Mechanisms of apoptosis in Crustacea: what conditions induce versus suppress cell death?

Abstract

Arthropoda is the largest of all animal phyla and includes about 90% of extant species. Our knowledge about regulation of apoptosis in this phylum is largely based on findings for the fruit fly Drosophila melanogaster. Recent work with crustaceans shows that apoptotic proteins, and presumably mechanisms of cell death regulation, are more diverse in arthropods than appreciated based solely on the excellent work with fruit flies. Crustacean homologs exist for many major proteins in the apoptotic networks of mammals and D. melanogaster, but integration of these proteins into the physiology and pathophysiology of crustaceans is far from complete. Whether apoptosis in crustaceans is mainly transcriptionally regulated as in D. melanogaster (e.g., RHG ‘killer’ proteins), or rather is controlled by pro- and anti-apoptotic Bcl-2 family proteins as in vertebrates needs to be clarified. Some phenomena like the calcium-induced opening of the mitochondrial permeability transition pore (MPTP) are apparently lacking in crustaceans and may represent a vertebrate invention. We speculate that differences in regulation of the intrinsic pathway of crustacean apoptosis might represent a prerequisite for some species to survive harsh environmental insults. Pro-apoptotic stimuli described for crustaceans include UV radiation, environmental toxins, and a diatom-produced chemical that promotes apoptosis in offspring of a copepod. Mechanisms that serve to depress apoptosis include the inhibition of caspase activity by high potassium in energetically healthy cells, alterations in nucleotide abundance during energy-limited states like diapause and anoxia, resistance to opening of the calcium-induced MPTP, and viral accommodation during persistent viral infection. Characterization of the players, pathways, and their significance in the core machinery of crustacean apoptosis is revealing new insights for the field of cell death.

Apoptosis and necrosis during the circadian cycle in the centipede midgut

“…Thus, it plays an important role in controlling the number of cells in each organ (Maghsoudi et al 2012). Many stress factors that originate from the external environment can disrupt and damage cell organelles, causing the activation of the cell death pathways (Okuda et al 2007;Menze et al 2010;Maghsoudi et al 2012;Jain et al 2013;Teixeira et al 2013;Lipovšek and Novak 2015). Among all of the processes of cell death that are known, only apoptosis, necrosis, and autophagy have been clearly described in the digestive epithelium of invertebrates (Parthasarathy and Palli 2007;Park and Takeda 2008;Park et al 2009;Tettamanti et al 2011;Franzetti et al 2012;Rost-Roszkowska et al 2008, 2015bLipovšek and Novak 2015).…”

Gene expression, metabolic regulation and stress tolerance during diapause

“…However, the Ca ?? -induced opening of mitochondrial pores commonly observed during apoptosis is lacking in Artemia although their mitochondria contain the main pore structural proteins, and cytochrome c is not released during diapause and anoxia [31,[165][166][167]. In addition, neither Artemia caspase-9 nor caspase-3 is regulated by cytochrome c, as occurs in mammalian cells, but caspase-9 activity is increased by exogenous Ca ??…”

“…During this time, and upon exposure of post-diapause encysted embryos to prolonged anoxia, internal ultrastructure and macromolecules are preserved, indicating inhibition of proteolytic activity and apoptosis [90,107,[162][163][164]. These findings are remarkable because energy limitation can stimulate liberation of pro-apoptotic factor(s) via opening of mitochondrial permeability transition pores, activating caspases and causing cell death [165]. However, the Ca ??…”

Physiological strategies during animal diapause: lessons from brine shrimp and annual killifish

“…One biological advantage for not defending Δp is that it reduces energy expenditure considerably during diapause. Some of the potential disadvantages have been treated elsewhere (Hand and Menze, 2008;Menze et al, 2010) and include an increased probability of opening of the mitochondrial permeability transition pore and the attendant signaling for cell death. However, all inducers for the mitochondrial permeability transition that have been tried so far are ineffective in promoting the transition in A. franciscana mitochondria (Menze et al, 2005).…”