Insulin-Like Peptide Receptor-Mediated Signaling Pathways Orchestrate Regulation of Growth in the Pacific Oyster (Crassostrea gigas), as Revealed by Gene Expression Profiles.

Yongjing Li,Fuqiang Zhang,Jing Tian,Huiru Fu,Shikai Liu,Qi Li,Liting Ren

doi:10.3390/ijms22105259

Abstract

The involvement of insulin/insulin-like growth factor signaling (IIS) pathways in the growth regulation of marine invertebrates remains largely unexplored. In this study, we used a fast-growing Pacific oyster (Crassostrea gigas) variety “Haida No.1” as the material with which to unravel the role of IIS systems in growth regulation in oysters. Systematic bioinformatics analyses allowed us to identify major components of the IIS signaling pathway and insulin-like peptide receptor (ILPR)-mediated signaling pathways, including PI3K-AKT, RAS-MAPK, and TOR, in C. gigas. The expression levels of the major genes in IIS and its downstream signaling pathways were significantly higher in “Haida No.1” than in wild oysters, suggesting their involvement in the growth regulation of C. gigas. The expression profiles of IIS and its downstream signaling pathway genes were significantly altered by nutrient abundance and culture temperature. These results suggest that the IIS signaling pathway coupled with the ILPR-mediated signaling pathways orchestrate the regulation of energy metabolism to control growth in Pacific oysters.

Highlights

Nutrient abundance is one of the most important environmental factors that are critical to the growth and reproduction of all organisms
One insulin-like peptide receptor (ILPR), one insulin receptor substrate (IRS), one insulin-like growth factor-binding proteins (IGFBPs), and seven IGFALS genes were identified in C. gigas through extensive genome and transcriptome data mining
Phylogenetic analysis showed that the C. gigas ILPR was clustered into one clade with the ILPRs of arthropods and other mollusks, while the vertebrate-specific IGF1R, IGF2R, insulin receptor (INSR), and INSRR were clustered into separate clades (Figure 1)

Summary

Introduction

Nutrient abundance is one of the most important environmental factors that are critical to the growth and reproduction of all organisms. Nutrient sensing and energy metabolism are coordinated by networks of signaling cascades, such as the insulin/insulin-like growth factor signaling (IIS), target of rapamycin (TOR), and adenosine monophosphate-activated protein kinase (AMPK) signaling pathways [1]. The IIS and AMPK signaling pathways are two critical coordinators of energy homeostasis and metabolic processes across diverse vertebrate and invertebrate species. The TOR signaling pathway integrates various environmental factors and the signal transduction from the IIS and AMPK pathways in order to direct cell growth [1,2]. As one of the most important nutrient sensors, the mechanism of the IIS pathway in the growth regulation of vertebrates has been well studied.

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Conclusion