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3D Reconstruction of the Clarified Rat Hindbrain Choroid Plexus

The choroid plexus (CP) acts as a regulated gate between blood and cerebrospinal fluid (CSF). Despite its simple histology (a monostratified cuboidal epithelium overlying a vascularized stroma), this organ has remarkably complex functions several of which involve local interaction with cells located...

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Autores principales: Perin, Paola, Rossetti, Riccardo, Ricci, Carolina, Cossellu, Daniele, Lazzarini, Simone, Bethge, Philipp, Voigt, Fabian F., Helmchen, Fritjof, Batti, Laura, Gantar, Ivana, Pizzala, Roberto
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8359725/
https://www.ncbi.nlm.nih.gov/pubmed/34395426
http://dx.doi.org/10.3389/fcell.2021.692617
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author Perin, Paola
Rossetti, Riccardo
Ricci, Carolina
Cossellu, Daniele
Lazzarini, Simone
Bethge, Philipp
Voigt, Fabian F.
Helmchen, Fritjof
Batti, Laura
Gantar, Ivana
Pizzala, Roberto
author_facet Perin, Paola
Rossetti, Riccardo
Ricci, Carolina
Cossellu, Daniele
Lazzarini, Simone
Bethge, Philipp
Voigt, Fabian F.
Helmchen, Fritjof
Batti, Laura
Gantar, Ivana
Pizzala, Roberto
author_sort Perin, Paola
collection PubMed
description The choroid plexus (CP) acts as a regulated gate between blood and cerebrospinal fluid (CSF). Despite its simple histology (a monostratified cuboidal epithelium overlying a vascularized stroma), this organ has remarkably complex functions several of which involve local interaction with cells located around ventricle walls. Our knowledge of CP structural organization is mainly derived from resin casts, which capture the overall features but only allow reconstruction of the vascular pattern surface, unrelated to the overlying epithelium and only loosely related to ventricular location. Recently, CP single cell atlases are starting to emerge, providing insight on local heterogeneities and interactions. So far, however, few studies have described CP spatial organization at the mesoscale level, because of its fragile nature and deep location within the brain. Here, using an iDISCO-based clearing approach and light-sheet microscopy, we have reconstructed the normal rat hindbrain CP (hCP) macro- and microstructure, using markers for epithelium, arteries, microvasculature, and macrophages, and noted its association with 4th ventricle-related neurovascular structures. The hCP is organized in domains associated to a main vessel (fronds) which carry a variable number of villi; the latter are enclosed by epithelium and may be flat (leaf-like) or rolled up to variable extent. Arteries feeding the hCP emerge from the cerebellar surface, and branch into straight arterioles terminating as small capillary anastomotic networks, which run within a single villus and terminate attaching multiple times to a large tortuous capillary (LTC) which ends into a vein. Venous outflow mostly follows arterial pathways, except for the lateral horizontal segment (LHS) and the caudal sagittal segment. The structure of fronds and villi is related to the microvascular pattern at the hCP surface: when LTCs predominate, leaflike villi are more evident and bulge from the surface; different, corkscrew-like villi are observed in association to arterioles reaching close to the CP surface with spiraling capillaries surrounding them. Both leaf-like and corkscrew-like villi may reach the 4th ventricle floor, making contact points at their tip, where no gap is seen between CP epithelium and ependyma. Contacts usually involve several adjacent villi and may harbor epiplexus macrophages. At the junction between medial (MHS) and lateral (LHS) horizontal segment, arterial supply is connected to the temporal bone subarcuate fossa, and venous outflow drains to a ventral vein which exits through the cochlear nuclei at the Luschka foramen. These vascular connections stabilize the hCP overall structure within the 4th ventricle but make MHS-LHS joint particularly fragile and very easily damaged when removing the brain from the skull. Even in damaged samples, however, CP fronds (or isolated villi) often remain strongly attached to the dorsal cochlear nucleus (DCN) surface; in these fronds, contacts are still present and connecting “bridges” may be seen, suggesting the presence of real molecular contacts rather than mere appositions.
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spelling pubmed-83597252021-08-13 3D Reconstruction of the Clarified Rat Hindbrain Choroid Plexus Perin, Paola Rossetti, Riccardo Ricci, Carolina Cossellu, Daniele Lazzarini, Simone Bethge, Philipp Voigt, Fabian F. Helmchen, Fritjof Batti, Laura Gantar, Ivana Pizzala, Roberto Front Cell Dev Biol Cell and Developmental Biology The choroid plexus (CP) acts as a regulated gate between blood and cerebrospinal fluid (CSF). Despite its simple histology (a monostratified cuboidal epithelium overlying a vascularized stroma), this organ has remarkably complex functions several of which involve local interaction with cells located around ventricle walls. Our knowledge of CP structural organization is mainly derived from resin casts, which capture the overall features but only allow reconstruction of the vascular pattern surface, unrelated to the overlying epithelium and only loosely related to ventricular location. Recently, CP single cell atlases are starting to emerge, providing insight on local heterogeneities and interactions. So far, however, few studies have described CP spatial organization at the mesoscale level, because of its fragile nature and deep location within the brain. Here, using an iDISCO-based clearing approach and light-sheet microscopy, we have reconstructed the normal rat hindbrain CP (hCP) macro- and microstructure, using markers for epithelium, arteries, microvasculature, and macrophages, and noted its association with 4th ventricle-related neurovascular structures. The hCP is organized in domains associated to a main vessel (fronds) which carry a variable number of villi; the latter are enclosed by epithelium and may be flat (leaf-like) or rolled up to variable extent. Arteries feeding the hCP emerge from the cerebellar surface, and branch into straight arterioles terminating as small capillary anastomotic networks, which run within a single villus and terminate attaching multiple times to a large tortuous capillary (LTC) which ends into a vein. Venous outflow mostly follows arterial pathways, except for the lateral horizontal segment (LHS) and the caudal sagittal segment. The structure of fronds and villi is related to the microvascular pattern at the hCP surface: when LTCs predominate, leaflike villi are more evident and bulge from the surface; different, corkscrew-like villi are observed in association to arterioles reaching close to the CP surface with spiraling capillaries surrounding them. Both leaf-like and corkscrew-like villi may reach the 4th ventricle floor, making contact points at their tip, where no gap is seen between CP epithelium and ependyma. Contacts usually involve several adjacent villi and may harbor epiplexus macrophages. At the junction between medial (MHS) and lateral (LHS) horizontal segment, arterial supply is connected to the temporal bone subarcuate fossa, and venous outflow drains to a ventral vein which exits through the cochlear nuclei at the Luschka foramen. These vascular connections stabilize the hCP overall structure within the 4th ventricle but make MHS-LHS joint particularly fragile and very easily damaged when removing the brain from the skull. Even in damaged samples, however, CP fronds (or isolated villi) often remain strongly attached to the dorsal cochlear nucleus (DCN) surface; in these fronds, contacts are still present and connecting “bridges” may be seen, suggesting the presence of real molecular contacts rather than mere appositions. Frontiers Media S.A. 2021-07-29 /pmc/articles/PMC8359725/ /pubmed/34395426 http://dx.doi.org/10.3389/fcell.2021.692617 Text en Copyright © 2021 Perin, Rossetti, Ricci, Cossellu, Lazzarini, Bethge, Voigt, Helmchen, Batti, Gantar and Pizzala. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cell and Developmental Biology
Perin, Paola
Rossetti, Riccardo
Ricci, Carolina
Cossellu, Daniele
Lazzarini, Simone
Bethge, Philipp
Voigt, Fabian F.
Helmchen, Fritjof
Batti, Laura
Gantar, Ivana
Pizzala, Roberto
3D Reconstruction of the Clarified Rat Hindbrain Choroid Plexus
title 3D Reconstruction of the Clarified Rat Hindbrain Choroid Plexus
title_full 3D Reconstruction of the Clarified Rat Hindbrain Choroid Plexus
title_fullStr 3D Reconstruction of the Clarified Rat Hindbrain Choroid Plexus
title_full_unstemmed 3D Reconstruction of the Clarified Rat Hindbrain Choroid Plexus
title_short 3D Reconstruction of the Clarified Rat Hindbrain Choroid Plexus
title_sort 3d reconstruction of the clarified rat hindbrain choroid plexus
topic Cell and Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8359725/
https://www.ncbi.nlm.nih.gov/pubmed/34395426
http://dx.doi.org/10.3389/fcell.2021.692617
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