skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Visualizing Metal Content and Intracellular Distribution in Primary Hippocampal Neurons with Synchrotron X-Ray Fluorescence

; ; ; ;
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
Alternate Identifier(s):
OSTI ID: 1339151
Grant/Contract Number:  
Resource Type:
Published Article
Journal Name:
Additional Journal Information:
Journal Name: PLoS ONE Journal Volume: 11 Journal Issue: 7; Journal ID: ISSN 1932-6203
Public Library of Science (PLoS)
Country of Publication:
United States

Citation Formats

Colvin, Robert A., Jin, Qiaoling, Lai, Barry, Kiedrowski, Lech, and Missirlis, ed., Fanis. Visualizing Metal Content and Intracellular Distribution in Primary Hippocampal Neurons with Synchrotron X-Ray Fluorescence. United States: N. p., 2016. Web. doi:10.1371/journal.pone.0159582.
Colvin, Robert A., Jin, Qiaoling, Lai, Barry, Kiedrowski, Lech, & Missirlis, ed., Fanis. Visualizing Metal Content and Intracellular Distribution in Primary Hippocampal Neurons with Synchrotron X-Ray Fluorescence. United States. doi:10.1371/journal.pone.0159582.
Colvin, Robert A., Jin, Qiaoling, Lai, Barry, Kiedrowski, Lech, and Missirlis, ed., Fanis. Tue . "Visualizing Metal Content and Intracellular Distribution in Primary Hippocampal Neurons with Synchrotron X-Ray Fluorescence". United States. doi:10.1371/journal.pone.0159582.
title = {Visualizing Metal Content and Intracellular Distribution in Primary Hippocampal Neurons with Synchrotron X-Ray Fluorescence},
author = {Colvin, Robert A. and Jin, Qiaoling and Lai, Barry and Kiedrowski, Lech and Missirlis, ed., Fanis},
abstractNote = {},
doi = {10.1371/journal.pone.0159582},
journal = {PLoS ONE},
number = 7,
volume = 11,
place = {United States},
year = {2016},
month = {7}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1371/journal.pone.0159582

Citation Metrics:
Cited by: 1 work
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

A quinoline fluorescence method for visualizing and assaying the histochemically reactive zinc (bouton zinc) in the brain
journal, June 1987

The interactive roles of zinc and calcium in mitochondrial dysfunction and neurodegeneration
journal, November 2013

  • Pivovarova, Natalia B.; Stanika, Ruslan I.; Kazanina, Galina
  • Journal of Neurochemistry, Vol. 128, Issue 4
  • DOI: 10.1111/jnc.12489

Understanding metal homeostasis in primary cultured neurons. Studies using single neuron subcellular and quantitative metallomics
journal, January 2015

  • Colvin, Robert A.; Lai, Barry; Holmes, William R.
  • Metallomics, Vol. 7, Issue 7
  • DOI: 10.1039/C5MT00084J

Metal imaging in neurodegenerative diseases
journal, January 2012

  • Bourassa, Megan W.; Miller, Lisa M.
  • Metallomics, Vol. 4, Issue 8
  • DOI: 10.1039/c2mt20052j

Zinquin identifies subcellular compartmentalization of zinc in cortical neurons. Relation to the trafficking of zinc and the mitochondrial compartment
journal, April 2006

Reversion of age-related recognition memory impairment by iron chelation in rats
journal, July 2008

Zinc transporters and the cellular trafficking of zinc
journal, July 2006

Cellular iron uptake, trafficking and metabolism: Key molecules and mechanisms and their roles in disease
journal, May 2015

  • Lane, D. J. R.; Merlot, A. M.; Huang, M. L. -H.
  • Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1853, Issue 5
  • DOI: 10.1016/j.bbamcr.2015.01.021

In Situ Imaging of Metals in Cells and Tissues
journal, October 2009

  • McRae, Reagan; Bagchi, Pritha; Sumalekshmy, S.
  • Chemical Reviews, Vol. 109, Issue 10
  • DOI: 10.1021/cr900223a

Elemental anomalies in the hippocampal formation after repetitive electrical stimulation: an X-ray fluorescence microscopy study
journal, July 2014

  • Chwiej, J.; Gabrys, H.; Janeczko, K.
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 19, Issue 7
  • DOI: 10.1007/s00775-014-1177-7

Iron metabolism in the CNS: implications for neurodegenerative diseases
journal, July 2013

  • Rouault, Tracey A.
  • Nature Reviews Neuroscience, Vol. 14, Issue 8
  • DOI: 10.1038/nrn3453

Biological metals and metal-targeting compounds in major neurodegenerative diseases
journal, January 2014

  • Barnham, Kevin J.; Bush, Ashley I.
  • Chem. Soc. Rev., Vol. 43, Issue 19
  • DOI: 10.1039/C4CS00138A

Ultrastructural localization of zinc transporter-3 (ZnT-3) to synaptic vesicle membranes within mossy fiber boutons in the hippocampus of mouse and monkey
journal, November 1997

  • Wenzel, H. J.; Cole, T. B.; Born, D. E.
  • Proceedings of the National Academy of Sciences, Vol. 94, Issue 23
  • DOI: 10.1073/pnas.94.23.12676

Synchrotron radiation X-ray fluorescence microscopy reveals a spatial association of copper on elastic laminae in rat aortic media
journal, January 2011

  • Qin, Zhenyu; Toursarkissian, Boulos; Lai, Barry
  • Metallomics, Vol. 3, Issue 8
  • DOI: 10.1039/c1mt00033k

Three-dimensional elemental bio-imaging of Fe, Zn, Cu, Mn and P in a 6-hydroxydopamine lesioned mouse brain
journal, January 2010

  • Hare, Dominic J.; George, Jessica L.; Grimm, Rudolph
  • Metallomics, Vol. 2, Issue 11
  • DOI: 10.1039/c0mt00039f

Manganese homeostasis in the nervous system
journal, June 2015

  • Chen, Pan; Chakraborty, Sudipta; Mukhopadhyay, Somshuvra
  • Journal of Neurochemistry, Vol. 134, Issue 4
  • DOI: 10.1111/jnc.13170

Impact of manganese on primary hippocampal neurons from rodents: Impact of Manganese on Primary Hippocampal Neurons from Rodents
journal, March 2014

  • Daoust, Alexia; Saoudi, Yasmina; Brocard, Jacques
  • Hippocampus, Vol. 24, Issue 5
  • DOI: 10.1002/hipo.22252

Alpha-Synuclein Regulates Neuronal Levels of Manganese and Calcium
journal, August 2015

Increased amount of zinc in the hippocampus and amygdala of Alzheimer's diseased brains
journal, September 1997

  • Danscher, Gorm; Jensen, Knud Bjarne; Frederickson, Christopher J.
  • Journal of Neuroscience Methods, Vol. 76, Issue 1
  • DOI: 10.1016/S0165-0270(97)00079-4

Al, Zn, Cu, Mn and Fe levels in brain in Alzheimer's disease
journal, July 1995

  • Andrási, Erzsébet; Farkas, Éva; Scheibler, Henning
  • Archives of Gerontology and Geriatrics, Vol. 21, Issue 1
  • DOI: 10.1016/0167-4943(95)00643-Y

Endogenous concentrations of biologically relevant metals in rat brain and cochlea determined by inductively coupled plasma mass spectrometry
journal, December 2014

X-ray fluorescence imaging of the hippocampal formation after manganese exposure
journal, January 2013

  • Robison, Gregory; Zakharova, Taisiya; Fu, Sherleen
  • Metallomics, Vol. 5, Issue 11
  • DOI: 10.1039/c3mt00133d

Quantitation and localization of intracellular redox active metals by X-ray fluorescence microscopy in cortical neurons derived from APP and APLP2 knockout tissue
journal, January 2014

  • Ciccotosto, Giuseppe D.; James, Simon A.; Altissimo, Matteo
  • Metallomics, Vol. 6, Issue 10
  • DOI: 10.1039/C4MT00176A

Three-Dimensional Atlas of Iron, Copper, and Zinc in the Mouse Cerebrum and Brainstem
journal, April 2012

  • Hare, Dominic J.; Lee, Jason K.; Beavis, Alison D.
  • Analytical Chemistry, Vol. 84, Issue 9
  • DOI: 10.1021/ac300374x

Combined use of hard X-ray phase contrast imaging and X-ray fluorescence microscopy for sub-cellular metal quantification
journal, February 2012

  • Kosior, Ewelina; Bohic, Sylvain; Suhonen, Heikki
  • Journal of Structural Biology, Vol. 177, Issue 2
  • DOI: 10.1016/j.jsb.2011.12.005

High field magnetic resonance microscopy of the human hippocampus in Alzheimer's disease: Quantitative imaging and correlation with iron
journal, January 2012

ZnT-3, a putative transporter of zinc into synaptic vesicles
journal, December 1996

  • Palmiter, R. D.; Cole, T. B.; Quaife, C. J.
  • Proceedings of the National Academy of Sciences, Vol. 93, Issue 25
  • DOI: 10.1073/pnas.93.25.14934

α-Synuclein Over-Expression Induces Increased Iron Accumulation and Redistribution in Iron-Exposed Neurons
journal, April 2015

  • Ortega, Richard; Carmona, Asuncion; Roudeau, Stéphane
  • Molecular Neurobiology, Vol. 53, Issue 3
  • DOI: 10.1007/s12035-015-9146-x

The role of iron and reactive oxygen species in cell death
journal, December 2013

  • Dixon, Scott J.; Stockwell, Brent R.
  • Nature Chemical Biology, Vol. 10, Issue 1
  • DOI: 10.1038/nchembio.1416

X-Ray Fluorescence Imaging: A New Tool for Studying Manganese Neurotoxicity
journal, November 2012

Concentrations of extracellular free zinc (pZn)e in the central nervous system during simple anesthetization, ischemia and reperfusion
journal, April 2006

Analytical methods for copper, zinc and iron quantification in mammalian cells
journal, January 2013

  • Cerchiaro, Giselle; Manieri, Tania Maria; Bertuchi, Fernanda Rodrigues
  • Metallomics, Vol. 5, Issue 10
  • DOI: 10.1039/c3mt00136a

High-Resolution Elemental Bioimaging of Ca, Mn, Fe, Co, Cu, and Zn Employing LA-ICP-MS and Hydrogen Reaction Gas
journal, July 2012

  • Lear, Jessica; Hare, Dominic J.; Fryer, Fred
  • Analytical Chemistry, Vol. 84, Issue 15
  • DOI: 10.1021/ac301156f

Biological applications of X-ray fluorescence microscopy: exploring the subcellular topography and speciation of transition metals
journal, April 2007

The distribution of Timm's stain in the nonsulphide-perfused human hippocampal formation
journal, January 1984

  • Cassell, M. D.; Brown, M. W.
  • The Journal of Comparative Neurology, Vol. 222, Issue 3
  • DOI: 10.1002/cne.902220311

Mammalian iron–sulphur proteins: novel insights into biogenesis and function
journal, November 2014

  • Rouault, Tracey A.
  • Nature Reviews Molecular Cell Biology, Vol. 16, Issue 1
  • DOI: 10.1038/nrm3909

Bio-metals imaging and speciation in cells using proton and synchrotron radiation X-ray microspectroscopy
journal, June 2009

  • Ortega, Richard; Devès, Guillaume; Carmona, Asunción
  • Journal of The Royal Society Interface, Vol. 6, Issue suppl_5
  • DOI: 10.1098/rsif.2009.0166.focus

Zinc-buffering capacity of a eukaryotic cell at physiological pZn
journal, August 2006

  • Krężel, Artur; Maret, Wolfgang
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 11, Issue 8
  • DOI: 10.1007/s00775-006-0150-5

Variations in elemental compositions of rat hippocampal formation between acute and latent phases of pilocarpine-induced epilepsy: an X-ray fluorescence microscopy study
journal, March 2012

  • Chwiej, J.; Dulinska, J.; Janeczko, K.
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 17, Issue 5
  • DOI: 10.1007/s00775-012-0892-1

Manganese Accumulates within Golgi Apparatus in Dopaminergic Cells as Revealed by Synchrotron X-ray Fluorescence Nanoimaging
journal, December 2009

  • Carmona, Asunción; Devès, Guillaume; Roudeau, Stéphane
  • ACS Chemical Neuroscience, Vol. 1, Issue 3
  • DOI: 10.1021/cn900021z

A delicate balance: Iron metabolism and diseases of the brain
journal, January 2013

Insights into Zn 2+ homeostasis in neurons from experimental and modeling studies
journal, March 2008

  • Colvin, Robert A.; Bush, Ashley I.; Volitakis, Irene
  • American Journal of Physiology-Cell Physiology, Vol. 294, Issue 3
  • DOI: 10.1152/ajpcell.00541.2007

Intracellular distribution of labile Zn(II) and zinc transporter expression in kidney and MDCK cells
journal, December 2002

  • Ranaldi, Giulia; Perozzi, Giuditta; Truong-Tran, Ai
  • American Journal of Physiology-Renal Physiology, Vol. 283, Issue 6
  • DOI: 10.1152/ajprenal.00094.2002

Copper, iron, and zinc imbalances in severely degenerated brain regions in Alzheimer's disease: possible relation to oxidative stress
journal, November 1996

Identification of dopaminergic neurons of the substantia nigra pars compacta as a target of manganese accumulation
journal, January 2015

  • Robison, Gregory; Sullivan, Brendan; Cannon, Jason R.
  • Metallomics, Vol. 7, Issue 5
  • DOI: 10.1039/C5MT00023H

Elimination of zinc from synaptic vesicles in the intact mouse brain by disruption of the ZnT3 gene
journal, February 1999

  • Cole, T. B.; Wenzel, H. J.; Kafer, K. E.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 4
  • DOI: 10.1073/pnas.96.4.1716

Proton-dependent zinc release from intracellular ligands
journal, March 2014

  • Kiedrowski, Lech
  • Journal of Neurochemistry, Vol. 130, Issue 1
  • DOI: 10.1111/jnc.12712

Increased Iron Levels and Decreased Tissue Integrity in Hippocampus of Alzheimer's Disease Detected in vivo with Magnetic Resonance Imaging
journal, August 2013

  • Raven, Erika P.; Lu, Po H.; Tishler, Todd A.
  • Journal of Alzheimer's Disease, Vol. 37, Issue 1
  • DOI: 10.3233/JAD-130209

Cytosolic zinc buffering and muffling: Their role in intracellular zinc homeostasis
journal, January 2010

  • Colvin, Robert A.; Holmes, William R.; Fontaine, Charles P.
  • Metallomics, Vol. 2, Issue 5
  • DOI: 10.1039/b926662c

Manganese Is Essential for Neuronal Health
journal, July 2015

Importance of Zinc in the Central Nervous System: The Zinc-Containing Neuron
journal, May 2000

  • Frederickson, Christopher J.; Suh, Sang Won; Silva, David
  • The Journal of Nutrition, Vol. 130, Issue 5
  • DOI: 10.1093/jn/130.5.1471S

Fluorescent Sensors for Zn 2+ Based on a Fluorescein Platform:  Synthesis, Properties and Intracellular Distribution
journal, August 2001

  • Burdette, Shawn C.; Walkup, Grant K.; Spingler, Bernhard
  • Journal of the American Chemical Society, Vol. 123, Issue 32
  • DOI: 10.1021/ja010059l

Role of Brain Iron Accumulation in Cognitive Dysfunction: Evidence from Animal Models and Human Studies
journal, March 2013

  • Schröder, Nadja; Figueiredo, Luciana Silva; de Lima, Maria Noêmia Martins
  • Journal of Alzheimer's Disease, Vol. 34, Issue 4
  • DOI: 10.3233/JAD-121996

Increased brain iron coincides with early plaque formation in a mouse model of Alzheimer's disease
journal, March 2011

pH dependence and compartmentalization of zinc transported across plasma membrane of rat cortical neurons
journal, February 2002

X-ray fluorescence analysis of iron and manganese distribution in primary dopaminergic neurons
journal, December 2012

  • Dučić, Tanja; Barski, Elisabeth; Salome, Murielle
  • Journal of Neurochemistry, Vol. 124, Issue 2
  • DOI: 10.1111/jnc.12073

Neuronal acid-induced [Zn 2+ ] i elevations calibrated using the low-affinity ratiometric probe FuraZin-1
journal, September 2015

  • Kiedrowski, Lech
  • Journal of Neurochemistry, Vol. 135, Issue 4
  • DOI: 10.1111/jnc.13282

Zinc homeostasis and signaling in glia
journal, February 2012

Ultrastructural and X-ray Microanalytical Observations of Minocycline-related Hyperpigmentation of the Skin
journal, September 1981

  • Sato, Syozo; Murphy, George F.; Bernhard, Jeffrey D.
  • Journal of Investigative Dermatology, Vol. 77, Issue 3
  • DOI: 10.1111/1523-1747.ep12482449

    Works referencing / citing this record:

    Esterification of the free carboxylic group from the lutidinic acid ligand as a tool to improve the cytotoxicity of Ru( ii ) complexes
    journal, January 2019

    • Honorato, João; Colina-Vegas, Legna; Correa, Rodrigo S.
    • Inorganic Chemistry Frontiers, Vol. 6, Issue 2
    • DOI: 10.1039/c8qi00941d