Role of the extracellular matrix during neural crest cell migration

Abstract

Once specified to become neural crest (NC), cells occupying the dorsal portion of the neural tube disrupt their cadherin-mediated cell-cell contacts, acquire motile properties, and embark upon an extensive migration through the embryo to reach their ultimate phenotype-specific sites. The understanding of how this movement is regulated is still rather fragmentary due to the complexity of the cellular and molecular interactions involved. An additional intricate aspect of the regulation of NC cell movement is that the timings, modes and patterns of NC cell migration are intimately associated with the concomitant phenotypic diversification that cells undergo during their migratory phase and the fact that these changes modulate the way that moving cells interact with their microenvironment. To date, two interplaying mechanisms appear central for the guidance of the migrating NC cells through the embryo: one involves secreted signalling molecules acting through their cognate protein kinase/phosphatase-type receptors and the other is contributed by the multivalent interactions of the cells with their surrounding extracellular matrix (ECM). The latter ones seem fundamental in light of the central morphogenetic role played by the intracellular signals transduced through the cytoskeleton upon integrin ligation, and the convergence of these signalling cascades with those triggered by cadherins, survival/growth factor receptors, gap junctional communications, and stretch-activated calcium channels. The elucidation of the importance of the ECM during NC cell movement is presently favoured by the augmenting knowledge about the macromolecular structure of the specific ECM assembled during NC development and the functional assaying of its individual constituents via molecular and genetic manipulations. Collectively, these data propose that NC cell migration may be governed by time- and space-dependent alterations in the expression of inhibitory ECM components; the relative ratio of permissive versus non-permissive ECM components; and the supramolecular assembly of permissive ECM components. Six multidomain ECM constituents encoded by a corresponding number of genes appear to date the master ECM molecules in the control of NC cell movement. These are fibronectin, laminin isoforms 1 and 8, aggrecan, and PG-M/version isoforms V0 and V1. This review revisits a number of original observations in amphibian and avian embryos and discusses them in light of more recent experimental data to explain how the interaction of moving NC cells with these ECM components may be coordinated to guide cells toward their final sites during the process of organogenesis.

Distribution and Extracellular Matrix Environment of Premelanoblasts during Skin Development in Xiphophorus Hybrids

“…Cryofractured specimens, which were prepared by removing separating the epidermis from the dermis to further analyze the underside of the epidermal tissue, were examined by SEM to confirm both the histological and histochemical data in platyfish-swordtail hybrid skin (Figure 4A-4C). They revealed that these neural crest/ premelanoblast cells exhibited their previously described characteristic morphology in Xiphophorus fish embryos [14] and other vertebrate embryos [27]. Thus they were pleomorphic with different elongated, spheroidal, spindle-like, flattened or irregular morphologies, and had intensive cell-ECM fibril contacts ( Figure 4A and 4B), as previously described in swordtail/platyfish [14].…”

Inhibiting Glycosaminoglycan Chain Polymerization Decreases the Inhibitory Activity of Astrocyte-Derived Chondroitin Sulfate Proteoglycans

“…CSPG GAG chains have been implicated in a variety of barrier-forming phenomena, including cell division (Mizuguchi et al, 2003), neural cell migration (Kubota et al, 1999;Perissinotto et al, 2000;Perris and Perissinotto, 2000), and inhibition of axon regeneration . cABC is effective at removal of GAG chains at the lesion site in vivo (McKeon et al, 1995;Moon et al, 2001;Bradbury et al, 2002), distal to the lesion site, when combined with a peripheral nerve graft (Houle et al, 2006), as well as in vitro.…”

Essential role of non-canonical Wnt signalling in neural crest migration

“…A number of molecules are known to participate in neural crest delamination and migration, such as cadherins, Rho GTPases, Noggin and several extracellular matrix molecules (Borchers et al, 2001;Bronner-Fraser et al, 1992;Henderson et al, 2000;Hoffmann and Balling, 1995;Kimura et al, 1995;Liu and Jessell, 1998;Nakagawa and Takeichi, 1995;Nakagawa and Takeichi, 1998;Perris and Perissinotto, 2000;Pla et al, 2001;Sela-Donenfeld and Kalcheim, 1999;Sela-Donenfeld and Kalcheim, 2000;Takeichi et al, 2000;Vallin et al, 1998; Van de Putte et al, 2003;Yagi and Takeichi, 2000). However, the mechanisms by which extracellular signals are integrated with cell adhesion and cytoskeletal modification to orchestrate the cell movements underlying delamination and movement of the neural crest are still unclear.…”