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

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,...

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Main Authors: Harterink, Martin, Middelkoop, Teije C., Doan, Thang Dinh, van Oudenaarden, Alexander, Korswagen, Hendrik C., Kim, Don H., 1972-
Other Authors: Massachusetts Institute of Technology. Department of Physics
Format: Article
Language:en_US
Published: Company of Biologists 2019
Online Access:https://hdl.handle.net/1721.1/121171
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author Harterink, Martin
Middelkoop, Teije C.
Doan, Thang Dinh
van Oudenaarden, Alexander
Korswagen, Hendrik C.
Kim, Don H., 1972-
author2 Massachusetts Institute of Technology. Department of Physics
author_facet Massachusetts Institute of Technology. Department of Physics
Harterink, Martin
Middelkoop, Teije C.
Doan, Thang Dinh
van Oudenaarden, Alexander
Korswagen, Hendrik C.
Kim, Don H., 1972-
author_sort Harterink, Martin
collection MIT
description 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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spelling mit-1721.1/1211712022-09-26T16:13:12Z Neuroblast migration along the anteroposterior axis of C. elegans is controlled by opposing gradients of Wnts and a secreted Frizzled-related protein Harterink, Martin Middelkoop, Teije C. Doan, Thang Dinh van Oudenaarden, Alexander Korswagen, Hendrik C. Kim, Don H., 1972- Massachusetts Institute of Technology. Department of Physics Massachusetts Institute of Technology. Department of Biology van Oudenaarden, Alexander 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. National Institutes of Health (U.S.) (Award 1DP1OD003936) 2019-05-24T13:48:38Z 2019-05-24T13:48:38Z 2011-06 2011-04 Article http://purl.org/eprint/type/JournalArticle 0950-1991 1477-9129 https://hdl.handle.net/1721.1/121171 Haterink, Martin et al. "Neuroblast migration along the anteroposterior axis of C. elegans is controlled by opposing gradients of Wnts and a secreted Frizzled-related protein." Development 138, 14 (June 2011): 2915-2924. © Company of Biologists en_US http://dx.doi.org/10.1242/dev.064733 Development Creative Commons Attribution-Noncommercial-Share Alike http://creativecommons.org/licenses/by-nc-sa/3.0/ application/pdf Company of Biologists Prof. van Oudenaarden via Mat Willmott
spellingShingle Harterink, Martin
Middelkoop, Teije C.
Doan, Thang Dinh
van Oudenaarden, Alexander
Korswagen, Hendrik C.
Kim, Don H., 1972-
Neuroblast migration along the anteroposterior axis of C. elegans is controlled by opposing gradients of Wnts and a secreted Frizzled-related protein
title Neuroblast migration along the anteroposterior axis of C. elegans is controlled by opposing gradients of Wnts and a secreted Frizzled-related protein
title_full Neuroblast migration along the anteroposterior axis of C. elegans is controlled by opposing gradients of Wnts and a secreted Frizzled-related protein
title_fullStr Neuroblast migration along the anteroposterior axis of C. elegans is controlled by opposing gradients of Wnts and a secreted Frizzled-related protein
title_full_unstemmed Neuroblast migration along the anteroposterior axis of C. elegans is controlled by opposing gradients of Wnts and a secreted Frizzled-related protein
title_short Neuroblast migration along the anteroposterior axis of C. elegans is controlled by opposing gradients of Wnts and a secreted Frizzled-related protein
title_sort neuroblast migration along the anteroposterior axis of c elegans is controlled by opposing gradients of wnts and a secreted frizzled related protein
url https://hdl.handle.net/1721.1/121171
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