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Astrocytic neuroligins control astrocyte morphogenesis and synaptogenesis

Author

Listed:
  • Jeff A. Stogsdill

    (Duke University Medical Center)

  • Juan Ramirez

    (Duke University Medical Center)

  • Di Liu

    (Duke University Medical Center)

  • Yong Ho Kim

    (Duke University Medical Center)

  • Katherine T. Baldwin

    (Duke University Medical Center)

  • Eray Enustun

    (Duke University Medical Center)

  • Tiffany Ejikeme

    (Duke University Medical Center)

  • Ru-Rong Ji

    (Duke University Medical Center
    Duke University Medical Center
    Duke Institute for Brain Sciences (DIBS))

  • Cagla Eroglu

    (Duke University Medical Center
    Duke University Medical Center
    Duke Institute for Brain Sciences (DIBS))

Abstract

Astrocytes are complex glial cells with numerous fine cellular processes that infiltrate the neuropil and interact with synapses. The mechanisms that control the establishment of astrocyte morphology are unknown, and it is unclear whether impairing astrocytic infiltration of the neuropil alters synaptic connectivity. Here we show that astrocyte morphogenesis in the mouse cortex depends on direct contact with neuronal processes and occurs in parallel with the growth and activity of synaptic circuits. The neuroligin family cell adhesion proteins NL1, NL2, and NL3, which are expressed by cortical astrocytes, control astrocyte morphogenesis through interactions with neuronal neurexins. Furthermore, in the absence of astrocytic NL2, the formation and function of cortical excitatory synapses are diminished, whereas inhibitory synaptic function is enhanced. Our findings highlight a previously undescribed mechanism of action for neuroligins and link astrocyte morphogenesis to synaptogenesis. Because neuroligin mutations have been implicated in various neurological disorders, these findings also point towards an astrocyte-based mechanism of neural pathology.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:nature:v:551:y:2017:i:7679:d:10.1038_nature24638
    DOI: 10.1038/nature24638
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    Cited by:

    1. 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.
    2. Hidenori Tabata & Megumi Sasaki & Masakazu Agetsuma & Hitomi Sano & Yuki Hirota & Michio Miyajima & Kanehiro Hayashi & Takao Honda & Masashi Nishikawa & Yutaka Inaguma & Hidenori Ito & Hirohide Takeba, 2022. "Erratic and blood vessel-guided migration of astrocyte progenitors in the cerebral cortex," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    3. Ken-ichi Dewa & Nariko Arimura & Wataru Kakegawa & Masayuki Itoh & Toma Adachi & Satoshi Miyashita & Yukiko U. Inoue & Kento Hizawa & Kei Hori & Natsumi Honjoya & Haruya Yagishita & Shinichiro Taya & , 2024. "Neuronal DSCAM regulates the peri-synaptic localization of GLAST in Bergmann glia for functional synapse formation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    4. Rui Dang & An Liu & Yu Zhou & Xingcan Li & Miao Wu & Kun Cao & Yanghong Meng & Haiwang Zhang & Guangming Gan & Wei Xie & Zhengping Jia, 2024. "Astrocytic neuroligin 3 regulates social memory and synaptic plasticity through adenosine signaling in male mice," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    5. Mian Wang & Wanlu Li & Jin Hao & Arthur Gonzales & Zhibo Zhao & Regina Sanchez Flores & Xiao Kuang & Xuan Mu & Terry Ching & Guosheng Tang & Zeyu Luo & Carlos Ezio Garciamendez-Mijares & Jugal Kishore, 2022. "Molecularly cleavable bioinks facilitate high-performance digital light processing-based bioprinting of functional volumetric soft tissues," Nature Communications, Nature, vol. 13(1), pages 1-18, December.

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