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Naphthylisoquinoline alkaloids, a new structural template inhibitor of Nav1.7 sodium channel

Qiao-qiao Wang1,2,3,4, Long Wang5,6, Wen-bo Zhang5,6, Chun-ping Tang1,2, Xue-qin Chen1,6, Yue-ming Zheng1,4,6, Sheng Yao1,2,4,7, Zhao-bing Gao1,4,5,6,7, Yang Ye1,2,4
1 State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai 201203, China
2 Natural Product Research Center, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai 201203, China
3 School of Life Science and Technology, ShanghaiTech University, Shanghai 201210, China
4 University of Chinese Academy of Sciences, Beijing 100049, China
5 School of Chinese Materia Medica, Nanjing University of Chinese Medicine, Nanjing 210046, China
6 Center for Neurological and Psychiatric Research and Drug Discovery, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai 201203, China
7 Zhongshan Institute of Drug Discovery, Institution for Drug Discovery Innovation, Chinese Academy of Science, Zhongshan 528400, China
Correspondence to: Yue-ming Zheng: zhengyueming@simm.ac.cn, Sheng Yao: yaosheng@simm.ac.cn, Zhao-bing Gao: zbgao@simm.ac.cn, Yang Ye: yye@simm.ac.cn,
DOI: 10.1038/s41401-023-01084-9
Received: 18 November 2022
Accepted: 27 March 2023
Advance online: 4 May 2023

Abstract

Voltage-gated sodium channel 1.7 (Nav1.7) remains one of the most promising drug targets for pain relief. In the current study, we conducted a high-throughput screening of natural products in our in-house compound library to discover novel Nav1.7 inhibitors, then characterized their pharmacological properties. We identified 25 naphthylisoquinoline alkaloids (NIQs) from Ancistrocladus tectorius to be a novel type of Nav1.7 channel inhibitors. Their stereostructures including the linkage modes of the naphthalene group at the isoquinoline core were revealed by a comprehensive analysis of HRESIMS, 1D, and 2D NMR spectra as well as ECD spectra and single-crystal X-ray diffraction analysis with Cu Kα radiation. All the NIQs showed inhibitory activities against the Nav1.7 channel stably expressed in HEK293 cells, and the naphthalene ring in the C-7 position displayed a more important role in the inhibitory activity than that in the C-5 site. Among the NIQs tested, compound 2 was the most potent with an IC50 of 0.73 ± 0.03 µM. We demonstrated that compound 2 (3 µM) caused dramatical shift of steady-state slow inactivation toward the hyperpolarizing direction (V1/2 values were changed from −39.54 ± 2.77 mV to −65.53 ± 4.39 mV, which might contribute to the inhibition of compound 2 against the Nav1.7 channel. In acutely isolated dorsal root ganglion (DRG) neurons, compound 2 (10 μM) dramatically suppressed native sodium currents and action potential firing. In the formalin-induced mouse inflammatory pain model, local intraplantar administration of compound 2 (2, 20, 200 nmol) dose-dependently attenuated the nociceptive behaviors. In summary, NIQs represent a new type of Nav1.7 channel inhibitors and may act as structural templates for the following analgesic drug development.

Keywords: Nav1.7 channel; naphthylisoquinolines; Ancistrocladus tectorius; dorsal root ganglion neurons; formalin-induced mouse inflammatory pain model; analgesics

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