Abstract
BackgroundApoptosis is a caspase regulated cell death present in all metazoans defined by a conserved set of morphological features. A well-described function of apoptosis is the removal of excessive cells during development and homeostasis. Recent studies have shown an unexpected signalling property of apoptotic cells, affecting cell fate and/or behaviour of neighbouring cells. In contrast to the apoptotic function of cell elimination, this new role of apoptosis is not well understood but seems caspase-dependent. To deepen our understanding of apoptotic functions, it is necessary to work on a biological model with a predictable apoptosis pattern affecting cell fate and/or behaviour. The tunicate Ciona intestinalis has a bi-phasic life cycle with swimming larvae which undergo metamorphosis after settlement. Previously, we have shown that the tail regression step during metamorphosis, characterized by a predictable polarized apoptotic wave, ensures elimination of most tail cells and controls primordial germ cells survival and migration.ResultsWe performed differential transcriptomic analysis between control metamorphosing larvae and larvae treated with the pan-caspase inhibitor Z-VAD-fmk in order to explore the transcriptional control of apoptotic cells on neighbouring cells that survive and migrate. When caspase activity was impaired, genes known to be involved in metamorphosis were downregulated along with other implicated in cell migration and survival molecular pathways.ConclusionWe propose these results as a confirmation that apoptotic cells can control surrounding cells fate and as a reference database to explore novel apoptotic functions in animals, including those related to migration and differentiation.
Highlights
Apoptosis is a caspase regulated cell death present in all metazoans defined by a conserved set of morphological features
Transcription is necessary for the primordial germ cells (PGC) migration We previously demonstrated that Z-VAD-fmk blocked both tail regression and PGC migration, and that apoptotic wave propagation and PGC migration speed were correlated [23]
Caspase activity modulates expression of genes implicated in cell death/survival Interestingly, the 2 genes most inhibited by caspase activity at the beginning of tail regression, girdin and mucin-5 AC, were both reported to promote survival in mammalian cells [32, 33]
Summary
Apoptosis is a caspase regulated cell death present in all metazoans defined by a conserved set of morphological features. In contrast to the apoptotic function of cell elimination, this new role of apoptosis is not well understood but seems caspase-dependent. To deepen our understanding of apoptotic functions, it is necessary to work on a biological model with a predictable apoptosis pattern affecting cell fate and/or behaviour. Apoptosis is a regulated cell death defined by morphological features and depending on caspases [1,2,3]. Accumulating evidence in many metazoans suggest that apoptotic cells can emit caspase-dependent signals to their neighbours, modulating their fate (survival/death, differentiation or proliferation) or behaviour (migration) [12, 13]. Apoptotic-induced proliferation was Krasovec et al BMC Molecular and Cell Biology (2021) 22:51 reported in several organisms, such as in the cnidarian Hydra, where apoptosis promotes proliferation of adjacent cells through emission of Wnt signalling in a caspasedependant manner during head regeneration [14]. In Xenopus laevis tadpole, an apoptotic-dependent axon guidance was suggested during tail regeneration after injury [20]
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