Quantitation and localization of intracellular redox active metals by X-ray fluorescence microscopy in cortical neurons derived from APP and APLP2 knockout tissue
Abstract
The amyloid precursor protein (APP) gene family includes APP and the amyloid precursor-like proteins, APLP1 and APLP2. These proteins contain metal binding sites for copper, zinc and iron and are known to have physiological roles in modulating the metal homeostasis in brain cells. Here we report the application of X-ray fluorescence microscopy (XFM) to investigate the subcellular distribution patterns of the metal ions Cu, Zn, Fe, and Ca in individual neurons derived from APP and APLP2 knockout mice brains to further define their role in metal homeostasis. These studies add to the growing body of data that the APP family of proteins are metalloproteins that have shared as well as distinct effects on metals. As we continue to delineate the cellular effects of the APP family of proteins it is important to consider how metals are involved in their actions.
- Authors:
-
- Univ. of Melbourne (Australia)
- Australian Nuclear Science and Technology Organisation (ANSTO), Melbourne, VIC (Australia). Australian Synchrotron; Commonwealth Scientific and Industrial Research Organization (CSIRO), Dickson ACT (Australia)
- Elettra Sincrotrone Trieste (Italy)
- Australian Nuclear Science and Technology Organisation (ANSTO), Melbourne, VIC
- Argonne National Lab. (ANL), Argonne, IL (United States)
- Publication Date:
- Research Org.:
- Argonne National Lab. (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1214335
- Grant/Contract Number:
- AC02-06CH11357
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Metallomics
- Additional Journal Information:
- Journal Volume: 6; Journal Issue: 10; Journal ID: ISSN 1756-5901
- Publisher:
- Royal Society of Chemistry
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Citation Formats
Ciccotosto, Giuseppe D., James, Simon A., Altissimo, Matteo, Paterson, David, Vogt, Stefan, Lai, Barry, de Jonge, Martin D., Howard, Daryl L., Bush, Ashley I., and Cappai, Roberto. Quantitation and localization of intracellular redox active metals by X-ray fluorescence microscopy in cortical neurons derived from APP and APLP2 knockout tissue. United States: N. p., 2014.
Web. doi:10.1039/C4MT00176A.
Ciccotosto, Giuseppe D., James, Simon A., Altissimo, Matteo, Paterson, David, Vogt, Stefan, Lai, Barry, de Jonge, Martin D., Howard, Daryl L., Bush, Ashley I., & Cappai, Roberto. Quantitation and localization of intracellular redox active metals by X-ray fluorescence microscopy in cortical neurons derived from APP and APLP2 knockout tissue. United States. https://doi.org/10.1039/C4MT00176A
Ciccotosto, Giuseppe D., James, Simon A., Altissimo, Matteo, Paterson, David, Vogt, Stefan, Lai, Barry, de Jonge, Martin D., Howard, Daryl L., Bush, Ashley I., and Cappai, Roberto. Wed .
"Quantitation and localization of intracellular redox active metals by X-ray fluorescence microscopy in cortical neurons derived from APP and APLP2 knockout tissue". United States. https://doi.org/10.1039/C4MT00176A. https://www.osti.gov/servlets/purl/1214335.
@article{osti_1214335,
title = {Quantitation and localization of intracellular redox active metals by X-ray fluorescence microscopy in cortical neurons derived from APP and APLP2 knockout tissue},
author = {Ciccotosto, Giuseppe D. and James, Simon A. and Altissimo, Matteo and Paterson, David and Vogt, Stefan and Lai, Barry and de Jonge, Martin D. and Howard, Daryl L. and Bush, Ashley I. and Cappai, Roberto},
abstractNote = {The amyloid precursor protein (APP) gene family includes APP and the amyloid precursor-like proteins, APLP1 and APLP2. These proteins contain metal binding sites for copper, zinc and iron and are known to have physiological roles in modulating the metal homeostasis in brain cells. Here we report the application of X-ray fluorescence microscopy (XFM) to investigate the subcellular distribution patterns of the metal ions Cu, Zn, Fe, and Ca in individual neurons derived from APP and APLP2 knockout mice brains to further define their role in metal homeostasis. These studies add to the growing body of data that the APP family of proteins are metalloproteins that have shared as well as distinct effects on metals. As we continue to delineate the cellular effects of the APP family of proteins it is important to consider how metals are involved in their actions.},
doi = {10.1039/C4MT00176A},
journal = {Metallomics},
number = 10,
volume = 6,
place = {United States},
year = {Wed Oct 01 00:00:00 EDT 2014},
month = {Wed Oct 01 00:00:00 EDT 2014}
}
Web of Science
Works referenced in this record:
Isolation and characterization of APLP2 encoding a homologue of the Alzheimer's associated amyloid β protein precursor
journal, September 1993
- Wasco, Wilma; Gurubhagavatula, Sarada; Paradis, Marc d.
- Nature Genetics, Vol. 5, Issue 1
The APP family of proteins: similarities and differences
journal, March 2007
- Walsh, D. M.; Minogue, A. M.; Sala Frigerio, C.
- Biochemical Society Transactions, Vol. 35, Issue 2
Mice with Combined Gene Knock-Outs Reveal Essential and Partially Redundant Functions of Amyloid Precursor Protein Family Members
journal, November 2000
- Heber, Sabine; Herms, Jochen; Gajic, Vladan
- The Journal of Neuroscience, Vol. 20, Issue 21
Identification of the Alzheimer's disease amyloid precursor protein (APP) and its homologue APLP2 as essential modulators of glucose and insulin homeostasis and growth: APP and APLP2 modulate glucose and insulin homeostasis and growth in vivo
journal, February 2008
- Needham, Be; Wlodek, Me; Ciccotosto, Gd
- The Journal of Pathology, Vol. 215, Issue 2
Iron-Export Ferroxidase Activity of β-Amyloid Precursor Protein Is Inhibited by Zinc in Alzheimer's Disease
journal, September 2010
- Duce, James A.; Tsatsanis, Andrew; Cater, Michael A.
- Cell, Vol. 142, Issue 6
Gene knockout of amyloid precursor protein and amyloid precursor-like protein-2 increases cellular copper levels in primary mouse cortical neurons and embryonic fibroblasts
journal, October 2004
- Bellingham, Shayne A.; Ciccotosto, Giuseppe D.; Needham, B. Elise
- Journal of Neurochemistry, Vol. 91, Issue 2
Combined deletions of amyloid precursor protein and amyloid precursor-like protein 2 reveal different effects on mouse brain metal homeostasis
journal, January 2014
- Needham, B. Elise; Ciccotosto, Giuseppe D.; Cappai, Roberto
- Metallomics, Vol. 6, Issue 3
The βA4 amyloid precursor protein binding to copper
journal, July 1994
- Hesse, Lars; Beher, Dirk; Masters, Colin L.
- FEBS Letters, Vol. 349, Issue 1
The Amyloid Precursor Protein of Alzheimer's Disease in the Reduction of Copper(II) to Copper(I)
journal, March 1996
- Multhaup, G.; Schlicksupp, A.; Hesse, L.
- Science, Vol. 271, Issue 5254
Cysteine 144 Is a Key Residue in the Copper Reduction by the β-Amyloid Precursor Protein
journal, September 1999
- Ruiz, Francisca H.; González, Mauricio; Bodini, Mario
- Journal of Neurochemistry, Vol. 73, Issue 3
Copper levels are increased in the cerebral cortex and liver of APP and APLP2 knockout mice
journal, September 1999
- White, Anthony R.; Reyes, Rosario; Mercer, Julian F. B.
- Brain Research, Vol. 842, Issue 2
Structure of the Alzheimer's Disease Amyloid Precursor Protein Copper Binding Domain: A REGULATOR OF NEURONAL COPPER HOMEOSTASIS
journal, February 2003
- Barnham, Kevin J.; McKinstry, William J.; Multhaup, Gerd
- Journal of Biological Chemistry, Vol. 278, Issue 19
Solution structure of the fourth metal-binding domain from the Menkes copper-transporting ATPase
journal, January 1998
- Gitschier, Jane; Moffat, Barbara; Reilly, Dorothea
- Nature Structural Biology, Vol. 5, Issue 1
Solution Structure of the Cu(I) and Apo Forms of the Yeast Metallochaperone, Atx1 † , ‡
journal, February 2001
- Arnesano, Fabio; Banci, Lucia; Bertini, Ivano
- Biochemistry, Vol. 40, Issue 6
Overexpression of Alzheimer's Disease Amyloid-β Opposes the Age-dependent Elevations of Brain Copper and Iron
journal, September 2002
- Maynard, Christa J.; Cappai, Roberto; Volitakis, Irene
- Journal of Biological Chemistry, Vol. 277, Issue 47
In vivo reduction of amyloid- by a mutant copper transporter
journal, November 2003
- Phinney, A. L.; Drisaldi, B.; Schmidt, S. D.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 24
Dietary Cu stabilizes brain superoxide dismutase 1 activity and reduces amyloid A production in APP23 transgenic mice
journal, November 2003
- Bayer, T. A.; Schafer, S.; Simons, A.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 24
β-amyloid precursor protein-deficient mice show reactive gliosis and decreased locomotor activity
journal, May 1995
- Zheng, Hui; Jiang, Minghao; Trumbauer, Myrna E.
- Cell, Vol. 81, Issue 4
Generation of APLP2 KO Mice and Early Postnatal Lethality in APLP2/APP Double KO Mice
journal, November 1997
- von Koch, C. S.; Zheng, H.; Chen, H.
- Neurobiology of Aging, Vol. 18, Issue 6
Enhanced Toxicity and Cellular Binding of a Modified Amyloid β Peptide with a Methionine to Valine Substitution
journal, July 2004
- Ciccotosto, Giuseppe D.; Tew, Deborah; Curtain, Cyril C.
- Journal of Biological Chemistry, Vol. 279, Issue 41
Stereospecific interactions are necessary for Alzheimer disease amyloid-β toxicity
journal, February 2011
- Ciccotosto, Giuseppe D.; Tew, Deborah J.; Drew, Simon C.
- Neurobiology of Aging, Vol. 32, Issue 2
Chemical alterations to murine brain tissue induced by formalin fixation: implications for biospectroscopic imaging and mapping studies of disease pathogenesis
journal, January 2011
- Hackett, Mark J.; McQuillan, James A.; El-Assaad, Fatima
- The Analyst, Vol. 136, Issue 14
The X-ray Fluorescence Microscopy Beamline at the Australian Synchrotron
conference, January 2011
- Paterson, D.; de Jonge, M. D.; Howard, D. L.
- THE 10TH INTERNATIONAL CONFERENCE ON X-RAY MICROSCOPY, AIP Conference Proceedings
Quantitative PIXE trace element imaging of minerals using the new CSIRO–GEMOC Nuclear Microprobe
journal, April 2002
- Ryan, C. G.; van Achterbergh, E.; Yeats, C. J.
- Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms, Vol. 189, Issue 1-4
Protein length in eukaryotic and prokaryotic proteomes
journal, June 2005
- Brocchieri, L.
- Nucleic Acids Research, Vol. 33, Issue 10
The Sulfur-Containing Amino Acids: An Overview
journal, June 2006
- Brosnan, John T.; Brosnan, Margaret E.
- The Journal of Nutrition, Vol. 136, Issue 6
Aging results in copper accumulations in glial fibrillary acidic protein-positive cells in the subventricular zone
journal, July 2013
- Pushkar, Yulia; Robison, Gregory; Sullivan, Brendan
- Aging Cell, Vol. 12, Issue 5
Copper and Zinc Metallation Status of Copper-Zinc Superoxide Dismutase from Amyotrophic Lateral Sclerosis Transgenic Mice
journal, November 2010
- Lelie, Herman L.; Liba, Amir; Bourassa, Megan W.
- Journal of Biological Chemistry, Vol. 286, Issue 4
β-Amyloid precursor protein localization in the Golgi apparatus in neuron and oligodendrocytes. An immunocytochemical structural and ultrastructural study in normal and axotomized neurons
journal, October 1992
- Palacios, G.; Palacios, J. M.; Mengod, G.
- Molecular Brain Research, Vol. 15, Issue 3-4
Copper Promotes the Trafficking of the Amyloid Precursor Protein
journal, December 2010
- Acevedo, Karla M.; Hung, Ya Hui; Dalziel, Andrew H.
- Journal of Biological Chemistry, Vol. 286, Issue 10
X-ray fluorescence microscopy reveals large-scale relocalization and extracellular translocation of cellular copper during angiogenesis
journal, February 2007
- Finney, L.; Mandava, S.; Ursos, L.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 7
Imaging of the intracellular topography of copper with a fluorescent sensor and by synchrotron x-ray fluorescence microscopy
journal, August 2005
- Yang, L.; McRae, R.; Henary, M. M.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 32
Novel Zinc-binding Site in the E2 Domain Regulates Amyloid Precursor-like Protein 1 (APLP1) Oligomerization
journal, May 2014
- Mayer, Magnus C.; Kaden, Daniela; Schauenburg, Linda
- Journal of Biological Chemistry, Vol. 289, Issue 27
Presynaptic and Postsynaptic Interaction of the Amyloid Precursor Protein Promotes Peripheral and Central Synaptogenesis
journal, September 2009
- Wang, Z.; Wang, B.; Yang, L.
- Journal of Neuroscience, Vol. 29, Issue 35
Mechanisms contributing to the deficits in hippocampal synaptic plasticity in mice lacking amyloid precursor protein
journal, March 1999
- Seabrook, G. R.; Smith, D. W.; Bowery, B. J.
- Neuropharmacology, Vol. 38, Issue 3
Increased asynchronous release and aberrant calcium channel activation in amyloid precursor protein deficient neuromuscular synapses
journal, November 2007
- Yang, L.; Wang, B.; Long, C.
- Neuroscience, Vol. 149, Issue 4
Works referencing / citing this record:
Quantitative Probing of Cu 2+ Ions Naturally Present in Single Living Cells
journal, March 2016
- Lee, Junho; Lee, Hwa-Rim; Pyo, Jaeyeon
- Advanced Materials, Vol. 28, Issue 21
Cross talk between neurometals and amyloidogenic proteins at the synapse and the pathogenesis of neurodegenerative diseases
journal, January 2017
- Kawahara, M.; Kato-Negishi, M.; Tanaka, K.
- Metallomics, Vol. 9, Issue 6