Mass spectrometry imaging of rat brain lipid profile changes over time following traumatic brain injury

Roux, Aurélie; Muller, Ludovic; Jackson, Shelley N.; Post, Jeremy; Baldwin, Katherine; Hoffer, Barry J.; Balaban, Carey D.; Barbacci, Damon C.; Schultz, J.; Gouty, Shawn; Cox, Brian M.; Woods, Amina S.

doi:10.1016/j.jneumeth.2016.02.004

Cited by 90 publications

(114 citation statements)

References 50 publications

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“…Roux et al have reported changes in other lipids, from an entire brain tissue section (namely, ceramide, SM, cholesterol derivatives, and other glycerophospholipids, (50 μ m resolution)) at later time points post-TBI using a combined sliver nanoparticle/ion mobility MALDI imaging technique. 44 …”

Section: Resultsmentioning

confidence: 99%

Gas Cluster Ion Beam Time-of-Flight Secondary Ion Mass Spectrometry High-Resolution Imaging of Cardiolipin Speciation in the Brain: Identification of Molecular Losses after Traumatic Injury

et al. 2017

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Gas cluster ion beam-secondary ion mass spectrometry (GCIB-SIMS) has shown the full potential of mapping intact lipids in biological systems with better than 10 μm lateral resolution. This study investigated further the capability of GCIB-SIMS in imaging high-mass signals from intact cardiolipin (CL) and gangliosides in normal brain and the effect of a controlled cortical impact model (CCI) of traumatic brain injury (TBI) on their distribution. A combination of enzymatic and chemical treatments was employed to suppress the signals from the most abundant phospholipids (phosphatidylcholine (PC) and phosphatidylethanolamine (PE)) and enhance the signals from the low-abundance CLs and gangliosides to allow their GCIB-SIMS detection at 8 and 16 μm spatial resolution. Brain CLs have not been observed previously using other contemporary imaging mass spectrometry techniques at better than 50 μm spatial resolution. High-resolution images of naive and injured brain tissue facilitated the comparison of CL species across three multicell layers in the CA1, CA3, and DG regions of the hippocampus. GCIB-SIMS also reliably mapped losses of oxidizable polyunsaturated CL species (but not the oxidation-resistant saturated and monounsaturated gangliosides) to regions including the CA1 and CA3 of the hippocampus after CCI. This work extends the detection range for SIMS measurements of intact lipids to above m/z 2000, bridging the mass range gap compared with MALDI. Further advances in high-resolution SIMS of CLs, with the potential for single cell or supra-cellular imaging, will be essential for the understanding of CL’s functional and structural organization in normal and injured brain.

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Section: Resultsmentioning

confidence: 99%

Gas Cluster Ion Beam Time-of-Flight Secondary Ion Mass Spectrometry High-Resolution Imaging of Cardiolipin Speciation in the Brain: Identification of Molecular Losses after Traumatic Injury

et al. 2017

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“…Gold cluster ion currents, although proving the potential of the technique, were insufficient for implantation of the large areas necessary for organ imaging. More recently, an alternative method for homogeneous implantation of metalnanoparticulate ions into tissue enables reproducible MILDI-MS imaging after 500 eV implantation of 8 nm AgNP into heart [5], kidney [6], and brain [7,8] unfixed cryostat sections. In the brain studies, MILDI-MS imaging was used to study injury and pathology in controlled cortical impact [7] and alcoholism [8] using rodent models.…”

Section: Introductionmentioning

confidence: 99%

Laser Desorption/Ionization Mass Spectrometric Imaging of Endogenous Lipids from Rat Brain Tissue Implanted with Silver Nanoparticles

Muller

Baldwin

Barbacci

et al. 2017

J. Am. Soc. Mass Spectrom.

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Mass spectrometry imaging (MSI) of tissue implanted with silver nanoparticulate (AgNP) matrix generates reproducible imaging of lipids in rodent models of disease and injury. Gas-phase production and acceleration of size-selected 8 nm AgNP is followed by controlled ion beam rastering and soft landing implantation of 500 eV AgNP into tissue. Focused 337 nm laser desorption produces high quality images for most lipid classes in rat brain tissue (in positive mode: galactoceramides, diacylglycerols, ceramides, phosphatidylcholines, cholesteryl ester, and cholesterol, and in negative ion mode: phosphatidylethanolamides, sulfatides, phosphatidylinositol, and sphingomyelins). Image reproducibility in serial sections of brain tissue is achieved within <10% tolerance by selecting argentated instead of alkali cationized ions. The imaging of brain tissues spotted with pure standards was used to demonstrate that Ag cationized ceramide and diacylglycerol ions are from intact, endogenous species. In contrast, almost all Ag cationized fatty acid ions are a result of fragmentations of numerous lipid types having the fatty acid as a subunit. Almost no argentated intact fatty acid ions come from the pure fatty acid standard on tissue. Graphical Abstract ᅟ.

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“…The resulting MALDI images, therefore, provide a multilipid spatially unbiased readout of lipid distributions compared with more traditional biochemical analysis of isolated brain regions. Although recent publications have shown the utility of MALDI IMS in assessing changes in lipid distributions in the brain after blast injury 45 and pericontusional changes after CCI, 46 the current study provides early postinjury evidence of altered changes in specific lipids related to LPA and LPA metabolites in both proximal and remote regions of the brain after injury. The most pronounced expression occurred in white matter tracts throughout the brain, including the corpus callosum and the cerebellum.…”

Section: Enhanced Lpa Metabolism As a Potential Marker Of Diaschisis mentioning

confidence: 65%

Matrix-Assisted Laser Desorption Ionization Mapping of Lysophosphatidic Acid Changes after Traumatic Brain Injury and the Relationship to Cellular Pathology

McDonald

Jones

Wojciak

et al. 2018

The American Journal of Pathology

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Lysophosphatidic acid (LPA) levels increase in the cerebrospinal fluid and blood within 24 hours after traumatic brain injury (TBI), indicating it may be a biomarker for subsequent cellular pathology. However, no data exist that document this association after TBI. We, therefore, acquired matrix-assisted laser desorption ionization imaging mass spectrometry data of LPA, major LPA metabolites, and hemoglobin from adult rat brains at 1 and 3 hours after controlled cortical impact injury. Data were semiquantitatively assessed by signal intensity analysis normalized to naïve rat brains acquired concurrently. Gray and white matter pathology was assessed on adjacent sections using immunohistochemistry for cell death, axonal injury, and intracellular LPA, to determine the spatiotemporal patterning of LPA corresponding to pathology. The results revealed significant increases in LPA and LPA precursors at 1 hour after injury and robust enhancement in LPA diffusively throughout the brain at 3 hours after injury. Voxel-wise analysis of LPA by matrix-assisted laser desorption ionization and β-amyloid precursor protein by immunohistochemistry in adjacent sections showed significant association, raising the possibility that LPA is linked to secondary axonal injury. Total LPA and metabolites were also present in remotely injured areas, including cerebellum and brain stem, and in particular thalamus, where intracellular LPA is associated with cell death. LPA may be a useful biomarker of cellular pathology after TBI.

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Mass spectrometry imaging of rat brain lipid profile changes over time following traumatic brain injury

Abstract: Lipid biochemical and structural changes after TBI could help highlighting molecules that can be used to determine the severity of such injuries as well as to evaluate the efficacy of potential treatments.

Cited by 90 publications

References 50 publications

Gas Cluster Ion Beam Time-of-Flight Secondary Ion Mass Spectrometry High-Resolution Imaging of Cardiolipin Speciation in the Brain: Identification of Molecular Losses after Traumatic Injury

Gas Cluster Ion Beam Time-of-Flight Secondary Ion Mass Spectrometry High-Resolution Imaging of Cardiolipin Speciation in the Brain: Identification of Molecular Losses after Traumatic Injury

Laser Desorption/Ionization Mass Spectrometric Imaging of Endogenous Lipids from Rat Brain Tissue Implanted with Silver Nanoparticles

Matrix-Assisted Laser Desorption Ionization Mapping of Lysophosphatidic Acid Changes after Traumatic Brain Injury and the Relationship to Cellular Pathology

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