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

SIMPLE SUMMARY: In insects, the insulin/insulin-like growth factor signalling (IIS) pathway regulates the carbohydrate and lipid metabolisms, and plays important roles in diapause regulation. Trehalose accumulates in many diapausing insects, as it is a major carbohydrate reserve and a stress protectant. Because of metabolism depression, the trehalose concentration is maintained at relatively high levels over the diapause phase. In the present study, bovine insulin injection triggered diapause termination and synchronous eclosion in Antheraea pernyi pupae. Moreover, treatment with bovine insulin elevated the trehalose catabolism in diapausing pupae. As a homologue of vertebrate insulin, insulin-like peptide (ApILP) enhances the trehalose catabolism during the diapause termination process. The transcription factor forkhead box O (ApFoxO)—the downstream target of the IIS pathway—exhibited a contrasting effect on the trehalose catabolism to that of ApILP. These results suggest that ApILP and ApFoxO are involved in the regulation of trehalose catabolism during diapause termination in A. pernyi pupae. ABSTRACT: In insects, trehalose accumulation is associated with the insulin/insulin-like growth factor signalling (IIS) pathway. However, whether insulin-like peptide is involved in the regulation of the trehalose metabolism during diapause termination remains largely unknown. This study assessed whether insulin-like peptide (ApILP) enhances the trehalose catabolism in the pupae of Antheraea pernyi during their diapause termination process. Injection of 10 μg of bovine insulin triggered diapause termination and synchronous adult eclosion in diapausing pupae. Moreover, treatment with bovine insulin increased the expression of trehalase 1A (ApTre-1A) and trehalase 2 (ApTre-2), as well as the activity of soluble and membrane-bound trehalase, resulting in a decline in trehalose levels in the haemolymph. Silencing ApILP via RNA interference significantly suppressed the expression of ApTre-1A and ApTre-2, thus leading to an increase in the trehalose concentration during diapause termination. However, neither injection with bovine insulin nor ApILP knockdown directly affected trehalase 1B (ApTre-1B) expression. Moreover, overexpression of the transcription factor forkhead box O (ApFoxO) induced an increase in trehalose levels during diapause termination; however, depletion of ApFoxO accelerated the breakdown of trehalose in diapausing pupae by increasing the expression of ApTre-1A and ApTre-2. The results of this study help to understand the contributions of ApILP and ApFoxO to the trehalose metabolism during diapause termination.