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Pericytes on placental capillaries in terminal villi preferentially cover endothelial junctions in regions furthest away from the trophoblast

Pericytes on placental capillaries in terminal villi preferentially cover endothelial junctions in regions furthest away from the trophoblast
Pericytes on placental capillaries in terminal villi preferentially cover endothelial junctions in regions furthest away from the trophoblast

Introduction: Pericytes are a common feature in the placental microvasculature but their roles are not well understood. Pericytes may provide physical or endocrine support for endothelium and in some tissues mediate vasoconstriction. Methods: This study uses serial block-face scanning electron microscopy (SBFSEM) to generate three-dimensional (3D) reconstructions of placental pericytes of the terminal villi and transmission electron microscopy (TEM) to study pericyte endothelial cell interactions. The proportion of endothelial cell junctions covered by pericytes was determined. Results: The detailed 3D models of placental pericytes show pericyte structure at a new level of detail. Placental pericytes have many fingers extending from the cell body which can span multiple capillary branches. The proportion of endothelial cell-cell junctions covered by pericytes was significantly higher than pericyte coverage of capillary endothelium as a whole (endothelium: 14%, junctions: 43%, p < 0.0001). However, the proportion of endothelial cell-cell junctions covered by pericytes in regions adjacent to trophoblast was reduced compared to regions >3 μm away from trophoblast (27% vs 62% respectively, p < 0.001). No junctional complexes were observed connecting pericytes and endothelial cells but there were regions of cell membrane with features suggestive of intercellular adhesions. Discussion: These data suggest that the localisation of pericytes on the villous capillary is not random but organised in relation to both endothelial junctions and the location of adjacent trophoblast. This further suggests that pericyte coverage may favour capillary permeability in regions that are most important for exchange, but limit capillary permeability in other regions.

Microvasculature, Pericytes, Placenta, Three-dimensional imaging
0143-4004
1-7
Harris, Shelley E.
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Matthews, Kate S.H.
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Palaiologou, Eleni
a1c591e4-6bc8-4859-93af-c2d0bb9101a6
Tashev, Stanimir A.
229727d7-5e88-483c-b64f-f524f7db1904
Lofthouse, Emma M.
c4004ff1-2ed3-4b80-9ade-583c742de59c
Pearson-Farr, Jennifer
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Goggin, Patricia
c2d225c4-b84d-4ead-a433-320057cb5fa9
Chatelet, David S.
6371fd7a-e274-4738-9ccb-3dd4dab32928
Johnston, David A.
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Jongen, Maaike SA
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Page, Anton M.
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Cleal, Jane K.
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Lewis, Rohan M.
caaeb97d-ea69-4f7b-8adb-5fa25e2d3502
Harris, Shelley E.
6efe8f50-354e-48ea-889e-c2d8293bb16a
Matthews, Kate S.H.
fa8b5bf2-1273-4708-ab95-796b99c9145c
Palaiologou, Eleni
a1c591e4-6bc8-4859-93af-c2d0bb9101a6
Tashev, Stanimir A.
229727d7-5e88-483c-b64f-f524f7db1904
Lofthouse, Emma M.
c4004ff1-2ed3-4b80-9ade-583c742de59c
Pearson-Farr, Jennifer
6c1e2bb4-ea4f-4fbe-a3fa-36a47757dc21
Goggin, Patricia
c2d225c4-b84d-4ead-a433-320057cb5fa9
Chatelet, David S.
6371fd7a-e274-4738-9ccb-3dd4dab32928
Johnston, David A.
b41163c9-b9d2-425c-af99-2a357204014e
Jongen, Maaike SA
13f00bd0-5bf2-400f-a3ac-aa90d2180327
Page, Anton M.
e315d159-536f-4d3d-83eb-5684ee42ada0
Cleal, Jane K.
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Lewis, Rohan M.
caaeb97d-ea69-4f7b-8adb-5fa25e2d3502

Harris, Shelley E., Matthews, Kate S.H., Palaiologou, Eleni, Tashev, Stanimir A., Lofthouse, Emma M., Pearson-Farr, Jennifer, Goggin, Patricia, Chatelet, David S., Johnston, David A., Jongen, Maaike SA, Page, Anton M., Cleal, Jane K. and Lewis, Rohan M. (2021) Pericytes on placental capillaries in terminal villi preferentially cover endothelial junctions in regions furthest away from the trophoblast. Placenta, 104, 1-7. (doi:10.1016/j.placenta.2020.10.032).

Record type: Article

Abstract

Introduction: Pericytes are a common feature in the placental microvasculature but their roles are not well understood. Pericytes may provide physical or endocrine support for endothelium and in some tissues mediate vasoconstriction. Methods: This study uses serial block-face scanning electron microscopy (SBFSEM) to generate three-dimensional (3D) reconstructions of placental pericytes of the terminal villi and transmission electron microscopy (TEM) to study pericyte endothelial cell interactions. The proportion of endothelial cell junctions covered by pericytes was determined. Results: The detailed 3D models of placental pericytes show pericyte structure at a new level of detail. Placental pericytes have many fingers extending from the cell body which can span multiple capillary branches. The proportion of endothelial cell-cell junctions covered by pericytes was significantly higher than pericyte coverage of capillary endothelium as a whole (endothelium: 14%, junctions: 43%, p < 0.0001). However, the proportion of endothelial cell-cell junctions covered by pericytes in regions adjacent to trophoblast was reduced compared to regions >3 μm away from trophoblast (27% vs 62% respectively, p < 0.001). No junctional complexes were observed connecting pericytes and endothelial cells but there were regions of cell membrane with features suggestive of intercellular adhesions. Discussion: These data suggest that the localisation of pericytes on the villous capillary is not random but organised in relation to both endothelial junctions and the location of adjacent trophoblast. This further suggests that pericyte coverage may favour capillary permeability in regions that are most important for exchange, but limit capillary permeability in other regions.

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More information

Accepted/In Press date: 27 October 2020
e-pub ahead of print date: 7 November 2020
Published date: 15 January 2021
Additional Information: Copyright © 2020. Published by Elsevier Ltd.
Keywords: Microvasculature, Pericytes, Placenta, Three-dimensional imaging

Identifiers

Local EPrints ID: 446252
URI: http://eprints.soton.ac.uk/id/eprint/446252
ISSN: 0143-4004
PURE UUID: 30c345c7-ccc0-43e9-80a6-7472ee26d8ca
ORCID for Emma M. Lofthouse: ORCID iD orcid.org/0000-0002-0175-5590
ORCID for Patricia Goggin: ORCID iD orcid.org/0000-0003-4730-0206
ORCID for David A. Johnston: ORCID iD orcid.org/0000-0001-6703-6014
ORCID for Jane K. Cleal: ORCID iD orcid.org/0000-0001-7978-4327
ORCID for Rohan M. Lewis: ORCID iD orcid.org/0000-0003-4044-9104

Catalogue record

Date deposited: 01 Feb 2021 17:32
Last modified: 26 Nov 2021 03:08

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Contributors

Author: Shelley E. Harris
Author: Kate S.H. Matthews
Author: Eleni Palaiologou
Author: Stanimir A. Tashev
Author: Emma M. Lofthouse ORCID iD
Author: Jennifer Pearson-Farr
Author: Patricia Goggin ORCID iD
Author: David S. Chatelet
Author: David A. Johnston ORCID iD
Author: Maaike SA Jongen
Author: Anton M. Page
Author: Jane K. Cleal ORCID iD
Author: Rohan M. Lewis ORCID iD

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