Prostaglandin catabolism in Spodoptera exigua, a lepidopteran insect

ABSTRACTSeveral 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 the presence of 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 those encoding 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, those treated with dsRNAs specific to PG-degrading enzyme genes kept a high PO activity for a longer period. These results suggest that SePGDH and SePGR are responsible for PG degradation at a late phase of the immune response.

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Prostaglandin catabolism in Spodoptera exigua, a lepidopteran insect

10.1101/2020.07.13.201608 ◽

2020 ◽

Author(s):

Shabbir Ahmed ◽

Yonggyun Kim

Keyword(s):

Immune Responses ◽

Spodoptera Exigua ◽

Inflammatory Mediator ◽

Late Phase ◽

Bacterial Challenge ◽

Expression Levels ◽

Humoral Immune ◽

Humoral Immune Responses ◽

Lepidopteran Insect ◽

Rnai Treatment

ABSTRACTSeveral 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.

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Various Eicosanoids Modulate the Cellular and Humoral Immune Responses of the Beet Armyworm,Spodoptera exigua

Bioscience Biotechnology and Biochemistry ◽

10.1271/bbb.90272 ◽

2009 ◽

Vol 73 (9) ◽

pp. 2077-2084 ◽

Cited By ~ 40

Author(s):

Sony SHRESTHA ◽

Yonggyun KIM

Keyword(s):

Immune Responses ◽

Spodoptera Exigua ◽

Beet Armyworm ◽

Humoral Immune ◽

Humoral Immune Responses

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

Scientific Reports ◽

10.1038/s41598-020-77325-2 ◽

2020 ◽

Vol 10 (1) ◽

Author(s):

Mohammad Vatanparast ◽

Shabbir Ahmed ◽

Dong-Hee Lee ◽

Sung Hee Hwang ◽

Bruce Hammock ◽

...

Keyword(s):

Immune Responses ◽

Epoxide Hydrolase ◽

Spodoptera Exigua ◽

Inflammatory Responses ◽

Soluble Epoxide Hydrolase ◽

Immune Defense ◽

Nodule Formation ◽

Dodecanoic Acid ◽

Bacterial Challenge ◽

Lepidopteran Insect

AbstractEpoxyoctadecamonoenoic 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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Immunosuppressive Activities of Novel PLA2 Inhibitors from Xenorhabdus hominickii, an Entomopathogenic Bacterium

Insects ◽

10.3390/insects11080505 ◽

2020 ◽

Vol 11 (8) ◽

pp. 505 ◽

Cited By ~ 1

Author(s):

Md. Mahi Imam Mollah ◽

Aman Dekebo ◽

Yonggyun Kim

Keyword(s):

Immune Responses ◽

Culture Broth ◽

Dependent Manner ◽

Bacterial Metabolites ◽

Humoral Immune ◽

Humoral Immune Responses ◽

Lepidopteran Insect ◽

Inhibitory Activities ◽

Main Components ◽

Ethylhexyl Phthalate

Eicosanoids mediate both cellular and humoral immune responses in insects. Phospholipase A2 (PLA2) catalyzes the first committed step in eicosanoid biosynthesis. It is a common pathogenic target of two entomopathogenic bacteria, Xenorhabdus and Photorhabdus. The objective of this study was to identify novel PLA2 inhibitors from X. hominickii and determine their immunosuppressive activities. To identify novel PLA2 inhibitors, stepwise fractionation of X. hominickii culture broth and subsequent enzyme assays were performed. Eight purified fractions of bacterial metabolites were obtained. Gas chromatography and mass spectrometry (GC-MS) analysis predicted that the main components in these eight fractions were 2-cyanobenzoic acid, dibutylamine, 2-ethyl 1-hexanol, phthalimide (PM), dioctyl terephthalate, docosane, bis (2-ethylhexyl) phthalate, and 3-ethoxy-4-methoxyphenol (EMP). Their synthetic compounds inhibited the activity of PLA2 in hemocytes of a lepidopteran insect, Spodoptera exigua, in a dose-dependent manner. They also showed significant inhibitory activities against immune responses such as prophenoloxidase activation and hemocytic nodulation of S. exigua larvae, with PM and EMP exhibiting the most potent inhibitory activities. These immunosuppressive activities were specific through PLA2 inhibition because an addition of arachidonic acid, a catalytic product of PLA2, significantly rescued such suppressed immune responses. The two most potent compounds (PM and EMP) showed significant insecticidal activities after oral administration. When the compounds were mixed with Bacillus thuringiensis (Bt), they markedly increased Bt pathogenicity. This study identified eight PLA2 inhibitors from bacterial metabolites of X. hominickii and demonstrated their potential as novel insecticides.

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Benzylideneacetone suppresses both cellular and humoral immune responses of Spodoptera exigua and enhances fungal pathogenicity

Journal of Asia-Pacific Entomology ◽

10.1016/j.aspen.2011.06.001 ◽

2011 ◽

Vol 14 (4) ◽

pp. 423-427 ◽

Cited By ~ 12

Author(s):

Junga Park ◽

Yonggyun Kim

Keyword(s):

Immune Responses ◽

Spodoptera Exigua ◽

Fungal Pathogenicity ◽

Humoral Immune ◽

Humoral Immune Responses

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

Insects ◽

10.3390/insects12050449 ◽

2021 ◽

Vol 12 (5) ◽

pp. 449

Author(s):

Md Tafim Hossain Hrithik ◽

Mohammad Vatanparast ◽

Shabbir Ahmed ◽

Yonggyun Kim

Keyword(s):

Immune Responses ◽

Gene Family ◽

Bacterial Infections ◽

Spodoptera Exigua ◽

Fat Body ◽

Expression Patterns ◽

Nodule Formation ◽

Physiological Functions ◽

Lepidopteran Insect ◽

Rnai Treatment

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.

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