Early Stages of Zebrafish Eye Formation Require the Coordinated Activity of Wnt11, Fz5, and the Wnt/beta-catenin Pathway

Overview

Journal Neuron

Publisher Cell Press

Specialty Neurology

Date 2005 Jul 6

PMID 15996547

Citations 96

Authors

Florencia Cavodeassi

Filipa Carreira-Barbosa

Rodrigo M Young

Miguel L Concha

Miguel L Allende

Corinne Houart

Masazumi Tada

Stephen W Wilson

Affiliations

Soon will be listed here.

Abstract

During regional patterning of the anterior neural plate, a medially positioned domain of cells is specified to adopt retinal identity. These eye field cells remain coherent as they undergo morphogenetic events distinct from other prospective forebrain domains. We show that two branches of the Wnt signaling pathway coordinate cell fate determination with cell behavior during eye field formation. Wnt/beta-catenin signaling antagonizes eye specification through the activity of Wnt8b and Fz8a. In contrast, Wnt11 and Fz5 promote eye field development, at least in part, through local antagonism of Wnt/beta-catenin signaling. Additionally, Wnt11 regulates the behavior of eye field cells, promoting their cohesion. Together, these results allow us to postulate a model in which Wnt11 and Fz5 signaling promotes early eye development through the coordinated antagonism of signals that suppress retinal identity and promotion of coherence of eye field cells.

Citing Articles

Homozygosity for a hypomorphic mutation in frizzled class receptor 5 causes syndromic ocular coloboma with microcornea in humans.

Cortes-Gonzalez V, Rodriguez-Morales M, Ataliotis P, Mayer C, Plaisancie J, Chassaing N Hum Genet. 2024; 143(12):1509-1521.

PMID: 39503780 PMC: 11576812. DOI: 10.1007/s00439-024-02712-y.

Maternal regulates zebrafish epiboly through Yap1 activity.

Camacho-Macorra C, Tabanera N, Sanchez-Bustamante E, Bovolenta P, Cardozo M Front Cell Dev Biol. 2024; 12:1362695.

PMID: 38444829 PMC: 10912589. DOI: 10.3389/fcell.2024.1362695.

Dissection of N-deacetylase and N-sulfotransferase activities of NDST1 and their effects on Wnt8 distribution and signaling in Xenopus embryos.

Suzuki M, Takada S, Mii Y Dev Growth Differ. 2024; 66(3):248-255.

PMID: 38326088 PMC: 11457514. DOI: 10.1111/dgd.12915.

Aicardi Syndrome Is a Genetically Heterogeneous Disorder.

Ha T, Burgess R, Newman M, Moey C, Mandelstam S, Gardner A Genes (Basel). 2023; 14(8).

PMID: 37628618 PMC: 10454071. DOI: 10.3390/genes14081565.

The temporal balance between self-renewal and differentiation of human neural stem cells requires the amyloid precursor protein.

Shabani K, Pigeon J, Benaissa Touil Zariouh M, Liu T, Saffarian A, Komatsu J Sci Adv. 2023; 9(24):eadd5002.

PMID: 37327344 PMC: 10275593. DOI: 10.1126/sciadv.add5002.

References

Hammerschmidt M, Kramer C, Nowak M, Herzog W, Wittbrodt J . Loss of maternal Smad5 in zebrafish embryos affects patterning and morphogenesis of optic primordia. Dev Dyn. 2003; 227(1):128-33. DOI: 10.1002/dvdy.10281. View

Momoi A, Yoda H, Steinbeisser H, Fagotto F, Kondoh H, Kudo A . Analysis of Wnt8 for neural posteriorizing factor by identifying Frizzled 8c and Frizzled 9 as functional receptors for Wnt8. Mech Dev. 2003; 120(4):477-89. DOI: 10.1016/s0925-4773(03)00003-0. View

Veeman M, Axelrod J, Moon R . A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev Cell. 2003; 5(3):367-77. DOI: 10.1016/s1534-5807(03)00266-1. View

Moore K, Mood K, Daar I, Moody S . Morphogenetic movements underlying eye field formation require interactions between the FGF and ephrinB1 signaling pathways. Dev Cell. 2004; 6(1):55-67. DOI: 10.1016/s1534-5807(03)00395-2. View

Wilson S, Houart C . Early steps in the development of the forebrain. Dev Cell. 2004; 6(2):167-81. PMC: 2789258. DOI: 10.1016/s1534-5807(04)00027-9. View

He X, Semenov M, Tamai K, Zeng X . LDL receptor-related proteins 5 and 6 in Wnt/beta-catenin signaling: arrows point the way. Development. 2004; 131(8):1663-77. DOI: 10.1242/dev.01117. View

Buckles G, Thorpe C, Ramel M, Lekven A . Combinatorial Wnt control of zebrafish midbrain-hindbrain boundary formation. Mech Dev. 2004; 121(5):437-47. DOI: 10.1016/j.mod.2004.03.026. View

Poliakov A, Cotrina M, Wilkinson D . Diverse roles of eph receptors and ephrins in the regulation of cell migration and tissue assembly. Dev Cell. 2004; 7(4):465-80. DOI: 10.1016/j.devcel.2004.09.006. View

Logan C, Nusse R . The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol. 2004; 20:781-810. DOI: 10.1146/annurev.cellbio.20.010403.113126. View

10.

Moon R, Christian J, Campbell R, McGrew L, DeMarais A, Torres M . Dissecting Wnt signalling pathways and Wnt-sensitive developmental processes through transient misexpression analyses in embryos of Xenopus laevis. Dev Suppl. 1993; :85-94. View

11.

Li Y, Allende M, Finkelstein R, Weinberg E . Expression of two zebrafish orthodenticle-related genes in the embryonic brain. Mech Dev. 1994; 48(3):229-44. DOI: 10.1016/0925-4773(94)90062-0. View

12.

Cui Y, Brown J, Moon R, Christian J . Xwnt-8b: a maternally expressed Xenopus Wnt gene with a potential role in establishing the dorsoventral axis. Development. 1995; 121(7):2177-86. DOI: 10.1242/dev.121.7.2177. View

13.

Woo K, Fraser S . Order and coherence in the fate map of the zebrafish nervous system. Development. 1995; 121(8):2595-609. DOI: 10.1242/dev.121.8.2595. View

14.

Ungar A, Kelly G, Moon R . Wnt4 affects morphogenesis when misexpressed in the zebrafish embryo. Mech Dev. 1995; 52(2-3):153-64. DOI: 10.1016/0925-4773(95)00386-f. View

15.

Xu Q, Alldus G, MacDonald R, Wilkinson D, Holder N . Function of the Eph-related kinase rtk1 in patterning of the zebrafish forebrain. Nature. 1996; 381(6580):319-22. DOI: 10.1038/381319a0. View

16.

Klein P, Melton D . A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci U S A. 1996; 93(16):8455-9. PMC: 38692. DOI: 10.1073/pnas.93.16.8455. View

17.

Hoppler S, Brown J, Moon R . Expression of a dominant-negative Wnt blocks induction of MyoD in Xenopus embryos. Genes Dev. 1996; 10(21):2805-17. DOI: 10.1101/gad.10.21.2805. View

18.

Heisenberg C, Nusslein-Volhard C . The function of silberblick in the positioning of the eye anlage in the zebrafish embryo. Dev Biol. 1997; 184(1):85-94. DOI: 10.1006/dbio.1997.8511. View

19.

Hedgepeth C, Conrad L, Zhang J, Huang H, Lee V, Klein P . Activation of the Wnt signaling pathway: a molecular mechanism for lithium action. Dev Biol. 1997; 185(1):82-91. DOI: 10.1006/dbio.1997.8552. View

20.

Ikeda S, Kishida S, Yamamoto H, Murai H, Koyama S, Kikuchi A . Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3beta and beta-catenin and promotes GSK-3beta-dependent phosphorylation of beta-catenin. EMBO J. 1998; 17(5):1371-84. PMC: 1170485. DOI: 10.1093/emboj/17.5.1371. View