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Erratic and blood vessel-guided migration of astrocyte progenitors in the cerebral cortex

Author

Listed:
  • Hidenori Tabata

    (Aichi Developmental Disability Center
    Keio University School of Medicine)

  • Megumi Sasaki

    (Keio University School of Medicine)

  • Masakazu Agetsuma

    (National Institute for Physiological Sciences)

  • Hitomi Sano

    (Keio University School of Medicine)

  • Yuki Hirota

    (Keio University School of Medicine)

  • Michio Miyajima

    (Keio University School of Medicine)

  • Kanehiro Hayashi

    (Keio University School of Medicine)

  • Takao Honda

    (Keio University School of Medicine)

  • Masashi Nishikawa

    (Aichi Developmental Disability Center)

  • Yutaka Inaguma

    (Aichi Developmental Disability Center)

  • Hidenori Ito

    (Aichi Developmental Disability Center)

  • Hirohide Takebayashi

    (Niigata University)

  • Masatsugu Ema

    (Shiga University of Medical Science)

  • Kazuhiro Ikenaka

    (National Institute for Physiological Sciences)

  • Junichi Nabekura

    (National Institute for Physiological Sciences)

  • Koh-ichi Nagata

    (Aichi Developmental Disability Center)

  • Kazunori Nakajima

    (Keio University School of Medicine)

Abstract

Astrocytes are one of the most abundant cell types in the mammalian brain. They play essential roles in synapse formation, maturation, and elimination. However, how astrocytes migrate into the gray matter to accomplish these processes is poorly understood. Here, we show that, by combinational analyses of in vitro and in vivo time-lapse observations and lineage traces, astrocyte progenitors move rapidly and irregularly within the developing cortex, which we call erratic migration. Astrocyte progenitors also adopt blood vessel-guided migration. These highly motile progenitors are generated in the restricted prenatal stages and differentiate into protoplasmic astrocytes in the gray matter, whereas postnatally generated progenitors do not move extensively and differentiate into fibrous astrocytes in the white matter. We found Cxcr4/7, and integrin β1 regulate the blood vessel-guided migration, and their functional blocking disrupts their positioning. This study provides insight into astrocyte development and may contribute to understanding the pathogenesis caused by their defects.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34184-x
    DOI: 10.1038/s41467-022-34184-x
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    1. Won-Suk Chung & Laura E. Clarke & Gordon X. Wang & Benjamin K. Stafford & Alexander Sher & Chandrani Chakraborty & Julia Joung & Lynette C. Foo & Andrew Thompson & Chinfei Chen & Stephen J. Smith & Be, 2013. "Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways," Nature, Nature, vol. 504(7480), pages 394-400, December.
    2. 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.
    3. Vikaas S. Sohal & Feng Zhang & Ofer Yizhar & Karl Deisseroth, 2009. "Parvalbumin neurons and gamma rhythms enhance cortical circuit performance," Nature, Nature, vol. 459(7247), pages 698-702, June.
    4. Mykhailo Y. Batiuk & Araks Martirosyan & Jérôme Wahis & Filip de Vin & Catherine Marneffe & Carola Kusserow & Jordan Koeppen & João Filipe Viana & João Filipe Oliveira & Thierry Voet & Chris P. Pontin, 2020. "Identification of region-specific astrocyte subtypes at single cell resolution," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    5. Knut Woltjen & Iacovos P. Michael & Paria Mohseni & Ridham Desai & Maria Mileikovsky & Riikka Hämäläinen & Rebecca Cowling & Wei Wang & Pentao Liu & Marina Gertsenstein & Keisuke Kaji & Hoon-Ki Sung &, 2009. "piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells," Nature, Nature, vol. 458(7239), pages 766-770, April.
    6. Solène Clavreul & Lamiae Abdeladim & Edwin Hernández-Garzón & Dragos Niculescu & Jason Durand & Sio-Hoï Ieng & Raphaëlle Barry & Gilles Bonvento & Emmanuel Beaurepaire & Jean Livet & Karine Loulier, 2019. "Cortical astrocytes develop in a plastic manner at both clonal and cellular levels," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
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