Abstract
Invasive cell growth and migration is usually considered a specifically metazoan phenomenon. However, common features and mechanisms of cytoskeletal rearrangements, membrane trafficking and signalling processes contribute to cellular invasiveness in organisms as diverse as metazoans and plants – two eukaryotic realms genealogically connected only through the last common eukaryotic ancestor (LECA). By comparing current understanding of cell invasiveness in model cell types of both metazoan and plant origin (invadopodia of transformed metazoan cells, neurites, pollen tubes and root hairs), we document that invasive cell behavior in both lineages depends on similar mechanisms. While some superficially analogous processes may have arisen independently by convergent evolution (e.g. secretion of substrate- or tissue-macerating enzymes by both animal and plant cells), at the heart of cell invasion is an evolutionarily conserved machinery of cellular polarization and oriented cell mobilization, involving the actin cytoskeleton and the secretory pathway. Its central components - small GTPases (in particular RHO, but also ARF and Rab), their specialized effectors, actin and associated proteins, the exocyst complex essential for polarized secretion, or components of the phospholipid- and redox- based signalling circuits (inositol-phospholipid kinases/PIP2, NADPH oxidases) are aparently homologous among plants and metazoans, indicating that they were present already in LECA.Reviewer: This article was reviewed by Arcady Mushegian, Valerian Dolja and Purificacion Lopez-Garcia.
Highlights
Invasive cell growth and migration, including processes such as tumor or immune cell invasion into tissues or neurite outgrowth, is usually considered a topic of biomedically relevant metazoan biology
The Rho/Rac/Rop GTPases are apparently as old as the eukaryotes [301], and they a playing a comparable part in organisms as diverse as opisthokonts and plants
While we cannot exclude the possibility that some of the components of the pathways leading from the small GTPases to their ultimate cytoskeletal or secretory effectors may have been recruited from a common cellular toolbox independently, i.e. in a convergent fashion, it is plausible that even these mechanisms are, at least to some extent, ancestral
Summary
Invasive cell growth and migration, including processes such as tumor or immune cell invasion into tissues or neurite outgrowth, is usually considered a topic of biomedically relevant metazoan biology. The small GTPase Ral-A controls the ability of the neuronal exocyst proteins to associate with molecular regulators of polarity and protrusion [217] Another small GTPase, TC10, interacts with Exo and triggers translocation of the exocyst to the plasma membrane during polarisation and neurite elongation; interestingly, the Exo70-TC101 complex can locally antagonize actin rearrangements induced by Cdc42 [162,226]. The importance of sterol-rich membrane domains as sites where signalling cascades are originated to organise local actin remodelling [256,257] is very much in accord with the finding that invadopodia, and neurites, plant root hairs and pollen tubes, are lipidraft enriched domains. NOX-ROS might modify local membrane lipid composition by lipid peroxidation and play important roles in membrane lipid raft organization
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