Regulation of long-range BMP gradients and embryonic polarity by propagation of local calcium-firing activity

Hyung Chul Lee; Nidia M M Oliveira; Cato Hastings; Peter Baillie-Benson; Adam A Moverley; Hui-Chun Lu; Yi Zheng; Elise L Wilby; Timothy T Weil; Karen M Page; Jianping Fu; Naomi Moris; Claudio D Stern

doi:10.1038/s41467-024-45772-4

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Regulation of long-range BMP gradients and embryonic polarity by propagation of local calcium-firing activity

Journal article

Open access

Peer reviewed

Regulation of long-range BMP gradients and embryonic polarity by propagation of local calcium-firing activity

Hyung Chul Lee, Nidia M M Oliveira, Cato Hastings, Peter Baillie-Benson, Adam A Moverley, Hui-Chun Lu, Yi Zheng, Elise L Wilby, Timothy T Weil, Karen M Page, …

Nature communications, Vol.15(1), 1463

2024

DOI: https://doi.org/10.1038/s41467-024-45772-4

PMID: 38368410

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Abstract

Animals

Bone Morphogenetic Proteins - metabolism

Calcium - metabolism

Chick Embryo

Gastrulation - physiology

Humans

Primitive Streak

Reproduction

Many amniote vertebrate species including humans can form identical twins from a single embryo, but this only occurs rarely. It has been suggested that the primitive-streak-forming embryonic region emits signals that inhibit streak formation elsewhere but the signals involved, how they are transmitted and how they act has not been elucidated. Here we show that short tracks of calcium firing activity propagate through extraembryonic tissue via gap junctions and prevent ectopic primitive streak formation in chick embryos. Cross-regulation of calcium activity and an inhibitor of primitive streak formation (Bone Morphogenetic Protein, BMP) via NF-κB and NFAT establishes a long-range BMP gradient spanning the embryo. This mechanism explains how embryos of widely different sizes can maintain positional information that determines embryo polarity. We provide evidence for similar mechanisms in two different human embryo models and in Drosophila, suggesting an ancient evolutionary origin.

Details

Title: Regulation of long-range BMP gradients and embryonic polarity by propagation of local calcium-firing activity
Authors/Creators: Hyung Chul Lee - University College London
Nidia M M Oliveira - University College London
Cato Hastings - University College London
Peter Baillie-Benson - The Francis Crick Institute
Adam A Moverley - University College London
Hui-Chun Lu - University College London
Yi Zheng - University of Michigan
Elise L Wilby - University of Cambridge
Timothy T Weil - University of Cambridge
Karen M Page - University College London
Jianping Fu - University of Michigan
Naomi Moris - The Francis Crick Institute
Claudio D Stern - University College London
Publication Details: Nature communications, Vol.15(1), 1463
Publisher: Springer Nature
Grant note: CC2186 / Arthritis Research UK CC2186 / Wellcome Trust Wellcome Trust R21 HD100931 / NICHD NIH HHS
Identifiers: 991005638670107891
Murdoch Affiliation: Murdoch University
Language: English
Resource Type: Journal article

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Collaboration types: Domestic collaboration; International collaboration
Citation topics: 1 Clinical & Life Sciences; 1.108 Molecular & Cell Biology - Cancer & Development; 1.108.207 Neural Crest
Web Of Science research areas: Developmental Biology
ESI research areas: Molecular Biology & Genetics