Article

Characterization of LTr1 derived from cruciferous vegetables as a novel anti-glioma agent via inhibiting TrkA/PI3K/AKT pathway

Qi-qi Song1, Li-ping Lin2, Ya-li Chen1, Jia-cheng Qian2, Ke Wei1, Jian-wei Su1, Jian-hua Ding3, Ming Lu3, Yang Liu1, Ren-xiang Tan2,4, Gang Hu1,3
1 Departments of Pharmacology, School of Medicine and Holistic Integrative Medicine, Nanjing University of Chinese Medicine, Nanjing 210023, China
2 State Key Laboratory Cultivation Base for TCM Quality and Efficacy, Nanjing University of Chinese Medicine, Nanjing 210023, China
3 Jiangsu Key Laboratory of Neurodegeneration, Department of Pharmacology, Nanjing Medical University, Nanjing 211100, China
4 State Key Laboratory of Pharmaceutical Biotechnology, Institute of Functional Biomolecules, Nanjing University, Nanjing 210023, China
Correspondence to: Yang Liu: liuyang@njucm.edu.cn, Ren-xiang Tan: liuyang@njucm.edu.cn, Gang Hu: liuyang@njucm.edu.cn,
DOI: 10.1038/s41401-022-01033-y
Received: 16 May 2022
Accepted: 15 December 2022
Advance online: 8 December 2022

Abstract

Malignant glioma is the most fatal, invasive brain cancer with limited treatment options. Our previous studies show that 2-(indol-3- ylmethyl)-3,3′-diindolylmethane (LTr1), a major metabolite of indole-3-carbinol (I3C) derived from cruciferous vegetables, produces anti-tumour effect against various tumour cell lines. In this study we characterized LTr1 as a novel anti-glioma agent. Based on screening 134 natural compounds and comparing the candidates’ efficacy and toxicity, LTr1 was selected as the lead compound. We showed that LTr1 potently inhibited the viability of human glioma cell lines (SHG-44, U87, and U251) with IC50 values of 1.97, 1.84, and 2.03 μM, respectively. Furthermore, administration of LTr1 (100,300 mg· kg−1 ·d−1, i.g. for 18 days) dose-dependently suppressed the tumour growth in a U87 xenograft nude mouse model. We demonstrated that LTr1 directly bound with TrkA to inhibit its kinase activity and the downstream PI3K/AKT pathway thus inducing significant S-phase cell cycle arrest and apoptosis in SHG-44 and U87 cells by activating the mitochondrial pathway and inducing the production of reactive oxygen species (ROS). Importantly, LTr1 could cross the blood-brain barrier to achieve the therapeutic concentration in the brain. Taken together, LTr1 is a safe and promising therapeutic agent against glioma through inhibiting TrkA/PI3K/AKT pathway.
Keywords: malignant glioma; 2-(indol-3-ylmethyl)-3 3′-diindolylmethane (LTr1); TrkA; reactive oxygen species; S phase cell cycle arrest; mitochondrial pathway; paclitaxel; cruciferous vegetables

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