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Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration

Krull, Catherine E. and Lansford, Rusty and Gale, Nicholas W. and Collazo, Andres and Marcelle, Christophe and Yancopoulos, George D. and Fraser, Scott E. and Bronner-Fraser, Marianne (1997) Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration. Current Biology, 7 (8). pp. 571-580. ISSN 0960-9822. https://resolver.caltech.edu/CaltechAUTHORS:20160323-141712284

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Abstract

Background: In the trunk of avian embryos, neural crest migration through the somites is segmental, with neural crest cells entering the rostral half of each somitic sclerotome but avoiding the caudal half. Little is known about the molecular nature of the cues – intrinsic to the somites – that are responsible for this segmental migration of neural crest cells. Results: We demonstrate that Eph-related receptor tyrosine kinases and their ligands are essential for the segmental migration of avian trunk neural crest cells through the somites. EphB3 localizes to the rostral half-sclerotome, including the neural crest, and the ligand ephrin-B1 has a complementary pattern of expression in the caudal half-sclerotome. To test the functional significance of this striking asymmetry, soluble ligand ephrin-B1 was added to interfere with receptor function in either whole trunk explants or neural crest cells cultured on alternating stripes of ephrin-B1 versus fibronection. Neural crest cells in vitro avoided migrating on lanes of immobilized ephrin-B1; the addition of soluble ephrin-B1 blocked this inhibition. Similarly, in whole trunk explants, the metameric pattern of neural crest migration was disrupted by addition of soluble ephrin-B1, allowing entry of neural crest cells into caudal portions of the sclerotome. Conclusions: Both in vivo and in vitro, the addition of soluble ephrin-B1 results in a loss of the metameric migratory pattern and a disorganization of neural crest cell movement. These results demonstrate that Eph-family receptor tyrosine kinases and their transmembrane ligands are involved in interactions between neural crest and sclerotomal cells, mediating an inhibitory activity necessary to constrain neural precursors to specific territories in the developing nervous system.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1016/S0960-9822(06)00256-9DOIArticle
http://www.sciencedirect.com/science/article/pii/S0960982206002569PublisherArticle
ORCID:
AuthorORCID
Lansford, Rusty0000-0002-2159-3699
Fraser, Scott E.0000-0002-5377-0223
Bronner-Fraser, Marianne0000-0003-4274-1862
Additional Information:© 1997 Current Biology Ltd. Received: 28 May 1997. Revised: 23 June 1997. Accepted: 23 June 1997. Published: 11 July 1997. Available online 10 April 2004. The first two authors contributed equally to this study. We thank J. Neri and P. Godoy for technical assistance, S. Ruffins for invaluable help with preparing figures, and M. Dickinson, D. Wilkinson, D. Anderson for helpful comments on the manuscript and for sharing results before publication. We thank D. Kenny for help with obtaining the full-length QEK10 probe. We thank M. Henkenmeyer and T. Pawson for providing anti-EphB2 antibody and H. Wang and D. Anderson for providing the ephrin-B2 (Htk-L) and ephrin-B1 (Elk-L) probes. We thank J. Solomon and S. Speicher for providing the cell tracking program used in this study. This work was supported by USPHS HD-15527 and a grant from the Muscular Dystrophy Association to M.B.F. and MH-49176 to S.E.F.
Funders:
Funding AgencyGrant Number
U.S. Public Health Service (USPHS)HD-15527
Muscular Dystrophy AssociationUNSPECIFIED
National Institute of Mental HealthMH-49176
Issue or Number:8
Record Number:CaltechAUTHORS:20160323-141712284
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20160323-141712284
Official Citation:Catherine E. Krull, Rusty Lansford, Nicholas W. Gale, Andres Collazo, Christophe Marcelle, George D. Yancopoulos, Scott E. Fraser, Marianne Bronner-Fraser, Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration, Current Biology, Volume 7, Issue 8, 1 August 1997, Pages 571-580, ISSN 0960-9822, http://dx.doi.org/10.1016/S0960-9822(06)00256-9. (http://www.sciencedirect.com/science/article/pii/S0960982206002569)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:65630
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:24 Mar 2016 17:29
Last Modified:14 Apr 2021 00:19

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