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α-Conotoxin Vc1.1 Structure–Activity Relationship at the Human α9α10 Nicotinic Acetylcholine Receptor Investigated by Minimal Side Chain Replacement
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    α-Conotoxin Vc1.1 Structure–Activity Relationship at the Human α9α10 Nicotinic Acetylcholine Receptor Investigated by Minimal Side Chain Replacement
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    • Xin Chu
      Xin Chu
      Key Laboratory of Marine Drugs, Chinese Ministry of Education, School of Medicine and Pharmacy, Ocean University of China, 5 Yushan Road, Qingdao 266003, China
      Laboratory for Marine Drugs and Bioproducts, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266003, China
      More by Xin Chu
    • Han-Shen Tae*
      Han-Shen Tae
      Illawarra Health and Medical Research Institute (IHMRI), University of Wollongong, Wollongong, New South Wales 2522, Australia
      *E-mail: [email protected]
      More by Han-Shen Tae
    • Qingliang Xu
      Qingliang Xu
      Key Laboratory of Marine Drugs, Chinese Ministry of Education, School of Medicine and Pharmacy, Ocean University of China, 5 Yushan Road, Qingdao 266003, China
      Laboratory for Marine Drugs and Bioproducts, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266003, China
      More by Qingliang Xu
    • Tao Jiang
      Tao Jiang
      Key Laboratory of Marine Drugs, Chinese Ministry of Education, School of Medicine and Pharmacy, Ocean University of China, 5 Yushan Road, Qingdao 266003, China
      Laboratory for Marine Drugs and Bioproducts, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266003, China
      More by Tao Jiang
    • David J. Adams
      David J. Adams
      Illawarra Health and Medical Research Institute (IHMRI), University of Wollongong, Wollongong, New South Wales 2522, Australia
    • Rilei Yu*
      Rilei Yu
      Key Laboratory of Marine Drugs, Chinese Ministry of Education, School of Medicine and Pharmacy, Ocean University of China, 5 Yushan Road, Qingdao 266003, China
      Laboratory for Marine Drugs and Bioproducts, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266003, China
      Innovation Center for Marine Drug Screening & Evaluation, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266003, China
      *E-mail: [email protected]
      More by Rilei Yu
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    ACS Chemical Neuroscience

    Cite this: ACS Chem. Neurosci. 2019, 10, 10, 4328–4336
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    https://doi.org/10.1021/acschemneuro.9b00389
    Published August 14, 2019
    Copyright © 2019 American Chemical Society

    Abstract

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    α-Conotoxin Vc1.1 inhibits the nicotinic acetylcholine receptor (nAChR) α9α10 subtype and has the potential to treat neuropathic chronic pain. To date, the crystal structure of Vc1.1-bound α9α10 nAChR remains unavailable; thus, understanding the structure–activity relationship of Vc1.1 with the α9α10 nAChR remains challenging. In this study, the Vc1.1 side chains were minimally modified to avoid introducing large local conformation perturbation to the interactions between Vc1.1 and α9α10 nAChR. The results suggest that the hydroxyl group of Vc1.1, Y10, forms a hydrogen bond with the carbonyl group of α9 N107 and a hydrogen bond donor is required. However, Vc1.1 S4 is adjacent to the α9 D166 and D169, and a positive charge residue at this position increases the binding affinity of Vc1.1. Furthermore, the carboxyl group of Vc1.1, D11, forms two hydrogen bonds with α9 N154 and R81, respectively, whereas introducing an extra carboxyl group at this position significantly decreases the potency of Vc1.1. Second-generation mutants of Vc1.1 [S4 Dab, N9A] and [S4 Dab, N9W] increased potency at the α9α10 nAChR by 20-fold compared with that of Vc1.1. The [S4 Dab, N9W] mutational effects at positions 4 and 9 of Vc1.1 are not cumulative but are coupled with each other. Overall, our findings provide valuable insights into the structure–activity relationship of Vc1.1 with the α9α10 nAChR and will contribute to further development of more potent and specific Vc1.1 analogues.

    Copyright © 2019 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.9b00389.

    • Figures showing the structure of unnatural amino acids, the circular dichroism, the root-mean-square deviation of α9α10 nAChR bound with Vc1.1 and its unnatural analogues, evolution of the distances between the pairwise interacting residues from Vc1.1 and α9α10 nAChR, and mass spectrometry spectra (PDF)

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    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

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    This article is cited by 17 publications.

    1. Xiao Li, Han-Shen Tae, Shen Chen, Arsalan Yousuf, Linhong Huang, Jinghui Zhang, Tao Jiang, David J. Adams, Rilei Yu. Dual Antagonism of α9α10 nAChR and GABAB Receptor-Coupled CaV2.2 Channels by an Analgesic αO-Conotoxin Analogue. Journal of Medicinal Chemistry 2024, 67 (2) , 971-987. https://doi.org/10.1021/acs.jmedchem.3c00979
    2. Jiazhen Liang, Han-Shen Tae, Zitong Zhao, Xiao Li, Jinghui Zhang, Shen Chen, Tao Jiang, David J. Adams, Rilei Yu. Mechanism of Action and Structure–Activity Relationship of α-Conotoxin Mr1.1 at the Human α9α10 Nicotinic Acetylcholine Receptor. Journal of Medicinal Chemistry 2022, 65 (24) , 16204-16217. https://doi.org/10.1021/acs.jmedchem.2c00494
    3. Han-Shen Tae, Andrew Hung, Richard J. Clark, David J. Adams. Molecular determinants of the selectivity and potency of α-conotoxin Vc1.1 for human nicotinic acetylcholine receptors. Journal of Biological Chemistry 2024, 89 , 108017. https://doi.org/10.1016/j.jbc.2024.108017
    4. Honglin Ge, Qingliang Xu, Lixia Pan, Haozhi Sun, Sihan Li, Rilei Yu, Xin Shen, Feng Su. One-pot synthesis of cysteine-rich peptide via ‘2,2’-dithiobispyridine’ mediated sulfur exchange reaction. Tetrahedron Letters 2024, 141 , 155057. https://doi.org/10.1016/j.tetlet.2024.155057
    5. Tianmiao Li, Han-Shen Tae, Jiazhen Liang, Zixuan Zhang, Xiao Li, Tao Jiang, David J. Adams, Rilei Yu. Rational Design of Potent α-Conotoxin PeIA Analogues with Non-Natural Amino Acids for the Inhibition of Human α9α10 Nicotinic Acetylcholine Receptors. Marine Drugs 2024, 22 (3) , 110. https://doi.org/10.3390/md22030110
    6. Alessandro Giraudo, Marco Pallavicini, Cristiano Bolchi. Small molecule ligands for α9 * and α7 nicotinic receptors: A survey and an update, respectively. Pharmacological Research 2023, 193 , 106801. https://doi.org/10.1016/j.phrs.2023.106801
    7. Zitong Zhao, Teng Pan, Shen Chen, Peta J. Harvey, Jinghui Zhang, Xiao Li, Mengke Yang, Linhong Huang, Shoushi Wang, David J. Craik, Tao Jiang, Rilei Yu. Design, synthesis, and mechanism of action of novel μ-conotoxin KIIIA analogues for inhibition of the voltage-gated sodium channel Nav1.7. Journal of Biological Chemistry 2023, 299 (4) , 103068. https://doi.org/10.1016/j.jbc.2023.103068
    8. Irina Shelukhina, Andrei Siniavin, Igor Kasheverov, Lucy Ojomoko, Victor Tsetlin, Yuri Utkin. α7- and α9-Containing Nicotinic Acetylcholine Receptors in the Functioning of Immune System and in Pain. International Journal of Molecular Sciences 2023, 24 (7) , 6524. https://doi.org/10.3390/ijms24076524
    9. Majbrit Frøsig-Jørgensen, Jing Ji, Declan M. Gorman, Meng-Wei Kan, David J. Craik, . Discovery and optimisation of conotoxin Vc1.1 and analogues with analgesic properties. Australian Journal of Chemistry 2023, 76 (10) , 655-670. https://doi.org/10.1071/CH23155
    10. Sarah Westlake, Matthew Jones, Krishna D. Sharma, Jennifer Yanhua Xie. Letters to the editor: Nicotinic acetylcholine receptor ligands as potential targets for managing neuropathic pain induced by diabetic peripheral neuropathy. eNeurologicalSci 2022, 28 , 100416. https://doi.org/10.1016/j.ensci.2022.100416
    11. Igor Kasheverov, Denis Kudryavtsev, Irina Shelukhina, Georgy Nikolaev, Yuri Utkin, Victor Tsetlin. Marine Origin Ligands of Nicotinic Receptors: Low Molecular Compounds, Peptides and Proteins for Fundamental Research and Practical Applications. Biomolecules 2022, 12 (2) , 189. https://doi.org/10.3390/biom12020189
    12. Xiao Li, Han-Shen Tae, Yanyan Chu, Tao Jiang, David J. Adams, Rilei Yu. Medicinal chemistry, pharmacology, and therapeutic potential of α-conotoxins antagonizing the α9α10 nicotinic acetylcholine receptor. Pharmacology & Therapeutics 2021, 222 , 107792. https://doi.org/10.1016/j.pharmthera.2020.107792
    13. Pengfei Sun, Zhonglei Ji, Zhengyong Li, Bo Pan. Prevention of scar hyperplasia in the skin by conotoxin: A prospective review. Journal of Cosmetic Dermatology 2021, 20 (6) , 1885-1888. https://doi.org/10.1111/jocd.13761
    14. Adam C. Kennedy, Alessia Belgi, Benjamin W. Husselbee, David Spanswick, Raymond S. Norton, Andrea J. Robinson. α-Conotoxin Peptidomimetics: Probing the Minimal Binding Motif for Effective Analgesia. Toxins 2020, 12 (8) , 505. https://doi.org/10.3390/toxins12080505
    15. Xiao Li, Hao Liu, Chunxiao Gao, Yangyang Li, Dongning Jia, Yanbo Yang, Jinbo Yang, Zhiqiang Wei, Tao Jiang, Rilei Yu. ConoMode, a database for conopeptide binding modes. Database 2020, 2020 https://doi.org/10.1093/database/baaa058
    16. Marineil C. Gomez, Alisha Marcelle C. Aquino, Andrea R. Matira, Riggs Anton D. Alvarico, Reincess E. Valbuena, Lemmuel L. Tayo. Alpha-family of Conotoxins. 2019, 40-46. https://doi.org/10.1145/3365966.3365977
    17. Marineil C. Gomez, Riggs Anton D. Alvarico, Reincess E. Valbuena, Alisha Marcelle C. Aquino, Andrea R. Matira, Lemmuel L. Tayo. In silico Protein Structure Comparison of Conotoxins with VI/VII Cysteine Framework. 2019, 52-57. https://doi.org/10.1145/3365966.3365978

    ACS Chemical Neuroscience

    Cite this: ACS Chem. Neurosci. 2019, 10, 10, 4328–4336
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acschemneuro.9b00389
    Published August 14, 2019
    Copyright © 2019 American Chemical Society

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