To coordinate cell fate with changes in spatial organization, stem cells (SCs) require specific and adaptable systems of signal exchange and cell-to-cell communication. Pluripotent embryonic stem cells (ESCs) use cytonemes to pair with trophoblast stem cells (TSCs) and form synthetic embryonic structures in a Wnt-dependent manner. How these interactions vary with pluripotency states remains elusive. Here we show that ESC transition to an early primed ESC (pESC) state reduces their pairing with TSCs and impairs synthetic embryogenesis. pESCs can activate the Wnt/β-catenin pathway in response to soluble Wnt ligands, but their cytonemes form unspecific and unstable interactions with localized Wnt sources. This is due to an impaired crosstalk between Wnt and glutamate receptor activity and reduced generation of Ca2+ transients on the cytonemes upon Wnt source contact. Induced iGluR activation can partially restore cytoneme function in pESCs, while transient overexpression of E-cadherin improves pESC–TSC pairing. Our results illustrate how changes in pluripotency state alter the mechanisms SCs use to self-organize.
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February 19 2021
Pluripotency state regulates cytoneme selectivity and self-organization of embryonic stem cells
Sergi Junyent
,
Sergi Junyent
1
Centre for Stem Cells and Regenerative Medicine, King’s College London, London, UK
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Joshua Reeves
,
Joshua Reeves
1
Centre for Stem Cells and Regenerative Medicine, King’s College London, London, UK
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Eileen Gentleman
,
Eileen Gentleman
2
Centre for Craniofacial and Regenerative Biology, King’s College London, London, UK
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Shukry J. Habib
1
Centre for Stem Cells and Regenerative Medicine, King’s College London, London, UK
Correspondence to Shukry J. Habib: shukry.habib@kcl.ac.uk
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Sergi Junyent
1
Centre for Stem Cells and Regenerative Medicine, King’s College London, London, UK
Joshua Reeves
1
Centre for Stem Cells and Regenerative Medicine, King’s College London, London, UK
Eileen Gentleman
2
Centre for Craniofacial and Regenerative Biology, King’s College London, London, UK
Shukry J. Habib
1
Centre for Stem Cells and Regenerative Medicine, King’s College London, London, UK
Correspondence to Shukry J. Habib: shukry.habib@kcl.ac.uk
Received:
May 13 2020
Revision Received:
December 09 2020
Accepted:
January 22 2021
Online Issn: 1540-8140
Print Issn: 0021-9525
© 2021 Habib et al. This article is available under a Creative Commons License (Attribution 4.0 International, as described at https://creativecommons.org/licenses/by/4.0/).
2021
J Cell Biol (2021) 220 (4): e202005095.
Article history
Received:
May 13 2020
Revision Received:
December 09 2020
Accepted:
January 22 2021
Citation
Sergi Junyent, Joshua Reeves, Eileen Gentleman, Shukry J. Habib; Pluripotency state regulates cytoneme selectivity and self-organization of embryonic stem cells. J Cell Biol 5 April 2021; 220 (4): e202005095. doi: https://doi.org/10.1083/jcb.202005095
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