Article

ErbB4 deficiency exacerbates olfactory dysfunction in an early-stage Alzheimer’s disease mouse model

Xian-hua Deng1,2, Xing-yang Liu1,2, Yi-hua Wei1,2, Ke Wang1,2, Jun-rong Zhu1, Jia-jun Zhong1, Jing-yuan Zheng1, Rui Guo1, Yi-fan Zhu1, Qiu-hong Ye1, Meng-dan Wang1, Ying-jie Chen1, Jian-quan He3, Ze-xu Chen1, Shu-qiong Huang1, Chong-shan Lv1, Guo-qing Zheng2, Sui-feng Liu3, Lei Wen1
1 Center for Brain Sciences, The First Affiliated Hospital of Xiamen University, State Key Laboratory of Cellular Stress Biology, Fujian Provincial Key Laboratory of Neurodegenerative Disease and Aging Research, Institute of Neuroscience, School of Medicine, Xiamen University, Xiamen 361000, China
2 Department of Neurology, The First Affiliated Hospital of Zhejiang Chinese Medical University (Zhejiang Provincial Hospital of Chinese Medicine), Hangzhou 310006, China
3 Zhongshan Hospital, School of Medicine, Xiamen University, Xiamen 361000, China
Correspondence to: Guo-qing Zheng: gq_zheng@sohu.com, Sui-feng Liu: liujiasuifeng@gmail.com, Lei Wen: wenlei@xmu.edu.cn,
DOI: 10.1038/s41401-024-01332-6
Received: 13 February 2024
Accepted: 2 June 2024
Advance online: 9 July 2024

Abstract

Olfactory dysfunction is increasingly recognized as an early indicator of Alzheimer’s disease (AD). Aberrations in GABAergic function and the excitatory/inhibitory (E/I) balance within the olfactory bulb (OB) have been implicated in olfactory impairment during the initial stages of AD. While the neuregulin 1 (NRG1)/ErbB4 signaling pathway is known to regulate GABAergic transmission in the brain and is associated with various neuropsychiatric disorders, its specific role in early AD-related olfactory impairment remains incompletely understood. This study demonstrated that olfactory dysfunction preceded cognitive decline in young adult APP/PS1 mice and was characterized by reduced levels of NRG1 and ErbB4 in the OB. Further investigation revealed that deletion of ErbB4 in parvalbumin interneurons reduced GABAergic transmission and increased hyperexcitability in mitral and tufted cells (M/Ts) in the OB, thereby accelerating olfactory dysfunction in young adult APP/PS1 mice. Additionally, ErbB4 deficiency was associated with increased accumulation of Aβ and BACE1-mediated cleavage of APP, along with enhanced CDK5 signaling in the OB. NRG1 infusion into the OB was found to enhance GABAergic transmission in M/Ts and alleviate olfactory dysfunction in young adult APP/PS1 mice. These findings underscore the critical role of NRG1/ErbB4 signaling in regulating GABAergic transmission and E/I balance within the OB, contributing to olfactory impairment in young adult APP/PS1 mice, and provide novel insights for early intervention strategies in AD.
Keywords: Alzheimer’s disease; olfactory impairment; NRG1/ErbB4 signaling; GABAergic transmission; excitation/inhibition (E/I) imbalance

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