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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

  • 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
  • , and 
  • 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]
Cite this: ACS Chem. Neurosci. 2019, 10, 10, 4394–4406
Publication Date (Web):September 12, 2019
https://doi.org/10.1021/acschemneuro.9b00435
Copyright © 2019 American Chemical Society

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    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.

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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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    Cited By

    This article is cited by 8 publications.

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    2. Yihan Wang, Shunxiang Li, Kun Qian. Nanoparticle-based applications by atmospheric pressure matrix assisted desorption/ionization mass spectrometry. Nanoscale Advances 2023, 5 (24) , 6804-6818. https://doi.org/10.1039/D3NA00734K
    3. Lanchi Zhang, Jingri Xie. Biosynthesis, structure and biological function of cholesterol glucoside in Helicobacter pylori: A review. Medicine 2023, 102 (36) , e34911. https://doi.org/10.1097/MD.0000000000034911
    4. Jessica Hernandez, Julia Schäffer, Christiane Herden, Fabian Johannes Pflieger, Sylvia Reiche, Svenja Körber, Hiromu Kitagawa, Joelle Welter, Susanne Michels, Carsten Culmsee, Jens Bier, Natascha Sommer, Jing X. Kang, Konstantin Mayer, Matthias Hecker, Christoph Rummel. n-3 Polyunsaturated Fatty Acids Modulate LPS-Induced ARDS and the Lung–Brain Axis of Communication in Wild-Type versus Fat-1 Mice Genetically Modified for Leukotriene B4 Receptor 1 or Chemerin Receptor 23 Knockout. International Journal of Molecular Sciences 2023, 24 (17) , 13524. https://doi.org/10.3390/ijms241713524
    5. Huihui Liu, Yixin Pan, Caiqiao Xiong, Jing Han, Xiao Wang, Junyu Chen, Zongxiu Nie. Matrix-assisted laser desorption/ionization mass spectrometry imaging (MALDI MSI) for in situ analysis of endogenous small molecules in biological samples. TrAC Trends in Analytical Chemistry 2022, 157 , 116809. https://doi.org/10.1016/j.trac.2022.116809
    6. Xiaoping Zhu, Tianyi Xu, Chen Peng, Shihua Wu. Advances in MALDI Mass Spectrometry Imaging Single Cell and Tissues. Frontiers in Chemistry 2022, 9 https://doi.org/10.3389/fchem.2021.782432
    7. Janne Bredehöft, Amalia M Dolga, Birgit Honrath, Sybille Wache, Sybille Mazurek, Carsten Culmsee, Regien G Schoemaker, Rüdiger Gerstberger, Joachim Roth, Christoph Rummel. SK-Channel Activation Alters Peripheral Metabolic Pathways in Mice, but Not Lipopolysaccharide-Induced Fever or Inflammation. Journal of Inflammation Research 2022, Volume 15 , 509-531. https://doi.org/10.2147/JIR.S338812
    8. Lina Xu, Maximilian V. Schmitt, Huabin Ruan, Yupei Jiao, Xueying Wang, Yusong Wang, Tao Yang, Philip Lienau, Andreas Reichel, Xiaohui Liu, . Systematic Analysis of the Whole-Body Tissue Distribution and Fatty Acid Compositions of Membrane Lipids in CD1 and NMRI Mice and Wistar Rats. International Journal of Analytical Chemistry 2020, 2020 , 1-12. https://doi.org/10.1155/2020/8819437

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