How Tissue Mechanical Properties Affect Enteric Neural Crest Cell Migration

Neural crest cells (NCCs) are a population of multipotent cells that migrate extensively during vertebrate development. Alterations to neural crest ontogenesis cause several diseases, including cancers and congenital defects, such as Hirschprung disease, which results from incomplete colonization of...

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Bibliographic Details
Published in:	Scientific reports Vol. 6; no. 1; p. 20927
Main Authors:	Chevalier, N.R., Gazquez, E., Bidault, L., Guilbert, T., Vias, C., Vian, E., Watanabe, Y., Muller, L., Germain, S., Bondurand, N., Dufour, S., Fleury, V.
Format:	Journal Article
Language:	English
Published:	London Nature Publishing Group UK 18-02-2016 Nature Publishing Group
Subjects:	13/51 14/19 14/63 14/69 631/136 631/57/343/1361 639/766/747 Animals Atomic force microscopy Biochemistry, Molecular Biology Cell adhesion & migration Cell migration Cell Movement - physiology Chick Embryo Collagen Collagenases - metabolism Colon Colonization Congenital defects Digestive system Embryo, Mammalian - embryology Embryo, Mammalian - ultrastructure Embryos Extracellular Matrix - metabolism Extracellular Matrix - ultrastructure Fibers Gastrointestinal tract Gastrointestinal Tract - embryology Gastrointestinal Tract - ultrastructure Gels Humanities and Social Sciences Life Sciences Mechanical properties Mesenchyme Metalloproteinase Mice Microscopy Microscopy, Atomic Force multidisciplinary Neural crest Neural Crest - embryology Neural Crest - ultrastructure Porosity Science
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Summary:	Neural crest cells (NCCs) are a population of multipotent cells that migrate extensively during vertebrate development. Alterations to neural crest ontogenesis cause several diseases, including cancers and congenital defects, such as Hirschprung disease, which results from incomplete colonization of the colon by enteric NCCs (ENCCs). We investigated the influence of the stiffness and structure of the environment on ENCC migration in vitro and during colonization of the gastrointestinal tract in chicken and mouse embryos. We showed using tensile stretching and atomic force microscopy (AFM) that the mesenchyme of the gut was initially soft but gradually stiffened during the period of ENCC colonization. Second-harmonic generation (SHG) microscopy revealed that this stiffening was associated with a gradual organization and enrichment of collagen fibers in the developing gut. Ex-vivo 2D cell migration assays showed that ENCCs migrated on substrates with very low levels of stiffness. In 3D collagen gels, the speed of the ENCC migratory front decreased with increasing gel stiffness, whereas no correlation was found between porosity and ENCC migration behavior. Metalloprotease inhibition experiments showed that ENCCs actively degraded collagen in order to progress. These results shed light on the role of the mechanical properties of tissues in ENCC migration during development.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Present address: INSERM U955, Equipe 6, F-94000 Créteil, France.
ISSN:	2045-2322 2045-2322
DOI:	10.1038/srep20927