Organization and Evolution of Brain Lipidome Revealed by Large-Scale Analysis of Human, Chimpanzee, Macaque, and Mouse Tissues

Katarzyna Bozek; Yuning Wei; Zheng Yan; Xiling Liu; Jieyi Xiong; Masahiro Sugimoto; Masaru Tomita; Svante Pääbo; Chet C. Sherwood; Patrick R. Hof; John J. Ely; Yan Li; Dirk Steinhauser; Lothar Willmitzer; Patrick Giavalisco; Philipp Khaitovich

doi:10.1016/j.neuron.2015.01.003

Organization and Evolution of Brain Lipidome Revealed by Large-Scale Analysis of Human, Chimpanzee, Macaque, and Mouse Tissues

Katarzyna Bozek, Yuning Wei, Zheng Yan, Xiling Liu, Jieyi Xiong, Masahiro Sugimoto, Masaru Tomita, Svante Pääbo, Chet C. Sherwood, Patrick R. Hof, John J. Ely, Yan Li, Dirk Steinhauser, Lothar Willmitzer, Patrick Giavalisco, Philipp Khaitovich

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106 Citations (Scopus)

Abstract

Lipids are prominent components of the nervous system. Here we performed a large-scale mass spectrometry-based analysis of the lipid composition of three brain regions as well as kidney and skeletal muscle of humans, chimpanzees, rhesus macaques, and mice. The human brain shows the most distinct lipid composition: 76% of 5,713 lipid compounds examined in our study are either enriched or depleted in the human brain. Concentration levels of lipids enriched in the brain evolve approximately four times faster among primates compared with lipids characteristic of non-neural tissues and show further acceleration of change in human neocortical regions but not in the cerebellum. Human-specific concentration changes are supported by human-specific expression changes for corresponding enzymes. These results provide the first insights into the role of lipids in human brain evolution.

Original language	English
Pages (from-to)	695-702
Number of pages	8
Journal	Neuron
Volume	85
Issue number	4
DOIs	https://doi.org/10.1016/j.neuron.2015.01.003
Publication status	Published - 2015 Feb 18

ASJC Scopus subject areas

Neuroscience(all)

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Bozek, K., Wei, Y., Yan, Z., Liu, X., Xiong, J., Sugimoto, M., Tomita, M., Pääbo, S., Sherwood, C. C., Hof, P. R., Ely, J. J., Li, Y., Steinhauser, D., Willmitzer, L., Giavalisco, P., & Khaitovich, P. (2015). Organization and Evolution of Brain Lipidome Revealed by Large-Scale Analysis of Human, Chimpanzee, Macaque, and Mouse Tissues. Neuron, 85(4), 695-702. https://doi.org/10.1016/j.neuron.2015.01.003

Bozek, K, Wei, Y, Yan, Z, Liu, X, Xiong, J, Sugimoto, M, Tomita, M, Pääbo, S, Sherwood, CC, Hof, PR, Ely, JJ, Li, Y, Steinhauser, D, Willmitzer, L, Giavalisco, P & Khaitovich, P 2015, 'Organization and Evolution of Brain Lipidome Revealed by Large-Scale Analysis of Human, Chimpanzee, Macaque, and Mouse Tissues', Neuron, vol. 85, no. 4, pp. 695-702. https://doi.org/10.1016/j.neuron.2015.01.003

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title = "Organization and Evolution of Brain Lipidome Revealed by Large-Scale Analysis of Human, Chimpanzee, Macaque, and Mouse Tissues",

abstract = "Lipids are prominent components of the nervous system. Here we performed a large-scale mass spectrometry-based analysis of the lipid composition of three brain regions as well as kidney and skeletal muscle of humans, chimpanzees, rhesus macaques, and mice. The human brain shows the most distinct lipid composition: 76% of 5,713 lipid compounds examined in our study are either enriched or depleted in the human brain. Concentration levels of lipids enriched in the brain evolve approximately four times faster among primates compared with lipids characteristic of non-neural tissues and show further acceleration of change in human neocortical regions but not in the cerebellum. Human-specific concentration changes are supported by human-specific expression changes for corresponding enzymes. These results provide the first insights into the role of lipids in human brain evolution.",

author = "Katarzyna Bozek and Yuning Wei and Zheng Yan and Xiling Liu and Jieyi Xiong and Masahiro Sugimoto and Masaru Tomita and Svante P{\"a}{\"a}bo and Sherwood, {Chet C.} and Hof, {Patrick R.} and Ely, {John J.} and Yan Li and Dirk Steinhauser and Lothar Willmitzer and Patrick Giavalisco and Philipp Khaitovich",

note = "Funding Information: This study was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (Grant XDB13010200), National Natural Science Foundation of China (grants 91331203, 31171232, and 31420103920), National One Thousand Foreign Experts Plan (grants WQ20123100078), Bureau of International Cooperation, Chinese Academy of Sciences (grant GJHZ201313), National Science Foundation (grant BCS-0824531), Russian Science Foundation (grant 14-28-00234), and James S. McDonnell Foundation (grants 22002078 and 220020293). K.B. was supported by a Chinese Academy of Sciences fellowship (2011Y1SB06). We thank Jerome Boyd-Kirkup for help with manuscript preparation. Publisher Copyright: {\textcopyright} 2015 Elsevier Inc.",

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doi = "10.1016/j.neuron.2015.01.003",

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AU - Bozek, Katarzyna

AU - Wei, Yuning

AU - Yan, Zheng

AU - Liu, Xiling

AU - Xiong, Jieyi

AU - Sugimoto, Masahiro

AU - Tomita, Masaru

AU - Pääbo, Svante

AU - Sherwood, Chet C.

AU - Hof, Patrick R.

AU - Ely, John J.

AU - Li, Yan

AU - Steinhauser, Dirk

AU - Willmitzer, Lothar

AU - Giavalisco, Patrick

AU - Khaitovich, Philipp

N1 - Funding Information: This study was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (Grant XDB13010200), National Natural Science Foundation of China (grants 91331203, 31171232, and 31420103920), National One Thousand Foreign Experts Plan (grants WQ20123100078), Bureau of International Cooperation, Chinese Academy of Sciences (grant GJHZ201313), National Science Foundation (grant BCS-0824531), Russian Science Foundation (grant 14-28-00234), and James S. McDonnell Foundation (grants 22002078 and 220020293). K.B. was supported by a Chinese Academy of Sciences fellowship (2011Y1SB06). We thank Jerome Boyd-Kirkup for help with manuscript preparation. Publisher Copyright: © 2015 Elsevier Inc.

PY - 2015/2/18

Y1 - 2015/2/18

N2 - Lipids are prominent components of the nervous system. Here we performed a large-scale mass spectrometry-based analysis of the lipid composition of three brain regions as well as kidney and skeletal muscle of humans, chimpanzees, rhesus macaques, and mice. The human brain shows the most distinct lipid composition: 76% of 5,713 lipid compounds examined in our study are either enriched or depleted in the human brain. Concentration levels of lipids enriched in the brain evolve approximately four times faster among primates compared with lipids characteristic of non-neural tissues and show further acceleration of change in human neocortical regions but not in the cerebellum. Human-specific concentration changes are supported by human-specific expression changes for corresponding enzymes. These results provide the first insights into the role of lipids in human brain evolution.

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Organization and Evolution of Brain Lipidome Revealed by Large-Scale Analysis of Human, Chimpanzee, Macaque, and Mouse Tissues

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