IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-023-44522-2.html
   My bibliography  Save this article

Embryos assist morphogenesis of others through calcium and ATP signaling mechanisms in collective teratogen resistance

Author

Listed:
  • Angela Tung

    (Allen Discovery Center at Tufts University)

  • Megan M. Sperry

    (Allen Discovery Center at Tufts University
    Wyss Institute for Biologically Inspired Engineering, Harvard University)

  • Wesley Clawson

    (Allen Discovery Center at Tufts University)

  • Ananya Pavuluri

    (Allen Discovery Center at Tufts University)

  • Sydney Bulatao

    (Allen Discovery Center at Tufts University)

  • Michelle Yue

    (Wyss Institute for Biologically Inspired Engineering, Harvard University)

  • Ramses Martinez Flores

    (Wyss Institute for Biologically Inspired Engineering, Harvard University)

  • Vaibhav P. Pai

    (Allen Discovery Center at Tufts University)

  • Patrick McMillen

    (Allen Discovery Center at Tufts University)

  • Franz Kuchling

    (Allen Discovery Center at Tufts University)

  • Michael Levin

    (Allen Discovery Center at Tufts University
    Wyss Institute for Biologically Inspired Engineering, Harvard University)

Abstract

Information for organismal patterning can come from a variety of sources. We investigate the possibility that instructive influences for normal embryonic development are provided not only at the level of cells within the embryo, but also via interactions between embryos. To explore this, we challenge groups of embryos with disruptors of normal development while varying group size. Here, we show that Xenopus laevis embryos are much more sensitive to a diverse set of chemical and molecular-biological perturbations when allowed to develop alone or in small groups, than in large groups. Keeping per-embryo exposure constant, we find that increasing the number of exposed embryos in a cohort increases the rate of survival while incidence of defects decreases. This inter-embryo assistance effect is mediated by short-range diffusible signals and involves the P2 ATP receptor. Our data and computational model emphasize that morphogenesis is a collective phenomenon not only at the level of cells, but also of whole bodies, and that cohort size is a crucial variable in studies of ecotoxicology, teratogenesis, and developmental plasticity.

Suggested Citation

  • Angela Tung & Megan M. Sperry & Wesley Clawson & Ananya Pavuluri & Sydney Bulatao & Michelle Yue & Ramses Martinez Flores & Vaibhav P. Pai & Patrick McMillen & Franz Kuchling & Michael Levin, 2024. "Embryos assist morphogenesis of others through calcium and ATP signaling mechanisms in collective teratogen resistance," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44522-2
    DOI: 10.1038/s41467-023-44522-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-44522-2
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-44522-2?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. Zohar Erez & Ida Steinberger-Levy & Maya Shamir & Shany Doron & Avigail Stokar-Avihail & Yoav Peleg & Sarah Melamed & Azita Leavitt & Alon Savidor & Shira Albeck & Gil Amitai & Rotem Sorek, 2017. "Communication between viruses guides lysis–lysogeny decisions," Nature, Nature, vol. 541(7638), pages 488-493, January.
    2. Karine Massé & Surinder Bhamra & Robert Eason & Nicholas Dale & Elizabeth A. Jones, 2007. "Purine-mediated signalling triggers eye development," Nature, Nature, vol. 449(7165), pages 1058-1062, October.
    3. Jeffrey T Leek & John D Storey, 2007. "Capturing Heterogeneity in Gene Expression Studies by Surrogate Variable Analysis," PLOS Genetics, Public Library of Science, vol. 3(9), pages 1-12, September.
    4. Peng He & Brian A. Williams & Diane Trout & Georgi K. Marinov & Henry Amrhein & Libera Berghella & Say-Tar Goh & Ingrid Plajzer-Frick & Veena Afzal & Len A. Pennacchio & Diane E. Dickel & Axel Visel &, 2020. "The changing mouse embryo transcriptome at whole tissue and single-cell resolution," Nature, Nature, vol. 583(7818), pages 760-767, July.
    5. Giacomo Cavalli & Edith Heard, 2019. "Advances in epigenetics link genetics to the environment and disease," Nature, Nature, vol. 571(7766), pages 489-499, July.
    6. Vaibhav P. Pai & Alexis Pietak & Valerie Willocq & Bin Ye & Nian-Qing Shi & Michael Levin, 2018. "HCN2 Rescues brain defects by enforcing endogenous voltage pre-patterns," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    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. Qiang Zhang & Sai Ma & Zhengzhi Liu & Bohan Zhu & Zirui Zhou & Gaoshan Li & J. Javier Meana & Javier González-Maeso & Chang Lu, 2023. "Droplet-based bisulfite sequencing for high-throughput profiling of single-cell DNA methylomes," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    2. repec:jss:jstsof:40:i14 is not listed on IDEAS
    3. Xiaoyan Wei & Angelos Rigopoulos & Matthias Lienhard & Sophie Pöhle-Kronawitter & Georgios Kotsaris & Julia Franke & Nikolaus Berndt & Joy Orezimena Mejedo & Hao Wu & Stefan Börno & Bernd Timmermann &, 2024. "Neurofibromin 1 controls metabolic balance and Notch-dependent quiescence of murine juvenile myogenic progenitors," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    4. Emanuele Aliverti & Kristian Lum & James E. Johndrow & David B. Dunson, 2021. "Removing the influence of group variables in high‐dimensional predictive modelling," Journal of the Royal Statistical Society Series A, Royal Statistical Society, vol. 184(3), pages 791-811, July.
    5. Seungchul Baek & Yen‐Yi Ho & Yanyuan Ma, 2020. "Using sufficient direction factor model to analyze latent activities associated with breast cancer survival," Biometrics, The International Biometric Society, vol. 76(4), pages 1340-1350, December.
    6. Griffin, Maryclare & Hoff, Peter D., 2019. "Lasso ANOVA decompositions for matrix and tensor data," Computational Statistics & Data Analysis, Elsevier, vol. 137(C), pages 181-194.
    7. Léa Maitre & Mariona Bustamante & Carles Hernández-Ferrer & Denise Thiel & Chung-Ho E. Lau & Alexandros P. Siskos & Marta Vives-Usano & Carlos Ruiz-Arenas & Dolors Pelegrí-Sisó & Oliver Robinson & Dan, 2022. "Multi-omics signatures of the human early life exposome," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    8. Chee Ho H’ng & Shanika L. Amarasinghe & Boya Zhang & Hojin Chang & Xinli Qu & David R. Powell & Alberto Rosello-Diez, 2024. "Compensatory growth and recovery of cartilage cytoarchitecture after transient cell death in fetal mouse limbs," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    9. Mark Reimers, 2010. "Making Informed Choices about Microarray Data Analysis," PLOS Computational Biology, Public Library of Science, vol. 6(5), pages 1-7, May.
    10. Leek Jeffrey T & Storey John D., 2011. "The Joint Null Criterion for Multiple Hypothesis Tests," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 10(1), pages 1-22, June.
    11. Nicoló Fusi & Oliver Stegle & Neil D Lawrence, 2012. "Joint Modelling of Confounding Factors and Prominent Genetic Regulators Provides Increased Accuracy in Genetical Genomics Studies," PLOS Computational Biology, Public Library of Science, vol. 8(1), pages 1-9, January.
    12. Suzanne Mavoa & Daniel Keevers & Stefan C. Kane & Melissa Wake & Rachel Tham & Kate Lycett & Yen Ting Wong & Katherine Chong, 2021. "Parental Preconception Exposures to Outdoor Neighbourhood Environments and Adverse Birth Outcomes: A Protocol for a Scoping Review and Evidence Map," IJERPH, MDPI, vol. 18(17), pages 1-10, August.
    13. Rachel K. Lex & Weiqiang Zhou & Zhicheng Ji & Kristin N. Falkenstein & Kaleigh E. Schuler & Kathryn E. Windsor & Joseph D. Kim & Hongkai Ji & Steven A. Vokes, 2022. "GLI transcriptional repression is inert prior to Hedgehog pathway activation," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    14. Yuto Hasegawa & Juhyun Kim & Gianluca Ursini & Yan Jouroukhin & Xiaolei Zhu & Yu Miyahara & Feiyi Xiong & Samskruthi Madireddy & Mizuho Obayashi & Beat Lutz & Akira Sawa & Solange P. Brown & Mikhail V, 2023. "Microglial cannabinoid receptor type 1 mediates social memory deficits in mice produced by adolescent THC exposure and 16p11.2 duplication," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    15. Martin Arostegui & R. Wilder Scott & Kerstin Böse & T. Michael Underhill, 2022. "Cellular taxonomy of Hic1+ mesenchymal progenitor derivatives in the limb: from embryo to adult," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    16. Sudhir Varma, 2020. "Blind estimation and correction of microarray batch effect," PLOS ONE, Public Library of Science, vol. 15(4), pages 1-15, April.
    17. Friguet, Chloé & Causeur, David, 2011. "Estimation of the proportion of true null hypotheses in high-dimensional data under dependence," Computational Statistics & Data Analysis, Elsevier, vol. 55(9), pages 2665-2676, September.
    18. Xuemeng Zhou & Tsz Wing Sam & Ah Young Lee & Danny Leung, 2021. "Mouse strain-specific polymorphic provirus functions as cis-regulatory element leading to epigenomic and transcriptomic variations," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    19. Michael W Nagle & Jeanne C Latourelle & Adam Labadorf & Alexandra Dumitriu & Tiffany C Hadzi & Thomas G Beach & Richard H Myers, 2016. "The 4p16.3 Parkinson Disease Risk Locus Is Associated with GAK Expression and Genes Involved with the Synaptic Vesicle Membrane," PLOS ONE, Public Library of Science, vol. 11(8), pages 1-14, August.
    20. Mattia Zaghi & Federica Banfi & Luca Massimino & Monica Volpin & Edoardo Bellini & Simone Brusco & Ivan Merelli & Cristiana Barone & Michela Bruni & Linda Bossini & Luigi Antonio Lamparelli & Laura Pi, 2023. "Balanced SET levels favor the correct enhancer repertoire during cell fate acquisition," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    21. Oliver Stegle & Leopold Parts & Richard Durbin & John Winn, 2010. "A Bayesian Framework to Account for Complex Non-Genetic Factors in Gene Expression Levels Greatly Increases Power in eQTL Studies," PLOS Computational Biology, Public Library of Science, vol. 6(5), pages 1-11, May.

    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_s41467-023-44522-2. 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.