Title: The development and use of metal-based probes for X-ray fluorescence microscopy

Journal Article · · Metallomics (Online)

Abstract X-ray fluorescence microscopy (XFM) has become a widely used technique for imaging the concentration and distribution of metal ions in cells and tissues. Recent advances in synchrotron sources, optics, and detectors have improved the spatial resolution of the technique to <10 nm with attogram detection sensitivity. However, to make XFM most beneficial for bioimaging—especially at the nanoscale—the metal ion distribution must be visualized within the subcellular context of the cell. Over the years, a number of approaches have been taken to develop X-ray-sensitive tags that permit the visualization of specific organelles or proteins using XFM. In this review, we examine the types of X-ray fluorophore used, including nanomaterials and metal ions, and the approaches used to incorporate the metal into their target binding site via antibodies, genetically encoded metal-binding peptides, affinity labeling, or cell-specific peptides. We evaluate their advantages and disadvantages, review the scientific findings, and discuss the needs for future development.

Research Organization:
Brookhaven National Laboratory (BNL), Upton, NY (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
SC0012704
OSTI ID:
1905940
Report Number(s):
BNL-223904-2023-JAAM; mfac093
Journal Information:
Metallomics (Online), Journal Name: Metallomics (Online) Journal Issue: 12 Vol. 14; ISSN 1756-591X
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (76)

Capillary optics and their use in x-ray analysis journal January 2000
Superparamagnetic Nanoparticles as a Powerful Systems Biology Characterization Tool in the Physiological Context journal September 2008
Synthesis of silver nanowires in a two‐phase system for biological applications journal February 2021
Development of SNAP-Tag Fluorogenic Probes for Wash-Free Fluorescence Imaging journal July 2011
Labeling TiO 2 Nanoparticles with Dyes for Optical Fluorescence Microscopy and Determination of TiO 2 -DNA Nanoconjugate Stability journal June 2009
Bioinspired Peptoid Nanotubes for Targeted Tumor Cell Imaging and Chemo‐Photodynamic Therapy journal August 2019
Near‐Infrared‐II Quantum Dots for In Vivo Imaging and Cancer Therapy journal November 2021
Gadolinium-based contrast agents for magnetic resonance cancer imaging: Gadolinium-based CA for MR cancer imaging journal October 2012
Metal ions in biological catalysis: from enzyme databases to general principles journal July 2008
Intracellular in situ labeling of TiO2 nanoparticles for fluorescence microscopy detection journal July 2017
Bioengineered Short Carbon Nanotubes as Tumor-Targeted Carriers for Biomedical Imaging journal May 2019
Development of X-ray excitable luminescent probes for scanning X-ray microscopy journal May 1999
Synchrotron-based X-ray fluorescence imaging of human cells labeled with CdSe quantum dots journal May 2009
Efficient generation of antigen-specific cellular immunity by vaccination with poly(γ-glutamic acid) nanoparticles entrapping endoplasmic reticulum-targeted peptides journal November 2007
Biological applications of X-ray fluorescence microscopy: exploring the subcellular topography and speciation of transition metals journal April 2007
Lanthanide-tagged proteins—an illuminating partnership journal April 2010
Advances in visualization of copper in mammalian systems using X-ray fluorescence microscopy journal April 2020
Chemical Tools for Endogenous Protein Labeling and Profiling journal August 2020
Correlative microXRF and optical immunofluorescence microscopy of adherent cells labeled with ultrasmall gold particles journal July 2006
KDEL peptide gold nanoconstructs: promising nanoplatforms for drug delivery journal April 2013
Fast Chemical Imaging at High Spatial Resolution by Laser Ablation Inductively Coupled Plasma Mass Spectrometry journal September 2013
Mass Cytometry: Technique for Real Time Single Cell Multitarget Immunoassay Based on Inductively Coupled Plasma Time-of-Flight Mass Spectrometry journal August 2009
Traceless Affinity Labeling of Endogenous Proteins for Functional Analysis in Living Cells journal June 2012
HaloTag: A Novel Protein Labeling Technology for Cell Imaging and Protein Analysis journal June 2008
In Situ Imaging of Metals in Cells and Tissues journal October 2009
Lanthanide-Binding Tags for 3D X-ray Imaging of Proteins in Cells at Nanoscale Resolution journal January 2020
Intracellular Distribution of TiO 2 −DNA Oligonucleotide Nanoconjugates Directed to Nucleolus and Mitochondria Indicates Sequence Specificity journal March 2007
Carbon Nanotubes in Macrophages: Imaging and Chemical Analysis by X-ray Fluorescence Microscopy journal August 2008
Cellular Uptake and Fate of PEGylated Gold Nanoparticles Is Dependent on Both Cell-Penetration Peptides and Particle Size journal July 2011
Engineered ascorbate peroxidase as a genetically encoded reporter for electron microscopy journal October 2012
A general method for the covalent labeling of fusion proteins with small molecules in vivo journal December 2002
Ligand-directed tosyl chemistry for protein labeling in vivo journal March 2009
Carbon nanotubes allow capture of krypton, barium and lead for multichannel biological X-ray fluorescence imaging journal October 2016
Highly multiplexed imaging of tumor tissues with subcellular resolution by mass cytometry journal March 2014
In vivo imaging of neural activity journal March 2017
Fluorescence microscopy today journal December 2005
Electron microscopy using the genetically encoded APEX2 tag in cultured mammalian cells journal August 2017
Fluorescence nanoscopy in cell biology journal September 2017
Cell-type and subcellular compartment-specific APEX2 proximity labeling reveals activity-dependent nuclear proteome dynamics in the striatum journal August 2021
Re-sizing of nuclear pores journal November 2021
Imaging of X-Ray-Excited Emissions from Quantum Dots and Biological Tissue in Whole Mouse journal December 2019
Three-dimensional ultrastructure of giant mitochondria in human non-alcoholic fatty liver disease journal February 2021
Application of d6 transition metal complexes in fluorescence cell imaging journal January 2010
Intracellular distribution and stability of a luminescent rhenium( i ) tricarbonyl tetrazolato complex using epifluorescence microscopy in conjunction with X-ray fluorescence imaging journal January 2017
Recent development of luminescent rhenium( i ) tricarbonyl polypyridine complexes as cellular imaging reagents, anticancer drugs, and antibacterial agents journal January 2017
Graftable SCoMPIs enable the labeling and X-ray fluorescence imaging of proteins journal January 2018
Rhenium carbonyl complexes bearing methylated triphenylphosphonium cations as antibody-free mitochondria trackers for X-ray fluorescence imaging journal January 2021
TiO2 nanoparticles as a soft X-ray molecular probe journal January 2008
Immunogold labeling and X-ray fluorescence microscopy reveal enrichment ratios of Cu and Zn, metabolism of APP and amyloid-β plaque formation in a mouse model of Alzheimer's disease journal January 2012
Site-specific cellular delivery of quantum dots with chemoselectively-assembled modular peptides journal January 2013
High resolution protein localization using soft X-ray microscopy journal March 2001
The Scanning Nanoprobe Beamline Nanoscopium at Synchrotron Soleil conference January 2011
Targeted nanoparticle enhanced proapoptotic peptide as potential therapy for glioblastoma journal October 2011
Metals in protein structures: a review of their principal features journal October 2010
Staining of Tissue Sections for Electron Microscopy with Heavy Metals journal November 1958
Zebrafish imaging and two-photon fluorescence imaging using ZnSe quantum dots* journal April 2021
Mitochondria are morphologically and functionally heterogeneous within cells journal April 2002
X-ray fluorescence microscopy methods for biological tissues journal May 2022
Genetically encoded X-ray cellular imaging for nanoscale protein localization journal April 2020
Three-dimensional imaging of human stem cells using soft X-ray tomography journal July 2015
Synchrotron-Based X-Ray Fluorescence Microscopy as a Technique for Imaging of Elements in Plants journal August 2018
The Bionanoprobe: hard X-ray fluorescence nanoprobe with cryogenic capabilities journal December 2013
Pushing the limits: an instrument for hard X-ray imaging below 20 nm journal January 2015
ID16B: a hard X-ray nanoprobe beamline at the ESRF for nano-analysis journal January 2016
Three-Dimensional Visualization of APEX2-Tagged Erg11 in Saccharomyces cerevisiae Using Focused Ion Beam Scanning Electron Microscopy journal February 2020
The Structure of the Nuclear Pore Complex (An Update) journal June 2019
Optimization of protocols for pre-embedding immunogold electron microscopy of neurons in cell cultures and brains journal June 2021
Lipid staining for the electron microscope: a new method journal December 1975
Striatal Medium-Sized Spiny Neurons: Identification by Nuclear Staining and Study of Neuronal Subpopulations in BAC Transgenic Mice journal March 2009
APEX2-enhanced electron microscopy distinguishes sigma-1 receptor localization in the nucleoplasmic reticulum journal May 2017
Quantitative Imaging of Cell-Permeable Magnetic Resonance Contrast Agents Using X-Ray Fluorescence journal October 2006
Nanobody-Based Probes for Subcellular Protein Identification and Visualization journal November 2020
Real-Time Fluorescence Imaging of His-Tag-Driven Conjugation of mCherry Proteins to Silver Nanowires journal April 2022
Quantum Dots for Live Cell and In Vivo Imaging journal February 2009
Antisense Oligonucleotides: An Emerging Area in Drug Discovery and Development journal June 2020
Ribosome surface properties may impose limits on the nature of the cytoplasmic proteome journal November 2017