IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-45772-4.html
   My bibliography  Save this article

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

Author

Listed:
  • Hyung Chul Lee

    (University College London
    Chonnam National University)

  • Nidia M. M. Oliveira

    (University College London
    Murdoch University)

  • Cato Hastings

    (University College London)

  • Peter Baillie-Benson

    (The Francis Crick Institute)

  • Adam A. Moverley

    (University College London
    University of Pennsylvania)

  • Hui-Chun Lu

    (University College London
    Centre for Craniofacial & Regenerative Biology, Faculty of Dentistry, Oral and Craniofacial Sciences, King’s College London)

  • Yi Zheng

    (University of Michigan
    Syracuse University
    Syracuse University)

  • 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)

Abstract

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.

Suggested Citation

  • 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 , 2024. "Regulation of long-range BMP gradients and embryonic polarity by propagation of local calcium-firing activity," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45772-4
    DOI: 10.1038/s41467-024-45772-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-45772-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-45772-4?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Ricardo E. Dolmetsch & Richard S. Lewis & Christopher C. Goodnow & James I. Healy, 1997. "Differential activation of transcription factors induced by Ca2+ response amplitude and duration," Nature, Nature, vol. 388(6639), pages 308-308, July.
    2. I. Martyn & T. Y. Kanno & A. Ruzo & E. D. Siggia & A. H. Brivanlou, 2018. "Self-organization of a human organizer by combined Wnt and Nodal signalling," Nature, Nature, vol. 558(7708), pages 132-135, June.
    3. Ricardo E. Dolmetsch & Richard S. Lewis & Christopher C. Goodnow & James I. Healy, 1997. "Differential activation of transcription factors induced by Ca2+ response amplitude and duration," Nature, Nature, vol. 386(6627), pages 855-858, April.
    4. Naomi Moris & Kerim Anlas & Susanne C. van den Brink & Anna Alemany & Julia Schröder & Sabitri Ghimire & Tina Balayo & Alexander van Oudenaarden & Alfonso Martinez Arias, 2020. "An in vitro model of early anteroposterior organization during human development," Nature, Nature, vol. 582(7812), pages 410-415, June.
    5. Tsai-Wen Chen & Trevor J. Wardill & Yi Sun & Stefan R. Pulver & Sabine L. Renninger & Amy Baohan & Eric R. Schreiter & Rex A. Kerr & Michael B. Orger & Vivek Jayaraman & Loren L. Looger & Karel Svobod, 2013. "Ultrasensitive fluorescent proteins for imaging neuronal activity," Nature, Nature, vol. 499(7458), pages 295-300, July.
    6. Yi Zheng & Xufeng Xue & Yue Shao & Sicong Wang & Sajedeh Nasr Esfahani & Zida Li & Jonathon M. Muncie & Johnathon N. Lakins & Valerie M. Weaver & Deborah L. Gumucio & Jianping Fu, 2019. "Controlled modelling of human epiblast and amnion development using stem cells," Nature, Nature, vol. 573(7774), pages 421-425, September.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Jason W Locasale & Arup K Chakraborty, 2008. "Regulation of Signal Duration and the Statistical Dynamics of Kinase Activation by Scaffold Proteins," PLOS Computational Biology, Public Library of Science, vol. 4(6), pages 1-12, June.
    2. Anchel de Jaime-Soguero & Janina Hattemer & Anja Bufe & Alexander Haas & Jeroen Berg & Vincent Batenburg & Biswajit Das & Barbara Marco & Stefania Androulaki & Nicolas Böhly & Jonathan J. M. Landry & , 2024. "Developmental signals control chromosome segregation fidelity during pluripotency and neurogenesis by modulating replicative stress," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    3. Andreja Jovic & Bryan Howell & Michelle Cote & Susan M Wade & Khamir Mehta & Atsushi Miyawaki & Richard R Neubig & Jennifer J Linderman & Shuichi Takayama, 2010. "Phase-Locked Signals Elucidate Circuit Architecture of an Oscillatory Pathway," PLOS Computational Biology, Public Library of Science, vol. 6(12), pages 1-8, December.
    4. Agne Tilūnaitė & Wayne Croft & Noah Russell & Tomas C Bellamy & Rüdiger Thul, 2017. "A Bayesian approach to modelling heterogeneous calcium responses in cell populations," PLOS Computational Biology, Public Library of Science, vol. 13(10), pages 1-25, October.
    5. Manasi Iyer & Husniye Kantarci & Madeline H. Cooper & Nicholas Ambiel & Sammy Weiser Novak & Leonardo R. Andrade & Mable Lam & Graham Jones & Alexandra E. Münch & Xinzhu Yu & Baljit S. Khakh & Uri Man, 2024. "Oligodendrocyte calcium signaling promotes actin-dependent myelin sheath extension," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    6. Aniruddha Das & Sarah Holden & Julie Borovicka & Jacob Icardi & Abigail O’Niel & Ariel Chaklai & Davina Patel & Rushik Patel & Stefanie Kaech Petrie & Jacob Raber & Hod Dana, 2023. "Large-scale recording of neuronal activity in freely-moving mice at cellular resolution," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    7. Haipeng Fu & Tingyu Wang & Xiaohui Kong & Kun Yan & Yang Yang & Jingyi Cao & Yafei Yuan & Nan Wang & Kehkooi Kee & Zhi John Lu & Qiaoran Xi, 2022. "A Nodal enhanced micropeptide NEMEP regulates glucose uptake during mesendoderm differentiation of embryonic stem cells," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    8. Luke Simpson & Andrew Strange & Doris Klisch & Sophie Kraunsoe & Takuya Azami & Daniel Goszczynski & Triet Minh & Benjamin Planells & Nadine Holmes & Fei Sang & Sonal Henson & Matthew Loose & Jennifer, 2024. "A single-cell atlas of pig gastrulation as a resource for comparative embryology," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    9. Johannes Friedrich & Pengcheng Zhou & Liam Paninski, 2017. "Fast online deconvolution of calcium imaging data," PLOS Computational Biology, Public Library of Science, vol. 13(3), pages 1-26, March.
    10. Jen-Chun Hsiang & Ning Shen & Florentina Soto & Daniel Kerschensteiner, 2024. "Distributed feature representations of natural stimuli across parallel retinal pathways," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    11. Sajedeh Nasr Esfahani & Yi Zheng & Auriana Arabpour & Agnes M. Resto Irizarry & Norio Kobayashi & Xufeng Xue & Yue Shao & Cheng Zhao & Nicole L. Agranonik & Megan Sparrow & Timothy J. Hunt & Jared Fai, 2024. "Derivation of human primordial germ cell-like cells in an embryonic-like culture," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    12. Norio Kobayashi & Hiroaki Okae & Hitoshi Hiura & Naoto Kubota & Eri H. Kobayashi & Shun Shibata & Akira Oike & Takeshi Hori & Chie Kikutake & Hirotaka Hamada & Hirokazu Kaji & Mikita Suyama & Marie-Li, 2022. "The microRNA cluster C19MC confers differentiation potential into trophoblast lineages upon human pluripotent stem cells," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    13. Omer Mano & Damon A Clark, 2017. "Graphics Processing Unit-Accelerated Code for Computing Second-Order Wiener Kernels and Spike-Triggered Covariance," PLOS ONE, Public Library of Science, vol. 12(1), pages 1-11, January.
    14. Xinyu Hu & Bob van Sluijs & Óscar García-Blay & Yury Stepanov & Koen Rietrae & Wilhelm T. S. Huck & Maike M. K. Hansen, 2024. "ARTseq-FISH reveals position-dependent differences in gene expression of micropatterned mESCs," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    15. Cassie L. Kemmler & Jana Smolikova & Hannah R. Moran & Brandon J. Mannion & Dunja Knapp & Fabian Lim & Anna Czarkwiani & Viviana Hermosilla Aguayo & Vincent Rapp & Olivia E. Fitch & Seraina Bötschi & , 2023. "Conserved enhancers control notochord expression of vertebrate Brachyury," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    16. Seth Teague & Gillian Primavera & Bohan Chen & Zong-Yuan Liu & LiAng Yao & Emily Freeburne & Hina Khan & Kyoung Jo & Craig Johnson & Idse Heemskerk, 2024. "Time-integrated BMP signaling determines fate in a stem cell model for early human development," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    17. Feng Lin & Xia Li & Shiyu Sun & Zhongyi Li & Chenglin Lv & Jianbo Bai & Lin Song & Yizhao Han & Bo Li & Jianping Fu & Yue Shao, 2023. "Mechanically enhanced biogenesis of gut spheroids with instability-driven morphomechanics," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    18. Che-Hang Yu & Jeffrey N. Stirman & Yiyi Yu & Riichiro Hira & Spencer L. Smith, 2021. "Diesel2p mesoscope with dual independent scan engines for flexible capture of dynamics in distributed neural circuitry," Nature Communications, Nature, vol. 12(1), pages 1-8, December.
    19. Zengpeng Han & Nengsong Luo & Wenyu Ma & Xiaodong Liu & Yuxiang Cai & Jiaxin Kou & Jie Wang & Lei Li & Siqi Peng & Zihong Xu & Wen Zhang & Yuxiang Qiu & Yang Wu & Chaohui Ye & Kunzhang Lin & Fuqiang X, 2023. "AAV11 enables efficient retrograde targeting of projection neurons and enhances astrocyte-directed transduction," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    20. Daniele Kunz & Anfu Wang & Chon U Chan & Robyn H. Pritchard & Wenyu Wang & Filomena Gallo & Charles R. Bradshaw & Elisa Terenzani & Karin H. Müller & Yan Yan Shery Huang & Fengzhu Xiong, 2023. "Downregulation of extraembryonic tension controls body axis formation in avian embryos," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45772-4. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.