Article

mTOR regulates cocaine-induced behavioural sensitization through the SynDIG1–GluA2 interaction in the nucleus accumbens

Hong-chun Li1, Jia-mei Zhang1, Rui Xu1, Yong-hai Wang2, Wei Xu1, Rong Chen1, Xue-mei Wan1, Hao-luo Zhang1, Liang Wang1, Xiao-jie Wang1, Lin-hong Jiang1, Bin Liu2, Ying Zhao1, Yuan-yuan Chen1, Yan-ping Dai1, Min Li1, Hua-qin Zhang1, Zhen Yang3, Lin Bai3, Jie Zhang3, Hong-bo Wang2, Jing-wei Tian2, Ying-lan Zhao1, Xiao-bo Cen1
1 National Chengdu Center for Safety Evaluation of Drugs, State Key Laboratory of Biotherapy/Collaborative Innovation Center for Biotherapy, West China Hospital, Sichuan University, Chengdu 610041, China
2 Ministry of Education, Collaborative Innovation Center of Advanced Drug Delivery System and Biotech Drugs in Universities of Shandong, Yantai University, Yantai 264005, China
3 Histology and Imaging Platform, Core Facilities of West China Hospital, Sichuan University, Chengdu 610041, China
Correspondence to: Xiao-bo Cen: xbcen@scu.edu.cn,
DOI: 10.1038/s41401-021-00760-y
Received: 10 April 2021
Accepted: 8 August 2021
Advance online: 14 September 2021

Abstract

Behavioral sensitization is a progressive increase in locomotor or stereotypic behaviours in response to drugs. It is believed to contribute to the reinforcing properties of drugs and to play an important role in relapse after cessation of drug abuse. However, the mechanism underlying this behaviour remains poorly understood. In this study, we showed that mTOR signaling was activated during the expression of behavioral sensitization to cocaine and that intraperitoneal or intra-nucleus accumbens (NAc) treatment with rapamycin, a specific mTOR inhibitor, attenuated cocaine-induced behavioural sensitization. Cocaine significantly modified brain lipid profiles in the NAc of cocaine-sensitized mice and markedly elevated the levels of phosphatidylinositol-4- monophosphates (PIPs), including PIP, PIP2, and PIP3. The behavioural effect of cocaine was attenuated by intra-NAc administration of LY294002, an AKT-specific inhibitor, suggesting that PIPs may contribute to mTOR activation in response to cocaine. An RNA- sequencing analysis of the downstream effectors of mTOR signalling revealed that cocaine significantly decreased the expression of SynDIG1, a known substrate of mTOR signalling, and decreased the surface expression of GluA2. In contrast, AAV-mediated SynDIG1 overexpression in NAc attenuated intracellular GluA2 internalization by promoting the SynDIG1–GluA2 interaction, thus maintaining GluA2 surface expression and repressing cocaine-induced behaviours. In conclusion, NAc SynDIG1 may play a negative regulatory role in cocaine-induced behavioural sensitization by regulating synaptic surface expression of GluA2.
Keywords: mTOR; behavioural sensitization; SynDIG1; GluA2; nucleus accumbens

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