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Microvillous tip vesicles may be an origin of placental extracellular vesicles

Microvillous tip vesicles may be an origin of placental extracellular vesicles
Microvillous tip vesicles may be an origin of placental extracellular vesicles

INTRODUCTION: Extracellular vesicles are now believed to be important mediators of placental-maternal communication. However, little is known about the formation of extracellular vesicles by human placenta. This study uses nanoscale three-dimensional imaging to investigate how and where placental extracellular vesicles form.

METHODS: Term and first trimester human placental villi were imaged by serial block face scanning electron microscopy. These images were analysed to quantify vesicle surface density. Segmentation was performed to reconstruct three-dimensional images of extracellular vesicles. Live imaging light microscopy of first trimester villous explants was performed.

RESULTS: Vesicles were observed on the tips of placental microvilli in term and first trimester placenta. In term placenta these microvillous tip vesicles had a median size of 0.55 μm and their surface area density exceeded 22000 per mm2. Microvillous tip vesicle membranes had a lower electron density than the microvillous plasma membrane. Thirty seven percent of vesicles had a complex membrane structure including double membranes, internal vesicles and vesicle chains. Budding of smaller secondary vesicles from microvillous tip vesicle membranes was observed. Live imaging of a first trimester villus explant observed formation of vesicles which were larger but visually similar to the secondary vesicles observed by electron microscopy.

DISCUSSION: These observations suggest that extracellular vesicles are forming on the tips of placental microvilli prior to release into maternal blood. However, it cannot be discounted that there are maternal extracellular vesicles that have bound to microvilli. In either case, the high surface area density of microvillous tip vesicles is consistent with an important role in placental-maternal signalling.

Exosome, Extracellular vesicle, Maternal-fetal signalling, Micro-vesicle, Microvilli, Plasma membrane
0143-4004
24-30
Davies, Rebecca
77311fdb-a6c9-4243-9b67-c89dbc439a81
Griffiths, Catherine
ffdcb5c0-b61a-4599-bd4e-43d0ac2b696d
Askelund, Kathryn
c85ae96b-f018-404d-b26c-378e8b4c68af
Palaiologou, Eleni
a1c591e4-6bc8-4859-93af-c2d0bb9101a6
Cleal, Jane K.
18cfd2c1-bd86-4a13-b38f-c321af56da66
Page, Anton
76ebbfb8-4fe3-495c-afff-1f2f34977fee
Chatelet, David S.
6371fd7a-e274-4738-9ccb-3dd4dab32928
Goggin, Patricia
90c80d17-9f7a-4401-8e6f-919c63efe5e6
Chamley, Larry
3cc84fe3-8a7d-4066-bf7e-6496f40ab1fc
Lewis, Rohan M.
caaeb97d-ea69-4f7b-8adb-5fa25e2d3502
Davies, Rebecca
77311fdb-a6c9-4243-9b67-c89dbc439a81
Griffiths, Catherine
ffdcb5c0-b61a-4599-bd4e-43d0ac2b696d
Askelund, Kathryn
c85ae96b-f018-404d-b26c-378e8b4c68af
Palaiologou, Eleni
a1c591e4-6bc8-4859-93af-c2d0bb9101a6
Cleal, Jane K.
18cfd2c1-bd86-4a13-b38f-c321af56da66
Page, Anton
76ebbfb8-4fe3-495c-afff-1f2f34977fee
Chatelet, David S.
6371fd7a-e274-4738-9ccb-3dd4dab32928
Goggin, Patricia
90c80d17-9f7a-4401-8e6f-919c63efe5e6
Chamley, Larry
3cc84fe3-8a7d-4066-bf7e-6496f40ab1fc
Lewis, Rohan M.
caaeb97d-ea69-4f7b-8adb-5fa25e2d3502

Davies, Rebecca, Griffiths, Catherine, Askelund, Kathryn, Palaiologou, Eleni, Cleal, Jane K., Page, Anton, Chatelet, David S., Goggin, Patricia, Chamley, Larry and Lewis, Rohan M. (2022) Microvillous tip vesicles may be an origin of placental extracellular vesicles. Placenta, 123, 24-30. (doi:10.1016/j.placenta.2022.04.003).

Record type: Article

Abstract

INTRODUCTION: Extracellular vesicles are now believed to be important mediators of placental-maternal communication. However, little is known about the formation of extracellular vesicles by human placenta. This study uses nanoscale three-dimensional imaging to investigate how and where placental extracellular vesicles form.

METHODS: Term and first trimester human placental villi were imaged by serial block face scanning electron microscopy. These images were analysed to quantify vesicle surface density. Segmentation was performed to reconstruct three-dimensional images of extracellular vesicles. Live imaging light microscopy of first trimester villous explants was performed.

RESULTS: Vesicles were observed on the tips of placental microvilli in term and first trimester placenta. In term placenta these microvillous tip vesicles had a median size of 0.55 μm and their surface area density exceeded 22000 per mm2. Microvillous tip vesicle membranes had a lower electron density than the microvillous plasma membrane. Thirty seven percent of vesicles had a complex membrane structure including double membranes, internal vesicles and vesicle chains. Budding of smaller secondary vesicles from microvillous tip vesicle membranes was observed. Live imaging of a first trimester villus explant observed formation of vesicles which were larger but visually similar to the secondary vesicles observed by electron microscopy.

DISCUSSION: These observations suggest that extracellular vesicles are forming on the tips of placental microvilli prior to release into maternal blood. However, it cannot be discounted that there are maternal extracellular vesicles that have bound to microvilli. In either case, the high surface area density of microvillous tip vesicles is consistent with an important role in placental-maternal signalling.

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Microvesicle paper final version resubmission LWC_PG - Accepted Manuscript
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More information

Accepted/In Press date: 15 April 2022
e-pub ahead of print date: 20 April 2022
Published date: 1 June 2022
Keywords: Exosome, Extracellular vesicle, Maternal-fetal signalling, Micro-vesicle, Microvilli, Plasma membrane

Identifiers

Local EPrints ID: 457460
URI: http://eprints.soton.ac.uk/id/eprint/457460
ISSN: 0143-4004
PURE UUID: 298b472f-2010-46db-b8ba-dbe8c09b965d
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: 09 Jun 2022 16:43
Last modified: 09 Nov 2022 02:37

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Contributors

Author: Rebecca Davies
Author: Catherine Griffiths
Author: Kathryn Askelund
Author: Eleni Palaiologou
Author: Jane K. Cleal ORCID iD
Author: Anton Page
Author: David S. Chatelet
Author: Patricia Goggin
Author: Larry Chamley
Author: Rohan M. Lewis ORCID iD

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