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Visualizing and Profiling Lipids in the OVLT of Fat-1 and Wild Type Mouse Brains during LPS-Induced Systemic Inflammation Using AP-SMALDI MSI
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    Visualizing and Profiling Lipids in the OVLT of Fat-1 and Wild Type Mouse Brains during LPS-Induced Systemic Inflammation Using AP-SMALDI MSI
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    • Janne Bredehöft
      Janne Bredehöft
      Institute of Veterinary Physiology and Biochemistry, Justus Liebig University Giessen, Frankfurter Strasse 100, D-35392 Giessen, Germany
    • Dhaka Ram Bhandari
      Dhaka Ram Bhandari
      Institute of Inorganic and Analytical Chemistry, Justus Liebig University Giessen, Heinrich-Buff-Ring 17, D-35392 Giessen, Germany
    • Fabian Johannes Pflieger
      Fabian Johannes Pflieger
      Institute of Veterinary Physiology and Biochemistry, Justus Liebig University Giessen, Frankfurter Strasse 100, D-35392 Giessen, Germany
    • Sabine Schulz
      Sabine Schulz
      Institute of Inorganic and Analytical Chemistry, Justus Liebig University Giessen, Heinrich-Buff-Ring 17, D-35392 Giessen, Germany
    • Jing X. Kang
      Jing X. Kang
      Laboratory for Lipid Medicine and Technology, Department of Medicine, Massachusetts General Hospital and Harvard Medical School, 149 13th Street, Charlestown, Massachusetts 02129, United States
      More by Jing X. Kang
    • Sophie Layé
      Sophie Layé
      UMR 1286, NutriNeuro: Laboratoire Nutrition et Neurobiologie Intégrée, Institut National de la Recherche Agronomique, Université de Bordeaux, Bordeaux 33076, France
      More by Sophie Layé
    • Joachim Roth
      Joachim Roth
      Institute of Veterinary Physiology and Biochemistry, Justus Liebig University Giessen, Frankfurter Strasse 100, D-35392 Giessen, Germany
      Center for Mind, Brain and Behavior (CMBB), University of Marburg and Justus Liebig University Giessen, Marburg 35032, Germany
      More by Joachim Roth
    • Rüdiger Gerstberger
      Rüdiger Gerstberger
      Institute of Veterinary Physiology and Biochemistry, Justus Liebig University Giessen, Frankfurter Strasse 100, D-35392 Giessen, Germany
    • Konstantin Mayer
      Konstantin Mayer
      University of Giessen and Marburg Lung Center (UGMLC), Justus Liebig University Giessen, Klinikstrasse 33, Giessen D-35392, Germany
    • Bernhard Spengler
      Bernhard Spengler
      Institute of Inorganic and Analytical Chemistry, Justus Liebig University Giessen, Heinrich-Buff-Ring 17, D-35392 Giessen, Germany
    • Christoph Rummel*
      Christoph Rummel
      Institute of Veterinary Physiology and Biochemistry, Justus Liebig University Giessen, Frankfurter Strasse 100, D-35392 Giessen, Germany
      Center for Mind, Brain and Behavior (CMBB), University of Marburg and Justus Liebig University Giessen, Marburg 35032, Germany
      *E-mail: [email protected]
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    ACS Chemical Neuroscience

    Cite this: ACS Chem. Neurosci. 2019, 10, 10, 4394–4406
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    https://doi.org/10.1021/acschemneuro.9b00435
    Published September 12, 2019
    Copyright © 2019 American Chemical Society

    Abstract

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    Lipids, including omega-3 polyunsaturated fatty acids (n-3-PUFAs), modulate brain-intrinsic inflammation during systemic inflammation. The vascular organ of the lamina terminalis (OVLT) is a brain structure important for immune-to-brain communication. We, therefore, aimed to profile the distribution of several lipids (e.g., phosphatidyl-choline/ethanolamine, PC/PE), including n-3-PUFA-carrying lipids (esterified in phospholipids), in the OVLT during systemic lipopolysaccharide(LPS)-induced inflammation. We injected wild type and endogenously n-3-PUFA producing fat-1 transgenic mice with LPS (i.p., 2.5 mg/kg) or PBS. Brain samples were analyzed using immunohistochemistry and high-resolution atmospheric-pressure scanning microprobe matrix-assisted laser desorption/ionization orbital trapping mass spectrometry imaging (AP-SMALDI-MSI) for spatial resolution of lipids. Depending on genotype and treatment, several distinct distribution patterns were observed for lipids [e.g., lyso(L)PC (16:0)/(18:0)] proposed to be involved in inflammation. The distribution patterns ranged from being homogeneously disseminated [LPC (18:1)], absent/reduced signaling within the OVLT relative to adjacent preoptic tissue [PE (38:6)], either treatment- and genotype-dependent or independent low signal intensities [LPC (18:0)], treatment- and genotype-dependent [PC 38:6)] or independent accumulation in the OVLT [PC (38:7)], and accumulation in commissures, e.g., nerve fibers like the optic nerve [LPE (18:1)]. Overall, screening of lipid distribution patterns revealed distinct inflammation-induced changes in the OVLT, highlighting the prominent role of lipid metabolism in brain inflammation. Moreover, known and novel candidates for brain inflammation and immune-to-brain communication were detected specifically within this pivotal brain structure, a window between the periphery and the brain. The biological significance of these newly identified lipids abundant in the OVLT and the adjacent preoptic area remains to be further analyzed.

    Copyright © 2019 American Chemical Society

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    Supporting Information

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    Supplementary Figures: The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acschemneuro.9b00435.

    • SMALDI-MS images from three biological replicates of PBS treated fat-1 mice; SMALDI-MS images of different ion adducts from measured phospholipids; SMALDI-MS images of the distribution of free fatty acids; SMALDI MS/MS spectra for detection of lipid head groups (PDF)

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    This article is cited by 8 publications.

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    ACS Chemical Neuroscience

    Cite this: ACS Chem. Neurosci. 2019, 10, 10, 4394–4406
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acschemneuro.9b00435
    Published September 12, 2019
    Copyright © 2019 American Chemical Society

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