Prostaglandin E₂ modulates the expression of antimicrobial peptides in the fat body and midgut of Anopheles albimanus

Abstract

Prostaglandins (PGs) participate in the regulation of vertebrate and in at least six insect orders' immune responses. We identified PGE 2 in midgut, fat body, Malpighian tubules, and ovarioles of Anopheles albimanus (Aa) mosquitoes. Our data indicate that PGE 2 synthesis in cultured midguts responds to the presence of two bacterial species, Micrococcus luteus and Klebsiella pneumoniae. The production of mRNA coding for antimicrobial peptides Aa-Attacin, Aa-Cecropin, and Aa-Gambicin was observed in cultured fat bodies and midguts. The production of these messengers was reduced in the presence of dexamethasone, and this effect was reversed by arachidonic acid. Adding PGE 2 to cultures resulted in increased Aa-cecropin mRNA and decreased Aa-attacin and Aa-gambicin mRNAs. Arch. Insect Biochem. Physiol. 68:14-25, 2008 KEYWORDS: insect immunity; arachidonic acid; dexamethasone; Anopheles albimanus; antimicrobial peptides INTRODUCTIONInsects resist the constant threat of invasion by microorganisms with integumental barriers and the presence of peritrophic matrix in their digestive tracts. When microbes overcome these first-line defenses, they encounter well-organized immune reactions that resemble mammalian innate immunity. Circulating hemocytes phagocytose microbial invaders and respond by forming microaggregates and nodules. Hemocytes also encapsulate those invaders, such as parasitoid eggs, too big to phagocytose (Stanley, 2006;Stanley and Miller, 2006). These cellular defense mechanisms are practically immediate upon microbial invasion, but complex humoral responses, including hemolymph clotting (Blandin and Levashina, 2004), melanization, and the production of antimicrobial peptides (Yu and Kanost, 2003;Lemaitre and Hoffmann, 2007) are deployed later.Eicosanoids including prostaglandins (PGs) are fatty acid metabolites that in mammals are produced by many cell types, including epithelial and immune cells, and play key roles in hemostasis and immune regulation, among many other functions (Harris et al., 2002). The biosynthesis of PGs in insects is initiated by a phospholipase A 2 (PLA 2 ) that cleaves membrane phospholipids (C20 polyunsaturated fatty acids including arachidonic acid [AA]), and the resulting products are converted to PGs' bioactive forms by cyclooxygenases (COX) (Stanley, 2000(Stanley, , 2006, but products of the lipoxygenase pathway (LOX) have been also documented (Galdelhak et al., 1995). The induction of eicosanoid biosynthesis by bacteria has been observed in several insect species (Stanley, 2006 and Miller, 2006). The information on the participation of eicosanoids in insect humoral immune responses is limited; PGs mediate the expression of genes encoding the antibacterial peptide cecropine and lysozime in the silkworm Bombyx mori (Morishima et al., 1997) and regulate the activation of prophenoloxidase (PPO) in two insect species, Galleria mellonella (Downer et al., 1997) and Rhodnius prolixus (García et al., 2004). However, they do not activate PPO in other insects (Lord et al., 2002;Goldswor...

DIFERENTIAL DNA SYNTHESIS IN Anopheles albimanus TISSUES INDUCED BY IMMUNE CHALLENGE WITH DIFFERENT MICROORGANISMS

“…The An. albimanus immune response against microorganisms is mediated by phagocytosis, nodule formation, encapsulation, melanization (including generation of reactive oxygen species), and AMPs (Hernández‐Martínez et al, ; Lanz‐Mendoza et al, ; García Gil de Muñoz et al, ). However, the mechanisms to produce the high amounts of AMP molecules required for effective immune responses still require elucidation.…”

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

“…In addition, previous studies have implicated PGE2 signaling on the synthesis of antimicrobial peptides (AMPs) in Anopheles albimanus (4). Therefore, we examined the expression of major AMPs in mosquitoes primed with PGE2 or following AgPGE2Rsilencing.…”

“…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).…”

“…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. Therefore, the aim of this study was to identify and characterize the PGE2 receptor (AgPGE2R) in the mosquito An.…”

Anopheles gambiae eicosanoids modulate Plasmodium berghei survival from oocyst to salivary gland invasion

“…These effects are reversed by AA treatment, suggesting that eicosanoids modulate this response (Garcia et al 2004a). It was also shown that in Anopheles albimanus , a primary vector for malaria vivax in Mexico, DEX inhibits the expression of mRNAs corresponding to specific antimicrobial peptides (AMPs), such as cecropin, gambicin and attacin (García-Gil-de-Muñoz et al 2008). …”