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Unique metabolic regulation of micromeres contributes to gastrulation in the sea urchin embryo

Author

Listed:
  • Shakson Isaac

    (Brown University)

  • Douglas Dubosky

    (Brown University)

  • Ashley Waldron

    (Brown University)

  • Natsuko Emura

    (Brown University)

  • Aidan Furze

    (Brown University)

  • Kavya Rao

    (Brown University)

  • Masaru Mori

    (Keio University
    Nagoya University)

  • Ashok Ragavendran

    (Brown University)

  • Hideki Makinoshima

    (Keio University
    National Cancer Center
    Shonai Regional Industry Promotion Center)

  • Mamiko Yajima

    (Brown University)

Abstract

During development, a group of cells called organizers plays critical roles by sending signals to adjacent cells and controlling embryonic and tissue patterning. Recent studies suggest that these inductive cells facilitate the downstream signaling pathways conserved across organisms. However, what makes these cells fundamentally inductive is little understood. In this study, we demonstrate that the micromeres of the sea urchin, one of the known organizers, have distinct metabolic properties compared to the rest of the embryo. The specific metabolic inhibitors for sugar metabolism (2-DG), fatty acid synthesis (cerulenin), and N-linked glycosylation (tunicamycin) compromise micromeres’ regulatory capacity, altering the downstream germ layer patterning in the resultant embryos. Notably, the endoplasmic reticulum (ER) asymmetrically localizes during asymmetric cell division, resulting in the enrichment of ER and Wnt protein at the vegetal cortex of micromeres. Metabolic inhibition appears to compromise ER activity in Wnt particle distribution. We propose that the micromere ER is sensitive to specific metabolic regulation, contributing to the inductive signaling activity. This study provides a paradigm of how ER and metabolic regulation contribute to the inductive capability of the cells.

Suggested Citation

  • Shakson Isaac & Douglas Dubosky & Ashley Waldron & Natsuko Emura & Aidan Furze & Kavya Rao & Masaru Mori & Ashok Ragavendran & Hideki Makinoshima & Mamiko Yajima, 2025. "Unique metabolic regulation of micromeres contributes to gastrulation in the sea urchin embryo," Nature Communications, Nature, vol. 16(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-62697-8
    DOI: 10.1038/s41467-025-62697-8
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    References listed on IDEAS

    as
    1. Jr-Kai Yu & Yutaka Satou & Nicholas D. Holland & Tadasu Shin-I & Yuji Kohara & Noriyuki Satoh & Marianne Bronner-Fraser & Linda Z. Holland, 2007. "Axial patterning in cephalochordates and the evolution of the organizer," Nature, Nature, vol. 445(7128), pages 613-617, February.
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    3. 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.
    4. Yulia Kraus & Andy Aman & Ulrich Technau & Grigory Genikhovich, 2016. "Pre-bilaterian origin of the blastoporal axial organizer," Nature Communications, Nature, vol. 7(1), pages 1-9, September.
    5. Claire Anderson & Mohsin A. F. Khan & Frances Wong & Tatiana Solovieva & Nidia M. M. Oliveira & Richard A. Baldock & Cheryll Tickle & Dave W. Burt & Claudio D. Stern, 2016. "A strategy to discover new organizers identifies a putative heart organizer," Nature Communications, Nature, vol. 7(1), pages 1-9, November.
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    7. Gregory A. Cary & Brenna S. McCauley & Olga Zueva & Joseph Pattinato & William Longabaugh & Veronica F. Hinman, 2020. "Systematic comparison of sea urchin and sea star developmental gene regulatory networks explains how novelty is incorporated in early development," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
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