Determinants of subtype-selectivity of the anthelmintic paraherquamide A on Caenorhabditis elegans nicotinic acetylcholine receptors.
Koizumi, W., Otsubo, S., Furutani, S., Niki, K., Takayama, K., Fujimura, S., Maekawa, T., Koyari, R., Ihara, M., Kai, K., Hayashi, H., Ali, M.S., Kage-Nakadai, E., Sattelle, D.B., Matsuda, K.(2023) Mol Pharmacol 
- PubMed: 36948535 
- DOI: https://doi.org/10.1124/molpharm.122.000601
- Primary Citation of Related Structures:  
7DJI - PubMed Abstract: 
The anthelmintic paraherquamide A acts selectively on the nematode L-type nicotinic acetylcholine receptors (nAChRs), but the mechanism of its selectivity is unknown. This study targeted the basis of paraherquamide A selectivity by determining an X-ray crystal structure of the acetylcholine binding protein (AChBP), a surrogate nAChR ligand-binding domain, complexed with the compound and by measuring its actions on wild-type and mutant Caenorhabditis elegans nematodes and functionally expressed C. elegans nAChRs. Paraherquamide A showed a higher efficacy for the levamisole-sensitive [L-type (UNC-38/UNC-29/UNC-63/LEV-1/LEV-8)] nAChR than the nicotine-sensitive [N-type (ACR-16)] nAChR, a result consistent with in vivo studies on wild-type worms and worms with mutations in subunits of these two classes of receptors. The X-ray crystal structure of the Ls -AChBP-paraherquamide A complex and site-directed amino acid mutation studies showed for the first time that loop C, loop E, and loop F of the orthosteric receptor binding site play critical roles in the observed L-type nAChR selective actions of paraherquamide A. SIGNIFICANCE STATEMENT: Paraherquamide A, an oxindole alkaloid, has been shown to act selectively on the L-type over N-type nAChRs in nematodes, but the mechanism of selectivity is unknown. We have co-crystallized paraherquamide A with the acetylcholine binding protein, a surrogate of nAChRs, and found that structural features of loop C, loop E, and loop F contribute to the L-type nAChR selectivity of the alkaloid. The results create a new platform for the design of anthelmintic drugs targeting cholinergic neurotransmission in parasitic nematodes.
Organizational Affiliation: 
Department of Applied Biological Chemistry, Faculty of Agriculture (W.K., S.O., S.Fur., K.N., K.T., S.Fuj., T.M., R.K., M.I., K.M.) and Agricultural Technology and Innovation Research Institute (K.M.), Kindai University, Nara, Japan; Graduate School of Agriculture (K.K., H.H.) and Graduate School of Human Life and Ecology (M.S.A., E.K-N.), Osaka Metropolitan University, Osaka, Japan; Faculty of Food Science and Technology, Chattogram Veterinary and Animal Sciences University, Chattogram, Bangladesh (M.S.A.); and Centre for Respiratory Biology, UCL Respiratory, Division of Medicine, University College London, London, UK (D.B.S.).