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

Catherine E. Krull, Rusty Lansford, Nicholas W. Gale, Andres Collazo, Christophe Marcelle, George D. Yancopoulos, Scott E. Fraser, Marianne Bronner-Fraser

Research output: Contribution to journalArticleResearchpeer-review

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 arian 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.

Original languageEnglish
Pages (from-to)571-580
Number of pages10
JournalCurrent Biology
Volume7
Issue number8
DOIs
Publication statusPublished - 1 Aug 1997
Externally publishedYes

Cite this

Krull, C. E., Lansford, R., Gale, N. W., Collazo, A., Marcelle, C., Yancopoulos, G. D., ... Bronner-Fraser, M. (1997). Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration. Current Biology, 7(8), 571-580. https://doi.org/10.1016/S0960-9822(06)00256-9
Krull, Catherine E. ; Lansford, Rusty ; Gale, Nicholas W. ; Collazo, Andres ; Marcelle, Christophe ; Yancopoulos, George D. ; Fraser, Scott E. ; Bronner-Fraser, Marianne. / Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration. In: Current Biology. 1997 ; Vol. 7, No. 8. pp. 571-580.
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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 arian 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.",
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Krull, CE, Lansford, R, Gale, NW, Collazo, A, Marcelle, C, Yancopoulos, GD, Fraser, SE & Bronner-Fraser, M 1997, 'Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration' Current Biology, vol. 7, no. 8, pp. 571-580. https://doi.org/10.1016/S0960-9822(06)00256-9

Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration. / Krull, Catherine E.; Lansford, Rusty; Gale, Nicholas W.; Collazo, Andres; Marcelle, Christophe; Yancopoulos, George D.; Fraser, Scott E.; Bronner-Fraser, Marianne.

In: Current Biology, Vol. 7, No. 8, 01.08.1997, p. 571-580.

Research output: Contribution to journalArticleResearchpeer-review

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T1 - Interactions of Eph-related receptors and ligands confer rostrocaudal pattern to trunk neural crest migration

AU - Krull, Catherine E.

AU - Lansford, Rusty

AU - Gale, Nicholas W.

AU - Collazo, Andres

AU - Marcelle, Christophe

AU - Yancopoulos, George D.

AU - Fraser, Scott E.

AU - Bronner-Fraser, Marianne

PY - 1997/8/1

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N2 - 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 arian 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.

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