The University of Southampton
University of Southampton Institutional Repository

Folding of the syncytiotrophoblast basal plasma membrane increases the surface area available for exchange in human placenta

Folding of the syncytiotrophoblast basal plasma membrane increases the surface area available for exchange in human placenta
Folding of the syncytiotrophoblast basal plasma membrane increases the surface area available for exchange in human placenta

INTRODUCTION: The placental syncytiotrophoblast is the primary barrier between the mother and the fetus. To cross the placenta, nutrients and wastes must be transported across the apical microvillous and basal plasma membranes. While the syncytiotrophoblast basal plasma membrane is typically represented as relatively smooth, it has been shown to have invaginations that may increase its surface area. This study aimed to quantify how folding of the syncytiotrophoblast basal membrane contributes to its surface area and to visualise three-dimensional structures of the basal membrane and cytotrophoblast cell structures.

METHODS: Transmission electron microscope images of human term placenta were analysed using stereological approaches to quantify how folding of the syncytiotrophoblast basal plasma membrane affected surface area. Serial block-face scanning electron microscopy was used to visualise the three-dimensional structure of the syncytiotrophoblast basal membrane and cytotrophoblast cells.

RESULTS: Syncytiotrophoblast basal membrane covered 69.1% of the basal lamina, with cytotrophoblast cells covering the remaining 30.9%. In basal lamina adjacent to syncytiotrophoblast, 34% was adjacent to smooth basal membrane and 66% to folded basal membrane. Syncytiotrophoblast basal membrane folds increased the surface area adjacent to basal lamina by 305%. Including regions overlying the cytotrophoblast cells, basal membrane folds increased syncytiotrophoblast basal membrane surface area by 4.4-fold relative to the basal lamina in terminal villi. Terminal and intermediate villi were similar in terms of trophoblast coverage of the basal lamina and basal membrane folding. The three-dimensional structures of the syncytiotrophoblast basal plasma membrane and cytotrophoblast cells were generated from serial block-face scanning electron microscopy image stacks.

DISCUSSION: These findings indicate that the surface area of the syncytiotrophoblast basal plasma membrane is far larger than had been appreciated. We suggest that these folds increase the surface area available for transport to and from the fetus. Changes in the extent of basal membrane folding could affect nutrient transfer capacity and underlie pathological fetal growth, including fetal growth restriction and macrosomia.

Basal lamina, Placenta, Placental transport, Ultrastructure
0143-4004
57-63
Tashev, Stanimir A
229727d7-5e88-483c-b64f-f524f7db1904
Parsons, Daisy
08b4de6e-3be3-4eea-a4bc-7c776e30414a
Hillman, Cameron
4867a2fb-1090-43ee-8f3b-6cb381eb795a
Harris, Shelley
6efe8f50-354e-48ea-889e-c2d8293bb16a
Lofthouse, Emma M
c4004ff1-2ed3-4b80-9ade-583c742de59c
Goggin, Patricia
90c80d17-9f7a-4401-8e6f-919c63efe5e6
Chatelet, David S
6371fd7a-e274-4738-9ccb-3dd4dab32928
Cleal, Jane K
18cfd2c1-bd86-4a13-b38f-c321af56da66
Smyth, Neil
0eba2a40-3b43-4d40-bb64-621bd7e9d505
Page, Anton M.
e315d159-536f-4d3d-83eb-5684ee42ada0
Lewis, Rohan M
caaeb97d-ea69-4f7b-8adb-5fa25e2d3502
Tashev, Stanimir A
229727d7-5e88-483c-b64f-f524f7db1904
Parsons, Daisy
08b4de6e-3be3-4eea-a4bc-7c776e30414a
Hillman, Cameron
4867a2fb-1090-43ee-8f3b-6cb381eb795a
Harris, Shelley
6efe8f50-354e-48ea-889e-c2d8293bb16a
Lofthouse, Emma M
c4004ff1-2ed3-4b80-9ade-583c742de59c
Goggin, Patricia
90c80d17-9f7a-4401-8e6f-919c63efe5e6
Chatelet, David S
6371fd7a-e274-4738-9ccb-3dd4dab32928
Cleal, Jane K
18cfd2c1-bd86-4a13-b38f-c321af56da66
Smyth, Neil
0eba2a40-3b43-4d40-bb64-621bd7e9d505
Page, Anton M.
e315d159-536f-4d3d-83eb-5684ee42ada0
Lewis, Rohan M
caaeb97d-ea69-4f7b-8adb-5fa25e2d3502

Tashev, Stanimir A, Parsons, Daisy, Hillman, Cameron, Harris, Shelley, Lofthouse, Emma M, Goggin, Patricia, Chatelet, David S, Cleal, Jane K, Smyth, Neil, Page, Anton M. and Lewis, Rohan M (2022) Folding of the syncytiotrophoblast basal plasma membrane increases the surface area available for exchange in human placenta. Placenta, 117, 57-63. (doi:10.1016/j.placenta.2021.11.002).

Record type: Article

Abstract

INTRODUCTION: The placental syncytiotrophoblast is the primary barrier between the mother and the fetus. To cross the placenta, nutrients and wastes must be transported across the apical microvillous and basal plasma membranes. While the syncytiotrophoblast basal plasma membrane is typically represented as relatively smooth, it has been shown to have invaginations that may increase its surface area. This study aimed to quantify how folding of the syncytiotrophoblast basal membrane contributes to its surface area and to visualise three-dimensional structures of the basal membrane and cytotrophoblast cell structures.

METHODS: Transmission electron microscope images of human term placenta were analysed using stereological approaches to quantify how folding of the syncytiotrophoblast basal plasma membrane affected surface area. Serial block-face scanning electron microscopy was used to visualise the three-dimensional structure of the syncytiotrophoblast basal membrane and cytotrophoblast cells.

RESULTS: Syncytiotrophoblast basal membrane covered 69.1% of the basal lamina, with cytotrophoblast cells covering the remaining 30.9%. In basal lamina adjacent to syncytiotrophoblast, 34% was adjacent to smooth basal membrane and 66% to folded basal membrane. Syncytiotrophoblast basal membrane folds increased the surface area adjacent to basal lamina by 305%. Including regions overlying the cytotrophoblast cells, basal membrane folds increased syncytiotrophoblast basal membrane surface area by 4.4-fold relative to the basal lamina in terminal villi. Terminal and intermediate villi were similar in terms of trophoblast coverage of the basal lamina and basal membrane folding. The three-dimensional structures of the syncytiotrophoblast basal plasma membrane and cytotrophoblast cells were generated from serial block-face scanning electron microscopy image stacks.

DISCUSSION: These findings indicate that the surface area of the syncytiotrophoblast basal plasma membrane is far larger than had been appreciated. We suggest that these folds increase the surface area available for transport to and from the fetus. Changes in the extent of basal membrane folding could affect nutrient transfer capacity and underlie pathological fetal growth, including fetal growth restriction and macrosomia.

Text
BM folds papers Authors accepted manuscript - Accepted Manuscript
Download (13MB)

More information

Accepted/In Press date: 2 November 2021
e-pub ahead of print date: 4 November 2021
Published date: January 2022
Additional Information: Funding Information: The staff and patients at the Princess Anne Hospital. Staff in the Biomedical Imaging Unit, University of Southampton. Equipment in the Biomedical Imaging Unit was supported by MR/L012626/1 Southampton Imaging under MRC UKRMP Funding.
Keywords: Basal lamina, Placenta, Placental transport, Ultrastructure

Identifiers

Local EPrints ID: 453163
URI: http://eprints.soton.ac.uk/id/eprint/453163
ISSN: 0143-4004
PURE UUID: d413f126-da7f-4aea-8d20-ffdbf6bde1eb
ORCID for Emma M Lofthouse: ORCID iD orcid.org/0000-0002-0175-5590
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: 10 Jan 2022 17:49
Last modified: 17 Mar 2024 06:58

Export record

Altmetrics

Contributors

Author: Stanimir A Tashev
Author: Daisy Parsons
Author: Cameron Hillman
Author: Shelley Harris
Author: Emma M Lofthouse ORCID iD
Author: Patricia Goggin
Author: David S Chatelet
Author: Jane K Cleal ORCID iD
Author: Neil Smyth
Author: Anton M. Page
Author: Rohan M Lewis ORCID iD

Download statistics

Downloads from ePrints over the past year. Other digital versions may also be available to download e.g. from the publisher's website.

View more statistics

Atom RSS 1.0 RSS 2.0

Contact ePrints Soton: eprints@soton.ac.uk

ePrints Soton supports OAI 2.0 with a base URL of http://eprints.soton.ac.uk/cgi/oai2

This repository has been built using EPrints software, developed at the University of Southampton, but available to everyone to use.

We use cookies to ensure that we give you the best experience on our website. If you continue without changing your settings, we will assume that you are happy to receive cookies on the University of Southampton website.

×