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A cross-species proteomic map reveals neoteny of human synapse development

Author

Listed:
  • Li Wang

    (University of California San Francisco
    University of California San Francisco)

  • Kaifang Pang

    (Jan and Dan Duncan Neurological Research Institute at Texas Children’s Hospital
    Baylor College of Medicine)

  • Li Zhou

    (University of California San Francisco
    University of California San Francisco)

  • Arantxa Cebrián-Silla

    (University of California San Francisco
    University of California San Francisco)

  • Susana González-Granero

    (University of Valencia and CIBERNED)

  • Shaohui Wang

    (University of California San Francisco
    University of California San Francisco)

  • Qiuli Bi

    (University of California San Francisco
    University of California San Francisco)

  • Matthew L. White

    (University of California San Francisco
    University of California San Francisco)

  • Brandon Ho

    (University of California San Francisco
    University of California San Francisco)

  • Jiani Li

    (Gilead Sciences)

  • Tao Li

    (University of California San Francisco)

  • Yonatan Perez

    (University of California San Francisco
    University of California San Francisco)

  • Eric J. Huang

    (University of California San Francisco)

  • Ethan A. Winkler

    (University of California San Francisco)

  • Mercedes F. Paredes

    (University of California San Francisco
    University of California San Francisco)

  • Rothem Kovner

    (Yale School of Medicine, Yale University)

  • Nenad Sestan

    (Yale School of Medicine, Yale University)

  • Alex A. Pollen

    (University of California San Francisco
    University of California San Francisco)

  • Pengyuan Liu

    (University of Massachusetts Lowell)

  • Jingjing Li

    (University of California San Francisco
    University of California San Francisco)

  • Xianhua Piao

    (University of California San Francisco
    University of California San Francisco
    University of California San Francisco)

  • José Manuel García-Verdugo

    (University of Valencia and CIBERNED)

  • Arturo Alvarez-Buylla

    (University of California San Francisco
    University of California San Francisco)

  • Zhandong Liu

    (Jan and Dan Duncan Neurological Research Institute at Texas Children’s Hospital
    Baylor College of Medicine)

  • Arnold R. Kriegstein

    (University of California San Francisco
    University of California San Francisco)

Abstract

The molecular mechanisms and evolutionary changes accompanying synapse development are still poorly understood1,2. Here we generate a cross-species proteomic map of synapse development in the human, macaque and mouse neocortex. By tracking the changes of more than 1,000 postsynaptic density (PSD) proteins from midgestation to young adulthood, we find that PSD maturation in humans separates into three major phases that are dominated by distinct pathways. Cross-species comparisons reveal that human PSDs mature about two to three times slower than those of other species and contain higher levels of Rho guanine nucleotide exchange factors (RhoGEFs) in the perinatal period. Enhancement of RhoGEF signalling in human neurons delays morphological maturation of dendritic spines and functional maturation of synapses, potentially contributing to the neotenic traits of human brain development. In addition, PSD proteins can be divided into four modules that exert stage- and cell-type-specific functions, possibly explaining their differential associations with cognitive functions and diseases. Our proteomic map of synapse development provides a blueprint for studying the molecular basis and evolutionary changes of synapse maturation.

Suggested Citation

  • Li Wang & Kaifang Pang & Li Zhou & Arantxa Cebrián-Silla & Susana González-Granero & Shaohui Wang & Qiuli Bi & Matthew L. White & Brandon Ho & Jiani Li & Tao Li & Yonatan Perez & Eric J. Huang & Ethan, 2023. "A cross-species proteomic map reveals neoteny of human synapse development," Nature, Nature, vol. 622(7981), pages 112-119, October.
    • Handle: RePEc:nat:nature:v:622:y:2023:i:7981:d:10.1038_s41586-023-06542-2
    DOI: 10.1038/s41586-023-06542-2
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    Cited by:

    1. Takeshi Kaizuka & Takehiro Suzuki & Noriyuki Kishi & Kota Tamada & Manfred W. Kilimann & Takehiko Ueyama & Masahiko Watanabe & Tomomi Shimogori & Hideyuki Okano & Naoshi Dohmae & Toru Takumi, 2024. "Remodeling of the postsynaptic proteome in male mice and marmosets during synapse development," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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