An insect prostaglandin E2 synthase acts in immunity and reproduction

Authors: AHMED, SHABBIR - Andong National University; Stanley, David; KIM, YONGGYUN - Andong National University

Submitted to: Frontiers in Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/15/2018
Publication Date: 9/4/2018
Citation: Ahmed, S., Stanley, D.W., Kim, Y. 2018. An insect prostaglandin E2 synthase acts in immunity and reproduction. Frontiers in Physiology. 9:1231. https://doi.org/10.3389/fphys.2018.01231.
DOI: https://doi.org/10.3389/fphys.2018.01231

Interpretive Summary: Chemical insecticides are effective pest insect management tools, however, negative effects, including environmental contamination and insect resistance to the insecticides attend use of these products. These negative effects drive research into alternative insect management technologies such as biological control based on deploying insect pathogenic microbes, known as microbial control. The problem with microbial insect control is insects have very powerful immune responses to pathogenic microbes, which reduces the efficacy of these microbes. We address this problem with research designed to understand and limit insect immunity. In this paper we report on how insects signal their immune responses to microbial infections. We identified a previously unknown protein that produces a key biochemical signal that mediates coordinated, controlled reactions to infections. This finding identifies a new, researchable target that may be exploited to increase the effectiveness of microbial biological controls of insect pests. This new finding will be used by scientists working to suppress insect immune systems and will ultimately benefit growers and consumers of vegetable and other food crops.

Technical Abstract: Eicosanoids, oxygenated metabolites of C20 polyunsaturated fatty acids, mediate fundamental physiological processes, including immune reactions and reproduction, in insects. Prostaglandins (PGs) make up one group of eicosanoids, of which PGE2 is a relatively well-known mediator in various insect taxa. While PG biosynthesis has been reported, the specific biosynthetic pathway for PGE2 is not known in insects. Here, we posed the hypothesis that Se-mPGES2 mediates biosynthesis of physiologically active PGE2 through its cognate protein. To test this hypothesis, we interrogated a transcriptome of the lepidopteran insect, Spodoptera exigua, to identify a candidate PGE2 synthase (Se-mPGES2) and analyzed its sequence and expression. Its predicted amino acid sequence contains a consensus thioredoxin homology sequence (Cys-x-x-Cys) responsible for catalytic activity along with an N-terminal membrane-associated hydrophobic domain and C-terminal cytosolic domain. It also shares sequence homology (36.5%) and shares almost overlapping three dimensional structures with a membrane-bound human PGES2 (mPGES2). Se-mPGES2 was expressed in all developmental stages with high peaks during the late larval instar and adult stages. Immune challenge significantly up-regulated its expression levels in hemocytes and fat body. Injecting double-stranded RNA (dsRNA) significantly impaired two cellular immune responses, hemocyte-spreading behavior and nodule formation following bacterial challenge. Humoral immunity was also significantly suppressed, registered as reduced phenoloxidase activity and antimicrobial peptide expression levels. The suppressed immune responses were reversed following PGE2, but not arachidonic acid, treatments. RNAi treatments also reduced the egg-laying behavior of females. Control females mated with the RNAi-treated males led to substantially reduced egg-laying behavior, which was also reversed following PGE2 injections into females. These results strongly bolster our hypothesis that Se-mPGES2 acts in the biosynthesis of PGE2, a crucial biochemical signal mediating immune and reproductive physiology of S. exigua.