• Chinese Journal of Lasers
  • Vol. 50, Issue 21, 2107102 (2023)
Weixing Li1, Jing Lu1, Ke Xiao1, and Wei Ji1、2、3、*
Author Affiliations
  • 1Key Laboratory of Interdisciplinary Research, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China
  • 2Innovative Development Center of Light Microscopy and Detection Technology, Bioland Laboratory, Guangzhou 510320, Guangdong, China
  • 3College of Life Science, University of Chinese Academy of Sciences, Beijing 100049, China
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    DOI: 10.3788/CJL230469 Cite this Article Set citation alerts
    Weixing Li, Jing Lu, Ke Xiao, Wei Ji. Recent Developments in Fluorescence-Guided Cryogenic Focused-Ion-Beam Milling[J]. Chinese Journal of Lasers, 2023, 50(21): 2107102 Copy Citation Text show less
    References

    [1] Turk M, Baumeister W. The promise and the challenges of cryo-electron tomography[J]. FEBS Letters, 594, 3243-3261(2020).

    [2] Hylton R K, Swulius M T. Challenges and triumphs in cryo-electron tomography[J]. iScience, 24, 102959(2021).

    [3] De Rosier D J, Klug A. Reconstruction of three dimensional structures from electron micrographs[J]. Nature, 217, 130-134(1968).

    [4] Dubochet J, Lepault J, Freeman R et al. Electron microscopy of frozen water and aqueous solutions[J]. Journal of Microscopy, 128, 219-237(1982).

    [5] Adrian M, Dubochet J, Lepault J et al. Cryo-electron microscopy of viruses[J]. Nature, 308, 32-36(1984).

    [6] Dubochet J, Adrian M, Lepault J et al. Emerging techniques: Cryo-electron microscopy of vitrified biological specimens[J]. Trends in Biochemical Sciences, 10, 143-146(1985).

    [7] Mahamid J, Baumeister W. Cryo-electron tomography: the realization of a vision[J]. Microscopy and Analysis, 26, 45-48(2012).

    [8] Beck M, Baumeister W. Cryo-electron tomography: can it reveal the molecular sociology of cells in atomic detail?[J]. Trends in Cell Biology, 26, 825-837(2016).

    [9] Oikonomou C M, Jensen G J. Cellular electron cryotomography: toward structural biology in situ[J]. Annual Review of Biochemistry, 86, 873-896(2017).

    [10] Lučič V, Rigort A, Baumeister W. Cryo-electron tomography: the challenge of doing structural biology in situ[J]. The Journal of Cell Biology, 202, 407-419(2013).

    [11] Shi S, Sun S, Andrews S B et al. Thickness measurement of hydrated and dehydrated cryosections by EELS[J]. Microscopy Research and Technique, 33, 241-250(1996).

    [12] Marko M, Hsieh C, Schalek R et al. Focused-ion-beam thinning of frozen-hydrated biological specimens for cryo-electron microscopy[J]. Nature Methods, 4, 215-217(2007).

    [13] Hsieh C, Schmelzer T, Kishchenko G et al. Practical workflow for cryo focused-ion-beam milling of tissues and cells for cryo-TEM tomography[J]. Journal of Structural Biology, 185, 32-41(2014).

    [14] Al-Amoudi A, Studer D, Dubochet J. Cutting artefacts and cutting process in vitreous sections for cryo-electron microscopy[J]. Journal of Structural Biology, 150, 109-121(2005).

    [15] Han H M, Zuber B, Dubochet J. Compression and crevasses in vitreous sections under different cutting conditions[J]. Journal of Microscopy, 230, 167-171(2008).

    [16] Villa E, Schaffer M, Plitzko J M et al. Opening windows into the cell: focused-ion-beam milling for cryo-electron tomography[J]. Current Opinion in Structural Biology, 23, 771-777(2013).

    [17] Rigort A, Plitzko J M. Cryo-focused-ion-beam applications in structural biology[J]. Archives of Biochemistry and Biophysics, 581, 122-130(2015).

    [18] Kuba J, Mitchels J, Hovorka M et al. Advanced cryo-tomography workflow developments-correlative microscopy, milling automation and cryo-lift-out[J]. Journal of Microscopy, 281, 112-124(2021).

    [19] Sartori A, Gatz R, Beck F et al. Correlative microscopy: bridging the gap between fluorescence light microscopy and cryo-electron tomography[J]. Journal of Structural Biology, 160, 135-145(2007).

    [20] Briegel A, Chen S Y, Koster A J et al. Correlated light and electron cryo-microscopy[J]. Methods in Enzymology, 481, 317-341(2010).

    [21] de Boer P, Hoogenboom J P, Giepmans B N G. Correlated light and electron microscopy: ultrastructure lights up![J]. Nature Methods, 12, 503-513(2015).

    [22] Karreman M A, Hyenne V, Schwab Y et al. Intravital correlative microscopy: imaging life at the nanoscale[J]. Trends in Cell Biology, 26, 848-863(2016).

    [23] van Driel L F, Valentijn J A, Valentijn K M et al. Tools for correlative cryo-fluorescence microscopy and cryo-electron tomography applied to whole mitochondria in human endothelial cells[J]. European Journal of Cell Biology, 88, 669-684(2009).

    [24] Jun S M, Ke D X, Debiec K et al. Direct visualization of HIV-1 with correlative live-cell microscopy and cryo-electron tomography[J]. Structure, 19, 1573-1581(2011).

    [25] Liu B, Xue Y H, Zhao W et al. Three-dimensional super-resolution protein localization correlated with vitrified cellular context[J]. Scientific Reports, 5, 1-11(2015).

    [26] Li S G, Ji G, Shi Y et al. High-vacuum optical platform for cryo-CLEM (HOPE): a new solution for non-integrated multiscale correlative light and electron microscopy[J]. Journal of Structural Biology, 201, 63-75(2018).

    [27] Moser F, Pražák V, Mordhorst V et al. Cryo-SOFI enabling low-dose super-resolution correlative light and electron cryo-microscopy[J]. Proceedings of the National Academy of Sciences of the United States of America, 116, 4804-4809(2019).

    [28] Rigort A, Kirmse R, Doring V et al. Imaging of vitrified biological specimens by confocal cryo-fluorescence microscopy and cryo-FIB/SEM tomography[J]. Microscopy and Microanalysis, 21, 1121-1122(2015).

    [29] Hoffman David P, Gleb S, Shan X C et al. Correlative three-dimensional super-resolution and block-face electron microscopy of whole vitreously frozen cells[J]. Science, 367, eaaz5357(2020).

    [30] Rigort A, Villa E, Bäuerlein F J B et al. Integrative approaches for cellular cryo-electron tomography: correlative imaging and focused ion beam micromachining[J]. Methods in Cell Biology, 111, 259-281(2012).

    [31] Huang B Q, Yeung E C. Chemical and physical fixation of cells and tissues: an overview[M]. Yeung E C T, Stasolla C, Sumner M J, et al. Plant microtechniques and protocols, 23-43(2015).

    [32] Moor H. Theory and practice of high pressure freezing[M]. Steinbrecht R A, Zierold K. Cryotechniques in biological electron microscopy, 175-191(1987).

    [33] Galway M E, Heckman J W, Jr, Hyde G J et al. Advances in high-pressure and plunge-freeze fixation[M]. Methods in cell biology, 3-19(1995).

    [34] Mielanczyk L, Matysiak N, Michalski M et al. Closer to the native state. Critical evaluation of cryo-techniques for Transmission Electron Microscopy: preparation of biological samples[J]. Folia Histochemica et Cytobiologica, 52, 1-17(2014).

    [35] Kanno H, Speedy R J, Angell C A. Supercooling of water to -92 ℃ under pressure[J]. Science, 189, 880-881(1975).

    [36] Handley D A, Alexander J T, Chien S. The design and use of a simple device for rapid quench-freezing of biological samples[J]. Journal of Microscopy, 121, 273-282(1981).

    [37] Dubochet J, McDowall A W, Menge B et al. Electron microscopy of frozen-hydrated bacteria[J]. Journal of Bacteriology, 155, 381-390(1983).

    [38] McDowall A W, Chang J J, Freeman R et al. Electron microscopy of frozen hydrated sections of vitreous ice and vitrified biological samples[J]. Journal of Microscopy, 131, 1-9(1983).

    [39] McDowall A W, Hofmann W, Lepault J et al. Cryo-electron microscopy of vitrified insect flight muscle[J]. Journal of Molecular Biology, 178, 105-111(1984).

    [40] Iancu C V, Tivol W F, Schooler J B et al. Electron cryotomography sample preparation using the Vitrobot[J]. Nature Protocols, 1, 2813-2819(2006).

    [41] Dobro M J, Melanson L A, Jensen G J et al. Plunge freezing for electron cryomicroscopy[J]. Methods in Enzymology, 481, 63-82(2010).

    [42] Swanson L W. Liquid metal ion sources: mechanism and applications[J]. Nuclear Instruments and Methods in Physics Research, 218, 347-353(1983).

    [43] Smith N S, Skoczylas W P, Kellogg S M et al. High brightness inductively coupled plasma source for high current focused ion beam applications[J]. Journal of Vacuum Science & Technology B: Microelectronics and Nanometer Structures, 24, 2902-2906(2006).

    [44] Orloff J. High‐resolution focused ion beams[J]. Review of Scientific Instruments, 64, 1105-1130(1993).

    [45] Giannuzzi L A, Stevie F A[M]. Introduction to focused ion beams instrumentation, theory, techniques and practice(2004).

    [46] Jin C Y, Wu W, Cao L et al. Fabrication of lithium niobate metasurfaces via a combination of FIB and ICP-RIE[J]. Chinese Optics Letters, 20, 113602(2022).

    [47] Dubochet J, Booy F P, Freeman R et al. Low temperature electron microscopy[J]. Annual Review of Biophysics and Bioengineering, 10, 133-149(1981).

    [48] Marko M, Hsieh C, Moberlychan W et al. Focused ion beam milling of vitreous water: prospects for an alternative to cryo-ultramicrotomy of frozen-hydrated biological samples[J]. Journal of Microscopy, 222, 42-47(2006).

    [49] Rigort A, Bäuerlein F J B, Villa E et al. Focused ion beam micromachining of eukaryotic cells for cryoelectron tomography[J]. Proceedings of the National Academy of Sciences of the United States of America, 109, 4449-4454(2012).

    [50] Rigort A, Bäuerlein F J B, Leis A et al. Micromachining tools and correlative approaches for cellular cryo-electron tomography[J]. Journal of Structural Biology, 172, 169-179(2010).

    [51] Schaffer M, Engel B D, Laugks T et al. Cryo-focused ion beam sample preparation for imaging vitreous cells by cryo-electron tomography[J]. Bio-protocol, 5, e1575(2015).

    [52] Medeiros J M, Böck D, Weiss G L et al. Robust workflow and instrumentation for cryo-focused ion beam milling of samples for electron cryotomography[J]. Ultramicroscopy, 190, 1-11(2018).

    [53] Hayles M F, Stokes D J, Phifer D et al. A technique for improved focused ion beam milling of cryo-prepared life science specimens[J]. Journal of Microscopy, 226, 263-269(2007).

    [54] Wolff G, Limpens R W A L, Zheng S et al. Mind the gap: micro-expansion joints drastically decrease the bending of FIB-milled cryo-lamellae[J]. Journal of Structural Biology, 208, 107389(2019).

    [55] Kaufmann R, Hagen C, Grünewald K. Fluorescence cryo-microscopy: current challenges and prospects[J]. Current Opinion in Chemical Biology, 20, 86-91(2014).

    [56] Gorelick S, Buckley G, Gervinskas G et al. PIE-scope, integrated cryo-correlative light and FIB/SEM microscopy[J]. eLife, 8, e45919(2019).

    [57] Smeets M, Bieber A, Capitanio C et al. Integrated cryo-correlative microscopy for targeted structural investigation in situ[J]. Microscopy Today, 29, 20-25(2021).

    [58] Li S G, Wang Z Y, Jia X et al. ELI trifocal microscope: a precise system to prepare target cryo-lamellae for in situ cryo-ET study[J]. Nature Methods, 20, 276-283(2023).

    [59] Arnold J, Mahamid J, Lucic V et al. Site-specific cryo-focused ion beam sample preparation guided by 3D correlative microscopy[J]. Biophysical Journal, 110, 860-869(2016).

    [60] Li W X, Lu J, Xiao K et al. Integrated multimodality microscope for accurate and efficient target-guided cryo-lamellae preparation[J]. Nature Methods, 20, 268-275(2023).

    [61] Sexton D L, Burgold S, Schertel A et al. Super-resolution confocal cryo-CLEM with cryo-FIB milling for in situ imaging of Deinococcus radiodurans[J]. Current Research in Structural Biology, 4, 1-9(2022).

    [62] Wu G H, Mitchell P G, Galaz-Montoya J G et al. Multi-scale 3D cryo-correlative microscopy for vitrified cells[J]. Structure, 28, 1231-1237(2020).

    [63] Schwartz C L, Sarbash V I, Ataullakhanov F I et al. Cryo-fluorescence microscopy facilitates correlations between light and cryo-electron microscopy and reduces the rate of photobleaching[J]. Journal of Microscopy, 227, 98-109(2007).

    [64] Le Gros M A, McDermott G, Uchida M et al. High-aperture cryogenic light microscopy[J]. Journal of Microscopy, 235, 1-8(2009).

    [65] Xu X J, Xue Y H, Tian B Y et al. Ultra-stable super-resolution fluorescence cryo-microscopy for correlative light and electron cryo-microscopy[J]. Science China Life Sciences, 61, 1312-1319(2018).

    [66] Li W X, Stein S C, Gregor I et al. Ultra-stable and versatile widefield cryo-fluorescence microscope for single-molecule localization with sub-nanometer accuracy[J]. Optics Express, 23, 3770-3783(2015).

    [67] Schorb M, Gaechter L, Avinoam O et al. New hardware and workflows for semi-automated correlative cryo-fluorescence and cryo-electron microscopy/tomography[J]. Journal of Structural Biology, 197, 83-93(2017).

    [68] Huff J, Bergter A, Birkenbeil J et al. The new 2D Superresolution mode for ZEISS Airyscan[J]. Nature Methods, 14, 1223(2017).

    [69] Reymann J. Lightning: image information extraction by adaptive deconvolution[EB/OL]. https:∥medschool.ucsd.edu/som/neurosciences/research/microscopy-core/resources/Documents/LIGHTNING_WhitePaper.pdf

    [70] Schumacher J, Bertrand L. Thunder imagers: how do they really work?[EB/OL]. https:∥7157e75ac0509b6a8f5c-5b19c577d01b9ccfe75d2f9e4b17ab55.ssl.cf1.rackcdn.com/EQZZKYFC-PDF-1-450123-4426040265.pdf

    [71] Kukulski W, Schorb M, Welsch S et al. Correlated fluorescence and 3D electron microscopy with high sensitivity and spatial precision[J]. Journal of Cell Biology, 192, 111-119(2011).

    [72] Kukulski W, Schorb M, Welsch S et al. Precise, correlated fluorescence microscopy and electron tomography of lowicryl sections using fluorescent fiducial markers[J]. Methods in Cell Biology, 111, 235-257(2012).

    [73] Fukuda Y, Schrod N, Schaffer M et al. Coordinate transformation based cryo-correlative methods for electron tomography and focused ion beam milling[J]. Ultramicroscopy, 143, 15-23(2014).

    [74] Hell S W, Wichmann J. Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy[J]. Optics Letters, 19, 780-782(1994).

    [75] Lelek M, Gyparaki M T, Beliu G et al. Single molecule localization microscopy[J]. Nature Reviews Methods Primers, 1, 39(2021).

    [76] Park J, Brady D J, Zheng G A et al. Review of bio-optical imaging systems with a high space-bandwidth product[J]. Advanced Photonics, 3, 044001(2021).

    [77] Wang Z J, Zhao T Y, Hao H W et al. High-speed image reconstruction for optically sectioned, super-resolution structured illumination microscopy[J]. Advanced Photonics, 4, 026003(2022).

    [78] Zachs T, Schertel A, Medeiros J et al. Fully automated, sequential focused ion beam milling for cryo-electron tomography[J]. eLife, 9, e52286(2020).

    Weixing Li, Jing Lu, Ke Xiao, Wei Ji. Recent Developments in Fluorescence-Guided Cryogenic Focused-Ion-Beam Milling[J]. Chinese Journal of Lasers, 2023, 50(21): 2107102
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