Lipids status and copper in a single astrocyte of the rat model for amyotrophic lateral sclerosis: Correlative synchrotron-based X-ray and infrared imaging

Kreuzer, Martin; Stamenković, Stefan; Chen, Si; Andjus, Pavle; Dučić, Tanja

doi:10.1002/jbio.202000069

Title: Lipids status and copper in a single astrocyte of the rat model for amyotrophic lateral sclerosis: Correlative synchrotron-based X-ray and infrared imaging

Journal Article · Thu May 28 00:00:00 EDT 2020 · Journal of Biophotonics

DOI:https://doi.org/10.1002/jbio.202000069· OSTI ID:1774634

Kreuzer, Martin ^[1]; Stamenković, Stefan ^[2]; Chen, Si ^[3]; Andjus, Pavle ^[2];

^[1]

ALBA Synchrotron Light Source, Cerdanyola del Valles, Barcelona (Spain)
University of Belgrade (Serbia)
Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Amyotrophic lateral sclerosis (ALS) is a fatal neurodegenerative disease, causing death of motor neurons controlling voluntary muscles. The pathological mechanisms of the disease are only partially understood. The hSOD1-G93A ALS rat model is characterized by an overexpression of human mutated SOD1, causing increased vulnerability by forming intracellular protein aggregates, inducing excitotoxicity, affecting oxidative balance and disturbing axonal transport. In this study we followed the bio-macromolecular organic composition and compartmentalization together with trace metal distribution in situ in single astrocytes from the ALS rat model and compared them to the control astrocytes from nontransgenic littermates by simultaneous use of two synchrotron radiation-based methods: Fourier transform infrared microspectroscopy (SRFTIR) and hard X-ray fluorescence microscopy (XRF). Here we show that ALS cells contained more Cu, which colocalized with total lipids, increased carbonyl groups and oxidized lipids, thus implying direct involvement of Cu in oxidative stress of lipidic components without direct connection to protein aggregation in situ.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); ALBA; Ministry of Education, Science and Technological Development of the Republic of Serbia (MESTD RS)

Grant/Contract Number:: AC02-06CH11357; III41005

OSTI ID:: 1774634

Journal Information:: Journal of Biophotonics, Vol. 13, Issue 10; ISSN 1864-063X

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (44)

Two-dimensional correlation spectroscopy and multivariate curve resolution for the study of lipid oxidation in edible oils monitored by FTIR and FT-Raman spectroscopy Muik, Barbara; Lendl, Bernhard; Molina-Diaz, Antonio Analytica Chimica Acta, Vol. 593, Issue 1 https://doi.org/10.1016/j.aca.2007.04.050	journal	June 2007
The Bionanoprobe: hard X-ray fluorescence nanoprobe with cryogenic capabilities Chen, S.; Deng, J.; Yuan, Y. Journal of Synchrotron Radiation, Vol. 21, Issue 1 https://doi.org/10.1107/S1600577513029676	journal	December 2013
Multimodal Synchrotron Radiation Microscopy of Intact Astrocytes from the hSOD1 G93A Rat Model of Amyotrophic Lateral Sclerosis Dučić, Tanja; Stamenković, Stefan; Lai, Barry Analytical Chemistry, Vol. 91, Issue 2 https://doi.org/10.1021/acs.analchem.8b04273	journal	November 2018
Determination of molecular conformation and permeation in skin via IR spectroscopy, microscopy, and imaging Mendelsohn, Richard; Flach, Carol R.; Moore, David J. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1758, Issue 7 https://doi.org/10.1016/j.bbamem.2006.04.009	journal	July 2006
Amphetamine effects on brain protein structure and oxidative stress as revealed by FTIR microspectroscopy Rodríguez-Casado, A.; Alvarez, I.; Toledano, A. Biopolymers, Vol. 86, Issue 5-6 https://doi.org/10.1002/bip.20753	journal	January 2007
Mitochondrial dysfunction in amyotrophic lateral sclerosis - a valid pharmacological target?: Mitochondrial dysfunction in ALS Muyderman, H.; Chen, T. British Journal of Pharmacology, Vol. 171, Issue 8 https://doi.org/10.1111/bph.12476	journal	March 2014
Application of FTIR-ATR Spectroscopy to Determine the Extent of Lipid Peroxidation in Plasma during Haemodialysis Oleszko, Adam; Olsztyńska-Janus, Sylwia; Walski, Tomasz BioMed Research International, Vol. 2015 https://doi.org/10.1155/2015/245607	journal	January 2015
Formation of 9-hydroxy linoleic acid as a product of phospholipid peroxidation in diabetic erythrocyte membranes Inouye, Masayuki; Mio, Takaya; Sumino, Kimiaki Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1438, Issue 2 https://doi.org/10.1016/S1388-1981(99)00052-9	journal	May 1999
Metal-deficient aggregates and diminished copper found in cells expressing SOD1 mutations that cause ALS Bourassa, Megan W.; Brown, Hilda H.; Borchelt, David R. Frontiers in Aging Neuroscience, Vol. 6 https://doi.org/10.3389/fnagi.2014.00110	journal	June 2014
Using Fourier transform IR spectroscopy to analyze biological materials Baker, Matthew J.; Trevisan, Júlio; Bassan, Paul Nature Protocols, Vol. 9, Issue 8 https://doi.org/10.1038/nprot.2014.110	journal	July 2014
Metal Concentrations in Cerebrospinal Fluid and Blood Plasma from Patients with Amyotrophic Lateral Sclerosis Roos, Per M.; Vesterberg, Olof; Syversen, Tore Biological Trace Element Research, Vol. 151, Issue 2 https://doi.org/10.1007/s12011-012-9547-x	journal	December 2012
In situ characterization of prion protein structure and metal accumulation in scrapie-infected cells by synchrotron infrared and X-ray imaging Wang, Qi; Kretlow, Ariane; Beekes, Michael Vibrational Spectroscopy, Vol. 38, Issue 1-2 https://doi.org/10.1016/j.vibspec.2005.02.023	journal	July 2005
Multiple quantum solid-state NMR indicates a parallel, not antiparallel, organization of beta -sheets in Alzheimer's beta -amyloid fibrils Antzutkin, O. N.; Balbach, J. J.; Leapman, R. D. Proceedings of the National Academy of Sciences, Vol. 97, Issue 24 https://doi.org/10.1073/pnas.230315097	journal	November 2000
Synchrotron-based infrared and X-ray imaging shows focalized accumulation of Cu and Zn co-localized with β-amyloid deposits in Alzheimer’s disease Miller, Lisa M.; Wang, Qi; Telivala, Tejas P. Journal of Structural Biology, Vol. 155, Issue 1 https://doi.org/10.1016/j.jsb.2005.09.004	journal	July 2006
Comparison of Fourier transform infrared (FTIR) spectra of individual cells acquired using synchrotron and conventional sources Diem, Max; Romeo, Melissa; Matthäus, Christian Infrared Physics & Technology, Vol. 45, Issue 5-6 https://doi.org/10.1016/j.infrared.2004.01.013	journal	October 2004
Mechanisms of mutant SOD1 induced mitochondrial toxicity in amyotrophic lateral sclerosis VehvilÃ¤inen, Piia; Koistinaho, Jari; Gundars, Goldsteins Frontiers in Cellular Neuroscience, Vol. 8 https://doi.org/10.3389/fncel.2014.00126	journal	May 2014
Role of transition metals in the pathogenesis of amyotrophic lateral sclerosis Vonk, Willianne I. M.; Klomp, Leo W. J. Biochemical Society Transactions, Vol. 36, Issue 6 https://doi.org/10.1042/BST0361322	journal	November 2008
Biomarkers of Amyotrophic Lateral Sclerosis: Current Status and Interest of Oxysterols and Phytosterols Vejux, Anne; Namsi, Amira; Nury, Thomas Frontiers in Molecular Neuroscience, Vol. 11 https://doi.org/10.3389/fnmol.2018.00012	journal	January 2018
Decreased Metallation and Activity in Subsets of Mutant Superoxide Dismutases Associated with Familial Amyotrophic Lateral Sclerosis Hayward, Lawrence J.; Rodriguez, Jorge A.; Kim, Ji W. Journal of Biological Chemistry, Vol. 277, Issue 18 https://doi.org/10.1074/jbc.M112087200	journal	February 2002
Unraveling the Mechanisms Involved in Motor Neuron Degeneration in als Bruijn, Lucie I.; Miller, Timothy M.; Cleveland, Don W. Annual Review of Neuroscience, Vol. 27, Issue 1 https://doi.org/10.1146/annurev.neuro.27.070203.144244	journal	July 2004
Evidence that accumulation of ceramides and cholesterol esters mediates oxidative stress-induced death of motor neurons in amyotrophic lateral sclerosis Cutler, Roy G.; Pedersen, Ward A.; Camandola, Simonetta Annals of Neurology, Vol. 52, Issue 4 https://doi.org/10.1002/ana.10312	journal	September 2002
Neuromuscular Junction Impairment in Amyotrophic Lateral Sclerosis: Reassessing the Role of Acetylcholinesterase Campanari, Maria-Letizia; García-Ayllón, María-Salud; Ciura, Sorana Frontiers in Molecular Neuroscience, Vol. 9 https://doi.org/10.3389/fnmol.2016.00160	journal	December 2016
Oxidative changes of lipids monitored by MALDI MS Fuchs, Beate; Bresler, Kristin; Schiller, Jürgen Chemistry and Physics of Lipids, Vol. 164, Issue 8 https://doi.org/10.1016/j.chemphyslip.2011.09.006	journal	November 2011
MIRAS: The Infrared Synchrotron Radiation Beamline at ALBA Yousef, I.; Ribó, L.; Crisol, A. Synchrotron Radiation News, Vol. 30, Issue 4 https://doi.org/10.1080/08940886.2017.1338410	journal	July 2017
Epidermal Growth Factor Receptor Targeted Nuclear Delivery and High-Resolution Whole Cell X-ray Imaging of Fe ₃ O ₄ @TiO ₂ Nanoparticles in Cancer Cells Yuan, Ye; Chen, Si; Paunesku, Tatjana ACS Nano, Vol. 7, Issue 12 https://doi.org/10.1021/nn4033294	journal	November 2013
Nano-FTIR Absorption Spectroscopy of Molecular Fingerprints at 20 nm Spatial Resolution Huth, Florian; Govyadinov, Alexander; Amarie, Sergiu Nano Letters, Vol. 12, Issue 8 https://doi.org/10.1021/nl301159v	journal	July 2012
Autophagy and Neurodegeneration: Insights from a Cultured Cell Model of ALS Navone, Francesca; Genevini, Paola; Borgese, Nica Cells, Vol. 4, Issue 3 https://doi.org/10.3390/cells4030354	journal	August 2015
Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons Nagai, Makiko; Re, Diane B.; Nagata, Tetsuya Nature Neuroscience, Vol. 10, Issue 5 https://doi.org/10.1038/nn1876	journal	April 2007
Lipid Biomarkers for Amyotrophic Lateral Sclerosis González De Aguilar, Jose-Luis Frontiers in Neurology, Vol. 10 https://doi.org/10.3389/fneur.2019.00284	journal	April 2019
MAPS : A set of software tools for analysis and visualization of 3D X-ray fluorescence data sets Vogt, S. Journal de Physique IV (Proceedings), Vol. 104 https://doi.org/10.1051/jp4:20030160	journal	March 2003
Levels of membrane fluidity in the spinal cord and the brain in an animal model of amyotrophic lateral sclerosis Miana-Mena, Francisco Javier; Piedrafita, Eduardo; González-Mingot, Cristina Journal of Bioenergetics and Biomembranes, Vol. 43, Issue 2 https://doi.org/10.1007/s10863-011-9348-5	journal	March 2011
Structural and elemental changes in glioblastoma cells in situ : complementary imaging with high resolution visible light- and X-ray microscopy Dučić, Tanja; Paunesku, Tatjana; Chen, Si The Analyst, Vol. 142, Issue 2 https://doi.org/10.1039/C6AN02532C	journal	January 2017
Lipidomics Reveals Cerebrospinal-Fluid Signatures of ALS Blasco, H.; Veyrat-Durebex, C.; Bocca, C. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-17389-9	journal	December 2017
Copper handling machinery of the brain Lutsenko, Svetlana; Bhattacharjee, Ashima; Hubbard, Ann L. Metallomics, Vol. 2, Issue 9 https://doi.org/10.1039/c0mt00006j	journal	January 2010
Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis Rosen, Daniel R.; Siddique, Teepu; Patterson, David Nature, Vol. 362, Issue 6415 https://doi.org/10.1038/362059a0	journal	March 1993
Mitochondrial dysfunction in ALS Cozzolino, Mauro; Carrì, Maria Teresa Progress in Neurobiology, Vol. 97, Issue 2 https://doi.org/10.1016/j.pneurobio.2011.06.003	journal	May 2012
Infrared Orange: Connecting Hyperspectral Data with Machine Learning Toplak, M.; Birarda, G.; Read, S. Synchrotron Radiation News, Vol. 30, Issue 4 https://doi.org/10.1080/08940886.2017.1338424	journal	July 2017
Lipid Raft Redox Signaling: Molecular Mechanisms in Health and Disease Jin, Si; Zhou, Fan; Katirai, Foad Antioxidants & Redox Signaling, Vol. 15, Issue 4 https://doi.org/10.1089/ars.2010.3619	journal	August 2011
Direct Observation of Defects and Increased Ion Permeability of a Membrane Induced by Structurally Disordered Cu/Zn-Superoxide Dismutase Aggregates Choi, Inhee; Song, Hyeon Don; Lee, Suseung PLoS ONE, Vol. 6, Issue 12 https://doi.org/10.1371/journal.pone.0028982	journal	December 2011
SOD1 in neurotoxicity and its controversial roles in SOD1 mutation-negative ALS Hayashi, Yuki; Homma, Kengo; Ichijo, Hidenori Advances in Biological Regulation, Vol. 60 https://doi.org/10.1016/j.jbior.2015.10.006	journal	January 2016
Oxidative and endoplasmic reticulum stress interplay in sporadic amyotrophic lateral sclerosis Ilieva, E. V.; Ayala, V.; Jove, M. Brain, Vol. 130, Issue 12 https://doi.org/10.1093/brain/awm190	journal	May 2007
Molecular immunocytochemistry of the CuZn superoxide dismutase in rat hepatocytes. Chang, L. Y.; Slot, J. W.; Geuze, H. J. Journal of Cell Biology, Vol. 107, Issue 6 https://doi.org/10.1083/jcb.107.6.2169	journal	December 1988
Supramolecular Structure in Full-Length Alzheimer's β-Amyloid Fibrils: Evidence for a Parallel β-Sheet Organization from Solid-State Nuclear Magnetic Resonance Balbach, John J.; Petkova, Aneta T.; Oyler, Nathan A. Biophysical Journal, Vol. 83, Issue 2 https://doi.org/10.1016/S0006-3495(02)75244-2	journal	August 2002
Amyotrophic lateral sclerosis and structural defects in Cu,Zn superoxide dismutase Deng, H.; Hentati, A.; Tainer, J. Science, Vol. 261, Issue 5124 https://doi.org/10.1126/science.8351519	journal	August 1993

Similar Records

Multimodal Synchrotron Radiation Microscopy of Intact Astrocytes from the hSOD1 G93A Rat Model of Amyotrophic Lateral Sclerosis

Journal Article · Thu Dec 20 00:00:00 EST 2018 · Analytical Chemistry · OSTI ID:1774634

Dučić, Tanja; Stamenković, Stefan; Lai, Barry; +2 more

Pigmented Creatine Deposits in Amyotrophic Lateral Sclerosis Central Nervous System Tissues Identified by Synchrotron Fourier Transform Infrared Microspectroscopy and X-ray Fluorescence Spectromicroscopy

Journal Article · Fri Jan 01 00:00:00 EST 2010 · Neuroscience · OSTI ID:1774634

Kastyak, M; Szczerbowska-Boruchowska, M; Adamek, D; +3 more

Copper and Zinc Metallation Status of Copper Zinc Superoxide Dismutase form Amyotrophic Lateral Sclerosis Transgenic Mice

Journal Article · Fri Sep 24 00:00:00 EDT 2010 · The Journal of Biological Chemistry · OSTI ID:1774634

Lelie, H L; Miller, L; Liba, A; +5 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
X-ray fluorescence microscopy
amyotrophic lateral sclerosis
copper
lipids
synchrotron based Fourier transformed infrared microscopy

Title: Lipids status and copper in a single astrocyte of the rat model for amyotrophic lateral sclerosis: Correlative synchrotron-based X-ray and infrared imaging

Citation Formats

References (44)

Similar Records

Related Subjects