Evolution of the Metazoan Extracellular Matrix

Abstract

The metazoan extracellular matrix (ECM), an extracellular system of insoluble networks, sheets and fibrils of proteinaceous material, is a central mediator of multicellularity that is required for developmental processes, tissue organisation, homoeostasis and control of cell phenotypes throughout life. Comparative genomics enables the repertoire of ECM components encoded by species from different phyla to be examined systematically. These studies have identified a core ECM adhesome that arose apparently on the metazoan stem lineage through gene and domain innovations and domain shuffling. In vertebrates, additional complexity of ECM structure and function has arisen through expansion of gene families, splice variants and the inception of novel ECM components including fibril‐associated collagen with interrupted triple helices collagens, fibronectin, hyaluronan, tenascins and secreted proteoglycans of bone and cartilage. Protostome phyla also include many lineage‐specific ECM innovations and diversifications that function in prey‐capture mechanisms, the assembly of protective exterior structures, and internal organs.

Key Concepts:

  • The extracellular matrix (ECM) is an insoluble network of collagens, glycoproteins, proteoglycans and glycosaminoglycans.

  • Different morphological forms of ECM are apparent in early diverging and bilaterian animals.

  • Comparative genomics has identified a conserved core ECM adhesome, that includes integrin adhesion receptors, matrix proteases and the central ECM components of connective ECM and basement membranes.

  • The ECM components of this core adhesome are specific to the metazoa.

  • It is likely that the ECM components of the core adhesome were important for evolution of multi‐cellularity in the metazoa.

  • Additional ECM diversity has arisen in vertebrates through large‐scale genome duplication events, domain innovations, and novel ECM components.

  • Lineage‐specific ECM diversity is also apparent in invertebrates; in cuticles, shells and specialised structures as well as internal organs.

  • Overall, the metazoan ECM shows extensive adaptive radiation as well as great conservation of the core ECM components.

Keywords: evolution; metazoa; multicellularity; connective ECM; basement membrane; collagen; thrombospondin; integrin; fibrillin; biomineralisation

Figure 1.

The relationships of the major phyla of animals discussed in this article.

Figure 2.

Neofunctionalisation by domain shuffling, an example from the thrombospondin family.

Figure 3.

Overview of major steps in the evolution of metazoan ECM.

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Adams, Josephine C(Apr 2013) Evolution of the Metazoan Extracellular Matrix. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0024606]