Regulation of trehalase expression inhibits apoptosis in diapause cysts ofArtemia

Abstract

Trehalase, which specifically hydrolyses trehalose into glucose, plays an important role in the metabolism of trehalose. Large amounts of trehalose are stored in the diapause encysted embryos (cysts) of Artemia, which are not only vital to their extraordinary stress resistance, but also provide a source of energy for development after diapause is terminated. In the present study, a mechanism for the transcriptional regulation of trehalase was described in Artemia parthenogenetica. A trehalase-associated protein (ArTAP) was identified in Artemia-producing diapause cysts. ArTAP was found to be expressed only in diapause-destined embryos. Further analyses revealed that ArTAP can bind to a specific intronic segment of a trehalase gene. Knockdown of ArTAP by RNAi resulted in the release of cysts with coarse shells in which two chitin-binding proteins were missing. Western blotting showed that the level of trehalase was increased and apoptosis was induced in these ArTAP-knockdown cysts compared with controls. Taken together, these results show that ArTAP is a key regulator of trehalase expression which, in turn, plays an important role in trehalose metabolism during the formation of diapause cysts.

Mechanisms of animal diapause: recent developments from nematodes, crustaceans, insects, and fish

“…These observations certainly do not preclude apoptosis in these embryos, because the extrinsic pathway to apoptosis, activated through ligation of death receptors located in the plasma membrane, frequently serves as a mechanism to eliminate cells during development, differentiation, and tissue remodeling, as tissues are removed and replaced (81). Under certain experimental conditions with selective protein knockdown, terminal deoxynucleotidyl transferase dUTP nick end labeling assays have shown apoptosis to occur in developing embryos of A. franciscana (110,202,204). It is, nevertheless, interesting that during energy-limited states like diapause and anoxia, these embryos survive for months to years without apoptosis.…”

Insulin-Like Peptide and FoxO Mediate the Trehalose Catabolism Enhancement during the Diapause Termination Period in the Chinese Oak Silkworm (Antheraea pernyi)

“…When A. pernyi larvae perceive unfavourable environmental signals, such as short daylengths or low temperatures, they are programmed to enter a stage of facultative diapause during their pupal development [ 10 ]. As trehalose is a major circulating sugar, and also serves as an agent protecting individuals against environmental stress, its concentration is closely related to the occurrence, maintenance, and termination of diapause in many insect species [ 11 , 12 , 13 , 14 , 15 ]. Previous studies have reported that trehalose accumulates in diapause-destined A. pernyi pupae, and relatively high trehalose levels are maintained throughout the diapause phase; however, these levels decrease significantly after diapause termination, suggesting close regulation of the level of trehalose from the onset to the termination of diapause [ 16 , 17 ].…”

Stress tolerance during diapause and quiescence of the brine shrimp, Artemia

“…The need for a termination cue differentiates diapause from quiescence, a hypometabolic, stress-tolerant state requiring only return to favorable growth parameters for termination (Drinkwater and Clegg 1991). Stress tolerance during diapause and quiescence in Artemia has been examined from several perspectives including the synthesis, composition, and structure of the cyst shell (Liu et al 2009;Dai et al 2011a;, the role of trehalose (Clegg 1965;Clegg and Jackson 1992;Yang et al 2013), the composition and activity of late embryogenesis abundant (LEA) proteins (Sharon et al 2009;Wu et al 2011;Toxopeus et al 2014), and the function of molecular chaperones such as small heat shock proteins (sHsps) and artemin (King and MacRae 2012;King et al 2013King et al , 2014.…”