Prostaglandin D2 synthase and its functional association with immune and reproductive processes in a lepidopteran insect, Spodoptera exigua

et al. 2021

Insects

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Repat (=response to pathogen) is proposed for an immune-associated gene family from Spodoptera exigua, a lepidopteran insect. In this gene family, 46 members (Repat1–Repat46) have been identified. They show marked variations in their inducible expression patterns in response to infections by different microbial pathogens. However, their physiological functions in specific immune responses and their interactions with other immune signaling pathways remain unclear. Repat33 is a gene highly inducible by bacterial infections. The objective of this study was to analyze the physiological functions of Repat33 in mediating cellular and humoral immune responses. Results showed that Repat33 was expressed in all developmental stages and induced in immune-associated tissues such as hemocytes and the fat body. RNA interference (RNAi) of Repat33 expression inhibited the hemocyte-spreading behavior which impaired nodule formation of hemocytes against bacterial infections. Such RNAi treatment also down-regulated expression levels of some antimicrobial genes. Interestingly, Repat33 expression was controlled by eicosanoids. Inhibition of eicosanoid biosynthesis by RNAi against a phospholipase A2 (PLA2) gene suppressed Repat33 expression while an addition of arachidonic acid (a catalytic product of PLA2) to RNAi treatment recovered such suppression of Repat33 expression. These results suggest that Repat33 is a downstream component of eicosanoids in mediating immune responses of S. exigua.

Section: Discussionmentioning

confidence: 99%

Repat33 Acts as a Downstream Component of Eicosanoid Signaling Pathway Mediating Immune Responses of Spodoptera exigua, a Lepidopteran Insect

Hrithik

Vatanparast

et al. 2021

Insects

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“…Based on these findings of PGE 2 in mosquitoes, this study tested melanogaster [11], B. mori [10], and S. exigua [18]. In both dipteran and lepidopteran insects, PGE 2 or PGD 2 can mediate choriogenesis by stimulating chorion-associated gene expression [10,19]. Machado et al [10] [34].…”

Section: Discussionmentioning

confidence: 99%

“…AA is oxygenated by cyclooxygenase (COX) to form various PGs in vertebrates [14]. In insects, specific peroxidases called peroxinectin [15,16] and heme peroxidase [17] are likely to act like COX, with additional specific PG synthases that catalyze the isomerization from PGH 2 to PGE 2 or PGD 2 [18,19]. PGE 2 plays a role in mediating cellular and humoral immune responses of several mosquitoes [17,20].…”

Section: Introductionmentioning

confidence: 99%

Aspirin inhibition of prostaglandin synthesis impairs egg development across mosquito taxa

Baki

Kwon

et al. 2020

Preprint

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Several endocrine signals are known to mediate mosquito egg development including insulin-like peptide, 20-hydroxyecdysone, and juvenile hormone. The objective of this study was to determine the effects of prostaglandin E2 (PGE2) as an additional mediator of oogenesis in the mosquitoes, Aedes albopictus and Anopheles gambiae. The injection of aspirin (an inhibitor of cyclooxygenase) shortly after blood-feeding significantly inhibited egg development at choriogenesis in a dose-dependent manner in Ae. albopictus. Moreover, oral administration of aspirin to An. albopictus and An. gambiae also inhibited egg production. The aspirin treatment suppressed expression of the genes (Yellow-g and Yellow-g2) associated with exochorion darkening and led to the production of a malformed egg shell in Ae. albopictus. These inhibitory effects of aspirin on egg development were rescued by the addition of PGE2, confirming the specificity of aspirin in inhibiting prostaglandin production. To validate these results, we identified a putative PGE2 receptor (Aa-PGE2R) in Ae. albopictus. Aa-PGE2R expression was highly inducible in adult ovary after blood-feeding. RNA interference of Aa-PGE2R expression resulted in the significant suppression of choriogenesis similar to aspirin treatment, where the addition of PGE2 to Aa-PGE2R-silenced females failed to rescue egg production. Together, these results suggest that PG synthesis and signaling are required for egg development across diverse mosquito taxa.

“…Several physiological processes mediated by PGs have been observed in S. exigua , including PO activation (Shrestha and Kim, 2008), egg-laying behavior (Ahmed et al, 2018), oocyte development (Al Baki and Kim, 2019), and various immune responses (Kim et al, 2018). Furthermore, biosynthetic pathways from PGH 2 to PGE 2 by catalytic activity of SePGES and from PGH 2 to PGD 2 by catalytic activity of SePGDS are known in S. exigua (Ahmed et al, 2018; Sajjadian et al, 2020). However, genetic factor involved in PG degradation in insects including S. exigua was not known.…”

Section: Discussionmentioning

confidence: 99%

“…PGH 2 is a common substrate to form various PGs including prostanoids and prostacyclins. For example, PGE 2 synthase (PGES) and PGD 2 synthase (PGDS) have been identified in beet armyworm, Spodoptera exigua , in which PGE 2 and PGD 2 can mediate immune and reproductive processes (Ahmed et al, 2018; Sajjadian et al, 2020). Especially, PGE 2 can stimulate melanization during cellular immune responses such as hemocytic nodulation and encapsulation by mediating the release of prophenoloxidase (PPO) from its synthetic hemocytes called oenocytoids (Shrestha and Kim, 2008).…”

Section: Introductionmentioning

confidence: 99%

Prostaglandin catabolism inSpodoptera exigua, a lepidopteran insect

Kim

2020

Preprint

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Several prostaglandins (PGs) and PG-synthesizing enzymes have been identified from insects. PGs can mediate cellular and humoral immune responses. However, uncontrolled and prolonged immune responses might have adverse effects on survival. PG catabolism in insects has not been reported. Here, using a transcriptomic analysis, we predicted two PG-degrading enzymes, PG dehydrogenase (SePGDH) and PG reductase (SePGR), in Spodoptera exigua, a lepidopteran insect. SePGDH and SePGR expression levels were upregulated after immune challenge. However, their expression peaks occurred after those of PG biosynthesis genes such as PGE2 synthase or PGD2 synthase. Indeed, SePGDH and SePGR expression levels were upregulated after injection with PGE2 or PGD2. In contrast, such upregulated expression was not detected after injection with leukotriene B4, an eicosanoid inflammatory mediator. RNA interference (RNAi) using double-stranded RNAs specific to SePGDH or SePGR suppressed their expression levels. The RNAi treatment resulted in an excessive and fatal melanization of larvae even after a non-pathogenic bacterial infection. Phenoloxidase (PO) activity mediating the melanization in larval plasma was induced by bacterial challenge or PGE2 injection. Although the induced PO activity decreased after 8 h in control, larvae treated with dsRNAs specific to PG-degrading enzyme genes kept the high PO activities for a longer period compared to control larvae. These results suggest that SePGDH and SePGR are responsible for PG degradation at a late phase of immune responses.