In situ label-free X-ray imaging for visualizing the localization of nanomedicines and subcellular architecture in intact single cells

Mingjing Cao, Chunying Chen, Yaling Wang, Liming Wang, Kai Zhang, Yong Guan, Yuecong Guo

Published: 2023-11-13 DOI: 10.1038/s41596-023-00902-y

X-ray microscopy

nanomedicine localization

subcellular architecture

label-free imaging

nano-bio interaction

AI 解读

Generation of mouse–human chimeric embryos

Genome-wide quantification of transcription factor binding at single-DNA-molecule resolution using methyl-transferase footprinting

Generation of CRISPR–Cas9-mediated genetic knockout human intestinal tissue–derived enteroid lines by lentivirus transduction and single-cell cloning

A puromycin-dependent activity-based sensing probe for histochemical staining of hydrogen peroxide in cells and animal tissues

Decoding personal biotic and abiotic airborne exposome

A clinically relevant model of focal embolic cerebral ischemia by thrombus and thrombolysis in rhesus monkeys

Bioengineering human intestinal mucosal grafts using patient-derived organoids, fibroblasts and scaffolds

Biomimetic tail-to-head terpene cyclizations using the resorcin[4]arene capsule catalyst

Neuroscience robotics for controlled induction and real-time assessment of hallucinations

Scanorama: integrating large and diverse single-cell transcriptomic datasets

Single-cell RNA sequencing (scRNA-seq)（单细胞RNA测序）

Data integration（数据集成）

Heterogeneity（异质性）

查看全部

Sections

Figures

References

Finney, L. A. & Jin, Q. Preparing adherent cells for X-ray fluorescence imaging by chemical fixation. J. Vis. Exp. 12, e52370 (2015).
Bissardon, C. et al. Cell culture on silicon nitride membranes and cryopreparation for synchrotron X-ray fluorescence nano-analysis. J. Vis. Exp. 10, e60461 (2019).
Zhang, C. et al. Progress, challenges, and future of nanomedicine. Nano Today 35, 101008 (2020).
Poon, W., Kingston, B., Ouyang, B., Ngo, W. & Chan, W. A framework for designing delivery systems. Nat. Nanotechnol. 15, 819–829 (2020).
Bourzac, K. Nanotechnology: carrying drugs. Nature 491, S58–S60 (2012).
Gewin, V. Big opportunities in a small world. Nature 460, 540–541 (2009).
Kim, B. Y., Rutka, J. T. & Chan, W. C. Nanomedicine. N. Engl. J. Med. 363, 2434–2443 (2010).
Wang, Y., Cai, R. & Chen, C. The nano–bio interactions of nanomedicines: understanding the biochemical driving forces and redox reactions. Acc. Chem. Res. 52, 1507–1518 (2019).
Cai, R. & Chen, C. The crown and the scepter: roles of the protein corona in nanomedicine. Adv. Mater. 31, 1805740 (2019).
Bondarenko, O. et al. Nanotoxicology and nanomedicine: the yin and yang of nano–bio interactions for the new decade. Nano Today 39, 101184 (2021).
Monopoli, M. P., Aberg, C., Salvati, A. & Dawson, K. A. Biomolecular coronas provide the biological identity of nanosized materials. Nat. Nanotechnol. 7, 779–786 (2012).
Cao, M. & Chen, C. Bioavailability of nanomaterials: bridging the gap between nanostructures and their bioactivity. Natl Sci. Rev. 9, nwac119 (2022).
Rosenblum, D., Joshi, N., Tao, W., Karp, J. M. & Peer, D. Progress and challenges towards targeted delivery of cancer therapeutics. Nat. Commun. 9, 1410 (2018).
Rennick, J. J., Johnston, A. P. R. & Parton, R. G. Key principles and methods for studying the endocytosis of biological and nanoparticle therapeutics. Nat. Nanotechnol. 16, 266–276 (2021).
Hubbell, J. A., Thomas, S. N. & Swartz, M. A. Materials engineering for immunomodulation. Nature 462, 449–460 (2009).
Stewart, M. P. et al. In vitro and ex vivo strategies for intracellular delivery. Nature 538, 183–192 (2016).
Korangath, P. et al. Nanoparticle interactions with immune cells dominate tumor retention and induce T cell-mediated tumor suppression in models of breast cancer. Sci. Adv. 6, eaay1601 (2020).
Cao, M., Zhang, K., Zhang, S., Wang, Y. & Chen, C. Advanced light source analytical techniques for exploring the biological behavior and fate of nanomedicines. ACS Cent. Sci. 8, 1063–1080 (2022).
Sanchez-Cano, C. et al. X-ray-based techniques to study the nano–bio interface. ACS Nano 15, 3754–3807 (2021).
Chen, C., Li, Y.-F., Qu, Y., Chai, Z. & Zhao, Y. Advanced nuclear analytical and related techniques for the growing challenges in nanotoxicology. Chem. Soc. Rev. 42, 8266–8303 (2013).
Yuan, Q. et al. A 30 nm-resolution hard X-ray microscope with X-ray fluorescence mapping capability at BSEF. J. Synchrotron Rad. 19, 1021–1028 (2012).
Liu, G., Chen, L. & Guan, Y. Three dimensional imaging of biological samples and nano-materials using soft X-ray microscopy. Microsc. Microanal. 24, 392–393 (2018).
Liu, H. et al. Soft X-ray spectroscopic endstation at beamline 08U1A of Shanghai Synchrotron Radiation Facility. Rev. Sci. Instrum. 90, 043103 (2019).
Howells, M., Jacobsen, C., Warwick, T. & Van den Bos, A. in Science of Microscopy (eds P. W. Hawkes & J. C. H. Spence) 835–926 (Springer, 2007).
Uchida, M. et al. Soft X-ray tomography of phenotypic switching and the cellular response to antifungal peptoids in candida albicans. Proc. Natl Acad. Sci. USA 106, 19375–19380 (2009).
Larabell, C. A. & Le Gros, M. A. X-ray tomography generates 3-D reconstructions of the yeast, Saccharomyces cerevisiae, at 60-nm resolution. Mol. Biol. Cell 15, 957–962 (2004).
Guo, A. et al. Quantitative, in situ visualization of intracellular insulin vesicles in pancreatic beta cells. Proc. Natl Acad. Sci. USA 119, e2202695119 (2022).
White, K. L. et al. Visualizing subcellular rearrangements in intact β cells using soft X-ray tomography. Sci. Adv. 6, eabc8262 (2020).
Krenkel, M. et al. Phase-contrast zoom tomography reveals precise s of macrophages in mouse lungs. Sci. Rep. 5, 9973 (2015).
Zhang, C. et al. 3D imaging and quantification of the integrin at a single-cell base on a multisignal nanoprobe and synchrotron radiation soft X-ray tomography microscopy. Anal. Chem. 93, 1237–1241 (2021).
Wang, J. et al. Gd-hybridized plasmonic Au-nanocomposites enhanced tumor-interior drug permeability in multimodal imaging-guided therapy. Adv. Mater. 28, 8950–8958 (2016).
Cagno, S. et al. Combined computed nanotomography and nanoscopic X-ray fluorescence imaging of cobalt nanoparticles in caenorhabditis elegans. Anal. Chem. 89, 11435–11442 (2017).
Ding, J. et al. Single-particle analysis for structure and iron chemistry of atmospheric particulate matter. Anal. Chem. 92, 975–982 (2020).
Qu, Y. et al. Full assessment of fate and physiological behavior of quantum dots utilizing caenorhabditis elegans as a model organism. Nano Lett. 11, 3174–3183 (2011).
Okolo, C. A. et al. Sample preparation strategies for efficient correlation of 3D SIM and soft X-ray tomography data at cryogenic temperatures. Nat. Protoc. 16, 2851–2885 (2021).
Matsuyama, S. et al. Elemental mapping of frozen-hydrated cells with cryo-scanning X-ray fluorescence microscopy. X-Ray Spectrom. 39, 260–266 (2010).
Jin, Q. et al. Preserving elemental content in adherent mammalian cells for analysis by synchrotron-based X-ray fluorescence microscopy. J. Microsc. 265, 81–93 (2017).
Chen, J. et al. 3D nanoscale imaging of the yeast, Schizosaccharomyces pombe, by full-field transmission X-ray microscopy at 5.4 keV. Anal. Bioanal. Chem. 397, 2117–2121 (2010).
Larabell, C. A. & Nugent, K. A. Imaging cellular architecture with X-rays. Curr. Opin. Struct. Biol. 20, 623–631 (2010).
Zhu, S., Wang, Y. & Chen, C. In situ analysis of the fate and behavior of inorganic nanomaterials in biological systems by synchrotron radiation X-ray probe techniques. Curr. Anal. Chem. 18, 723–738 (2022).
Zhang, M. et al. Directly observing intracellular nanoparticle formation with nanocomputed tomography. Sci. Adv. 6, eaba3190 (2020).
Wang, J. et al. 3D chemical and elemental imaging by STXM spectrotomography. AIP Conf. Proc. 1365, 215–218 (2011).
Guo, Z. et al. Biotransformation modulates the penetration of metallic nanomaterials across an artificial blood–brain barrier model. Proc. Natl Acad. Sci. USA 118, e2105245118 (2021).
Jonge, M. D. D. et al. Quantitative 3D elemental microtomography of Cyclotella meneghiniana at 400-nm resolution. Proc. Natl Acad. Sci. USA 107, 15676–15680 (2010).
Kounatidis, I. et al. 3D correlative cryo-structured illumination fluorescence and soft X-ray microscopy elucidates reovirus intracellular release pathway. Cell 182, 515.e17–530.e17 (2020).
Mendonça, L. et al. Correlative multi-scale cryo-imaging unveils SARS-CoV-2 assembly and egress. Nat. Commun. 12, 4629 (2021).
Schrand, A. M., Schlager, J. J., Dai, L. & Hussain, S. M. Preparation of cells for assessing ultrastructural localization of nanoparticles with transmission electron microscopy. Nat. Protoc. 5, 744–757 (2010).
Peddie, C. J. et al. Volume electron microscopy. Nat. Rev. Methods Prim. 2, 51 (2022).
Heinrich, L. et al. Whole-cell organelle segmentation in volume electron microscopy. Nature 599, 141–146 (2021).
Xu, C. S. et al. An open-access volume electron microscopy atlas of whole cells and tissues. Nature 599, 147–151 (2021).
Huang, B., Bates, M. & Zhuang, X. Super-resolution fluorescence microscopy. Annu. Rev. Biochem. 78, 993–1016 (2009).
Schermelleh, L. et al. Super-resolution microscopy demystified. Nat. Cell Biol. 21, 72–84 (2019).
Thomsen, T., Ayoub, A. B., Psaltis, D. & Klok, H.-A. Fluorescence-based and fluorescent label-free characterization of polymer nanoparticle decorated T cells. Biomacromolecules 22, 190–200 (2021).
Bernhardt, M. et al. Correlative microscopy approach for biology using X-ray holography, X-ray scanning diffraction and sted microscopy. Nat. Commun. 9, 3641 (2018).
Varsano, N. et al. Development of correlative cryo-soft X-ray tomography and stochastic reconstruction microscopy. A study of cholesterol crystal early formation in cells. J. Am. Chem. Soc. 138, 14931–14940 (2016).
Fan, J. et al. Single-pulse enhanced coherent diffraction imaging of bacteria with an X-ray free-electron laser. Sci. Rep. 6, 34008 (2016).
Seibert, M. M. et al. Single mimivirus particles intercepted and imaged with an X-ray laser. Nature 470, 78–81 (2011).
van der Schot, G. et al. Imaging single cells in a beam of live cyanobacteria with an X-ray laser. Nat. Commun. 6, 5704 (2015).
Kimura, T. et al. Imaging live cell in micro-liquid enclosure by X-ray laser diffraction. Nat. Commun. 5, 3052 (2014).
Cao, M. et al. Molybdenum derived from nanomaterials incorporates into molybdenum enzymes and affects their activities in vivo. Nat. Nanotechnol. 16, 708–716 (2021).
Zhang, G. et al. A nanomaterial targeting the spike protein captures SARS-CoV-2 variants and promotes viral elimination. Nat. Nanotechnol. 17, 993–1003 (2022).
Wang, Y. et al. Engineering a self-navigated MnARK nanovaccine for inducing potent protective immunity against novel coronavirus. Nano Today 38, 101139 (2021).
Chen, Z. et al. Polyhydroxylated metallofullerenols stimulate IL-1β secretion of macrophage through TLRs/MyD88/NF-κB pathway and NLRP3 inflammasome activation. Small 10, 2362–2372 (2014).
Cao, M. et al. Gadolinium(III)-chelated silica nanospheres integrating chemotherapy and photothermal therapy for cancer treatment and magnetic resonance imaging. ACS Appl. Mater. Interfaces 7, 25014–25023 (2015).
Cao, M., Li, J., Tang, J., Chen, C. & Zhao, Y. Gold nanomaterials in consumer cosmetics nanoproducts: analyses, characterization, and dermal safety assessment. Small 12, 5488–5496 (2016).
Bai, H. et al. Precise correlative method of cryo-SXT and cryo-FM for organelle identification. J. Synchrotron Radiat. 27, 176–184 (2020).
Dang, Z. et al. Regulating the synthesis rate and yield of bio-assembled FeS nanoparticles for efficient cancer therapy. Nanoscale 13, 18977–18986 (2021).
Studer, D. et al. Capture of activity-induced ultrastructural changes at synapses by high-pressure freezing of brain tissue. Nat. Protoc. 9, 1480–1495 (2014).
Zhang, X. et al. Ratio-contrast imaging of dual-energy absorption for element mapping with a scanning transmission X-ray microscope. J. Synchrotron. Rad 17, 804–809 (2010).
Yao, S. et al. Three-dimensional ultrastructural imaging reveals the nanoscale architecture of mammalian cells. IUCrJ 5, 141–149 (2018).
Peng, M. W. et al. Quantitative three-dimensional nondestructive imaging of whole anaerobic ammonium-oxidizing bacteria. J. Synchrotron Radiat. 27, 753–761 (2020).
Beucher, S. & Meyer, F. in Mathematical Morphology in Image Processing (ed. Dougherty, E. R.) 433–481 (Marcel Dekker, 1993).
Wang, L. et al. Use of synchrotron radiation-analytical techniques to reveal chemical origin of silver-nanoparticle cytotoxicity. ACS Nano 9, 6532–6547 (2015).

In situ label-free X-ray imaging for visualizing the localization of nanomedicines and subcellular architecture in intact single cells

Supplementary information

Reporting Summary

推荐阅读