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The Role of a Novel Wolbachia (Rickettsiales: Anaplasmataceae

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The Role of a Novel Wolbachia (Rickettsiales: Anaplasmataceae Turkish Journal of Zoology Turk J Zool (2018) 42: 422-431 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1801-14 The role of a novel Wolbachia (Rickettsiales: Anaplasmataceae) synthetic peptide, WolFar, in regulating prostaglandin levels in the hemolymph of Acheta domesticus (Orthoptera: Gryllidae) 1 1 Muhamad Azmi MOHAMMED , Ameyra AMAN-ZUKI , 1 2 1, Nurul Othman WAHIDA , Yohsuke TAGAMI , Salmah YAAKOP * 1 School of Environmental and Natural Resource Sciences, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, Bangi, Malaysia 2 Laboratory of Applied Entomology, Faculty of Agriculture, Shizuoka University, Shizuoka, Japan Received: 09.01.2018 Accepted/Published Online: 26.06.2018 Final Version: 26.07.2018 Abstract: Prostaglandins and other eicosanoids are known as regulating agents for cellular immune responses to pathogen threats in an insect’s hemolymph. A novel synthetic peptide, WolFar, was customized from a conserved region of the Wolbachia surface protein (WSP), isolated from an economically important endoparasitoid species, Fopius arisanus. WolFar consists of nine amino acids (SYY VRL QYN) and was tested on the house cricket, Acheta domesticus. Three concentrations of peptides, 0.83 mmol/L (100%), 0.63 mmol/L (75%), and 0.42 mmol/L (50%), were injected and observed for 72 h. The regulation of prostaglandin 2E (PGE2) in the hemolymph of A. domesticus was determined using ELISA and by observation of nodules in the internal system of A. domesticus. The results showed that there were significant increases in PGE2 in response to peptide injection at 24, 48, and 72 h after treatment. Furthermore, higher concentrations of peptide were directly proportional to the level of PGE2 activity. These findings were supported by the abundance of nodules that formed in the internal system and fat body of A. domesticus, detectable at 72 h into the treatment. This indicates that WolFar is able to stimulate the immune system of insects and can be further developed as a potential biopesticide. Key words: Prostaglandin, hemolymph, Acheta domesticus, WSP, peptide 1. Introduction and hemocytes, which initiates the release of the PSP that Insect immunology consists of three main components: binds to the hemocyte receptor. The binding induces the physical barriers, humoral immune response, and cellular activation of phospholipase A2 to hydrolyze arachidonic immune response. Physical barriers include structures acids (AA) from phospholipid substrates. The AA is then such as cuticle-protecting epidermis, peritrophic matrix- oxygenated by cyclooxygenase or lipoxygenase enzymes to covering midgut lumen, and chitin lining of the tracheal form PGs and other eicosanoids, which later mediate the system (Wigglesworth, 1972; Billingsley and Lehane, 1996), hemocyte-spreading behavior (Strand, 2008; Stanley and which prevent unwanted pathogens from entering the Kim, 2011, 2014; Stanley et al., 2012). A study by Jurenka et hemolymph system of insects. Humoral immune response al. (1999) showed that levels of PG in the true armyworm, involves activities of biosynthesis to produce antimicrobial Pseudaletia unipuncta, were produced fourfold in relation peptide (AMP), enzyme lysozyme, and discharge of to injections of heat-killed bacteria (Serratia marcescens) prophenoloxidase (PPO), which results in melanization compared with saline-injected larvae. of the affected areas (Lemaitre and Hoffmann, 2007). As The endosymbiont Wolbachia (Rickettsiales: for cellular immune response, cellular actions—such as Anaplasmataceae) is considered to be among the most microaggregation of pathogens, followed by encapsulation significant and successful endosymbionts and has been and then nodulation—are controlled and signaled by estimated to infect 70% of arthropod hosts, such as prostaglandins (PGs) (Stanley and Kim, 2011) and other insects, mites, crustaceans, and nematodes (Saridaki eicosanoids (Büyükgüzel et al., 2007). One of the possible and Bourtzis, 2009). However, most of the discussions signaling pathways for cellular immune response is the regarding the roles played by this endosymbiont have mechanism of plasmatocyte-spreading peptide (Srikanth focused primarily on reproductive effects, such as et al., 2011). First, pathogens are detected by the fat body cytoplasmic incompatibility (Bordenstein and Werren, * Correspondence: [email protected] 422 MOHAMMED et al. / Turk J Zool 2007), male feminization (Asgharian et al., 2014), peptide was made using mild 9-fluorenylmethoxycarbonyl induction of parthenogenesis (Watanabe et al., 2013), and (Fmoc) chemistry methods (Sheppard, 2003). The peptide male mortality (Rasgon, 2012). The reproductive effects assembly and purification were computer-controlled to exerted by Wolbachia on their hosts make it possible to ensure the authenticity of the sequences. The synthesized implement biological control measures, thereby reducing peptides were then purified in an automated preparative populations of pests or increasing populations of beneficial HPLC system, and the best fractions were selected as the insects such as predators and parasitoids (Zabalou et al., final product, with a final mass of 509.7 mg at 93% of 2004; Brelsfoard and Dobson, 2009). Recent studies have purity by HPLC. The customized peptide was 1205.34 g/ shown that Wolbachia proteins are also able to interfere mol. The purified peptides were consistently estimated in the immune systems of their hosts. Pinto et al. (2012) by analytical reverse-phase HPLC (RP-HPLC), and they reported that recombinant Wolbachia surface protein were checked for correct identity using mass spectrometry (WSP) was shown to be a stimulator that increases the (MS). The peptide treatments were prepared by diluting transcription of immune genes (TEP1 and APL1), known the peptide in solid form with deionized distilled water at to be crucial in the killing of Plasmodium in the mosquito a ratio of 1:1 (100%) to produce molarity of 0.83 mmol/L. Anopheles gambiae, which is naturally uninfected with The 100% peptide then underwent a series of dilutions to Wolbachia. When tested on the mosquito Aedes albopictus, produce concentrations of 75% (0.63 mmol/L) and 50% which is naturally Wolbachia-infected, the upregulations (0.42 mmol/L). of immune genes were lower than in the A. gambiae cells. 2.2. Insect rearing In another study, Wolbachia lipoproteins were proven to Fifth instar females of Acheta domesticus, weighing 200 ± stimulate innate and adaptive immunity in the filarial 10 mg, were used as a model species. The cricket nymphs nematode, Brugia malayi, through toll-like receptors 2 and were bought from a pet shop and underwent a selective 6 (TLR2/6) (Turner et al., 2009). procedure for the fifth instar stage: the nymphs must Wolbachia has been proven to be effective when wholly not yet have formed the protruding ovipositor structure. introduced as a functional unit, a process that involves According to Patton (1978), female A. domesticus reach artificial infection or transinfection into novel hosts. A their fifth instar stage when the ovipositor structure begins number of case studies have reported on the intentional to show. Accordingly, all nymphs without ovipositors introduction of this endosymbiont into new hosts. were brought to the lab, placed in transparent plastic Most of these studies have focused on the properties of containers (24.5 cm × 13.5 cm × 13.0 cm), and reared reproduction manipulators in controlling vector diseases, under lab conditions until the emergence of the ovipositor for example in the mosquitoes Aedes albopictus (Xi et structure. The plastic containers were provided with al., 2006; Fu et al., 2010) and Ae. aegypti (Johnson, 2015; pieces of cotton wool soaked in water as a drinking supply Joubert and O’Neill, 2017). However, no study has yet and a few dry twigs for the nymphs to jump on. Rabbit been carried out on novel peptide synthesis isolated from pellets (Harringtons, UK) and larvae of the mealworm Wolbachia DNA sequences, and its potential for other Tenebrio molitor were supplied as food. The female useful effects is unknown. The objectives of the present crickets with newly formed ovipositor structures were study are first to investigate the effects of Wolbachia selected and relocated into new plastic containers prior peptide synthesized from the WSP gene on the regulations to the biochemical assay. All the rearing procedures were of PGs in the hemolymph of A. domesticus as a cellular conducted at 28 °C with 68% relative humidity. immune response and second to visualize the effects of the 2.3. Peptide treatment assay peptide on the internal system of A. domesticus. A total of 10 fifth instar nymphs of female A. domesticus, chilled to 2 °C for 10 min, were injected dorsoventrally 2. Materials and methods between the third and fourth abdominal segments with 2.1. Designation of Wolbachia synthesis peptide (WolFar) 15 µL of Wolbachia synthetic peptide. As a negative A total of 17 sequences of WSP were obtained from control, 10 samples were injected with 15 µL of deionized Mohammed et al. (2017). These sequences were amplified distilled water. The synthetic peptide injection assays from an endoparasitoid species, Fopius arisanus, which were set to 24 h, 48 h, and 72 h, in line with previous was collected from five carambola cultivation sites in biochemical assay studies on insect immune response (Bali Peninsular Malaysia. The WSP sequences were aligned and Kaur, 2013; Prisco et al., 2013), and the hemolymph to search for the conserved region that comprises 29 was collected with micropipettes 24, 48, and 72 h after nucleotides (5’-AGC TAC TAC GTT CGT TTG CAA injection. The hemolymph was collected by piercing the TAC AAC GG-3’) translated into nine amino acids (SYY prothoracic legs with a fine and sterile needle and pooled VRL QYN), and they were sent to Mimotopes Pty. Ltd. into Eppendorf tubes from all 10 samples. The average (Australia) for peptide synthesis. The custom-synthesized quantity of hemolymph collected was about 30.0 µL 423 MOHAMMED et al. / Turk J Zool per insect. The tubes were then centrifuged (12,000 × g, plate was covered with the plate sealer provided to avoid 27 °C, 10 min) to remove cell wastes.
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