Breaking down barriers: the evolution of cell invasion

Abstract

Cell invasion is a specialized cell behavior that likely co-evolved with the emergence of basement membranes in metazoans as a mechanism to break down the barriers that separate tissues. A variety of conserved and lineage-specific biological processes that occur during development and homeostasis rely on cell invasive behavior. Recent innovations in genome editing and live-cell imaging have shed some light on the programs that mediate acquisition of an invasive phenotype; however, comparative approaches among species are necessary to understand how this cell behavior evolved. Here, we discuss the contexts of cell invasion, highlighting both established and emerging model systems, and underscore gaps in our understanding of the evolution of this key cellular behavior.

Figure 1. Cellular and phylogenetic contexts to study cell invasive behavior

Cell invasion has been observed in a variety of contexts during embryonic development and homeostasis. (A–D) Invasive cell behaviors that may be more generally conserved between taxa include EMT (A), gastrulation (B), immune cell trafficking (C), and neural crest delamination (D). (E–H) Lineage-restricted cell invasive behaviors include deciduate placentation (E), mouth formation (F), AC invasion (G), wing disc eversion (H). Phylogeny based on [,–89].

Figure 2. Conserved features of cellular invasion programs

Schematic depicts key shared autonomous and non-autonomous genetic programs that appear to regulate cell invasive behavior.

Figure 3. Heterochrony in AC invasion timing observed in rhabditid nematodes

Changes in the timing of nematode AC invasion in relation to vulval precursor cell division. A) Simplified rhabditid nematode phylogeny (left) depicts timing when AC invasion is complete based on DIC imaging [34]. B) Changes in timing of AC invasion have occurred in the evolution of the Oscheius genus (yellow). Red bar denotes invasion at the P6.p 1-cell stage, orange at the 2-cell stage, and blue at the 4-cell stage, summarized in the schematic (right). Micrographs modified from [34].