Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues

Abstract

The role of the cellular microenvironment in enabling metazoan tissue genesis remains obscure. Ctenophora has recently emerged as one of the earliest-branching extant animal phyla, providing a unique opportunity to explore the evolutionary role of the cellular microenvironment in tissue genesis. Here, we characterized the extracellular matrix (ECM), with a focus on collagen IV and its variant, spongin short-chain collagens, of non-bilaterian animal phyla. We identified basement membrane (BM) and collagen IV in Ctenophora, and show that the structural and genomic features of collagen IV are homologous to those of non-bilaterian animal phyla and Bilateria. Yet, ctenophore features are more diverse and distinct, expressing up to twenty genes compared to six in vertebrates. Moreover, collagen IV is absent in unicellular sister-groups. Collectively, we conclude that collagen IV and its variant, spongin, are primordial components of the extracellular microenvironment, and as a component of BM, collagen IV enabled the assembly of a fundamental architectural unit for multicellular tissue genesis.DOI: http://dx.doi.org/10.7554/eLife.24176.001

Breaking down barriers: the evolution of cell invasion

“…Thus, in many contexts where BM traversal is necessary, EMT and cell invasion function concomitantly. As EMT-like cellular behaviors have been observed in early branching phyla (i.e., sponges [25]), we posit here that EMT-driven invasive behaviors may be evolutionarily ancient in the Metazoa, coinciding with the evolution of the BM itself [3] (Figure 1A). …”

“…The basement membrane (BM) is a metazoan innovation that arose at the dawn of multicellularity [1–3]. Comprised of basal and reticular laminae, this specialized extracellular matrix functions to separate epithelial, mesothelial, and endothelial tissues from adjacent connective tissue through a scaffold comprised mainly of collagen IV and laminin along with other structural proteins [4,5].…”

“…Comprised of basal and reticular laminae, this specialized extracellular matrix functions to separate epithelial, mesothelial, and endothelial tissues from adjacent connective tissue through a scaffold comprised mainly of collagen IV and laminin along with other structural proteins [4,5]. Recent genomic profiling of the earliest branching extant members of the Metazoa, the sponges and ctenophores, has identified that the evolution of collagen IV is likely to be correlated with the metazoan transition to multicellularity and epithelial organization [3,6]. Although evolution of the BM was pivotal to providing the mechanical structure and compartmentalization necessary to support multicellularity [3,7,8], it is likely that cells simultaneously needed to co-evolve the ability to cross these boundaries, to both migrate between, and anchor together, different tissues.…”

“…Recent genomic profiling of the earliest branching extant members of the Metazoa, the sponges and ctenophores, has identified that the evolution of collagen IV is likely to be correlated with the metazoan transition to multicellularity and epithelial organization [3,6]. Although evolution of the BM was pivotal to providing the mechanical structure and compartmentalization necessary to support multicellularity [3,7,8], it is likely that cells simultaneously needed to co-evolve the ability to cross these boundaries, to both migrate between, and anchor together, different tissues. Whether cell invasive behavior has a single evolutionary origin, or is a product of convergent evolution, remains unclear.…”

A scar-like lesion is apparent in basement membrane after wound repair in vivo

“…Basement membrane is the most ancient and conserved type of extracellular matrix in the animal kingdom [1], and it lies under the basal surface of epithelia and wraps around muscles, nerves, and other organs [2]. Basement membrane is also important for signaling, as it can interact with signaling ligands both to promote their activity [3] and conversely to constrain their diffusion [4].…”