Genome-Wide Analysis Indicates a Complete Prostaglandin Pathway from Synthesis to Inactivation in Pacific White Shrimp, Litopenaeus vannamei.

Hao Yang,Xiaoli Chen,Yuying Sun,Ting Chen,Jiquan Zhang,Yujie Liu,Chunhua Zhu,Qiuhui Guo,Xugan Wu,Zhi Li,Xin Zhang,Mingyu Zhou

doi:10.3390/ijms23031654

Abstract

Prostaglandins (PGs) play many essential roles in the development, immunity, metabolism, and reproduction of animals. In vertebrates, arachidonic acid (ARA) is generally converted to prostaglandin G2 (PGG2) and H2 (PGH2) by cyclooxygenase (COX); then, various biologically active PGs are produced through different downstream prostaglandin synthases (PGSs), while PGs are inactivated by 15-hydroxyprostaglandin dehydrogenase (PGDH). However, there is very limited knowledge of the PG biochemical pathways in invertebrates, particularly for crustaceans. In this study, nine genes involved in the prostaglandin pathway, including a COX, seven PGSs (PGES, PGES2, PGDS1/2, PGFS, AKR1C3, and TXA2S), and a PGDH were identified based on the Pacific white shrimp (Litopenaeus vannamei) genome, indicating a more complete PG pathway from synthesis to inactivation in crustaceans than in insects and mollusks. The homologous genes are conserved in amino acid sequences and structural domains, similar to those of related species. The expression patterns of these genes were further analyzed in a variety of tissues and developmental processes by RNA sequencing and quantitative real-time PCR. The mRNA expression of PGES was relatively stable in various tissues, while other genes were specifically expressed in distant tissues. During embryo development to post-larvae, COX, PGDS1, GDS2, and AKR1C3 expressions increased significantly, and increasing trends were also observed on PGES, PGDS2, and AKR1C3 at the post-molting stage. During the ovarian maturation, decreasing trends were found on PGES1, PGDS2, and PGDH in the hepatopancreas, but all gene expressions remained relatively stable in ovaries. In conclusion, this study provides basic knowledge for the synthesis and inactivation pathway of PG in crustaceans, which may contribute to the understanding of their regulatory mechanism in ontogenetic development and reproduction.

Highlights

Prostaglandins (PGs) are an important class of eicosanoids, which are lipid signals derived from polyunsaturated fatty acids (PUFAs) [1,2,3,4]
For the three types of PGES, prostaglandin E synthase 1 (PGES1) were rarely identified in vertebrates, prostaglandin E synthase 2 (PGES2) were observed in all 20 species, and cytosolic prostaglandin E synthase (cPGES) were present in vertebrates and crustaceans
prostaglandin D synthases (PGDS), PGFS, and AKR1C3 were found in crustaceans

Summary

Introduction

Prostaglandins (PGs) are an important class of eicosanoids, which are lipid signals derived from polyunsaturated fatty acids (PUFAs) [1,2,3,4]. PGs are produced in almost every tissue [5] as autocrine and paracrine regulators and may regulate many physiological processes within the central nervous system [6,7], gastrointestinal system [8,9], and cardiovascular system [10,11,12]. PGs are produced by the serial metabolic cascades of phospholipids cyclooxygenase (COX) and prostaglandin synthases (PGSs) and inactivated by 15hydroxyprostaglandin dehydrogenase (PGDH). The synthesis and inactivation pathways of PGs are conserved in mammals but partially missing in other animal groups, such as fish [14] and insects [15,16]. Little is known regarding the PG synthesis and inactivation pathways of crustaceans

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