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The Sea Cucumber Thyonella gemmata Contains a Low Anticoagulant Sulfated Fucan with High Anti-SARS-CoV-2 Actions against Wild-Type and Delta Variants

  • Rohini Dwivedi
    Rohini Dwivedi
    Department of BioMolecular Sciences, University of Mississippi, Oxford, Mississippi 38677, United States
  • Marwa Farrag
    Marwa Farrag
    Department of BioMolecular Sciences, University of Mississippi, Oxford, Mississippi 38677, United States
    Department of Pharmacognosy, Faculty of Pharmacy, Assiut University, Assiut 71515, Egypt
    More by Marwa Farrag
  • Poonam Sharma
    Poonam Sharma
    Center for Immunology and Microbial Research, Department of Cell and Molecular Biology, University of Mississippi Medical Center, Jackson, Mississippi 39216, United States
  • Deling Shi
    Deling Shi
    Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, New York 12180, United States
    More by Deling Shi
  • Anter A. Shami
    Anter A. Shami
    Department of BioMolecular Sciences, University of Mississippi, Oxford, Mississippi 38677, United States
  • Sandeep K. Misra
    Sandeep K. Misra
    Department of BioMolecular Sciences, University of Mississippi, Oxford, Mississippi 38677, United States
  • Priya Ray
    Priya Ray
    Center for Immunology and Microbial Research, Department of Cell and Molecular Biology, University of Mississippi Medical Center, Jackson, Mississippi 39216, United States
    More by Priya Ray
  • Jayanti Shukla
    Jayanti Shukla
    Center for Immunology and Microbial Research, Department of Cell and Molecular Biology, University of Mississippi Medical Center, Jackson, Mississippi 39216, United States
  • Fuming Zhang
    Fuming Zhang
    Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, New York 12180, United States
    More by Fuming Zhang
  • Robert J. Linhardt
    Robert J. Linhardt
    Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, Troy, New York 12180, United States
  • Joshua S. Sharp
    Joshua S. Sharp
    Department of BioMolecular Sciences, University of Mississippi, Oxford, Mississippi 38677, United States
    Department of Chemistry and Biochemistry, University of Mississippi, Oxford, Mississippi 38677, United States
    Research Institute of Pharmaceutical Sciences, School of Pharmacy, University of Mississippi, Oxford, Mississippi 38677, United States
  • Ritesh Tandon
    Ritesh Tandon
    Department of BioMolecular Sciences, University of Mississippi, Oxford, Mississippi 38677, United States
    Center for Immunology and Microbial Research, Department of Cell and Molecular Biology, University of Mississippi Medical Center, Jackson, Mississippi 39216, United States
    Department of Medicine, University of Mississippi Medical Center, Jackson, Mississippi 39216, United States
  • , and 
  • Vitor H. Pomin*
    Vitor H. Pomin
    Department of BioMolecular Sciences, University of Mississippi, Oxford, Mississippi 38677, United States
    Research Institute of Pharmaceutical Sciences, School of Pharmacy, University of Mississippi, Oxford, Mississippi 38677, United States
    *Email: [email protected]. Tel: +01-662-915-3114.
Cite this: J. Nat. Prod. 2023, 86, 6, 1463–1475
Publication Date (Web):June 12, 2023
https://doi.org/10.1021/acs.jnatprod.3c00151
Copyright © 2023 American Chemical Society and American Society of Pharmacognosy

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    Supporting Info (1)»

    Abstract

    Abstract Image

    In this work, we isolated two new sulfated glycans from the body wall of the sea cucumber Thyonella gemmata: one fucosylated chondroitin sulfate (TgFucCS) (17.5 ± 3.5% kDa) and one sulfated fucan (TgSF) (383.3 ± 2.1% kDa). NMR results showed the TgFucCS backbone composed of [→3)-β-N-acetylgalactosamine-(1→4)-β-glucuronic acid-(1→] with 70% 4-sulfated and 30% 4,6-disulfated GalNAc units and one-third of the GlcA units decorated at the C3 position with branching α-fucose (Fuc) units either 4-sulfated (65%) or 2,4-disulfated (35%) and the TgSF structure composed of a tetrasaccharide repeating unit of [→3)-α-Fuc2,4S-(1→2)-α-Fuc4S-(1→3)-α-Fuc2S-(1→3)-α-Fuc2S-(1→]n. Inhibitory properties of TgFucCS and TgSF were investigated using SARS-CoV-2 pseudovirus coated with S-proteins of the wild-type (Wuhan-Hu-1) or the delta (B.1.617.2) strains and in four different anticoagulant assays, comparatively with unfractionated heparin. Molecular binding to coagulation (co)-factors and S-proteins was investigated by competitive surface plasmon resonance spectroscopy. Among the two sulfated glycans tested, TgSF showed significant anti-SARS-CoV-2 activity against both strains together with low anticoagulant properties, indicating a good candidate for future studies in drug development.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.jnatprod.3c00151.

    • Additional 2D NMR spectra of TgFucCS and TgSF; fluorescence micrographs showing SARS-CoV-2 wild-type and delta titers; tables presenting IC50 and Imax values of biological activities; SPR sensorgrams (PDF)

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