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Spatiotemporal proteomic atlas of multiple brain regions across early fetal to neonatal stages in cynomolgus monkey

Author

Listed:
  • Jingkuan Wei

    (Kunming University of Science and Technology
    Yunnan Key Laboratory of Primate Biomedical Research)

  • Shaoxing Dai

    (Kunming University of Science and Technology
    Yunnan Key Laboratory of Primate Biomedical Research)

  • Yaping Yan

    (Kunming University of Science and Technology
    Yunnan Key Laboratory of Primate Biomedical Research)

  • Shulin Li

    (Kunming University of Science and Technology)

  • Pengpeng Yang

    (Kunming University of Science and Technology)

  • Ran Zhu

    (Kunming University of Science and Technology)

  • Tianzhuang Huang

    (Kunming University of Science and Technology
    Yunnan Key Laboratory of Primate Biomedical Research)

  • Xi Li

    (Kunming University of Science and Technology
    Yunnan Key Laboratory of Primate Biomedical Research)

  • Yanchao Duan

    (Kunming University of Science and Technology
    Yunnan Key Laboratory of Primate Biomedical Research)

  • Zhengbo Wang

    (Kunming University of Science and Technology
    Yunnan Key Laboratory of Primate Biomedical Research)

  • Weizhi Ji

    (Kunming University of Science and Technology
    Yunnan Key Laboratory of Primate Biomedical Research
    Chinese Primate Biomedical Research Alliance (CPBRA))

  • Wei Si

    (Kunming University of Science and Technology
    Yunnan Key Laboratory of Primate Biomedical Research
    Chinese Primate Biomedical Research Alliance (CPBRA))

Abstract

Fetal stages are critical periods for brain development. However, the protein molecular signature and dynamics of the human brain remain unclear due to sampling difficulty and ethical limitations. Non-human primates present similar developmental and neuropathological features to humans. This study constructed a spatiotemporal proteomic atlas of cynomolgus macaque brain development from early fetal to neonatal stages. Here we showed that (1) the variability across stages was greater than that among brain regions, and comparisons of cerebellum vs. cerebrum and cortical vs. subcortical regions revealed region-specific dynamics across early fetal to neonatal stages; (2) fluctuations in abundance of proteins associated with neural disease suggest the risk of nervous disorder at early fetal stages; (3) cross-species analysis (human, monkey, and mouse) and comparison between proteomic and transcriptomic data reveal the proteomic specificity and genes with mRNA/protein discrepancy. This study provides insight into fetal brain development in primates.

Suggested Citation

  • Jingkuan Wei & Shaoxing Dai & Yaping Yan & Shulin Li & Pengpeng Yang & Ran Zhu & Tianzhuang Huang & Xi Li & Yanchao Duan & Zhengbo Wang & Weizhi Ji & Wei Si, 2023. "Spatiotemporal proteomic atlas of multiple brain regions across early fetal to neonatal stages in cynomolgus monkey," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39411-7
    DOI: 10.1038/s41467-023-39411-7
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    References listed on IDEAS

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    1. Velina Kozareva & Caroline Martin & Tomas Osorno & Stephanie Rudolph & Chong Guo & Charles Vanderburg & Naeem Nadaf & Aviv Regev & Wade G. Regehr & Evan Macosko, 2021. "A transcriptomic atlas of mouse cerebellar cortex comprehensively defines cell types," Nature, Nature, vol. 598(7879), pages 214-219, October.
    2. Senlin Yin & Keying Lu & Tao Tan & Jie Tang & Jingkuan Wei & Xu Liu & Xinlei Hu & Haisu Wan & Wei Huang & Yong Fan & Dan Xie & Yang Yu, 2020. "Transcriptomic and open chromatin atlas of high-resolution anatomical regions in the rhesus macaque brain," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    3. Marianne L. Seney & Kelly Cahill & John F. Enwright & Ryan W. Logan & Zhiguang Huo & Wei Zong & George Tseng & Colleen A. McClung, 2019. "Diurnal rhythms in gene expression in the prefrontal cortex in schizophrenia," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    4. Hyo Jung Kang & Yuka Imamura Kawasawa & Feng Cheng & Ying Zhu & Xuming Xu & Mingfeng Li & André M. M. Sousa & Mihovil Pletikos & Kyle A. Meyer & Goran Sedmak & Tobias Guennel & Yurae Shin & Matthew B., 2011. "Spatio-temporal transcriptome of the human brain," Nature, Nature, vol. 478(7370), pages 483-489, October.
    5. Trygve E. Bakken & Jeremy A. Miller & Song-Lin Ding & Susan M. Sunkin & Kimberly A. Smith & Lydia Ng & Aaron Szafer & Rachel A. Dalley & Joshua J. Royall & Tracy Lemon & Sheila Shapouri & Kaylynn Aion, 2016. "A comprehensive transcriptional map of primate brain development," Nature, Nature, vol. 535(7612), pages 367-375, July.
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