The first report of prostacyclin and its physiological roles in insects

Abstract

Prostaglandins (PGs) mediate physiological processes of insects as well as mammals. Prostaglandin I2 (PGI2) is a relatively well-known eicosanoid with potent hormone-like actions on various tissues of vertebrates, however, its presence and biosynthetic pathway have not been described in insects. This study demonstrated that fat bodies of the lepidopteran species, Spodoptera exigua, contained ~ 3.6 pg/g PGI2. To identify its biosynthetic pathway, a PGI2 synthase gene of S. exigua (Se-PGIS) was predicted from a transcriptome of S. exigua; 25.6% homology with human PGIS was demonstrated. Furthermore, a predicted three-dimensional structure of Se-PGIS was demonstrated to be 38.3% similar to the human PGIS ortholog, including catalytic residues. Se-PGIS was expressed in all developmental stages of S. exigua and most abundant larval and adult stages; immune challenging of larvae significantly up-regulated these expression levels. The inducible expression of Se-PGIS expression was followed by a greater than four-fold increase in the concentration of PGI2 in fat bodies 10 h after immune challenge. RNA interference (RNAi) against Se-PGIS was performed by injecting double-stranded RNA (dsRNA). Under these RNAi conditions, cellular immune responses (e.g., hemocyte-spreading behavior, nodulation, phenoloxidase activity) were not affected by bacterial challenge. The addition of PGI2 to larvae treated with an eicosanoid biosynthesis inhibitor did not rescue the immunosuppression. Interestingly, PGI2 injection significantly suppressed nodule formation in response to bacterial challenge. In addition to the negative effect of PGI2 against immunity, the Se-PGIS-RNAi treatment significantly interfered with immature development and severely impaired oocyte development in female adults; the addition of PGI2 to RNAi-treated females significantly recovered oocyte development. Se-PGIS RNAi treatment also impaired male fertility by reducing fecundity after mating with untreated females. These results suggest that PGI2 acts as a negative regulator of immune responses initiated by other factors and mediates S. exigua development and reproduction.