In vivo imaging of basement membrane movement: ECM patterning shapesHydrapolyps

Abstract

SummaryGrowth and morphogenesis during embryonic development, asexual reproduction and regeneration require extensive remodeling of the extracellular matrix (ECM). We used the simple metazoan Hydra to examine the fate of ECM during tissue morphogenesis and asexual budding. In growing Hydra, epithelial cells constantly move towards the extremities of the animal and into outgrowing buds. It is not known, whether these tissue movements involve epithelial migration relative to the underlying matrix or whether cells and ECM are displaced as a composite structure. Furthermore, it is unclear, how the ECM is remodeled to adapt to the shape of developing buds and tentacles. To address these questions, we used a new in vivo labeling technique for Hydra collagen-1 and laminin, and tracked the fate of ECM in all body regions of the animal. Our results reveal that Hydra 'tissue movements' are largely displacements of epithelial cells together with associated ECM. By contrast, during the evagination of buds and tentacles, extensive movement of epithelial cells relative to the matrix is observed, together with local ECM remodeling. These findings provide new insights into the nature of growth and morphogenesis in epithelial tissues.

Cell migration: from tissue culture to embryos

“…Recent in vivo studies have shown that the ECM itself displays tissue-level movements that have been suggested to direct cell and tissue locomotion (Aufschnaiter et al, 2011;Benazeraf et al, 2010;Czirok et al, 2004;Filla et al, 2004;Zamir et al, 2006Zamir et al, , 2008. For example, during avian gastrulation the epiblast and the underlying sub-epiblastic ECM move together as a tissue composite (Zamir et al, 2008) and similar large-scale coordinated movements are observed among mesodermal cells and their surrounding ECM (Czirok et al, 2004;Zamir et al, 2006).…”

Extracellular matrix motion and early morphogenesis

“…Nonetheless, the evolutionary conservation of common ECM components and assembly processes across all extant eumetazoans (radiata and bilateria) (Fidler et al, 2014;Hynes, 2012) leaves tissue-scale motion in anamniotes (amphibia and fish) and invertebrates a distinct possibility. For example, in growing Hydra (an invertebrate with a relatively simple two cell-layered body plan), epithelial cells move towards the extremities and into the outgrowing buds, along with the associated primitive ECM (collagen 1 and laminin-rich mesoglea) via tissue-scale motion (Aufschnaiter et al, 2011). Thus, in the Hydra body column, the mesoglea is surprisingly dynamic, and is continuously displaced towards the ends of the animal (Fig.…”

Hydra, a fruitful model system for 270 years

“…Concerning the functions of the ECM, it was tested with multiple approaches (pharmacological, blocking antibodies, gene silencing via antisense RNA or insertion of exogenous ECM) in a variety of contexts, especially during reaggregation from dissociated tissues when the two epithelial cell layers come into contact in the absence of any ECM (Kishimoto et al, 1996;Murate et al, 1997), but also during regeneration and budding (Aufschnaiter et al, 2011). It turned out that the ECM plays an essential role for all these processes that are blocked when the ECM cannot form properly (see in Sarras, 2012).…”