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

Elife. 2017 Apr 18:6:e24176. doi: 10.7554/eLife.24176.

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.

Keywords: Basement Membrane; Collagen IV; Ctenophora; developmental biology; epithelial cells; evolutionary biology; genomics; stem cells.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Basement Membrane / chemistry*
  • Collagen Type IV / analysis*
  • Collagen Type IV / genetics*
  • Ctenophora / cytology
  • Ctenophora / genetics
  • Ctenophora / metabolism
  • Ctenophora / physiology*
  • Evolution, Molecular
  • Extracellular Matrix / chemistry*

Substances

  • Collagen Type IV