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Featured ArticleResearch Articles, Cellular/Molecular

Embryonic Pericytes Promote Microglial Homeostasis and Their Effects on Neural Progenitors in the Developing Cerebral Cortex

Yuki Hattori, Haruka Itoh, Yoji Tsugawa, Yusuke Nishida, Kaori Kurata, Akiyoshi Uemura and Takaki Miyata
Journal of Neuroscience 19 January 2022, 42 (3) 362-376; DOI: https://doi.org/10.1523/JNEUROSCI.1201-21.2021
Yuki Hattori
1Department of Anatomy and Cell Biology, Graduate School of Medicine, Nagoya University, Nagoya, Aichi 466-8550, Japan
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Haruka Itoh
1Department of Anatomy and Cell Biology, Graduate School of Medicine, Nagoya University, Nagoya, Aichi 466-8550, Japan
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Yoji Tsugawa
2Department of Biologics 1 group, Laboratory for Advanced Medicine Research, Shionogi & Company, Toyonaka, Osaka 561-0825, Japan
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Yusuke Nishida
1Department of Anatomy and Cell Biology, Graduate School of Medicine, Nagoya University, Nagoya, Aichi 466-8550, Japan
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Kaori Kurata
3Department of Retinal Vascular Biology, Graduate School of Medical Sciences, Nagoya City University, Nagoya, Aichi 467-8601, Japan
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Akiyoshi Uemura
3Department of Retinal Vascular Biology, Graduate School of Medical Sciences, Nagoya City University, Nagoya, Aichi 467-8601, Japan
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Takaki Miyata
1Department of Anatomy and Cell Biology, Graduate School of Medicine, Nagoya University, Nagoya, Aichi 466-8550, Japan
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Abstract

Multifaceted microglial functions in the developing brain, such as promoting the differentiation of neural progenitors and contributing to the positioning and survival of neurons, have been progressively revealed. Although previous studies have noted the relationship between vascular endothelial cells and microglia in the developing brain, little attention has been given to the importance of pericytes, the mural cells surrounding endothelial cells. In this study, we attempted to dissect the role of pericytes in microglial distribution and function in developing mouse brains. Our immunohistochemical analysis showed that approximately half of the microglia attached to capillaries in the cerebral walls. Notably, a magnified observation of the position of microglia, vascular endothelial cells and pericytes demonstrated that microglia were preferentially associated with pericytes that covered 79.8% of the total capillary surface area. Through in vivo pericyte depletion induced by the intraventricular administration of a neutralizing antibody against platelet-derived growth factor receptor (PDGFR)β (clone APB5), we found that microglial density was markedly decreased compared with that in control antibody-treated brains because of their low proliferative capacity. Moreover, in vitro coculture of isolated CD11b+ microglia and NG2+PDGFRα– cells, which are mostly composed of pericytes, from parenchymal cells indicated that pericytes promote microglial proliferation via the production of soluble factors. Furthermore, pericyte depletion by APB5 treatment resulted in a failure of microglia to promote the differentiation of neural stem cells into intermediate progenitors. Taken together, our findings suggest that pericytes facilitate microglial homeostasis in the developing brains, thereby indirectly supporting microglial effects on neural progenitors.

SIGNIFICANCE STATEMENT This study highlights the novel effect of pericytes on microglia in the developing mouse brain. Through multiple analyses using an in vivo pericyte depletion mouse model and an in vitro coculture study of isolated pericytes and microglia from parenchymal cells, we demonstrated that pericytes contribute to microglial proliferation and support microglia in efficiently promoting the differentiation of neural stem cells into intermediate progenitors. Our present data provide evidence that pericytes function not only in the maintenance of cerebral microcirculation and blood brain barrier (BBB) integrity but also in microglial homeostasis in the developing cerebral walls. These findings will expand our knowledge and help elucidate the mechanism of brain development both in healthy and disease conditions.

  • cerebral cortex
  • developing brain
  • microglia
  • neural progenitors
  • neurovascular unit
  • pericyte

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The Journal of Neuroscience: 42 (3)
Journal of Neuroscience
Vol. 42, Issue 3
19 Jan 2022
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Embryonic Pericytes Promote Microglial Homeostasis and Their Effects on Neural Progenitors in the Developing Cerebral Cortex
Yuki Hattori, Haruka Itoh, Yoji Tsugawa, Yusuke Nishida, Kaori Kurata, Akiyoshi Uemura, Takaki Miyata
Journal of Neuroscience 19 January 2022, 42 (3) 362-376; DOI: 10.1523/JNEUROSCI.1201-21.2021

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Embryonic Pericytes Promote Microglial Homeostasis and Their Effects on Neural Progenitors in the Developing Cerebral Cortex
Yuki Hattori, Haruka Itoh, Yoji Tsugawa, Yusuke Nishida, Kaori Kurata, Akiyoshi Uemura, Takaki Miyata
Journal of Neuroscience 19 January 2022, 42 (3) 362-376; DOI: 10.1523/JNEUROSCI.1201-21.2021
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Keywords

  • cerebral cortex
  • developing brain
  • microglia
  • neural progenitors
  • neurovascular unit
  • pericyte

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