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

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

doi:10.1038/s41467-022-34184-x

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

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

Department of Anatomy

Research output: Contribution to journal › Article › peer-review

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.

Original language	English
Article number	6571
Journal	Nature communications
Volume	13
Issue number	1
DOIs	https://doi.org/10.1038/s41467-022-34184-x
Publication status	Published - 2022 Dec

ASJC Scopus subject areas

Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
General
Physics and Astronomy(all)

Access to Document

10.1038/s41467-022-34184-x

Cite this

Tabata, H., Sasaki, M., Agetsuma, M., Sano, H., Hirota, Y., Miyajima, M., Hayashi, K., Honda, T., Nishikawa, M., Inaguma, Y., Ito, H., Takebayashi, H., Ema, M., Ikenaka, K., Nabekura, J., Nagata, K. I., & Nakajima, K. (2022). Erratic and blood vessel-guided migration of astrocyte progenitors in the cerebral cortex. Nature communications, 13(1), [6571]. https://doi.org/10.1038/s41467-022-34184-x

Tabata, H, Sasaki, M, Agetsuma, M, Sano, H, Hirota, Y, Miyajima, M, Hayashi, K, Honda, T, Nishikawa, M, Inaguma, Y, Ito, H, Takebayashi, H, Ema, M, Ikenaka, K, Nabekura, J, Nagata, KI & Nakajima, K 2022, 'Erratic and blood vessel-guided migration of astrocyte progenitors in the cerebral cortex', Nature communications, vol. 13, no. 1, 6571. https://doi.org/10.1038/s41467-022-34184-x

@article{741849170b2843baaecc035cff1e75b4,

title = "Erratic and blood vessel-guided migration of astrocyte progenitors in the cerebral cortex",

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.",

author = "Hidenori Tabata and Megumi Sasaki and Masakazu Agetsuma and Hitomi Sano and Yuki Hirota and Michio Miyajima and Kanehiro Hayashi and Takao Honda and Masashi Nishikawa and Yutaka Inaguma and Hidenori Ito and Hirohide Takebayashi and Masatsugu Ema and Kazuhiro Ikenaka and Junichi Nabekura and Nagata, {Koh ichi} and Kazunori Nakajima",

note = "Funding Information: We are grateful to C.G.Lobe for Z/EG mice, K. Kawakami and Y. Takahashi for pCAGGS-T2TP and pT2K-CAGGS-mCherry, A. Miyawaki for kikGR cDNA, J. Miyazaki for CAG promoter, U. Lendahl for nestin promoter, C. Cepko for pCALNL-DsRed, S. Miyagawa for codon usage-optimized Cre, Y. Mizutani and K. Yoshizaki for manipulation of Flt1-DsRed mouse embryos, Y. Gotoh and K. Nakashima for their help to breed the Aldh1l1-GFP mice, N. Hane, T. Nagano, I. Iwamoto and H. Arai for technical supports, and M. Yoshitomo and T. Kobayashi for their assistance in preparing two-photon imaging. We also thank N. Hiroi for technical supports in single cell RNA-seq data analysis. This work was supported by JSPS KAKENHI [Grant Number JP21K07309 to H.Tabata, JP20H05688, JP16H06482, and JP22K19365 to K.Nakajima, JP16H06280 (Platforms for Advanced Technologies and Research Resources “Advanced Bioimaging Support”) to M.A. and J.N., JP21K06413, and JP18K06508 to T.H.], Takeda Science Foundation, Keio Gijuku Academic Development Funds, and Keio Gijuku Fukuzawa Memorial Fund to K.Nakajima. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

year = "2022",

month = dec,

doi = "10.1038/s41467-022-34184-x",

language = "English",

volume = "13",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Publishing Group",

number = "1",

}

TY - JOUR

T1 - Erratic and blood vessel-guided migration of astrocyte progenitors in the cerebral cortex

AU - Tabata, Hidenori

AU - Sasaki, Megumi

AU - Agetsuma, Masakazu

AU - Sano, Hitomi

AU - Hirota, Yuki

AU - Miyajima, Michio

AU - Hayashi, Kanehiro

AU - Honda, Takao

AU - Nishikawa, Masashi

AU - Inaguma, Yutaka

AU - Ito, Hidenori

AU - Takebayashi, Hirohide

AU - Ema, Masatsugu

AU - Ikenaka, Kazuhiro

AU - Nabekura, Junichi

AU - Nagata, Koh ichi

AU - Nakajima, Kazunori

N1 - Funding Information: We are grateful to C.G.Lobe for Z/EG mice, K. Kawakami and Y. Takahashi for pCAGGS-T2TP and pT2K-CAGGS-mCherry, A. Miyawaki for kikGR cDNA, J. Miyazaki for CAG promoter, U. Lendahl for nestin promoter, C. Cepko for pCALNL-DsRed, S. Miyagawa for codon usage-optimized Cre, Y. Mizutani and K. Yoshizaki for manipulation of Flt1-DsRed mouse embryos, Y. Gotoh and K. Nakashima for their help to breed the Aldh1l1-GFP mice, N. Hane, T. Nagano, I. Iwamoto and H. Arai for technical supports, and M. Yoshitomo and T. Kobayashi for their assistance in preparing two-photon imaging. We also thank N. Hiroi for technical supports in single cell RNA-seq data analysis. This work was supported by JSPS KAKENHI [Grant Number JP21K07309 to H.Tabata, JP20H05688, JP16H06482, and JP22K19365 to K.Nakajima, JP16H06280 (Platforms for Advanced Technologies and Research Resources “Advanced Bioimaging Support”) to M.A. and J.N., JP21K06413, and JP18K06508 to T.H.], Takeda Science Foundation, Keio Gijuku Academic Development Funds, and Keio Gijuku Fukuzawa Memorial Fund to K.Nakajima. Publisher Copyright: © 2022, The Author(s).

PY - 2022/12

Y1 - 2022/12

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85141171357&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85141171357&partnerID=8YFLogxK

U2 - 10.1038/s41467-022-34184-x

DO - 10.1038/s41467-022-34184-x

M3 - Article

C2 - 36323680

AN - SCOPUS:85141171357

SN - 2041-1723

VL - 13

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 6571

ER -

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

Abstract

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Cite this