Olfactory sensory experience regulates gliomagenesis via neuronal IGF1

Pengxiang Chen, Wei Wang, Rui Liu, Jiahui Lyu, Lei Zhang, Baizhou Li, Biying Qiu, Anhao Tian, Wenhong Jiang, Honggang Ying, Rui Jing, Qianqian Wang, Keqing Zhu, Ruiliang Bai, Linghui Zeng, Shumin Duan and Chong Liu ()
Additional contact information
Pengxiang Chen: Zhejiang University School of Medicine
Wei Wang: Zhejiang University School of Medicine
Rui Liu: Zhejiang University School of Medicine
Jiahui Lyu: Fudan University
Lei Zhang: Zhejiang University School of Medicine
Baizhou Li: Zhejiang University School of Medicine
Biying Qiu: Zhejiang University School of Medicine
Anhao Tian: Zhejiang University School of Medicine
Wenhong Jiang: Zhejiang University School of Medicine
Honggang Ying: Zhejiang University School of Medicine
Rui Jing: Zhejiang University School of Medicine
Qianqian Wang: Laboratory Animal Center of Zhejiang University
Keqing Zhu: Zhejiang University School of Medicine
Ruiliang Bai: Zhejiang University School of Medicine
Linghui Zeng: Zhejiang University City College
Shumin Duan: Zhejiang University School of Medicine
Chong Liu: Zhejiang University School of Medicine

Nature, 2022, vol. 606, issue 7914, 550-556

Abstract: Abstract Animals constantly receive various sensory stimuli, such as odours, sounds, light and touch, from the surrounding environment. These sensory inputs are essential for animals to search for food and avoid predators, but they also affect their physiological status, and may cause diseases such as cancer. Malignant gliomas—the most lethal form of brain tumour1—are known to intimately communicate with neurons at the cellular level2,3. However, it remains unclear whether external sensory stimuli can directly affect the development of malignant glioma under normal living conditions. Here we show that olfaction can directly regulate gliomagenesis. In an autochthonous mouse model that recapitulates adult gliomagenesis4–6 originating in oligodendrocyte precursor cells (OPCs), gliomas preferentially emerge in the olfactory bulb—the first relay of brain olfactory circuitry. Manipulating the activity of olfactory receptor neurons (ORNs) affects the development of glioma. Mechanistically, olfaction excites mitral and tufted (M/T) cells, which receive sensory information from ORNs and release insulin-like growth factor 1 (IGF1) in an activity-dependent manner. Specific knockout of Igf1 in M/T cells suppresses gliomagenesis. In addition, knocking out the IGF1 receptor in pre-cancerous mutant OPCs abolishes the ORN-activity-dependent mitogenic effects. Our findings establish a link between sensory experience and gliomagenesis through their corresponding sensory neuronal circuits.

Date: 2022
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DOI: 10.1038/s41586-022-04719-9

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