Characterization of the first insect prostaglandin (PGE2) receptor: MansePGE2R is expressed in oenocytoids and lipoteichoic acid (LTA) increases transcript expression

Kwon, Hyeogsun; Yang, Yunlong; Kumar, Sunil; Lee, Dae-Weon; Bajracharya, Prati; Calkins, Travis L.; Kim, Yonggyun; Pietrantonio, Patricia V.

doi:10.1016/j.ibmb.2019.103290

Cited by 24 publications

(32 citation statements)

References 84 publications

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“…gambiae, exhibiting similarities to recently characterized insect PGE2 receptors in M. sexta (8) and S. exigua (13). With prostaglandin signaling implicated in diverse physiological roles in insects such as cellular immunity, renal physiology and reproduction (1,8,11,(32)(33)(34), we examined AgPGE2R expression across tissues and feeding status, finding that AgPGE2R was most prevalent in populations of hemocytes and malphigian tubules. While we did not further explore the role of AgPGE2R in the malpighian tubule, previous studies in other insect systems suggest potential roles for AgPGE2R in water homeostasis (33,35,36).…”

Section: Discussionmentioning

confidence: 98%

“…Based on the prostaglandin E2 receptor from the tobacco hornworm, Manduca sexta (8), a putative PGE2 receptor (AgPGE2R; AGAP001561) was identified in An. gambiae.…”

Section: Characterization Of the Agpge2 Receptormentioning

confidence: 99%

“…Eicosanoids are lipid-derived signaling molecules that include prostaglandins (PGs), leukotrienes (LTs), lipoxins (LXAs), and epoxyeicosatrienoic acid (EETs), that serve important roles in immune regulation (1)(2)(3). Evidence suggests that these responses are evolutionally conserved across metazoa, where eicosanoids significantly influence insect cellular immunity (4)(5)(6)(7)(8)(9)(10). In the mosquito, Anopheles gambiae, eicosanoids such as prostaglandin E2 (PGE2) and lipoxins have integral roles in mediating immune priming and mosquito susceptibility to malaria parasite infection (11,12).…”

Section: Introductionmentioning

confidence: 99%

“…The recent characterization of a PGE2 receptor in the lepidopteran systems Manduca sexta (8) and Spodoptera exigua (10) have implicated the PGE2 receptor in immune activation pathogen-associated molecular patterns (PAMPs) (8) and cellular immune function (13). Yet, despite the implication of PGE2 on mosquito immunity (4,11), the cognate prostaglandin receptor has not yet been described in mosquitoes.…”

Section: Introductionmentioning

confidence: 99%

“…Based on in silico analyses using the Manduca PGE2 receptor (8) and human PG receptors, we identified a putative PGE2 receptor (AgPGE2R) in An. gambiae orthologous to human PGE2-EP2 and EP4 receptors.…”

Section: Introductionmentioning

confidence: 99%

See 4 more Smart Citations

Identification of a prostaglandin E2 receptor that regulates mosquito oenocytoid immune cell function in limiting bacteria and parasite infection

Kwon

Smith

2020

Preprint

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Lipid-derived signaling molecules known as eicosanoids have integral roles in mediating immune and inflammatory processes across metazoans. This includes the function of prostaglandins and their cognate G protein-coupled receptors (GPCRs) to employ their immunological actions. In insects, prostaglandins have been implicated in the regulation of both cellular and humoral immune responses, yet studies have been limited by the absence of a described prostaglandin receptor. Here, we characterize a prostaglandin E2 receptor (AgPGE2R) in the mosquito Anopheles gambiae and examine its contributions to innate immunity. AgPGE2R expression is most abundant in circulating hemocytes where it is primarily localized to oenocytoid immune cell populations. Through the administration of prostaglandin E2 (PGE2) and AgPGE2R-silencing by RNAi, we demonstrate that PGE2 signaling regulates the expression of a subset of prophenoloxidases (PPOs) and antimicrobial peptides (AMPs). PGE2 priming via the AgPGE2R significantly limited bacterial replication and suppressed Plasmodium oocyst survival. Additional experiments establish that PGE2 priming increases phenoloxidase (PO) activity through the increased expression of PPO1 and PPO3, which significantly influence Plasmodium oocyst survival. We also provide evidence that PGE2 priming is concentration-dependent, where high concentrations of PGE2 promote oenocytoid lysis, negating the protective effects of PGE2 priming on anti-Plasmodium immunity. Taken together, our results characterize the AgPGE2R and the role of prostaglandin signaling on immune cell function, providing new insights into the role of PGE2 on anti-bacterial and anti-Plasmodium immune responses in the mosquito host.

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Section: Discussionmentioning

confidence: 98%

“…Based on the prostaglandin E2 receptor from the tobacco hornworm, Manduca sexta (8), a putative PGE2 receptor (AgPGE2R; AGAP001561) was identified in An. gambiae.…”

Section: Characterization Of the Agpge2 Receptormentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Identification of a prostaglandin E2 receptor that regulates mosquito oenocytoid immune cell function in limiting bacteria and parasite infection

Kwon

Smith

2020

Preprint

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PGE₂ mediation of egg development in Western flower thrip, Frankliniella occidentalis

Choi

Kim

2022

Arch Insect Biochem Physiol

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Eicosanoids mediate various insect physiological processes, including reproduction. Especially, the eicosanoid prostaglandin E 2 (PGE 2 ) is known to mediate oocyte development in some insects. The explosive reproductive potential of the Western flower thrips, Frankliniella occidentalis, damages various agricultural crops. However, little is known about the underlying physiological processes of egg development in this pest. This study found that treatment with aspirin (ASP) (a specific cyclooxygenase (COX) inhibitor) used to inhibit PGE 2 biosynthesis during ovarian development significantly suppressed the reproduction of female F. occidentalis. However, the addition of PGE 2 to ASPtreated females significantly rescued the suppressed reproduction. PGE 2 was detected in growing ovarian follicles in an immunofluorescence assay. The hypothetical biosynthetic machinery of PGE 2 was predicted from the F. occidentalis genome and included phospholipase A 2 (PLA 2 ), COX-like peroxidase (POX), and PGE 2 synthase (PGES). Three specific PLA 2 s were highly expressed in female adults during active oogenesis. Specific POX and PGES genes also showed high expression during active oogenesis. The adverse effect of ASP treatment on oogenesis was observed in follicle formation in the germarium where the follicle numbers in an ovariole were decreased, which resulted in hypotrophied ovaries. This impairment was rescued by the addition of PGE 2 . ASP treatment also significantly inhibited chorion formation and

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PGE₂ Binding Affinity of Hemocyte Membrane Preparations of Manduca sexta and Identification of the Receptor‐Associated G Proteins in Two Lepidopteran Species

Khan,

Tunaz,

Haas

et al. 2024

Arch Insect Biochem Physiol

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Prostaglandin E2 (PGE2) is an eicosanoid that mediates a range of physiological actions in vertebrates and invertebrates, including reproduction and immunity. The PGE2 receptor was identified and functionally assessed in two lepidopteran insects, Manduca sexta and Spodoptera exigua. However, its binding affinity to the receptor has not been reported. The PGE2 receptor is a G‐protein coupled receptor (GPCR) although its corresponding G‐protein is not identified. PGE2 binding assays were performed with membrane preparations from hemocytes of M. sexta larvae. We recorded an optimal binding in 4 h reactions conducted at pH 7.5 with 12 nM tritium‐labeled PGE2. We found that hemocytes express a single population of PGE2 binding sites with a high affinity (Kd = 35 pmol/mg protein), which are specific and saturable. The outcomes of experiments on the influence of purine nucleotides suggested these are functional GPCRs. A bioinformatics analysis led to a proposed trimeric G‐protein in the S. exigua transcriptome, in which the Gα subunit is classified into five different types: Gα(o), Gα(q), Gα(s), Gα(12), and Gα(f). After confirming expressions of these five types in S. exigua, individual RNA interference (RNAi) treatments were applied to the larvae using gene‐specific double‐stranded RNAs. RNAi treatments specific to Gα(s) or Gα(12) gene expression significantly suppressed the cellular immune responses although the RNAi treatments specific to other three Gα components did not. While PGE2 treatments led to elevated hemocyte cAMP or Ca2+ levels, the RNAi treatments specific to Gα(s) or Gα(12) genes led to significantly reduced second messenger levels under PGE2, although the RNAi treatments specific to the other three Gα components did not. These results showed that the PGE2 receptor has high PGE2 affinity in the nanomolar range and binds G‐proteins containing a Gα(s) or Gα(12) trimeric component in S. exigua and M. sexta, and likely, all lepidopteran insects.

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Characterization of the first insect prostaglandin (PGE2) receptor: MansePGE2R is expressed in oenocytoids and lipoteichoic acid (LTA) increases transcript expression

Cited by 24 publications

References 84 publications

Identification of a prostaglandin E2 receptor that regulates mosquito oenocytoid immune cell function in limiting bacteria and parasite infection

Identification of a prostaglandin E2 receptor that regulates mosquito oenocytoid immune cell function in limiting bacteria and parasite infection

PGE₂ mediation of egg development in Western flower thrip, Frankliniella occidentalis

PGE₂ Binding Affinity of Hemocyte Membrane Preparations of Manduca sexta and Identification of the Receptor‐Associated G Proteins in Two Lepidopteran Species

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Characterization of the first insect prostaglandin (PGE2) receptor: MansePGE2R is expressed in oenocytoids and lipoteichoic acid (LTA) increases transcript expression

Cited by 24 publications

References 84 publications

Identification of a prostaglandin E2 receptor that regulates mosquito oenocytoid immune cell function in limiting bacteria and parasite infection

Identification of a prostaglandin E2 receptor that regulates mosquito oenocytoid immune cell function in limiting bacteria and parasite infection

PGE2 mediation of egg development in Western flower thrip, Frankliniella occidentalis

PGE2 Binding Affinity of Hemocyte Membrane Preparations of Manduca sexta and Identification of the Receptor‐Associated G Proteins in Two Lepidopteran Species

Contact Info

Product

Resources

About

PGE₂ mediation of egg development in Western flower thrip, Frankliniella occidentalis

PGE₂ Binding Affinity of Hemocyte Membrane Preparations of Manduca sexta and Identification of the Receptor‐Associated G Proteins in Two Lepidopteran Species