Erratic and Blood Vessel-guided Migration of Astrocyte Progenitors in the Cerebral Cortex

Overview

Journal Nat Commun

Specialty Biology

Date 2022 Nov 3

PMID 36323680

Authors

Hidenori Tabata

Megumi Sasaki

Masakazu Agetsuma

Hitomi Sano

Yuki Hirota

Michio Miyajima

Kanehiro Hayashi

Takao Honda

Masashi Nishikawa

Yutaka Inaguma

Hidenori Ito

Hirohide Takebayashi

Masatsugu Ema

Kazuhiro Ikenaka

Junichi Nabekura

Koh-Ichi Nagata

Kazunori Nakajima

Affiliations

Soon will be listed here.

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.

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References

Hama H, Hara C, Yamaguchi K, Miyawaki A . PKC signaling mediates global enhancement of excitatory synaptogenesis in neurons triggered by local contact with astrocytes. Neuron. 2004; 41(3):405-15. DOI: 10.1016/s0896-6273(04)00007-8. View

Stogsdill J, Ramirez J, Liu D, Kim Y, Baldwin K, Enustun E . Astrocytic neuroligins control astrocyte morphogenesis and synaptogenesis. Nature. 2017; 551(7679):192-197. PMC: 5796651. DOI: 10.1038/nature24638. View

Tsai H, Niu J, Munji R, Davalos D, Chang J, Zhang H . Oligodendrocyte precursors migrate along vasculature in the developing nervous system. Science. 2016; 351(6271):379-84. PMC: 5472053. DOI: 10.1126/science.aad3839. View

Tanaka D, Nakajima K . Migratory pathways of GABAergic interneurons when they enter the neocortex. Eur J Neurosci. 2012; 35(11):1655-60. DOI: 10.1111/j.1460-9568.2012.08111.x. View

Tsutsui H, Karasawa S, Shimizu H, Nukina N, Miyawaki A . Semi-rational engineering of a coral fluorescent protein into an efficient highlighter. EMBO Rep. 2005; 6(3):233-8. PMC: 1299271. DOI: 10.1038/sj.embor.7400361. View

Gloster A, Wu W, Speelman A, Weiss S, Causing C, Pozniak C . The T alpha 1 alpha-tubulin promoter specifies gene expression as a function of neuronal growth and regeneration in transgenic mice. J Neurosci. 1994; 14(12):7319-30. PMC: 6576916. View

Mao T, Kusefoglu D, Hooks B, Huber D, Petreanu L, Svoboda K . Long-range neuronal circuits underlying the interaction between sensory and motor cortex. Neuron. 2011; 72(1):111-23. PMC: 5047281. DOI: 10.1016/j.neuron.2011.07.029. View

Gressens P, Richelme C, Kadhim H, Gadisseux J, Evrard P . The germinative zone produces the most cortical astrocytes after neuronal migration in the developing mammalian brain. Biol Neonate. 1992; 61(1):4-24. DOI: 10.1159/000243526. View

Yusa K, Zhou L, Li M, Bradley A, Craig N . A hyperactive piggyBac transposase for mammalian applications. Proc Natl Acad Sci U S A. 2011; 108(4):1531-6. PMC: 3029773. DOI: 10.1073/pnas.1008322108. View

10.

Tinevez J, Perry N, Schindelin J, Hoopes G, Reynolds G, Laplantine E . TrackMate: An open and extensible platform for single-particle tracking. Methods. 2016; 115:80-90. DOI: 10.1016/j.ymeth.2016.09.016. View

11.

Woltjen K, Michael I, Mohseni P, Desai R, Mileikovsky M, Hamalainen R . piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature. 2009; 458(7239):766-70. PMC: 3758996. DOI: 10.1038/nature07863. View

12.

Chen F, LoTurco J . A method for stable transgenesis of radial glia lineage in rat neocortex by piggyBac mediated transposition. J Neurosci Methods. 2012; 207(2):172-80. PMC: 3972033. DOI: 10.1016/j.jneumeth.2012.03.016. View

13.

Takebayashi H, Nabeshima Y, Yoshida S, Chisaka O, Ikenaka K, Nabeshima Y . The basic helix-loop-helix factor olig2 is essential for the development of motoneuron and oligodendrocyte lineages. Curr Biol. 2002; 12(13):1157-63. DOI: 10.1016/s0960-9822(02)00926-0. View

14.

Naka-Kaneda H, Nakamura S, Igarashi M, Aoi H, Kanki H, Tsuyama J . The miR-17/106-p38 axis is a key regulator of the neurogenic-to-gliogenic transition in developing neural stem/progenitor cells. Proc Natl Acad Sci U S A. 2014; 111(4):1604-9. PMC: 3910627. DOI: 10.1073/pnas.1315567111. View

15.

Martin-Lopez E, Garcia-Marques J, Nunez-Llaves R, Lopez-Mascaraque L . Clonal astrocytic response to cortical injury. PLoS One. 2013; 8(9):e74039. PMC: 3769363. DOI: 10.1371/journal.pone.0074039. View

16.

Zhuo L, Theis M, Alvarez-Maya I, Brenner M, Willecke K, Messing A . hGFAP-cre transgenic mice for manipulation of glial and neuronal function in vivo. Genesis. 2001; 31(2):85-94. DOI: 10.1002/gene.10008. View

17.

Kawakami K, Takeda H, Kawakami N, Kobayashi M, Matsuda N, Mishina M . A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev Cell. 2004; 7(1):133-44. DOI: 10.1016/j.devcel.2004.06.005. View

18.

Higuchi Y, Kita Y, Murakami F . In vivo imaging of cortical interneurons migrating in the intermediate/subventricular zones. Neurosci Res. 2016; 110:68-71. DOI: 10.1016/j.neures.2016.03.005. View

19.

Yao X, Zhang M, Wang X, Ying W, Hu X, Dai P . Tild-CRISPR Allows for Efficient and Precise Gene Knockin in Mouse and Human Cells. Dev Cell. 2018; 45(4):526-536.e5. DOI: 10.1016/j.devcel.2018.04.021. View

20.

Hirota Y, Sawada M, Kida Y, Huang S, Yamada O, Sakaguchi M . Roles of planar cell polarity signaling in maturation of neuronal precursor cells in the postnatal mouse olfactory bulb. Stem Cells. 2012; 30(8):1726-33. DOI: 10.1002/stem.1137. View