Phase transition specified by a binary code patterns the vertebrate eye cup

Revathi Balasubramanian; Xuanyu Min; Peter M.J. Quinn; Quentin Lo Giudice; Chenqi Tao; Karina Polanco; Neoklis Makrides; John Peregrin; Michael Bouaziz; Yingyu Mao; Qian Wang; Bruna L. da Costa; Diego Buenaventura; Fen Wang; Liang Ma; Stephen H. Tsang; Pierre J. Fabre; Xin Zhang

doi:10.1126/sciadv.abj9846

Phase transition specified by a binary code patterns the vertebrate eye cup

Revathi Balasubramanian, Xuanyu Min, Peter M.J. Quinn, Quentin Lo Giudice, Chenqi Tao, Karina Polanco, Neoklis Makrides, John Peregrin, Michael Bouaziz, Yingyu Mao, Qian Wang, Bruna L. da Costa, Diego Buenaventura, Fen Wang, Liang Ma, Stephen H. Tsang, Pierre J. Fabre, Xin Zhang

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Abstract

The developing vertebrate eye cup is partitioned into the neural retina (NR), the retinal pigmented epithelium (RPE), and the ciliary margin (CM). By single-cell analysis, we showed that fibroblast growth factor (FGF) signaling regulates the CM in its stem cell-like property of self-renewal, differentiation, and survival, which is balanced by an evolutionarily conserved Wnt signaling gradient. FGF promotes Wnt signaling in the CM by stabilizing β-catenin in a GSK3β-independent manner. While Wnt signaling converts the NR to either the CM or the RPE depending on FGF signaling, FGF transforms the RPE to the NR or CM dependent on Wnt activity. The default fate of the eye cup is the NR, but synergistic FGF and Wnt signaling promotes CM formation both in vivo and in human retinal organoid. Our study reveals that the vertebrate eye develops through phase transition determined by a combinatorial code of FGF and Wnt signaling.

Original language	English (US)
Article number	eabj9846
Journal	Science Advances
Volume	7
Issue number	46
DOIs	https://doi.org/10.1126/sciadv.abj9846
State	Published - Nov 2021

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Balasubramanian, R., Min, X., Quinn, P. M. J., Giudice, Q. L., Tao, C., Polanco, K., Makrides, N., Peregrin, J., Bouaziz, M., Mao, Y., Wang, Q., da Costa, B. L., Buenaventura, D., Wang, F., Ma, L., Tsang, S. H., Fabre, P. J., & Zhang, X. (2021). Phase transition specified by a binary code patterns the vertebrate eye cup. Science Advances, 7(46), Article eabj9846. https://doi.org/10.1126/sciadv.abj9846

Balasubramanian, R, Min, X, Quinn, PMJ, Giudice, QL, Tao, C, Polanco, K, Makrides, N, Peregrin, J, Bouaziz, M, Mao, Y, Wang, Q, da Costa, BL, Buenaventura, D, Wang, F, Ma, L, Tsang, SH, Fabre, PJ & Zhang, X 2021, 'Phase transition specified by a binary code patterns the vertebrate eye cup', Science Advances, vol. 7, no. 46, eabj9846. https://doi.org/10.1126/sciadv.abj9846

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abstract = "The developing vertebrate eye cup is partitioned into the neural retina (NR), the retinal pigmented epithelium (RPE), and the ciliary margin (CM). By single-cell analysis, we showed that fibroblast growth factor (FGF) signaling regulates the CM in its stem cell-like property of self-renewal, differentiation, and survival, which is balanced by an evolutionarily conserved Wnt signaling gradient. FGF promotes Wnt signaling in the CM by stabilizing β-catenin in a GSK3β-independent manner. While Wnt signaling converts the NR to either the CM or the RPE depending on FGF signaling, FGF transforms the RPE to the NR or CM dependent on Wnt activity. The default fate of the eye cup is the NR, but synergistic FGF and Wnt signaling promotes CM formation both in vivo and in human retinal organoid. Our study reveals that the vertebrate eye develops through phase transition determined by a combinatorial code of FGF and Wnt signaling.",

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AU - Mao, Yingyu

AU - Wang, Qian

AU - da Costa, Bruna L.

AU - Buenaventura, Diego

AU - Wang, Fen

AU - Ma, Liang

AU - Tsang, Stephen H.

AU - Fabre, Pierre J.

AU - Zhang, Xin

N1 - Publisher Copyright: © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

PY - 2021/11

Y1 - 2021/11

N2 - The developing vertebrate eye cup is partitioned into the neural retina (NR), the retinal pigmented epithelium (RPE), and the ciliary margin (CM). By single-cell analysis, we showed that fibroblast growth factor (FGF) signaling regulates the CM in its stem cell-like property of self-renewal, differentiation, and survival, which is balanced by an evolutionarily conserved Wnt signaling gradient. FGF promotes Wnt signaling in the CM by stabilizing β-catenin in a GSK3β-independent manner. While Wnt signaling converts the NR to either the CM or the RPE depending on FGF signaling, FGF transforms the RPE to the NR or CM dependent on Wnt activity. The default fate of the eye cup is the NR, but synergistic FGF and Wnt signaling promotes CM formation both in vivo and in human retinal organoid. Our study reveals that the vertebrate eye develops through phase transition determined by a combinatorial code of FGF and Wnt signaling.

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Phase transition specified by a binary code patterns the vertebrate eye cup

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