Components, structure, biogenesis and function of the Hydra extracellular matrix in regeneration, pattern formation and cell differentiation

Abstract

The body wall of Hydra is organized as an epithelial bilayer (ectoderm and endoderm) with an intervening extracellular matrix (ECM), termed mesoglea by early biologists. Morphological studies have determined that Hydra ECM is composed of two basal lamina layers positioned at the base of each epithelial layer with an intervening interstitial matrix. Molecular and biochemical analyses of Hydra ECM have established that it contains components similar to those seen in more complicated vertebrate species. These components include such macromolecules as laminin, type IV collagen, and various fibrillar collagens. These components are synthesized in a complicated manner involving cross-talk between the epithelial bilayer. Any perturbation to ECM biogenesis leads to a blockage in Hydra morphogenesis. Blockage in ECM/cell interactions in the adult polyp also leads to problems in epithelial transdifferentiation processes. In terms of biophysical parameters, Hydra ECM is highly flexible; a property that facilitates continuous movements along the organism's longitudinal and radial axis. This is in contrast to the more rigid matrices often found in vertebrates. The flexible nature of Hydra ECM can in part now be explained by the unique structure of the organism's type IV collagen and fibrillar collagens. This review will focus on Hydra ECM in regard to: 1) its general structure, 2) its molecular composition, 3) the biophysical basis for the flexible nature of Hydra's ECM, 4) the relationship of the biogenesis of Hydra ECM to regeneration of body form, and 5) the functional role of Hydra ECM during pattern formation and cell differentiation.

Scleractinian coral cell proliferation is reduced in primary culture of suspended multicellular aggregates compared to polyps

“…Enzyme digestion induces dissociation of individual cells and small cell clusters, which remain suspended or adhere to the culture substrate and may aggregate over time (Gates and Muscatine 1992;Frank et al 1994;Helman et al 2008;Downs et al 2010). The mesoglea gel separating the two epithelial layers (epiderm and gastroderm) of cnidaria is an extracellular matrix (ECM) which, in Hydra, has been reported to contain collagen type IV (Fowler et al 2000) associated to laminin in the subepithelial basal lamina and to fibrillar collagen type I (Shimizu et al 2008;Sarras 2012). Collagenase is the most widely used enzyme for cnidarian tissue dissociation, with protocols first developed for hydrozoans, jellyfish and sea anemones, then adapted to the octocorals and stony corals (Gates and Muscatine 1992;Frank et al 1994;Helman et al 2008).…”

Phylogenetic evidence for the modular evolution of metazoan signalling pathways

“…Combinations of in vivo and in vitro assays have revealed the numerous important roles cnidarian basement membrane plays in directing cell differentiation, cell migration and tissue regeneration (see [155] for a review of these processes in Hydra). However, because the focus of these studies has largely been on hydrozoans, little is known about the development of the basement membrane in other cnidarians.…”

Laminins of Hydra ECM: A Comparative Analysis of Hydra and Vertebrate Laminins Based on Current Genomic and ETS DataBases

“…Using a combination of biochemical, cellular, and molecular approaches, studies were initiated in the 1980's to elucidate the structure and function of hydra ECM components [11]. The work involved:…”

“…In addition, Hydra-specific antibodies and isolated matrix component domains were also used as blocking reagents to study the role of cell-ECM interactions in Hydra using a number of regeneration bioassays [14]. These functional studies were later complimented with antisense RNA studies to selectively knockdown Hydra ECM components during regenerative processes [11].…”