---
_id: '10825'
abstract:
- lang: eng
text: In development, lineage segregation is coordinated in time and space. An important
example is the mammalian inner cell mass, in which the primitive endoderm (PrE,
founder of the yolk sac) physically segregates from the epiblast (EPI, founder
of the fetus). While the molecular requirements have been well studied, the physical
mechanisms determining spatial segregation between EPI and PrE remain elusive.
Here, we investigate the mechanical basis of EPI and PrE sorting. We find that
rather than the differences in static cell surface mechanical parameters as in
classical sorting models, it is the differences in surface fluctuations that robustly
ensure physical lineage sorting. These differential surface fluctuations systematically
correlate with differential cellular fluidity, which we propose together constitute
a non-equilibrium sorting mechanism for EPI and PrE lineages. By combining experiments
and modeling, we identify cell surface dynamics as a key factor orchestrating
the correct spatial segregation of the founder embryonic lineages.
acknowledgement: We are grateful to H. Niwa for Dox regulatable PB vector; G. Charras
for EzrinT567D cDNA; K. Jones for tdTomato ESCs, R26-Confetti ESCs, and laboratory
assistance; M. Kinoshita for pPB-CAG-H2B-BFP plasmid; P. Humphreys and D. Clements
for imaging support; G. Chu, P. Attlesey, and staff for animal husbandry; S. Pallett
for laboratory assistance; C. Mulas for critical feedback on the project; T. Boroviak
for single-cell RNA-seq; the EMBL Genomics Core Facility for sequencing; and M.
Merkel for developing and sharing the original version of the 3D Voronoi code. This
work was financially supported by BBSRC ( BB/Moo4023/1 and BB/T007044/1 to K.J.C.
and J.N., Alert16 grant BB/R000042 to E.K.P.), Leverhulme Trust ( RPG-2014-080 to
K.J.C. and J.N.), European Research Council ( 772798 -CellFateTech to K.J.C., 311637
-MorphoCorDiv and 820188 -NanoMechShape to E.K.P., Starting Grant 851288 to E.H.,
and 772426 -MeChemGui to K.F.), the Isaac Newton Trust (to E.K.P.), Medical Research
Council UK (MRC program award MC_UU_00012/5 to E.K.P.), the European Union’s Horizon
2020 research and innovation program under the Marie Sklodowska-Curie grant agreement
no. 641639 ( ITN Biopol , H.D.B. and E.K.P.), the Alexander von Humboldt Foundation
(Alexander von Humboldt Professorship to K.F.), EMBO ALTF 522-2021 (to P.S.), Centre
for Trophoblast Research (Next Generation fellowship to S.A.), and JSPS Overseas
Research Fellowships (to A.Y.). The Wellcome-MRC Cambridge Stem Cell Institute receives
core funding from Wellcome Trust ( 203151/Z/16/Z ) and MRC ( MC_PC_17230 ). For
the purpose of open access, the author has applied a CC BY public copyright licence
to any Author Accepted Manuscript version arising from this submission.
article_processing_charge: No
article_type: original
author:
- first_name: Ayaka
full_name: Yanagida, Ayaka
last_name: Yanagida
- first_name: Elena
full_name: Corujo-Simon, Elena
last_name: Corujo-Simon
- first_name: Christopher K.
full_name: Revell, Christopher K.
last_name: Revell
- first_name: Preeti
full_name: Sahu, Preeti
id: 55BA52EE-A185-11EA-88FD-18AD3DDC885E
last_name: Sahu
- first_name: Giuliano G.
full_name: Stirparo, Giuliano G.
last_name: Stirparo
- first_name: Irene M.
full_name: Aspalter, Irene M.
last_name: Aspalter
- first_name: Alex K.
full_name: Winkel, Alex K.
last_name: Winkel
- first_name: Ruby
full_name: Peters, Ruby
last_name: Peters
- first_name: Henry
full_name: De Belly, Henry
last_name: De Belly
- first_name: Davide A.D.
full_name: Cassani, Davide A.D.
last_name: Cassani
- first_name: Sarra
full_name: Achouri, Sarra
last_name: Achouri
- first_name: Raphael
full_name: Blumenfeld, Raphael
last_name: Blumenfeld
- first_name: Kristian
full_name: Franze, Kristian
last_name: Franze
- first_name: Edouard B
full_name: Hannezo, Edouard B
id: 3A9DB764-F248-11E8-B48F-1D18A9856A87
last_name: Hannezo
orcid: 0000-0001-6005-1561
- first_name: Ewa K.
full_name: Paluch, Ewa K.
last_name: Paluch
- first_name: Jennifer
full_name: Nichols, Jennifer
last_name: Nichols
- first_name: Kevin J.
full_name: Chalut, Kevin J.
last_name: Chalut
citation:
ama: Yanagida A, Corujo-Simon E, Revell CK, et al. Cell surface fluctuations regulate
early embryonic lineage sorting. Cell. 2022;185(5):777-793.e20. doi:10.1016/j.cell.2022.01.022
apa: Yanagida, A., Corujo-Simon, E., Revell, C. K., Sahu, P., Stirparo, G. G., Aspalter,
I. M., … Chalut, K. J. (2022). Cell surface fluctuations regulate early embryonic
lineage sorting. Cell. Cell Press. https://doi.org/10.1016/j.cell.2022.01.022
chicago: Yanagida, Ayaka, Elena Corujo-Simon, Christopher K. Revell, Preeti Sahu,
Giuliano G. Stirparo, Irene M. Aspalter, Alex K. Winkel, et al. “Cell Surface
Fluctuations Regulate Early Embryonic Lineage Sorting.” Cell. Cell Press,
2022. https://doi.org/10.1016/j.cell.2022.01.022.
ieee: A. Yanagida et al., “Cell surface fluctuations regulate early embryonic
lineage sorting,” Cell, vol. 185, no. 5. Cell Press, p. 777–793.e20, 2022.
ista: Yanagida A, Corujo-Simon E, Revell CK, Sahu P, Stirparo GG, Aspalter IM, Winkel
AK, Peters R, De Belly H, Cassani DAD, Achouri S, Blumenfeld R, Franze K, Hannezo
EB, Paluch EK, Nichols J, Chalut KJ. 2022. Cell surface fluctuations regulate
early embryonic lineage sorting. Cell. 185(5), 777–793.e20.
mla: Yanagida, Ayaka, et al. “Cell Surface Fluctuations Regulate Early Embryonic
Lineage Sorting.” Cell, vol. 185, no. 5, Cell Press, 2022, p. 777–793.e20,
doi:10.1016/j.cell.2022.01.022.
short: A. Yanagida, E. Corujo-Simon, C.K. Revell, P. Sahu, G.G. Stirparo, I.M. Aspalter,
A.K. Winkel, R. Peters, H. De Belly, D.A.D. Cassani, S. Achouri, R. Blumenfeld,
K. Franze, E.B. Hannezo, E.K. Paluch, J. Nichols, K.J. Chalut, Cell 185 (2022)
777–793.e20.
date_created: 2022-03-06T23:01:52Z
date_published: 2022-02-22T00:00:00Z
date_updated: 2023-08-02T14:43:50Z
day: '22'
ddc:
- '570'
department:
- _id: EdHa
doi: 10.1016/j.cell.2022.01.022
ec_funded: 1
external_id:
isi:
- '000796293700007'
pmid:
- '35196500'
file:
- access_level: open_access
checksum: ae305060e8031297771b89dae9e36a29
content_type: application/pdf
creator: dernst
date_created: 2022-03-07T07:55:23Z
date_updated: 2022-03-07T07:55:23Z
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file_name: 2022_Cell_Yanagida.pdf
file_size: 8478995
relation: main_file
success: 1
file_date_updated: 2022-03-07T07:55:23Z
has_accepted_license: '1'
intvolume: ' 185'
isi: 1
issue: '5'
language:
- iso: eng
month: '02'
oa: 1
oa_version: Published Version
page: 777-793.e20
pmid: 1
project:
- _id: 05943252-7A3F-11EA-A408-12923DDC885E
call_identifier: H2020
grant_number: '851288'
name: Design Principles of Branching Morphogenesis
publication: Cell
publication_identifier:
eissn:
- '10974172'
issn:
- '00928674'
publication_status: published
publisher: Cell Press
quality_controlled: '1'
scopus_import: '1'
status: public
title: Cell surface fluctuations regulate early embryonic lineage sorting
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 185
year: '2022'
...
---
_id: '10178'
abstract:
- lang: eng
text: In dense biological tissues, cell types performing different roles remain
segregated by maintaining sharp interfaces. To better understand the mechanisms
for such sharp compartmentalization, we study the effect of an imposed heterotypic
tension at the interface between two distinct cell types in a fully 3D Voronoi
model for confluent tissues. We find that cells rapidly sort and self-organize
to generate a tissue-scale interface between cell types, and cells adjacent to
this interface exhibit signature geometric features including nematic-like ordering,
bimodal facet areas, and registration, or alignment, of cell centers on either
side of the two-tissue interface. The magnitude of these features scales directly
with the magnitude of the imposed tension, suggesting that biologists can estimate
the magnitude of tissue surface tension between two tissue types simply by segmenting
a 3D tissue. To uncover the underlying physical mechanisms driving these geometric
features, we develop two minimal, ordered models using two different underlying
lattices that identify an energetic competition between bulk cell shapes and tissue
interface area. When the interface area dominates, changes to neighbor topology
are costly and occur less frequently, which generates the observed geometric features.
acknowledgement: "We thank Paula Sanematsu, Matthias Merkel, Daniel Sussman, Cristina
Marchetti and Edouard Hannezo for helpful discussions, and M Merkel for developing
and sharing the original version of the 3D Voronoi code. This work was primarily
funded by NSF-PHY-1607416, NSF-PHY-2014192 , and are in the division of physics
at the National Science Foundation. PS and MLM acknowledge additional support from
Simons Grant No. 454947.\r\n"
article_number: '093043'
article_processing_charge: Yes
article_type: original
arxiv: 1
author:
- first_name: Preeti
full_name: Sahu, Preeti
id: 55BA52EE-A185-11EA-88FD-18AD3DDC885E
last_name: Sahu
- first_name: J. M.
full_name: Schwarz, J. M.
last_name: Schwarz
- first_name: M. Lisa
full_name: Manning, M. Lisa
last_name: Manning
citation:
ama: Sahu P, Schwarz JM, Manning ML. Geometric signatures of tissue surface tension
in a three-dimensional model of confluent tissue. New Journal of Physics.
2021;23(9). doi:10.1088/1367-2630/ac23f1
apa: Sahu, P., Schwarz, J. M., & Manning, M. L. (2021). Geometric signatures
of tissue surface tension in a three-dimensional model of confluent tissue. New
Journal of Physics. IOP Publishing. https://doi.org/10.1088/1367-2630/ac23f1
chicago: Sahu, Preeti, J. M. Schwarz, and M. Lisa Manning. “Geometric Signatures
of Tissue Surface Tension in a Three-Dimensional Model of Confluent Tissue.” New
Journal of Physics. IOP Publishing, 2021. https://doi.org/10.1088/1367-2630/ac23f1.
ieee: P. Sahu, J. M. Schwarz, and M. L. Manning, “Geometric signatures of tissue
surface tension in a three-dimensional model of confluent tissue,” New Journal
of Physics, vol. 23, no. 9. IOP Publishing, 2021.
ista: Sahu P, Schwarz JM, Manning ML. 2021. Geometric signatures of tissue surface
tension in a three-dimensional model of confluent tissue. New Journal of Physics.
23(9), 093043.
mla: Sahu, Preeti, et al. “Geometric Signatures of Tissue Surface Tension in a Three-Dimensional
Model of Confluent Tissue.” New Journal of Physics, vol. 23, no. 9, 093043,
IOP Publishing, 2021, doi:10.1088/1367-2630/ac23f1.
short: P. Sahu, J.M. Schwarz, M.L. Manning, New Journal of Physics 23 (2021).
date_created: 2021-10-24T22:01:34Z
date_published: 2021-09-29T00:00:00Z
date_updated: 2023-08-14T08:10:31Z
day: '29'
ddc:
- '570'
department:
- _id: EdHa
doi: 10.1088/1367-2630/ac23f1
external_id:
arxiv:
- '2102.05397'
isi:
- '000702042400001'
file:
- access_level: open_access
checksum: ace603e8f0962b3ba55f23fa34f57764
content_type: application/pdf
creator: cziletti
date_created: 2021-10-28T12:06:01Z
date_updated: 2021-10-28T12:06:01Z
file_id: '10193'
file_name: 2021_NewJPhys_Sahu.pdf
file_size: 2215016
relation: main_file
success: 1
file_date_updated: 2021-10-28T12:06:01Z
has_accepted_license: '1'
intvolume: ' 23'
isi: 1
issue: '9'
language:
- iso: eng
month: '09'
oa: 1
oa_version: Published Version
publication: New Journal of Physics
publication_identifier:
eissn:
- '13672630'
publication_status: published
publisher: IOP Publishing
quality_controlled: '1'
scopus_import: '1'
status: public
title: Geometric signatures of tissue surface tension in a three-dimensional model
of confluent tissue
tmp:
image: /images/cc_by.png
legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
short: CC BY (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 23
year: '2021'
...