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Cell. 2018 Jun 14;173(7):1716-1727.e17. doi: 10.1016/j.cell.2018.04.014. Epub 2018 May 17.

Moderate UV Exposure Enhances Learning and Memory by Promoting a Novel Glutamate Biosynthetic Pathway in the Brain.

Author information

1
Hefei National Laboratory for Physical Sciences at the Microscale, Neurodegenerative Disorder Research Center, School of Life Sciences, University of Science and Technology of China, 230026 Hefei, China; Hefei National Laboratory for Physical Sciences at the Microscale, School of Chemistry and Materials Science, University of Science and Technology of China, 230026 Hefei, China.
2
Hefei National Laboratory for Physical Sciences at the Microscale, Neurodegenerative Disorder Research Center, School of Life Sciences, University of Science and Technology of China, 230026 Hefei, China.
3
High Magnetic Field Laboratory, Chinese Academy of Sciences, 230031 Hefei, China.
4
Key Laboratory of Animal Models and Human Disease Mechanisms of Chinese Academy of Sciences & Yunnan Province, Kunming Institute of Zoology, Chinese Academy of Sciences, 650223 Kunming, China.
5
Hefei National Laboratory for Physical Sciences at the Microscale, Neurodegenerative Disorder Research Center, School of Life Sciences, University of Science and Technology of China, 230026 Hefei, China; Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, 200031 Shanghai, China.
6
Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, 200031 Shanghai, China; High Magnetic Field Laboratory, Chinese Academy of Sciences, 230031 Hefei, China.
7
Hefei National Laboratory for Physical Sciences at the Microscale, School of Chemistry and Materials Science, University of Science and Technology of China, 230026 Hefei, China. Electronic address: gmhuang@ustc.edu.cn.
8
Hefei National Laboratory for Physical Sciences at the Microscale, Neurodegenerative Disorder Research Center, School of Life Sciences, University of Science and Technology of China, 230026 Hefei, China; Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, 200031 Shanghai, China. Electronic address: wxiong@ustc.edu.cn.

Abstract

Sunlight exposure is known to affect mood, learning, and cognition. However, the molecular and cellular mechanisms remain elusive. Here, we show that moderate UV exposure elevated blood urocanic acid (UCA), which then crossed the blood-brain barrier. Single-cell mass spectrometry and isotopic labeling revealed a novel intra-neuronal metabolic pathway converting UCA to glutamate (GLU) after UV exposure. This UV-triggered GLU synthesis promoted its packaging into synaptic vesicles and its release at glutamatergic terminals in the motor cortex and hippocampus. Related behaviors, like rotarod learning and object recognition memory, were enhanced after UV exposure. All UV-induced metabolic, electrophysiological, and behavioral effects could be reproduced by the intravenous injection of UCA and diminished by the application of inhibitor or short hairpin RNA (shRNA) against urocanase, an enzyme critical for the conversion of UCA to GLU. These findings reveal a new GLU biosynthetic pathway, which could contribute to some of the sunlight-induced neurobehavioral changes.

KEYWORDS:

UV light; glutamate; hippocampus; learning; mass spectrometry; memory; motor cortex; single cell; sunlight; urocanic acid

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PMID:
29779945
DOI:
10.1016/j.cell.2018.04.014
[Indexed for MEDLINE]
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