First insights into region-specific lipidome alterations of prefrontal cortex and hippocampus of mice exposed chronically to microcystins

Jun He; Yang Chen; Shiming Dai; Feng Chen; Yeke Wang; Ting Shi; Liang Chen; Ying Liu; Jun Chen; Ping Xie

Environment International (Jul 2023)

First insights into region-specific lipidome alterations of prefrontal cortex and hippocampus of mice exposed chronically to microcystins

Jun He,
Yang Chen,
Shiming Dai,
Feng Chen,
Yeke Wang,
Ting Shi,
Liang Chen,
Ying Liu,
Jun Chen,
Ping Xie

Affiliations

Jun He: Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; University of Chinese Academy of Sciences (UCAS), Beijing 100049, China
Yang Chen: Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; University of Chinese Academy of Sciences (UCAS), Beijing 100049, China
Shiming Dai: Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; University of Chinese Academy of Sciences (UCAS), Beijing 100049, China
Feng Chen: Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; University of Chinese Academy of Sciences (UCAS), Beijing 100049, China
Yeke Wang: Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; University of Chinese Academy of Sciences (UCAS), Beijing 100049, China
Ting Shi: Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; University of Chinese Academy of Sciences (UCAS), Beijing 100049, China
Liang Chen: Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; University of Chinese Academy of Sciences (UCAS), Beijing 100049, China; Institute for Ecological Research and Pollution Control of Plateau Lakes, School of Ecology and Environmental Science, Yunnan University, Kunming 650500, China
Ying Liu: Institute for Ecological Research and Pollution Control of Plateau Lakes, School of Ecology and Environmental Science, Yunnan University, Kunming 650500, China
Jun Chen: Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; University of Chinese Academy of Sciences (UCAS), Beijing 100049, China; Corresponding authors at: Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China.
Ping Xie: Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; University of Chinese Academy of Sciences (UCAS), Beijing 100049, China; Institute for Ecological Research and Pollution Control of Plateau Lakes, School of Ecology and Environmental Science, Yunnan University, Kunming 650500, China; Corresponding authors at: Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China.

Journal volume & issue: Vol. 177
p. 108018

Abstract

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Microcystins (MCs), a group of most widespread freshwater cyanotoxins that possess strong neurotoxicity, can adversely affect brain structures and functions and are linked to neurodegenerative diseases. Despite the essential role of lipids in brain structures and functions, the brain lipidome profile of mammals exposed to MCs remains unexplored, hindering a clear understanding of the neurotoxic effects of MCs and underlying mechanisms. In this study, we performed untargeted lipidomic profiling using ultra-performance liquid chromatography–mass spectrometry (UPLC-MS) on the prefrontal cortex and hippocampus of mice orally exposed to 30 and 300 μg/kg body mass/day of microcystin-leucine arginine (MC-LR) for 180 days to evaluate the impacts of MC-LR on the brain lipidome profile and functions. Our results show that MC-LR resulted in a decline in cognitive parameters, as assessed by the Morris water maze test. Interestingly, apparent neurodegenerative changes were observed in the prefrontal cortex, but not in the hippocampus. Comprehensive lipidomic analyses uncovered profound, region-specific changes in the phospholipid and sphingolipid profile at the levels of lipid subclasses, lipid species, and fatty acyl composition. These changes showed overall decrease trends of lipid content in the prefrontal cortex yet increasing trends in the hippocampus. We identified distinct transcriptional regulations of lipid metabolism and apoptosis by MC-LR in the two regions, which appeared to underlie the neurodegenerative changes. Collectively, this study uncovers region-specific changes in the brain lipidome profile and functions induced by MCs, shedding light on the role of lipid dysfunction in neurotoxicity mechanism of MCs.

Published in Environment International

ISSN: 0160-4120 (Print)
Publisher: Elsevier
Country of publisher: United Kingdom
LCC subjects: Geography. Anthropology. Recreation: Environmental sciences
Website: https://www.journals.elsevier.com/environment-international

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