Biosynthetic pathway of arachidonic acid in Spodoptera exigua in response to bacterial challenge

Hasan, Ariful; Ahmed, Shabbir; Kim, Yonggyun

doi:10.1016/j.ibmb.2019.103179

Cited by 42 publications

(30 citation statements)

References 56 publications

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“…Due to LA-rich composition in S. exigua PLs 5 , a biosynthetic pathway for EpOMEs may be initiated from the catalytic activities of phospholipases including PLA 2 (Fig. 1 A).…”

Section: Resultsmentioning

confidence: 99%

“…LC-PUFAs are also rich (7–25%) in aquatic insects 3 , but are rare in terrestrial insects due to evolutionary adaptations to prevent oxidative stress 4 . However, terrestrial insects are rich in linoleic acid (LA: 18 carbon atoms) present in phospholipids (PLs), and this fatty acid might be available for the production of LC-PUFAs with the help of elongase and desaturase activities 5 .…”

Section: Introductionmentioning

confidence: 99%

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EpOMEs act as immune suppressors in a lepidopteran insect, Spodoptera exigua

Vatanparast

Ahmed

Lee

et al. 2020

Sci Rep

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Epoxyoctadecamonoenoic acids (EpOMEs) are epoxide derivatives of linoleic acid (9,12-octadecadienoic acid) and include 9,10-EpOME and 12,13-EpOME. They are synthesized by cytochrome P450 monooxygenases (CYPs) and degraded by soluble epoxide hydrolase (sEH). Although EpOMEs are well known to play crucial roles in mediating various physiological processes in mammals, their role is not well understood in insects. This study chemically identified their presence in insect tissues: 941.8 pg/g of 9,10-EpOME and 2,198.3 pg/g of 12,13-EpOME in fat body of a lepidopteran insect, Spodoptera exigua. Injection of 9,10-EpOME or 12,13-EpOME into larvae suppressed the cellular immune responses induced by bacterial challenge. EpOME treatment also suppressed the expression of antimicrobial peptide (AMP) genes. Among 139 S. exigua CYPs, an ortholog (SE51385) to human EpOME synthase was predicted and its expression was highly inducible upon bacterial challenge. RNA interference (RNAi) of SE51385 prevented down-regulation of immune responses at a late stage (> 24 h) following bacterial challenge. A soluble epoxide hydrolase (Se-sEH) of S. exigua was predicted and showed specific expression in all development stages and in different larval tissues. Furthermore, its expression levels were highly enhanced by bacterial challenge in different tissues. RNAi reduction of Se-sEH interfered with hemocyte-spreading behavior, nodule formation, and AMP expression. To support the immune association of EpOMEs, urea-based sEH inhibitors were screened to assess their inhibitory activities against cellular and humoral immune responses of S. exigua. 12-(3-adamantan-1-yl-ureido) dodecanoic acid (AUDA) was highly potent in suppressing the immune responses. The addition of AUDA to a pathogenic bacterium significantly increased bacterial pathogenicity by suppressing host immune defense. In sum, this study demonstrated that EpOMEs play a crucial role in facilitating anti-inflammatory responses in S. exigua.

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“…Due to LA-rich composition in S. exigua PLs 5 , a biosynthetic pathway for EpOMEs may be initiated from the catalytic activities of phospholipases including PLA 2 (Fig. 1 A).…”

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

EpOMEs act as immune suppressors in a lepidopteran insect, Spodoptera exigua

Vatanparast

Ahmed

Lee

et al. 2020

Sci Rep

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“…Elongation/desaturation pathways that convert LA into AA were documented in the 1980s [16], however the research was conducted in a biochemical, rather than a physiological context. Hasan et al [17] reported three major advances in understanding PUFA metabolism. One, bacterial infections led to increased proportions of AA, up from undetectable in naïve S. exigua larvae to less than 1% following infections.…”

Section: Biosynthesis Of Aamentioning

confidence: 99%

Eicosanoid Signaling in Insect Immunology: New Genes and Unresolved Issues

Kim

Stanley

2021

Genes

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This paper is focused on eicosanoid signaling in insect immunology. We begin with eicosanoid biosynthesis through the actions of phospholipase A2, responsible for hydrolyzing the C18 polyunsaturated fatty acid, linoleic acid (18:2n-6), from cellular phospholipids, which is subsequently converted into arachidonic acid (AA; 20:4n-6) via elongases and desaturases. The synthesized AA is then oxygenated into one of three groups of eicosanoids, prostaglandins (PGs), epoxyeicosatrienoic acids (EETs) and lipoxygenase products. We mark the distinction between mammalian cyclooxygenases and insect peroxynectins, both of which convert AA into PGs. One PG, PGI2 (also called prostacyclin), is newly discovered in insects, as a negative regulator of immune reactions and a positive signal in juvenile development. Two new elements of insect PG biology are a PG dehydrogenase and a PG reductase, both of which enact necessary PG catabolism. EETs, which are produced from AA via cytochrome P450s, also act in immune signaling, acting as pro-inflammatory signals. Eicosanoids signal a wide range of cellular immune reactions to infections, invasions and wounding, including nodulation, cell spreading, hemocyte migration and releasing prophenoloxidase from oenocytoids, a class of lepidopteran hemocytes. We briefly review the relatively scant knowledge on insect PG receptors and note PGs also act in gut immunity and in humoral immunity. Detailed new information on PG actions in mosquito immunity against the malarial agent, Plasmodium berghei, has recently emerged and we treat this exciting new work. The new findings on eicosanoid actions in insect immunity have emerged from a very broad range of research at the genetic, cellular and organismal levels, all taking place at the international level.

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“…Thus, insects should have an alternative strategy to provide substrates for PG biosynthesis. Relatively high linoleic acid (LA) content in insect PLs suggested that LA is released by phospholipase A2 (PLA2) and subsequently elongated/desaturated to be AA (Hasan et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Prostaglandin catabolism in Spodoptera exigua, a lepidopteran insect

Ahmed

Kim

2020

Journal of Experimental Biology

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Several prostaglandins (PGs) and PG-synthesizing enzymes have been identified from insects. PGs 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. 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.

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Biosynthetic pathway of arachidonic acid in Spodoptera exigua in response to bacterial challenge

Cited by 42 publications

References 56 publications

EpOMEs act as immune suppressors in a lepidopteran insect, Spodoptera exigua

EpOMEs act as immune suppressors in a lepidopteran insect, Spodoptera exigua

Eicosanoid Signaling in Insect Immunology: New Genes and Unresolved Issues

Prostaglandin catabolism in Spodoptera exigua, a lepidopteran insect

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