference Data, Vol. 4, Issue 3 https://doi.org/10.1063/1.555523	journal	July 1975
Dose requirements for resolving a given feature in an object by coherent x-ray diffraction imaging Schropp, Andreas; Schroer, Christian G. New Journal of Physics, Vol. 12, Issue 3 https://doi.org/10.1088/1367-2630/12/3/035016	journal	March 2010
Electron microscopy of frozen water and aqueous solutions Dubochet, J.; Lepault, J.; Freeman, R. Journal of Microscopy, Vol. 128, Issue 3 https://doi.org/10.1111/j.1365-2818.1982.tb04625.x	journal	December 1982
Macromolecular Architecture in Eukaryotic Cells Visualized by Cryoelectron Tomography Medalia, O. Science, Vol. 298, Issue 5596 https://doi.org/10.1126/science.1076184	journal	November 2002
Computer averaging of electron micrographs of 40S ribosomal subunits Frank, J.; Verschoor, A.; Boublik, M. Science, Vol. 214, Issue 4527 https://doi.org/10.1126/science.7313694	journal	December 1981
Potential operating region for ultrasoft x-ray microscopy of biological materials Sayre, D.; Kirz, J.; Feder, R. Science, Vol. 196, Issue 4296 https://doi.org/10.1126/science.867033	journal	June 1977
The LD ₅₀ for uniform low LET irradiation of man Mole, R. H. The British Journal of Radiology, Vol. 57, Issue 677 https://doi.org/10.1259/0007-1285-57-677-355	journal	May 1984
Berechnung der differentiellen Wirkungsquerschnitte für die Streuung mittelschneller Elektronen an Atomen aus Hartree-Funktionen Wyrwich, Herbert; Lenz, Friedrich Zeitschrift für Naturforschung A, Vol. 13, Issue 7 https://doi.org/10.1515/zna-1958-0705	journal	July 1958
Miniature Pig Performance after Fractionated Supralethal Doses of Ionizing Radiation Chaput, Raymond L.; Kovacic, Roger T. Radiation Research, Vol. 44, Issue 3 https://doi.org/10.2307/3573158	journal	December 1970
A Unified Approach to the Performance of Photographic Film, Television Pickup Tubes, and the Human Eye Rose, Albert Journal of the Society of Motion Picture Engineers, Vol. 47, Issue 4 https://doi.org/10.5594/j12772	journal	October 1946
Theorie der Beugung von Elektronen an Kristallen Bethe, H. Annalen der Physik, Vol. 392, Issue 17 https://doi.org/10.1002/andp.19283921704	journal	January 1928
Spiegelsysteme streifenden Einfalls als abbildende Optiken für Röntgenstrahlen Wolter, Hans Annalen der Physik, Vol. 445, Issue 1-2 https://doi.org/10.1002/andp.19524450108	journal	January 1952
X-Ray Interactions: Photoabsorption, Scattering, Transmission, and Reflection at E = 50-30,000 eV, Z = 1-92 Henke, B. L.; Gullikson, E. M.; Davis, J. C. Atomic Data and Nuclear Data Tables, Vol. 54, Issue 2, p. 181-342 https://doi.org/10.1006/adnd.1993.1013	journal	July 1993
Making Soft X-Ray Microscopy Harder: Considerations for Sub-0.1 µm Resolution Imaging at ~ 4 Å Wavelengths Jacobsen, C. X-Ray Microscopy III https://doi.org/10.1007/978-3-540-46887-5_62	book	January 1992
Calculations on Radiation Dosages of Biological Materials in Phase Contrast and Amplitude Contrast X-Ray Microscopy Gölz, P. X-Ray Microscopy III https://doi.org/10.1007/978-3-540-46887-5_71	book	January 1992
Optimum energies for x-ray transmission tomography of small samples Grodzins, L. Nuclear Instruments and Methods in Physics Research, Vol. 206, Issue 3 https://doi.org/10.1016/0167-5087(83)90393-9	journal	March 1983
Quantitative energy-filtered electron microscopy of biological molecules in ice Langmore, John P.; Smith, Michael F. Ultramicroscopy, Vol. 46, Issue 1-4 https://doi.org/10.1016/0304-3991(92)90024-E	journal	October 1992
Cryo-electron energy loss spectroscopy: observations on vitrified hydrated specimens and radiation damage Leapman, Richard D.; Sun, Songquan Ultramicroscopy, Vol. 59, Issue 1-4 https://doi.org/10.1016/0304-3991(95)00019-W	journal	July 1995
The relevance of dose-fractionation in tomography of radiation-sensitive specimens McEwen, Bruce F.; Downing, Kenneth H.; Glaeser, Robert M. Ultramicroscopy, Vol. 60, Issue 3 https://doi.org/10.1016/0304-3991(95)00082-8	journal	October 1995
Zero-loss energy filtering as improved imaging mode in cryoelectronmicroscopy of frozen-hydrated specimens Schröder, Rasmus R.; Hofmann, Waltraud; Ménétret, Jean-François Journal of Structural Biology, Vol. 105, Issue 1-3 https://doi.org/10.1016/1047-8477(90)90095-T	journal	October 1990
Electron Tomography of Ice-Embedded Prokaryotic Cells Grimm, Rudo; Singh, Hapreet; Rachel, Reinhard Biophysical Journal, Vol. 74, Issue 2 https://doi.org/10.1016/S0006-3495(98)74028-7	journal	February 1998
Limitations to significant information in biological electron microscopy as a result of radiation damage Glaeser, Robert M. Journal of Ultrastructure Research, Vol. 36, Issue 3-4 https://doi.org/10.1016/S0022-5320(71)80118-1	journal	August 1971
Beugungstheorie des schneidenver-fahrens und seiner verbesserten form, der phasenkontrastmethode Zernike, von F. Physica, Vol. 1, Issue 7-12 https://doi.org/10.1016/S0031-8914(34)80259-5	journal	May 1934
Phase contrast, a new method for the microscopic observation of transparent objects Zernike, F. Physica, Vol. 9, Issue 7 https://doi.org/10.1016/S0031-8914(42)80035-X	journal	July 1942
Phase contrast, a new method for the microscopic observation of transparent objects part II Zernike, F. Physica, Vol. 9, Issue 10 https://doi.org/10.1016/S0031-8914(42)80079-8	journal	December 1942
Transmission microscopy of unmodified biological materials. Comparative radiation dosages with electrons and ultrasoft X-ray photons Sayre, D.; Kirz, J.; Feder, R. Ultramicroscopy, Vol. 2 https://doi.org/10.1016/S0304-3991(76)91997-5	journal	January 1976
Reconstruction of glutamine synthetase using computer averaging Frank, J.; Goldfarb, W.; Eisenberg, D. Ultramicroscopy, Vol. 3 https://doi.org/10.1016/S0304-3991(78)80038-2	journal	January 1978
Some remarks concerning the influence of electron noise on 3D reconstruction Hoppe, W.; Hegerl, R. Ultramicroscopy, Vol. 6, Issue 1 https://doi.org/10.1016/S0304-3991(81)80200-8	journal	January 1981
Cryo X-ray microscopy with high spatial resolution in amplitude and phase contrast Schneider, Gerd Ultramicroscopy, Vol. 75, Issue 2 https://doi.org/10.1016/S0304-3991(98)00054-0	journal	November 1998
A new atomic database for X-ray spectroscopic calculations Elam, W. T.; Ravel, B. D.; Sieber, J. R. Radiation Physics and Chemistry, Vol. 63, Issue 2 https://doi.org/10.1016/S0969-806X(01)00227-4	journal	February 2002
Advantages of intermediate X-ray energies in Zernike phase contrast X-ray microscopy Wang, Zhili; Gao, Kun; Chen, Jian Biotechnology Advances, Vol. 31, Issue 3 https://doi.org/10.1016/j.biotechadv.2012.04.001	journal	May 2013
An assessment of the resolution limitation due to radiation-damage in X-ray diffraction microscopy Howells, M. R.; Beetz, T.; Chapman, H. N. Journal of Electron Spectroscopy and Related Phenomena, Vol. 170, Issue 1-3 https://doi.org/10.1016/j.elspec.2008.10.008	journal	March 2009
Retrospective: Radiation damage and its associated “Information Limitations” Glaeser, Robert M. Journal of Structural Biology, Vol. 163, Issue 3 https://doi.org/10.1016/j.jsb.2008.06.001	journal	September 2008
The xraylib library for X-ray–matter interactions. Recent developments Schoonjans, Tom; Brunetti, Antonio; Golosio, Bruno Spectrochimica Acta Part B: Atomic Spectroscopy, Vol. 66, Issue 11-12 https://doi.org/10.1016/j.sab.2011.09.011	journal	November 2011
Fourier-ratio deconvolution techniques for electron energy-loss spectroscopy (EELS) Wang, Feng; Egerton, Ray; Malac, Marek Ultramicroscopy, Vol. 109, Issue 10 https://doi.org/10.1016/j.ultramic.2009.05.011	journal	September 2009
Optimizing detector geometry for trace element mapping by X-ray fluorescence Sun, Yue; Gleber, Sophie-Charlotte; Jacobsen, Chris Ultramicroscopy, Vol. 152 https://doi.org/10.1016/j.ultramic.2014.12.014	journal	May 2015
The potential and limitations of neutrons, electrons and X-rays for atomic resolution microscopy of unstained biological molecules Henderson, Richard Quarterly Reviews of Biophysics, Vol. 28, Issue 2 https://doi.org/10.1017/S003358350000305X	journal	May 1995
Soft X-ray microscopes and their biological applications Kirz, Janos; Jacobsen, Chris; Howells, Malcolm Quarterly Reviews of Biophysics, Vol. 28, Issue 1 https://doi.org/10.1017/S0033583500003139	journal	February 1995
Cryo-electron microscopy of vitrified specimens Dubochet, Jacques; Adrian, Marc; Chang, Jiin-Ju Quarterly Reviews of Biophysics, Vol. 21, Issue 2 https://doi.org/10.1017/S0033583500004297	journal	May 1988
Structural Changes In Cells Imaged by Soft X-ray Cryo-Tomography During Hepatitis C Virus Infection Pérez-Berná, Ana Joaquina; Rodríguez, Maria José; Chichón, Francisco Javier ACS Nano, Vol. 10, Issue 7 https://doi.org/10.1021/acsnano.6b01374	journal	June 2016
Spectromicroscopy of Poly(ethylene terephthalate): Comparison of Spectra and Radiation Damage Rates in X-ray Absorption and Electron Energy Loss Rightor, E. G.; Hitchcock, A. P.; Ade, H. The Journal of Physical Chemistry B, Vol. 101, Issue 11 https://doi.org/10.1021/jp9622748	journal	March 1997
Potential for biomolecular imaging with femtosecond X-ray pulses Neutze, Richard; Wouts, Remco; van der Spoel, David Nature, Vol. 406, Issue 6797 https://doi.org/10.1038/35021099	journal	August 2000
Electron tomography reveals unbranched networks of actin filaments in lamellipodia Urban, Edit; Jacob, Sonja; Nemethova, Maria Nature Cell Biology, Vol. 12, Issue 5 https://doi.org/10.1038/ncb2044	journal	April 2010
X-ray ptychographic and fluorescence microscopy of frozen-hydrated cells using continuous scanning Deng, Junjing; Vine, David J.; Chen, Si Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-00569-y	journal	March 2017
Tomographic brain imaging with nucleolar detail and automatic cell counting Hieber, Simone E.; Bikis, Christos; Khimchenko, Anna Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep32156	journal	September 2016
Three-dimensional X-ray visualization of axonal tracts in mouse brain hemisphere Mizutani, Ryuta; Saiga, Rino; Ohtsuka, Masato Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep35061	journal	October 2016
Zero‐loss energy filtering under low‐dose conditions using a post‐column energy filter Grimm, R.; Koster, A. J.; Ziese, U. Journal of Microscopy, Vol. 183, Issue 1 https://doi.org/10.1046/j.1365-2818.1996.77441.x	journal	July 1996
Soft X-ray microscopy with a cryo scanning transmission X-ray microscope: I. Instrumentation, imaging and spectroscopy Journal of Microscopy, Vol. 197, Issue 1 https://doi.org/10.1046/j.1365-2818.2000.00630.x	journal	January 2000
Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. SHORT COMMUNICATION Gustafsson, M. G. L. Journal of Microscopy, Vol. 198, Issue 2 https://doi.org/10.1046/j.1365-2818.2000.00710.x	journal	May 2000
Ultrafast electron microscopy in materials science, biology, and chemistry King, Wayne E.; Campbell, Geoffrey H.; Frank, Alan Journal of Applied Physics, Vol. 97, Issue 11 https://doi.org/10.1063/1.1927699	journal	June 2005
Invited Review Article: Methods for imaging weak-phase objects in electron microscopy Glaeser, Robert M. Review of Scientific Instruments, Vol. 84, Issue 11 https://doi.org/10.1063/1.4830355	journal	November 2013
Atomic form factors, incoherent scattering functions, and photon scattering cross sections Hubbell, J. H.; Veigele, Wm. J.; Briggs, E. A. Journal of Physical and Chemical Reference Data, Vol. 4, Issue 3 https://doi.org/10.1063/1.555523	journal	July 1975
Pair, Triplet, and Total Atomic Cross Sections (and Mass Attenuation Coefficients) for 1 MeV‐100 GeV Photons in Elements Z =1 to 100 Hubbell, J. H.; Gimm, H. A.; O/verbo/, I. Journal of Physical and Chemical Reference Data, Vol. 9, Issue 4 https://doi.org/10.1063/1.555629	journal	October 1980
Experimental determination of the radiation dose limit for cryocooled protein crystals Owen, R. L.; Rudino-Pinera, E.; Garman, E. F. Proceedings of the National Academy of Sciences, Vol. 103, Issue 13 https://doi.org/10.1073/pnas.0600973103	journal	March 2006
Studies of Insulin Crystals at low Temperatures: Effects on Mosaic Character and Radiation Sensitivity Low, B. W.; Chen, C. C. H.; Berger, J. E. Proceedings of the National Academy of Sciences, Vol. 56, Issue 6 https://doi.org/10.1073/pnas.56.6.1746	journal	December 1966
CXVII. The total reflexion of X-rays Compton, Arthur H. The London, Edinburgh, and Dublin Philosophical Magazine and Journal of Science, Vol. 45, Issue 270 https://doi.org/10.1080/14786442308634208	journal	June 1923
Determination of the single-scattering probability distribution from plural-scattering data Johnson, D. W.; Spence, J. C. H. Journal of Physics D: Applied Physics, Vol. 7, Issue 6 https://doi.org/10.1088/0022-3727/7/6/304	journal	April 1974
Dose requirements for resolving a given feature in an object by coherent x-ray diffraction imaging Schropp, Andreas; Schroer, Christian G. New Journal of Physics, Vol. 12, Issue 3 https://doi.org/10.1088/1367-2630/12/3/035016	journal	March 2010
X-ray Tomography Generates 3-D Reconstructions of the Yeast, Saccharomyces cerevisiae , at 60-nm Resolution Larabell, Carolyn A.; Le Gros, Mark A. Molecular Biology of the Cell, Vol. 15, Issue 3 https://doi.org/10.1091/mbc.e03-07-0522	journal	March 2004
SASBDB, a repository for biological small-angle scattering data Valentini, Erica; Kikhney, Alexey G.; Previtali, Gianpietro Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1047	journal	October 2014
The Reconstruction of a Three-Dimensional Structure from Projections and its Application to Electron Microscopy Crowther, R. A.; DeRosier, D. J.; Klug, A. Proceedings of the Royal Society A: Mathematical, Physical and Engineering Sciences, Vol. 317, Issue 1530 https://doi.org/10.1098/rspa.1970.0119	journal	June 1970
Cryo-protection of protein crystals against radiation damage in electron and X-ray diffraction Henderson, Richard Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 241, Issue 1300, p. 6-8 https://doi.org/10.1098/rspb.1990.0057	journal	July 1990
Crystallographic studies on lactate dehydrogenase at –75°C Haas, D. J.; Rossmann, M. G. Acta Crystallographica Section B Structural Crystallography and Crystal Chemistry, Vol. 26, Issue 7 https://doi.org/10.1107/S0567740870003485	journal	July 1970
Soft X-ray radiation-damage studies in PMMA using a cryo-STXM Beetz, Tobias; Jacobsen, Chris Journal of Synchrotron Radiation, Vol. 10, Issue 3 https://doi.org/10.1107/S0909049503003261	journal	April 2003
Diffractive imaging of nonperiodic materials with future coherent X-ray sources Shen, Qun; Bazarov, Ivan; Thibault, Pierre Journal of Synchrotron Radiation, Vol. 11, Issue 5 https://doi.org/10.1107/S0909049504016772	journal	August 2004
Dose, exposure time and resolution in serial X-ray crystallography Starodub, D.; Rez, P.; Hembree, G. Journal of Synchrotron Radiation, Vol. 15, Issue 1 https://doi.org/10.1107/S0909049507048893	journal	December 2007
Coherent diffractive imaging: towards achieving atomic resolution Dietze, S. H.; Shpyrko, O. G. Journal of Synchrotron Radiation, Vol. 22, Issue 6 https://doi.org/10.1107/S1600577515017336	journal	October 2015
Amplitude and phase contrast in electron-microscope images of molecular structures Johnson, D. J. Journal of the Royal Microscopical Society, Vol. 88, Issue 1 https://doi.org/10.1111/j.1365-2818.1968.tb00596.x	journal	February 1968
Phase contrast electron microscopy of biological materials Unwin, P. N. T. Journal of Microscopy, Vol. 98, Issue 3 https://doi.org/10.1111/j.1365-2818.1973.tb03834.x	journal	August 1973
Defocusing phase contrast effects in electron microscopy Johnson, D. J.; Crawford, D. Journal of Microscopy, Vol. 98, Issue 3 https://doi.org/10.1111/j.1365-2818.1973.tb03835.x	journal	August 1973
Electron microscopy of frozen water and aqueous solutions Dubochet, J.; Lepault, J.; Freeman, R. Journal of Microscopy, Vol. 128, Issue 3 https://doi.org/10.1111/j.1365-2818.1982.tb04625.x	journal	December 1982
Zero-loss energy-filtered imaging of frozen-hydrated proteins: model calculations and implications for future developments Schröder, R. R. Journal of Microscopy, Vol. 166, Issue 3 https://doi.org/10.1111/j.1365-2818.1992.tb01537.x	journal	June 1992
The effect of soft X-radiation on myofibrils Bennett, P. M.; Foster, G. F.; Buckley, C. J. Journal of Microscopy, Vol. 172, Issue 2 https://doi.org/10.1111/j.1365-2818.1993.tb03402.x	journal	November 1993
Comparative Analysis of X-Ray Emission Microscopies for Biological Specimens Kirz, Janos; Sayre, David; Dilger, James Annals of the New York Academy of Sciences, Vol. 306, Issue 1 Short Wavelen https://doi.org/10.1111/j.1749-6632.1978.tb25655.x	journal	March 1978
Photodecomposition of poly(methylmethacrylate) thin films by monochromatic soft x‐ray radiation Tinone, Marcia C. K.; Tanaka, Kenichiro; Ueno, Nobuo Journal of Vacuum Science & Technology A: Vacuum, Surfaces, and Films, Vol. 13, Issue 4 https://doi.org/10.1116/1.579675	journal	July 1995
Exposure strategies for polymethyl methacrylate from in situ x-ray absorption near edge structure spectroscopy Zhang, X. Journal of Vacuum Science & Technology B: Microelectronics and Nanometer Structures, Vol. 13, Issue 4 https://doi.org/10.1116/1.588175	journal	July 1995
Macromolecular Architecture in Eukaryotic Cells Visualized by Cryoelectron Tomography Medalia, O. Science, Vol. 298, Issue 5596 https://doi.org/10.1126/science.1076184	journal	November 2002
The Resolution Revolution Kuhlbrandt, W. Science, Vol. 343, Issue 6178 https://doi.org/10.1126/science.1251652	journal	March 2014
Chemical contrast in X-ray microscopy and spatially resolved XANES spectroscopy of organic specimens Ade, H.; Zhang, X.; Cameron, S. Science, Vol. 258, Issue 5084 https://doi.org/10.1126/science.1439809	journal	November 1992
Molecular Microscopy: Fundamental Limitations Breedlove, J. R.; Trammell, G. T. Science, Vol. 170, Issue 3964 https://doi.org/10.1126/science.170.3964.1310	journal	December 1970
Electron Diffraction of Frozen, Hydrated Protein Crystals Taylor, K. A.; Glaeser, R. M. Science, Vol. 186, Issue 4168 https://doi.org/10.1126/science.186.4168.1036	journal	December 1974
Microholography of Living Organisms Solem, J. C.; Baldwin, G. C. Science, Vol. 218, Issue 4569 https://doi.org/10.1126/science.218.4569.229	journal	October 1982
Computer averaging of electron micrographs of 40S ribosomal subunits Frank, J.; Verschoor, A.; Boublik, M. Science, Vol. 214, Issue 4527 https://doi.org/10.1126/science.7313694	journal	December 1981
Potential operating region for ultrasoft x-ray microscopy of biological materials Sayre, D.; Kirz, J.; Feder, R. Science, Vol. 196, Issue 4296 https://doi.org/10.1126/science.867033	journal	June 1977
Single-Particle Imaging of Macromolecules by Cryo-Electron Microscopy Frank, Joachim Annual Review of Biophysics and Biomolecular Structure, Vol. 31, Issue 1 https://doi.org/10.1146/annurev.biophys.31.082901.134202	journal	June 2002
The LD ₅₀ for uniform low LET irradiation of man Mole, R. H. The British Journal of Radiology, Vol. 57, Issue 677 https://doi.org/10.1259/0007-1285-57-677-355	journal	May 1984
Wavelength choice for soft x-ray laser holography of biological samples London, Richard A.; Rosen, Mordecai D.; Trebes, James E. Applied Optics, Vol. 28, Issue 16 https://doi.org/10.1364/AO.28.003397	journal	January 1989
Imaging biological specimens with high-intensity soft x rays Solem, Johndale C. Journal of the Optical Society of America B, Vol. 3, Issue 11 https://doi.org/10.1364/JOSAB.3.001551	journal	January 1986
Signal-to-noise and radiation exposure considerations in conventional and diffraction x-ray microscopy Huang, Xiaojing; Miao, Huijie; Steinbrener, Jan Optics Express, Vol. 17, Issue 16 https://doi.org/10.1364/OE.17.013541	journal	January 2009
Miniature Pig Performance after Fractionated Supralethal Doses of Ionizing Radiation Chaput, Raymond L.; Kovacic, Roger T. Radiation Research, Vol. 44, Issue 3 https://doi.org/10.2307/3573158	journal	December 1970
Electron Beam Excitation and Damage of Biological Molecules; Its Implications for Specimen Damage in Electron Microscopy Isaacson, M.; Johnson, D.; Crewe, A. V. Radiation Research, Vol. 55, Issue 2 https://doi.org/10.2307/3573678	journal	August 1973
Incapacitation and Performance Decrement in Rats Following Split Doses of Fission Spectrum Radiation Casarett, Alison P.; Comar, Cyril L. Radiation Research, Vol. 53, Issue 3 https://doi.org/10.2307/3573778	journal	March 1973
A Unified Approach to the Performance of Photographic Film, Television Pickup Tubes, and the Human Eye Rose, Albert Journal of the Society of Motion Picture Engineers, Vol. 47, Issue 4 https://doi.org/10.5594/J12772	journal	October 1946

Cited By (12)

Correlative 3D x-ray fluorescence and ptychographic tomography of frozen-hydrated green algae Deng, Junjing; Lo, Yuan Hung; Gallagher-Jones, Marcus Science Advances, Vol. 4, Issue 11 https://doi.org/10.1126/sciadv.aau4548	journal	November 2018
Three dimensions, two microscopes, one code: Automatic differentiation for x-ray nanotomography beyond the depth of focus limit Du, Ming; Nashed, Youssef S. G.; Kandel, Saugat Science Advances, Vol. 6, Issue 13 https://doi.org/10.1126/sciadv.aay3700	journal	March 2020
X-ray Microscopy Jacobsen, Chris Cambridge University Press https://doi.org/10.1017/9781139924542	book	January 2019
X-ray microscopy Cosslett, V. E. Reports on Progress in Physics, Vol. 28, Issue 1 https://doi.org/10.1088/0034-4885/28/1/311	journal	July 1965
Visualization of protein crystals by high-energy phase-contrast X-ray imaging Polikarpov, Maxim; Bourenkov, Gleb; Snigireva, Irina Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 11 https://doi.org/10.1107/s2059798319011379	journal	October 2019
3D x-ray imaging of continuous objects beyond the depth of focus limit Gilles, M. A.; Nashed, Y. S. G.; Du, M. Optica, Vol. 5, Issue 9 https://doi.org/10.1364/optica.5.001078	journal	January 2018
Multimodal x-ray nanotomography Gürsoy, Doğa; Jacobsen, Chris MRS Bulletin, Vol. 45, Issue 4 https://doi.org/10.1557/mrs.2020.85	journal	April 2020
Ab initio nonrigid X-ray nanotomography. Odstrcil, Michal; Holler, Mirko; Raabe, Jörg Springer Science and Business Media LLC https://doi.org/10.17863/cam.43115	journalarticle	January 2019
Visualization of protein crystals by high-energy phase-contrast X-ray imaging Polikarpov, Maxim; Bourenkov, Gleb; Snigireva, Irina FID GEO https://doi.org/10.23689/fidgeo-4718	text	January 2019
Visualization of protein crystals by high-energy phase-contrast X-ray imaging Polikarpov, Maxim; Bourenkov, Gleb; Snigireva, Irina Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2020-00013	text	January 2019
Ab initio nonrigid X-ray nanotomography Odstrcil, Michal; Holler, Mirko; Raabe, Jörg Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2020-00848	text	January 2019
X-ray microscopy Lider, V. V. Physics-Uspekhi, Vol. 60, Issue 2 https://doi.org/10.3367/ufne.2016.06.037830	journal	February 2017

Similar Records

Laboratory-Based Cryogenic Soft X-ray Tomography with Correlative Cryo-Light and Electron Microscopy

Journal Article · 2013 · Microscopy and Microanalysis, 19(1):22-29 · OSTI ID:1063698

Carlson, David B.; Gelb, Jeff; Palshin, Vadim; +1 more

The prospects for soft x-ray contact microscopy using laser plasmas as an x-ray source

Conference · 1995 · OSTI ID:379727

Stead, A D; Page, A M; Ford, T W

Plans for a scanning transmission x-ray microscope

Journal Article · 1979 · Ann. N.Y. Acad. Sci.; (United States) · OSTI ID:6590042

Kirz, J; Burg, R; Rarback, H

Related Subjects

36 MATERIALS SCIENCE
electron
radiation damage
thick specimen
x-ray

Title: Relative merits and limiting factors for x-ray and electron microscopy of thick, hydrated organic materials

Citation Formats

References (102)

Cited By (12)

Similar Records

Related Subjects