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Astroglial exosome HepaCAM signaling and ApoE antagonization coordinates early postnatal cortical pyramidal neuronal axon growth and dendritic spine formation

Author

Listed:
  • Shijie Jin

    (Department of Neuroscience, Tufts University School of Medicine)

  • Xuan Chen

    (Department of Neuroscience, Tufts University School of Medicine)

  • Yang Tian

    (Department of Neuroscience, Tufts University School of Medicine)

  • Rachel Jarvis

    (Department of Neuroscience, Tufts University School of Medicine)

  • Vanessa Promes

    (Department of Neuroscience, Tufts University School of Medicine)

  • Yongjie Yang

    (Department of Neuroscience, Tufts University School of Medicine
    Graduate School of Biomedical Sciences, Tufts University)

Abstract

Developing astroglia play important roles in regulating synaptogenesis through secreted and contact signals. Whether they regulate postnatal axon growth is unknown. By selectively isolating exosomes using size-exclusion chromatography (SEC) and employing cell-type specific exosome reporter mice, our current results define a secreted astroglial exosome pathway that can spread long-range in vivo and stimulate axon growth of cortical pyramidal neurons. Subsequent biochemical and genetic studies found that surface expression of glial HepaCAM protein essentially and sufficiently mediates the axon-stimulating effect of astroglial exosomes. Interestingly, apolipoprotein E (ApoE), a major astroglia-secreted cholesterol carrier to promote synaptogenesis, strongly inhibits the stimulatory effect of astroglial exosomes on axon growth. Developmental ApoE deficiency also significantly reduces spine density of cortical pyramidal neurons. Together, our study suggests a surface contact mechanism of astroglial exosomes in regulating axon growth and its antagonization by ApoE, which collectively coordinates early postnatal pyramidal neuronal axon growth and dendritic spine formation.

Suggested Citation

  • Shijie Jin & Xuan Chen & Yang Tian & Rachel Jarvis & Vanessa Promes & Yongjie Yang, 2023. "Astroglial exosome HepaCAM signaling and ApoE antagonization coordinates early postnatal cortical pyramidal neuronal axon growth and dendritic spine formation," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40926-2
    DOI: 10.1038/s41467-023-40926-2
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    1. Nicola J. Allen & Mariko L. Bennett & Lynette C. Foo & Gordon X. Wang & Chandrani Chakraborty & Stephen J. Smith & Ben A. Barres, 2012. "Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors," Nature, Nature, vol. 486(7403), pages 410-414, June.
    2. Maja B. Hoegg-Beiler & Sònia Sirisi & Ian J. Orozco & Isidre Ferrer & Svea Hohensee & Muriel Auberson & Kathrin Gödde & Clara Vilches & Miguel López de Heredia & Virginia Nunes & Raúl Estévez & Thomas, 2014. "Disrupting MLC1 and GlialCAM and ClC-2 interactions in leukodystrophy entails glial chloride channel dysfunction," Nature Communications, Nature, vol. 5(1), pages 1-16, May.
    3. Tetsuya Takano & John T. Wallace & Katherine T. Baldwin & Alicia M. Purkey & Akiyoshi Uezu & Jamie L. Courtland & Erik J. Soderblom & Tomomi Shimogori & Patricia F. Maness & Cagla Eroglu & Scott H. So, 2020. "Chemico-genetic discovery of astrocytic control of inhibition in vivo," Nature, Nature, vol. 588(7837), pages 296-302, December.
    4. Jeff A. Stogsdill & Juan Ramirez & Di Liu & Yong Ho Kim & Katherine T. Baldwin & Eray Enustun & Tiffany Ejikeme & Ru-Rong Ji & Cagla Eroglu, 2017. "Astrocytic neuroligins control astrocyte morphogenesis and synaptogenesis," Nature, Nature, vol. 551(7679), pages 192-197, November.
    5. Yuqin Men & Julia Yelick & Shijie Jin & Yang Tian & Ming Sum R. Chiang & Haruki Higashimori & Eoin Brown & Rachel Jarvis & Yongjie Yang, 2019. "Exosome reporter mice reveal the involvement of exosomes in mediating neuron to astroglia communication in the CNS," Nature Communications, Nature, vol. 10(1), pages 1-18, December.
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