Autonomous vascular networks synchronize GABA neuron migration in the embryonic forebrain

Won, Chung-Kil; Lin, Zhicheng; T, Peeyush Kumar; Li, Suyan; Ding, Lai; Elkhal, Abdallah; Szabó, Gábor; Vasudevan, Anju

doi:10.1038/ncomms3149

Cited by 73 publications

(113 citation statements)

References 58 publications

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“…This problem is accounted to the absence of substrates that facilitate neuronal migration like radial glial guides 9 . Vasculature is increasingly being appreciated as substrates for neuronal migration 6,10,11 . PVECs may offer a solution for these stalled neuronal precursors at transplantation sites.…”

Section: Discussionmentioning

confidence: 99%

“…PVECs are then isolated from Tie2GFP embryos (in which only endothelial cells express GFP) and stringently sorted by dual FACS analysis. The purity of sorted endothelial cells are ensured by collection of cells that are double positive for GFP and CD31/PECAM-1 6 .…”

Section: Discussionmentioning

confidence: 99%

“…The direction of propagation of the periventricular angiogenesis gradient matches the telencephalic transverse neurogenetic gradient. Within the telencephalon, the periventricular angiogenesis gradient and the gradient of GABA neurons migrating tangentially overlaps spatially as well 6 . With respect to timing, the angiogenesis gradient is in advance of the neurogenetic gradient and GABA neuron gradient by about a day.…”

Section: Introductionmentioning

confidence: 99%

“…With respect to timing, the angiogenesis gradient is in advance of the neurogenetic gradient and GABA neuron gradient by about a day. Thus, periventricular endothelial cells are spatially and temporally well positioned to provide critical cues to support telencephalic neurogenesis and neuronal migration 4,6 . Therefore, use of embryonic periventricular endothelial cells in coculture experiments with neuronal progenitors and/or neurons would provide a more favorable model for studying neurovascular interactions and developing novel avenues for treatment of neurodegenerative disease or ischemic/traumatic brain injury.…”

Section: Introductionmentioning

confidence: 99%

“…We emphasize the importance of removing the pial membrane, not only to limit epithelial cell contamination but also to separate pial endothelial cells which are molecularly and functionally distinct from endothelial cells of the periventricular vascular network 4,6 (termed PVECs to distinguish from pial ECs). Here, we describe the method that we routinely use in our laboratory to obtain a rich and pure yield of PVECs.…”

Section: Introductionmentioning

confidence: 99%

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Isolation and Culture of Endothelial Cells from the Embryonic Forebrain

Kumar

Vasudevan

2014

JoVE

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Embryonic brain endothelial cells can serve as an important tool in the study of angiogenesis and neurovascular development and interactions. The two vascular networks of the embryonic forebrain, pial and periventricular, are spatially distinctive and have different origins and growth patterns. Endothelial cells from the pial and periventricular vascular networks have unique gene expression profiles and functions. Here we present a step-by-step protocol for isolation, culture, and verification of pure populations of endothelial cells from the periventricular vascular network (PVECs) of the embryonic forebrain (telencephalon). In this approach, telencephalon devoid of pial membrane obtained from embryonic day 15 mice is minced, digested with collagenase/dispase, and dispersed mechanically into a single cell suspension. PVECs are purified from cell suspension using positive selection with anti-CD-31/PECAM-1 antibody conjugated to MicroBeads using a strong magnetic separation method. Purified cells are cultured on collagen 1 coated culture dishes in endothelial cell culture medium until they become confluent and further subcultured. PVECs obtained with this protocol exhibit cobblestone and spindle shaped phenotypes, as visualized by phase-contrast light microscopy and fluorescence microscopy. Purity of PVEC cultures was established with endothelial cell markers. In our hands, this method reliably and consistently yields pure populations of PVECs. This protocol will benefit studies aimed at gaining mechanistic insights into forebrain angiogenesis, understanding PVEC interactions, and cross-talks with neuronal cell types and holds tremendous potential for therapeutic angiogenesis. Video LinkThe video component of this article can be found at

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Isolation and Culture of Endothelial Cells from the Embryonic Forebrain

Kumar

Vasudevan

2014

JoVE

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Spatially Self‐Organized Three‐Dimensional Neural Concentroid as a Novel Reductionist Humanized Model to Study Neurovascular Development

Chai,

To,

Simorgh

et al. 2023

Advanced Science

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Although human pluripotent stem cell (PSC)‐derived brain organoids have enabled researchers to gain insight into human brain development and disease, these organoids contain solely ectodermal cells and are not vascularized as occurs during brain development. Here it is created less complex and more homogenous large neural constructs starting from PSC‐derived neuroprogenitor cells (NPC), by fusing small NPC spheroids into so‐called concentroids. Such concentroids consisted of a pro‐angiogenic core, containing neuronal and outer radial glia cells, surrounded by an astroglia‐dense outer layer. Incorporating PSC‐derived endothelial cells (EC) around and/or in the concentroids promoted vascularization, accompanied by differential outgrowth and differentiation of neuronal and astroglia cells, as well as the development of ectodermal‐derived pericyte‐like mural cells co‐localizing with EC networks. Single nucleus transcriptomic analysis revealed an enhanced neural cell subtype maturation and diversity in EC‐containing concentroids, which better resemble the fetal human brain compared to classical organoids or NPC‐only concentroids. This PSC‐derived “vascularized” concentroid brain model will facilitate the study of neurovascular/blood‐brain barrier development, neural cell migration, and the development of effective in vitro vascularization strategies of brain mimics.

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Interactions between neural cells and blood vessels in central nervous system development

Morimoto,

Tabata,

Takahashi

et al. 2023

BioEssays

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The sophisticated function of the central nervous system (CNS) is largely supported by proper interactions between neural cells and blood vessels. Accumulating evidence has demonstrated that neurons and glial cells support the formation of blood vessels, which in turn, act as migratory scaffolds for these cell types. Neural progenitors are also involved in the regulation of blood vessel formation. This mutual interaction between neural cells and blood vessels is elegantly controlled by several chemokines, growth factors, extracellular matrix, and adhesion molecules such as integrins. Recent research has revealed that newly migrating cell types along blood vessels repel other preexisting migrating cell types, causing them to detach from the blood vessels. In this review, we discuss vascular formation and cell migration, particularly during development. Moreover, we discuss how the crosstalk between blood vessels and neurons and glial cells could be related to neurodevelopmental disorders.

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Autonomous vascular networks synchronize GABA neuron migration in the embryonic forebrain

Cited by 73 publications

References 58 publications

Isolation and Culture of Endothelial Cells from the Embryonic Forebrain

Isolation and Culture of Endothelial Cells from the Embryonic Forebrain

Spatially Self‐Organized Three‐Dimensional Neural Concentroid as a Novel Reductionist Humanized Model to Study Neurovascular Development

Interactions between neural cells and blood vessels in central nervous system development

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