Wnt Signaling Regulates Postembryonic Hypothalamic Progenitor Differentiation

Overview

Journal Dev Cell

Publisher Cell Press

Specialties Cell Biology
Reproductive Medicine

Date 2012 Sep 15

PMID 22975330

Citations 52

Authors

Xu Wang

Daniel Kopinke

Junji Lin

Adam D McPherson

Robert N Duncan

Hideo Otsuna

Enrico Moro

Kazuyuki Hoshijima

David J Grunwald

Francesco Argenton

Chi-Bin Chien

L Charles Murtaugh

Richard I Dorsky

Affiliations

Soon will be listed here.

Abstract

Previous studies have raised the possibility that Wnt signaling may regulate both neural progenitor maintenance and neuronal differentiation within a single population. Here we investigate the role of Wnt/β-catenin activity in the zebrafish hypothalamus and find that the pathway is first required for the proliferation of unspecified hypothalamic progenitors in the embryo. At later stages, including adulthood, sequential activation and inhibition of Wnt activity is required for the differentiation of neural progenitors and negatively regulates radial glia differentiation. The presence of Wnt activity is conserved in hypothalamic progenitors of the adult mouse, where it plays a conserved role in inhibiting the differentiation of radial glia. This study establishes the vertebrate hypothalamus as a model for Wnt-regulated postembryonic neural progenitor differentiation and defines specific roles for Wnt signaling in neurogenesis.

Citing Articles

Bio-characteristics, tissue expression of miR-375 in hypothalamic-pituitary-ovarian axis and its regulation in reproduction-related diseases.

Sun S, Zhang B, Jia W, Yang J, Wang S, Zhao L Sci Rep. 2024; 14(1):27353.

PMID: 39521862 PMC: 11550468. DOI: 10.1038/s41598-024-79062-2.

Exploring the dynamics of adult cell lineage integration into dentate gyrus granule neurons.

Sharifi K, Farzad F, Soldozy S, DeWitt M, Price R, Sheehan J Front Neurosci. 2024; 18:1353142.

PMID: 38449734 PMC: 10915230. DOI: 10.3389/fnins.2024.1353142.

Social withdrawal and anxiety-like behavior have an impact on zebrafish adult neurogenesis.

Perdikaris P, Prouska P, Dermon C Front Behav Neurosci. 2023; 17:1244075.

PMID: 37908201 PMC: 10614005. DOI: 10.3389/fnbeh.2023.1244075.

β-Catenin and SOX2 Interaction Regulate Visual Experience-Dependent Cell Homeostasis in the Developing Thalamus.

Gao J, Lu Y, Luo Y, Duan X, Chen P, Zhang X Int J Mol Sci. 2023; 24(17).

PMID: 37686400 PMC: 10488257. DOI: 10.3390/ijms241713593.

A Critical Review of Zebrafish Neurological Disease Models-2. Application: Functional and Neuroanatomical Phenotyping Strategies and Chemical Screens.

Burton E, Burgess H Oxf Open Neurosci. 2023; 2.

PMID: 37637775 PMC: 10455049. DOI: 10.1093/oons/kvac019.

References

Dorsky R, Sheldahl L, Moon R . A transgenic Lef1/beta-catenin-dependent reporter is expressed in spatially restricted domains throughout zebrafish development. Dev Biol. 2002; 241(2):229-37. DOI: 10.1006/dbio.2001.0515. View

Yuan T, Arias-Carrion O . Adult neurogenesis in the hypothalamus: evidence, functions, and implications. CNS Neurol Disord Drug Targets. 2011; 10(4):433-9. DOI: 10.2174/187152711795563985. View

Maretto S, Cordenonsi M, Dupont S, Braghetta P, Broccoli V, Hassan A . Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc Natl Acad Sci U S A. 2003; 100(6):3299-304. PMC: 152286. DOI: 10.1073/pnas.0434590100. View

Pierce A, Xu A . De novo neurogenesis in adult hypothalamus as a compensatory mechanism to regulate energy balance. J Neurosci. 2010; 30(2):723-30. PMC: 3080014. DOI: 10.1523/JNEUROSCI.2479-09.2010. View

Lee J, Wu S, Goering L, Dorsky R . Canonical Wnt signaling through Lef1 is required for hypothalamic neurogenesis. Development. 2006; 133(22):4451-61. DOI: 10.1242/dev.02613. View

Muncan V, Faro A, Haramis A, Hurlstone A, Wienholds E, van Es J . T-cell factor 4 (Tcf7l2) maintains proliferative compartments in zebrafish intestine. EMBO Rep. 2007; 8(10):966-73. PMC: 2002560. DOI: 10.1038/sj.embor.7401071. View

Tang M, Villaescusa J, Luo S, Guitarte C, Lei S, Miyamoto Y . Interactions of Wnt/beta-catenin signaling and sonic hedgehog regulate the neurogenesis of ventral midbrain dopamine neurons. J Neurosci. 2010; 30(27):9280-91. PMC: 3578394. DOI: 10.1523/JNEUROSCI.0860-10.2010. View

Stoick-Cooper C, Weidinger G, Riehle K, Hubbert C, Major M, Fausto N . Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development. 2006; 134(3):479-89. DOI: 10.1242/dev.001123. View

Ming G, Song H . Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron. 2011; 70(4):687-702. PMC: 3106107. DOI: 10.1016/j.neuron.2011.05.001. View

10.

Megason S, McMahon A . A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development. 2002; 129(9):2087-98. DOI: 10.1242/dev.129.9.2087. View

11.

Grupp L, Wolburg H, Mack A . Astroglial structures in the zebrafish brain. J Comp Neurol. 2010; 518(21):4277-87. DOI: 10.1002/cne.22481. View

12.

Srinivas S, Watanabe T, Lin C, WILLIAM C, Tanabe Y, Jessell T . Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol. 2001; 1:4. PMC: 31338. DOI: 10.1186/1471-213x-1-4. View

13.

Kizil C, Kaslin J, Kroehne V, Brand M . Adult neurogenesis and brain regeneration in zebrafish. Dev Neurobiol. 2011; 72(3):429-61. DOI: 10.1002/dneu.20918. View

14.

Galceran J, Devaney E, Rubenstein J, Grosschedl R . Hippocampus development and generation of dentate gyrus granule cells is regulated by LEF1. Development. 2000; 127(3):469-82. DOI: 10.1242/dev.127.3.469. View

15.

Yee C, Wang Y, Anderson S, Ekker M, Rubenstein J . Arcuate nucleus expression of NKX2.1 and DLX and lineages expressing these transcription factors in neuropeptide Y(+), proopiomelanocortin(+), and tyrosine hydroxylase(+) neurons in neonatal and adult mice. J Comp Neurol. 2009; 517(1):37-50. PMC: 3021751. DOI: 10.1002/cne.22132. View

16.

Moro E, Ozhan-Kizil G, Mongera A, Beis D, Wierzbicki C, Young R . In vivo Wnt signaling tracing through a transgenic biosensor fish reveals novel activity domains. Dev Biol. 2012; 366(2):327-40. DOI: 10.1016/j.ydbio.2012.03.023. View

17.

Maeder M, Thibodeau-Beganny S, Sander J, Voytas D, Joung J . Oligomerized pool engineering (OPEN): an 'open-source' protocol for making customized zinc-finger arrays. Nat Protoc. 2009; 4(10):1471-501. PMC: 2858690. DOI: 10.1038/nprot.2009.98. View

18.

Zhou C, Zhao C, Pleasure S . Wnt signaling mutants have decreased dentate granule cell production and radial glial scaffolding abnormalities. J Neurosci. 2004; 24(1):121-6. PMC: 6729560. DOI: 10.1523/JNEUROSCI.4071-03.2004. View

19.

McGraw H, Drerup C, Culbertson M, Linbo T, Raible D, Nechiporuk A . Lef1 is required for progenitor cell identity in the zebrafish lateral line primordium. Development. 2011; 138(18):3921-30. PMC: 3160089. DOI: 10.1242/dev.062554. View

20.

Lee S, Tole S, Grove E, McMahon A . A local Wnt-3a signal is required for development of the mammalian hippocampus. Development. 2000; 127(3):457-67. DOI: 10.1242/dev.127.3.457. View