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Evolution of Osteocrin as an activity-regulated factor in the primate brain

Author

Listed:
  • Bulent Ataman

    (Harvard Medical School)

  • Gabriella L. Boulting

    (Harvard Medical School)

  • David A. Harmin

    (Harvard Medical School)

  • Marty G. Yang

    (Harvard Medical School)

  • Mollie Baker-Salisbury

    (Harvard Medical School)

  • Ee-Lynn Yap

    (Harvard Medical School)

  • Athar N. Malik

    (Harvard Medical School)

  • Kevin Mei

    (Harvard Medical School)

  • Alex A. Rubin

    (Harvard Medical School)

  • Ivo Spiegel

    (Harvard Medical School)

  • Ershela Durresi

    (Harvard Medical School)

  • Nikhil Sharma

    (Harvard Medical School)

  • Linda S. Hu

    (Harvard Medical School)

  • Mihovil Pletikos

    (Yale School of Medicine)

  • Eric C. Griffith

    (Harvard Medical School)

  • Jennifer N. Partlow

    (Boston Children's Hospital, Harvard Medical School)

  • Christine R. Stevens

    (Broad Institute of MIT and Harvard)

  • Mazhar Adli

    (University of Virginia, School of Medicine)

  • Maria Chahrour

    (McDermott Center for Human Growth and Development, University of Texas Southwestern Medical Center)

  • Nenad Sestan

    (Yale School of Medicine)

  • Christopher A. Walsh

    (Boston Children's Hospital, Harvard Medical School)

  • Vladimir K. Berezovskii

    (Harvard Medical School)

  • Margaret S. Livingstone

    (Harvard Medical School)

  • Michael E. Greenberg

    (Harvard Medical School)

Abstract

Sensory stimuli drive the maturation and function of the mammalian nervous system in part through the activation of gene expression networks that regulate synapse development and plasticity. These networks have primarily been studied in mice, and it is not known whether there are species- or clade-specific activity-regulated genes that control features of brain development and function. Here we use transcriptional profiling of human fetal brain cultures to identify an activity-dependent secreted factor, Osteocrin (OSTN), that is induced by membrane depolarization of human but not mouse neurons. We find that OSTN has been repurposed in primates through the evolutionary acquisition of DNA regulatory elements that bind the activity-regulated transcription factor MEF2. In addition, we demonstrate that OSTN is expressed in primate neocortex and restricts activity-dependent dendritic growth in human neurons. These findings suggest that, in response to sensory input, OSTN regulates features of neuronal structure and function that are unique to primates.

Suggested Citation

  • Bulent Ataman & Gabriella L. Boulting & David A. Harmin & Marty G. Yang & Mollie Baker-Salisbury & Ee-Lynn Yap & Athar N. Malik & Kevin Mei & Alex A. Rubin & Ivo Spiegel & Ershela Durresi & Nikhil Sha, 2016. "Evolution of Osteocrin as an activity-regulated factor in the primate brain," Nature, Nature, vol. 539(7628), pages 242-247, November.
    • Handle: RePEc:nat:nature:v:539:y:2016:i:7628:d:10.1038_nature20111
    DOI: 10.1038/nature20111
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    Cited by:

    1. Yueqi Wang & Simone Chiola & Guang Yang & Chad Russell & Celeste J. Armstrong & Yuanyuan Wu & Jay Spampanato & Paisley Tarboton & H. M. Arif Ullah & Nicolas U. Edgar & Amelia N. Chang & David A. Harmi, 2022. "Modeling human telencephalic development and autism-associated SHANK3 deficiency using organoids generated from single neural rosettes," Nature Communications, Nature, vol. 13(1), pages 1-25, December.
    2. Jialiang S. Wang & Tushar Kamath & Courtney M. Mazur & Fatemeh Mirzamohammadi & Daniel Rotter & Hironori Hojo & Christian D. Castro & Nicha Tokavanich & Rushi Patel & Nicolas Govea & Tetsuya Enishi & , 2021. "Control of osteocyte dendrite formation by Sp7 and its target gene osteocrin," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
    3. Lu Jin & Shuang Han & Xue Lv & Xiaofei Li & Ziyin Zhang & Henry Kuang & Zhimin Chen & Cheng-an Lv & Wei Peng & Zhuoying Yang & Miqi Yang & Lin Mi & Tongyu Liu & Shengshan Ma & Xinyuan Qiu & Qintao Wan, 2023. "The muscle-enriched myokine Musclin impairs beige fat thermogenesis and systemic energy homeostasis via Tfr1/PKA signaling in male mice," Nature Communications, Nature, vol. 14(1), pages 1-23, December.

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