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Lipid-Based Inhibitors Act Directly on GlyT2
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    Research Article

    Lipid-Based Inhibitors Act Directly on GlyT2
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    ACS Chemical Neuroscience

    Cite this: ACS Chem. Neurosci. 2019, 10, 3, 1668–1678
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    https://doi.org/10.1021/acschemneuro.8b00586
    Published December 5, 2018
    Copyright © 2018 American Chemical Society

    Abstract

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    The endogenous lipids N-arachidonylglycine and oleoyl-l-carnitine are potential therapeutic leads in the treatment of chronic pain through their inhibition of the glycine transporter GlyT2. However, their mechanism of action is unknown. It has been hypothesized that these “bioactive” lipids either inhibit GlyT2 indirectly, by significantly perturbing the biophysical properties of the membrane, or directly, by binding directly to the transporter (either from a membrane-exposed or solvent-exposed binding site). Here, we used molecular dynamics simulations to study the effects of the lipids anandamide, N-arachidonylglycine, and oleoyl-l-carnitine on (a) the biophysical properties of the bilayer and (b) direct binding interactions with GlyT2. During the simulations, the biophysical properties of the bilayer itself, for example, the area per lipid, bilayer thickness, and order parameters, were not significantly altered by the presence or type of bioactive lipid, regardless of the presence of GlyT2. Our work, together with previous computational and experimental data, suggests that these acyl-inhibitors of GlyT2 inhibit the transporter by directly binding to it. However, these bioactive lipids bound to various parts of GlyT2 and did not prefer a single binding site during 4.5 μs of simulation. We postulate that the binding site is located at the solvent-exposed regions of GlyT2. Understanding the mechanism of action of these and related bioactive lipids is essential in effectively developing high-affinity GlyT2 inhibitors for the treatment of pain.

    Copyright © 2018 American Chemical Society

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    Supporting Information

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acschemneuro.8b00586.

    • Order parameters for larger bilayer lacking GlyT2; root-mean-square deviation of GlyT2; and bioactive lipid binding patterns over time (PDF)

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    Cited By

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    This article is cited by 10 publications.

    1. Haina Gao, Bing Fang, Zhe Sun, Xiaoyu Du, Huiyuan Guo, Liang Zhao, Ming Zhang. Effect of Human Milk Oligosaccharides on Learning and Memory in Mice with Alzheimer’s Disease. Journal of Agricultural and Food Chemistry 2024, 72 (2) , 1067-1081. https://doi.org/10.1021/acs.jafc.3c05949
    2. Zachary J Frangos, Katie A Wilson, Heather M Aitken, Ryan Cantwell Chater, Robert J Vandenberg, Megan L O’Mara. Membrane cholesterol regulates inhibition and substrate transport by the glycine transporter, GlyT2. Life Science Alliance 2023, 6 (4) , e202201708. https://doi.org/10.26508/lsa.202201708
    3. Theodosia Vallianatou, Nicholas B. Bèchet, Mario S. P. Correia, Iben Lundgaard, Daniel Globisch. Regional Brain Analysis of Modified Amino Acids and Dipeptides during the Sleep/Wake Cycle. Metabolites 2022, 12 (1) , 21. https://doi.org/10.3390/metabo12010021
    4. Zachary J. Frangos, Ryan P. Cantwell Chater, Robert J. Vandenberg. Glycine Transporter 2: Mechanism and Allosteric Modulation. Frontiers in Molecular Biosciences 2021, 8 https://doi.org/10.3389/fmolb.2021.734427
    5. Tomasz Róg, Mykhailo Girych, Alex Bunker. Mechanistic Understanding from Molecular Dynamics in Pharmaceutical Research 2: Lipid Membrane in Drug Design. Pharmaceuticals 2021, 14 (10) , 1062. https://doi.org/10.3390/ph14101062
    6. Thomas M. Ackermann, Lars Allmendinger, Georg Höfner, Klaus T. Wanner. MS Binding Assays for Glycine Transporter 2 (GlyT2) Employing Org25543 as Reporter Ligand. ChemMedChem 2021, 16 (1) , 199-215. https://doi.org/10.1002/cmdc.202000342
    7. Stephen J. Fairweather, Nishank Shah, Stefan Brӧer. Heteromeric Solute Carriers: Function, Structure, Pathology and Pharmacology. 2020, 13-127. https://doi.org/10.1007/5584_2020_584
    8. Katie A. Wilson, Lily Wang, Hugo MacDermott-Opeskin, Megan L. O'Mara. The Fats of Life: Using Computational Chemistry to Characterise the Eukaryotic Cell Membrane. Australian Journal of Chemistry 2020, 73 (3) , 85. https://doi.org/10.1071/CH19353
    9. Shannon N Mostyn, Katie A Wilson, Alexandra Schumann-Gillett, Zachary J Frangos, Susan Shimmon, Tristan Rawling, Renae M Ryan, Megan L O'Mara, Robert J Vandenberg. Identification of an allosteric binding site on the human glycine transporter, GlyT2, for bioactive lipid analgesics. eLife 2019, 8 https://doi.org/10.7554/eLife.47150
    10. Mahmoud Al-Khrasani, Amir Mohammadzadeh, Mihály Balogh, Kornél Király, Szilvia Barsi, Benjamin Hajnal, László Köles, Zoltán S. Zádori, Laszlo G. Harsing. Glycine transporter inhibitors: A new avenue for managing neuropathic pain. Brain Research Bulletin 2019, 152 , 143-158. https://doi.org/10.1016/j.brainresbull.2019.07.008

    ACS Chemical Neuroscience

    Cite this: ACS Chem. Neurosci. 2019, 10, 3, 1668–1678
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acschemneuro.8b00586
    Published December 5, 2018
    Copyright © 2018 American Chemical Society

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