Antagonism between PTP1B and PTK Mediates Adults' Insulin-Like Signaling Regulation of Egg Diapause in the Migratory Locust.

Shuang Li,Kun Hao,Xiongbing Tu,Jie Wang,Jun Chen,Dongnan Cui,Zehua Zhang

doi:10.3390/insects12030253

Abstract

Simple SummaryIt was reported that insulin-like and fork head transcription factor (FOXO) are involved in the regulation of diapause in insects. However, the upstream modulators of the insulin-like signaling pathway (ISP) involved in diapause regulation are still unknown. We used RNAi and an inhibitor to treat PTK and PTP1B in adult tissues and injected Prx V protein or RNAi Prx V under both short and long photoperiod conditions to identify both proteins and broader cellular metabolism influences on diapause regulation. We found that under short photoperiod conditions PTP1B in female adults induces egg diapause, whereas PTK in female adults inhibits egg diapause. Intriguingly, we also found that the antioxidant enzyme Prx V is a negative regulator of NADPH oxidizing reaction, and apparently decreases reactive oxygen species (ROS) production and NADPH-OX activity. Thus, these results indicate that PTP1B, PTK and Prx V are upstream modulators that regulate diapause in eggs via the insulin signaling pathway. Furthermore, these findings have revealed a possible bridge connecting diapause hormone signaling to the insulin-like signaling pathway.Diapause is a physiological development arrest state that helps insects to adapt to seasonality and overcome adverse environmental conditions. Numerous reports have indicated that insulinlike and fork head transcription factor (FOXO) are involved in the regulation of diapause in insects. However, the upstream modulators of the insulin-like signaling pathway (ISP) involved in diapause regulation are still unknown. Here, we used RNAi and an inhibitor to treat PTK and PTP1B in adult tissues and injected Prx V or RNAi Prx V under both short and long photoperiod conditions and monitored effects on the expression of ISP genes, the phosphorylation levels for IR and IRS, the activity of NADPH oxidase, the accumulation of reactive oxygen species (ROS) and energy metabolism, seeking to identify both proteins and broader cellular metabolism influences on diapause regulation. We found that under short photoperiod conditions PTP1B in female adults induces egg diapause, whereas PTK in female adults inhibits egg diapause. Intriguingly, we also found that the antioxidant enzyme Prx V is a negative regulator of NADPH oxidizing reaction and apparently decreases ROS production and NADPH-OX activity. In contrast, all the eggs laid by adults that were treated with a series of knockdown or purified-protein injection experiments or inhibitor studies and that were reared under long photoperiod conditions hatched successfully. Thus, our results suggest a mechanism wherein diapause-related proteins (PTP1B, PTK, and Prx V) of female adults are the upstream modulators that regulate offspring eggs’ diapause process through the insulin-like signaling pathway under short photoperiod conditions.

Highlights

Diapause is a seasonal adaptation to the environment, widely existing in invertebrate taxa so that allows insects at different stages of development to respond to periodic environment changes
All the eggs laid by RNAi protein tyrosine phosphatase 1 B (PTP1B) treated adults that were reared under long photoperiod conditions hatched successfully; yet RNAi PTP1B gene treatment under long photoperiod condition did result in a significant increase in expression of the insulin receptor (IR), IRS, PI3K and AKT genes in the fat bodies, ovaries and hind legs (Appendix A Figure A1)
We propose that Prx V can regulate the activity of PTP1B and protein tyrosine kinases (PTK) by regulating the extent of nicotinamide adenine dinucleotide phosphate (NADPH) oxidation and thereby controls the insulin-like signaling pathway (ISP) signaling that mediates the diapause of locust eggs (Figure 6A,B)

Summary

Introduction

Diapause is a seasonal adaptation to the environment, widely existing in invertebrate taxa so that allows insects at different stages of development to respond to periodic environment changes. Experiments with adult diapause in Drosophila melanogaster [10,11] and the mosquito Culex pipiens [12,13], as well as with pupal diapause in the flesh fly Sarcophaga crassipalpis [14], have provided strong evidence that insulin-like signaling is an important component of the regulatory pathway controlling diapause. Insulin-like signaling and FOXO have been confirmed as regulators of diapause in mosquito [17] and in fruit flies [18]. There is a consensus that a shutdown of insulin-like signaling prompts the activation of the downstream gene FOXO, thereby leading to diapause phenotypes [17,18]

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Discussion

Conclusion