Literature DB >> 21653614

Neuroblast migration along the anteroposterior axis of C. elegans is controlled by opposing gradients of Wnts and a secreted Frizzled-related protein.

Martin Harterink1, Dong Hyun Kim, Teije C Middelkoop, Thang Dinh Doan, Alexander van Oudenaarden, Hendrik C Korswagen.   

Abstract

The migration of neuroblasts along the anteroposterior body axis of C. elegans is controlled by multiple Wnts that act partially redundantly to guide cells to their precisely defined final destinations. How positional information is specified by this system is, however, still largely unknown. Here, we used a novel fluorescent in situ hybridization methods to generate a quantitative spatiotemporal expression map of the C. elegans Wnt genes. We found that the five Wnt genes are expressed in a series of partially overlapping domains along the anteroposterior axis, with a predominant expression in the posterior half of the body. Furthermore, we show that a secreted Frizzled-related protein is expressed at the anterior end of the body axis, where it inhibits Wnt signaling to control neuroblast migration. Our findings reveal that a system of regionalized Wnt gene expression and anterior Wnt inhibition guides the highly stereotypic migration of neuroblasts in C. elegans. Opposing expression of Wnts and Wnt inhibitors has been observed in basal metazoans and in the vertebrate neurectoderm. Our results in C. elegans support the notion that a system of posterior Wnt signaling and anterior Wnt inhibition is an evolutionarily conserved principle of primary body axis specification.

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Year:  2011        PMID: 21653614      PMCID: PMC3119304          DOI: 10.1242/dev.064733

Source DB:  PubMed          Journal:  Development        ISSN: 0950-1991            Impact factor:   6.868


  54 in total

Review 1.  A WNT of things to come: evolution of Wnt signaling and polarity in cnidarians.

Authors:  Patricia N Lee; Kevin Pang; David Q Matus; Mark Q Martindale
Journal:  Semin Cell Dev Biol       Date:  2006-05-07       Impact factor: 7.727

2.  Wnt gradient formation requires retromer function in Wnt-producing cells.

Authors:  Damien Y M Coudreuse; Giulietta Roël; Marco C Betist; Olivier Destrée; Hendrik C Korswagen
Journal:  Science       Date:  2006-04-27       Impact factor: 47.728

Review 3.  The Wnt code: cnidarians signal the way.

Authors:  C Guder; I Philipp; T Lengfeld; H Watanabe; B Hobmayer; T W Holstein
Journal:  Oncogene       Date:  2006-12-04       Impact factor: 9.867

4.  Smed-betacatenin-1 is required for anteroposterior blastema polarity in planarian regeneration.

Authors:  Christian P Petersen; Peter W Reddien
Journal:  Science       Date:  2007-12-06       Impact factor: 47.728

Review 5.  Beyond Wnt inhibition: new functions of secreted Frizzled-related proteins in development and disease.

Authors:  Paola Bovolenta; Pilar Esteve; Jose Maria Ruiz; Elsa Cisneros; Javier Lopez-Rios
Journal:  J Cell Sci       Date:  2008-03-15       Impact factor: 5.285

6.  Wnt signaling requires retromer-dependent recycling of MIG-14/Wntless in Wnt-producing cells.

Authors:  Pei-Tzu Yang; Magdalena J Lorenowicz; Marie Silhankova; Damien Y M Coudreuse; Marco C Betist; Hendrik C Korswagen
Journal:  Dev Cell       Date:  2007-12-20       Impact factor: 12.270

7.  Multiple redundant Wnt signaling components function in two processes during C. elegans vulval development.

Authors:  Julie E Gleason; Elizabeth A Szyleyko; David M Eisenmann
Journal:  Dev Biol       Date:  2006-07-07       Impact factor: 3.582

Review 8.  Function and biological roles of the Dickkopf family of Wnt modulators.

Authors:  C Niehrs
Journal:  Oncogene       Date:  2006-12-04       Impact factor: 9.867

9.  Wnt signaling positions neuromuscular connectivity by inhibiting synapse formation in C. elegans.

Authors:  Matthew P Klassen; Kang Shen
Journal:  Cell       Date:  2007-08-24       Impact factor: 41.582

Review 10.  Migration of neuronal cells along the anterior-posterior body axis of C. elegans: Wnts are in control.

Authors:  Marie Silhankova; Hendrik C Korswagen
Journal:  Curr Opin Genet Dev       Date:  2007-07-20       Impact factor: 5.578

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  45 in total

1.  Dishevelled attenuates the repelling activity of Wnt signaling during neurite outgrowth in Caenorhabditis elegans.

Authors:  Chaogu Zheng; Margarete Diaz-Cuadros; Martin Chalfie
Journal:  Proc Natl Acad Sci U S A       Date:  2015-10-12       Impact factor: 11.205

Review 2.  Wnt Signaling Polarizes C. elegans Asymmetric Cell Divisions During Development.

Authors:  Arielle Koonyee Lam; Bryan T Phillips
Journal:  Results Probl Cell Differ       Date:  2017

3.  Regulation of maternal Wnt mRNA translation in C. elegans embryos.

Authors:  Marieke Oldenbroek; Scott M Robertson; Tugba Guven-Ozkan; Caroline Spike; David Greenstein; Rueyling Lin
Journal:  Development       Date:  2013-10-16       Impact factor: 6.868

4.  The fat-like cadherin CDH-4 acts cell-non-autonomously in anterior-posterior neuroblast migration.

Authors:  Lakshmi Sundararajan; Megan L Norris; Sebastian Schöneich; Brian D Ackley; Erik A Lundquist
Journal:  Dev Biol       Date:  2014-06-19       Impact factor: 3.582

5.  The conserved transmembrane RING finger protein PLR-1 downregulates Wnt signaling by reducing Frizzled, Ror and Ryk cell-surface levels in C. elegans.

Authors:  Laura L Moffat; Ryan E Robinson; Anastasia Bakoulis; Scott G Clark
Journal:  Development       Date:  2014-01-08       Impact factor: 6.868

6.  Reciprocal signaling by Wnt and Notch specifies a muscle precursor in the C. elegans embryo.

Authors:  Scott M Robertson; Jessica Medina; Marieke Oldenbroek; Rueyling Lin
Journal:  Development       Date:  2017-01-03       Impact factor: 6.868

7.  RPM-1 and DLK-1 regulate pioneer axon outgrowth by controlling Wnt signaling.

Authors:  Eun Chan Park; Christopher Rongo
Journal:  Development       Date:  2018-09-21       Impact factor: 6.868

8.  Transmembrane proteins UNC-40/DCC, PTP-3/LAR, and MIG-21 control anterior-posterior neuroblast migration with left-right functional asymmetry in Caenorhabditis elegans.

Authors:  Lakshmi Sundararajan; Erik A Lundquist
Journal:  Genetics       Date:  2012-10-10       Impact factor: 4.562

9.  A lineage-resolved molecular atlas of C. elegans embryogenesis at single-cell resolution.

Authors:  Jonathan S Packer; Qin Zhu; Chau Huynh; Priya Sivaramakrishnan; Elicia Preston; Hannah Dueck; Derek Stefanik; Kai Tan; Cole Trapnell; Junhyong Kim; Robert H Waterston; John I Murray
Journal:  Science       Date:  2019-09-05       Impact factor: 47.728

Review 10.  Wnt-signaling and planar cell polarity genes regulate axon guidance along the anteroposterior axis in C. elegans.

Authors:  Brian D Ackley
Journal:  Dev Neurobiol       Date:  2013-12-31       Impact factor: 3.964

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