Journal of Cell Science, Vol 110, Issue 21 2729-2744, Copyright © 1997 by Company of Biologists

JOURNAL ARTICLES

Avian neural crest cell migration on laminin: interaction of the alpha1beta1 integrin with distinct laminin-1 domains mediates different adhesive responses

N Desban and JL Duband
Institut Jacques Monod, CNRS et Universite Denis Diderot, Paris, France.

In the present study, to further elucidate the molecular events that control neural crest cell migration, we have analyzed in vitro the adhesive and locomotory response of avian trunk neural crest cells to laminin-1 and searched for the integrin receptors involved in this process. Adhesion of crest cells on laminin-1 was comparable to that found on fibronectin or vitronectin. By contrast, migration was significantly greater on laminin-1 than on the other substrate molecules. Interaction of crest cells with laminin-1 involved two major cell-binding domains situated in different portions of the molecule, namely the E1' and E8 fragments, which elicited different cellular responses. Cells were poorly spread on the E1' fragment whereas, on E8, they were extremely flattened and cohesive. Either fragment supported cell locomotion, albeit not as efficiently as laminin-1. Immunoprecipitation and immunocytochemistry analyses revealed that crest cells expressed the alpha1beta1, alpha3beta1, alpha6beta1 and alpha vbeta3 integrins, as well as beta8 integrins, as presumptive laminin-1 receptors, but not alpha6beta4 and alpha2beta1. Immunofluorescence labeling of cultured cells showed that the alpha1, alpha v, beta1 and beta3 subunits were diffuse on the cell surface and in focal contacts. In contrast, alpha3 and beta8 were diffuse, while alpha6 was mostly intracytoplasmic and, secondarily, in focal contacts. Inhibition assays of cell adhesion and migration with function-perturbing antibodies demonstrated that alpha1beta1 played a predominant role in both adhesion and migration on laminin-1 and interacted with either binding sites in the E1' and E8 fragments. Alpha vbeta3 was also implicated in neural crest cell migration. In contrast, alpha3beta1, alpha6beta1 and the beta8 integrins appeared to play only subsidiary roles in cell adhesion and migration. Finally, the ability of neural crest cells to interact with laminin-1 was found to increase with time in culture, possibly in correlation with changes in alpha3 distribution on the cell surface. In conclusion, our study indicates that (1) the preferential migration of neural crest cells along basal laminae can be accounted for by the ability of laminin-1 to promote migration with great efficiency; (2) interaction with laminin-1 involves two major cell binding domains that are both recognized by the alpha1beta1 integrin; (3) alpha1beta1 integrin can elicit different cellular responses depending on the laminin-1 domains with which it interacts; and (4) changes in the repertoire of integrins expressed by neural crest cells are consistent with the modulations of cell-substratum adhesion occurring throughout migration.
CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

				M. Otis, S. Campbell, M. D Payet, and N. Gallo-Payet Expression of extracellular matrix proteins and integrins in rat adrenal gland: importance for ACTH-associated functions J. Endocrinol., June 1, 2007; 193(3): 331 - 347. [Abstract] [Full Text] [PDF]

				N. Desban, J.-C. Lissitzky, P. Rousselle, and J.-L. Duband {alpha}1{beta}1-integrin engagement to distinct laminin-1 domains orchestrates spreading, migration and survival of neural crest cells through independent signaling pathways J. Cell Sci., August 1, 2006; 119(15): 3206 - 3218. [Abstract] [Full Text] [PDF]

				T. Pietri, O. Eder, M. A. Breau, P. Topilko, M. Blanche, C. Brakebusch, R. Fassler, J.-P. Thiery, and S. Dufour Conditional {beta}1-integrin gene deletion in neural crest cells causes severe developmental alterations of the peripheral nervous system Development, August 15, 2004; 131(16): 3871 - 3883. [Abstract] [Full Text] [PDF]

				S. Testaz, A. Jarov, K. P. Williams, L. E. Ling, V. E. Koteliansky, C. Fournier-Thibault, and J.-L. Duband Sonic hedgehog restricts adhesion and migration of neural crest cells independently of the Patched- Smoothened-Gli signaling pathway PNAS, October 5, 2001; (2001) 221108698. [Abstract] [Full Text] [PDF]

				E. Chamoux, L. Bolduc, J.-G. Lehoux, and N. Gallo-Payet Identification of Extracellular Matrix Components and Their Integrin Receptors in the Human Fetal Adrenal Gland J. Clin. Endocrinol. Metab., May 1, 2001; 86(5): 2090 - 2098. [Abstract] [Full Text]

				S Testaz, M Delannet, and J Duband Adhesion and migration of avian neural crest cells on fibronectin require the cooperating activities of multiple integrins of the (beta)1 and (beta)3 families J. Cell Sci., January 12, 1999; 112(24): 4715 - 4728. [Abstract] [PDF]

				S. Testaz, A. Jarov, K. P. Williams, L. E. Ling, V. E. Koteliansky, C. Fournier-Thibault, and J.-L. Duband Sonic hedgehog restricts adhesion and migration of neural crest cells independently of the Patched- Smoothened-Gli signaling pathway PNAS, October 23, 2001; 98(22): 12521 - 12526. [Abstract] [Full Text] [PDF]