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Phased ERK responsiveness and developmental robustness regulate teleost skin morphogenesis.

Publication ,  Journal Article
Ramkumar, N; Richardson, C; O'Brien, M; Butt, FA; Park, J; Chao, AT; Bagnat, M; Poss, KD; Di Talia, S
Published in: Proc Natl Acad Sci U S A
March 11, 2025

Elongation of the vertebrate embryonic axis necessitates rapid expansion of the epidermis to accommodate the growth of underlying tissues. Here, we generated a toolkit to visualize and quantify signaling in entire cell populations of the periderm, the outermost layer of the epidermis, in live developing zebrafish. We find that oriented cell divisions facilitate growth of the early periderm during axial elongation rather than cell addition from the basal layer. Activity levels of Extracellular signal-regulated kinase (ERK), a downstream effector of the MAPK pathway, gauged by a live biosensor, predict cell cycle entry, and optogenetic ERK activation regulates cell cycling dynamics. As development proceeds, rates of peridermal cell proliferation decrease, and ERK activity becomes more pulsatile and functionally transitions to promote hypertrophic cell growth. Targeted genetic blockade of cell division generates animals with oversized periderm cells, yet, unexpectedly, development to adulthood is not impaired. Our findings reveal stage-dependent differential responsiveness to ERK signaling and marked developmental robustness in growing teleost skin.

Duke Scholars

Published In

Proc Natl Acad Sci U S A

DOI

EISSN

1091-6490

Publication Date

March 11, 2025

Volume

122

Issue

10

Start / End Page

e2410430122

Location

United States

Related Subject Headings

  • Zebrafish Proteins
  • Zebrafish
  • Skin
  • Morphogenesis
  • MAP Kinase Signaling System
  • Extracellular Signal-Regulated MAP Kinases
  • Epidermis
  • Cell Proliferation
  • Cell Cycle
  • Animals
 

Citation

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Ramkumar, N., Richardson, C., O’Brien, M., Butt, F. A., Park, J., Chao, A. T., … Di Talia, S. (2025). Phased ERK responsiveness and developmental robustness regulate teleost skin morphogenesis. Proc Natl Acad Sci U S A, 122(10), e2410430122. https://doi.org/10.1073/pnas.2410430122
Ramkumar, Nitya, Christian Richardson, Makinnon O’Brien, Faraz Ahmed Butt, Jieun Park, Anna T. Chao, Michel Bagnat, Kenneth D. Poss, and Stefano Di Talia. “Phased ERK responsiveness and developmental robustness regulate teleost skin morphogenesis.Proc Natl Acad Sci U S A 122, no. 10 (March 11, 2025): e2410430122. https://doi.org/10.1073/pnas.2410430122.
Ramkumar N, Richardson C, O’Brien M, Butt FA, Park J, Chao AT, et al. Phased ERK responsiveness and developmental robustness regulate teleost skin morphogenesis. Proc Natl Acad Sci U S A. 2025 Mar 11;122(10):e2410430122.
Ramkumar, Nitya, et al. “Phased ERK responsiveness and developmental robustness regulate teleost skin morphogenesis.Proc Natl Acad Sci U S A, vol. 122, no. 10, Mar. 2025, p. e2410430122. Pubmed, doi:10.1073/pnas.2410430122.
Ramkumar N, Richardson C, O’Brien M, Butt FA, Park J, Chao AT, Bagnat M, Poss KD, Di Talia S. Phased ERK responsiveness and developmental robustness regulate teleost skin morphogenesis. Proc Natl Acad Sci U S A. 2025 Mar 11;122(10):e2410430122.
Journal cover image

Published In

Proc Natl Acad Sci U S A

DOI

EISSN

1091-6490

Publication Date

March 11, 2025

Volume

122

Issue

10

Start / End Page

e2410430122

Location

United States

Related Subject Headings

  • Zebrafish Proteins
  • Zebrafish
  • Skin
  • Morphogenesis
  • MAP Kinase Signaling System
  • Extracellular Signal-Regulated MAP Kinases
  • Epidermis
  • Cell Proliferation
  • Cell Cycle
  • Animals