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.

Cancer across the tree of life: cooperation and cheating in multicellularity

“…Multicellularity evolved because the formation of groups of cells with new physiological and behavioural capacities provided advantages over some forms of unicellular living [ 1 , 2 ]. The five most important novelties, which we here term the five foundations of multicellularity ( figure 1 ), involve cell-level cooperative capacities [ 5 ]: (i) inhibiting cell proliferation [ 1 ], (ii) regulation of cell death [ 17 – 19 ], (iii) division of labour [ 1 , 6 ], (iv) resource transport [ 7 , 20 ] and (v) creation and maintenance of the extracellular environment [ 21 , 22 ].

Figure 1.

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“…Waste produced by normally functioning cells in a multicellular body needs to be cleared, and dead cells need to be identified and properly recycled. Moreover, cells need to maintain the extracellular matrix [ 22 ], which is made up of networks of proteins that form supporting structures, such as basement membranes [ 21 ]. Cancer cells destroy the extracellular matrix using a variety of factors (e.g.…”

Extracellular Matrix Components in Bivalvia: Shell and ECM Components in Developmental and Adult Tissues

“…For example, genes encoding several adhesome components from the annotated oyster genome database were published. These were found in non-metazoan and metazoan [6,7]. Expression of the main ECM components, including interstitial/connective ECM elements, basement membrane components, ECM receptors, and certain matrix metalloproteinases, was identified in the Oyster Genes website.…”

“…Apparently, the adhesome evolved during the major wave of biotic innovation that occurred with the origin of Metazoa. Adhesomes consist of ECM components, ECM proteases, and cell surface receptors, all of which are broadly conserved throughout the Metazoa [6]. Among them, collagens are the most extensively studied of all the adhesome molecules.…”