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Culex Pipiens Pallens (Diptera: Culicidae) Xiaoshan Yang, Qi Yin, Yang Xu, Xixi Li, Yan Sun, Lei Ma, Dan Zhou* and Bo Shen*

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Culex Pipiens Pallens (Diptera: Culicidae) Xiaoshan Yang, Qi Yin, Yang Xu, Xixi Li, Yan Sun, Lei Ma, Dan Zhou* and Bo Shen* Yang et al. Parasites Vectors (2019) 12:614 https://doi.org/10.1186/s13071-019-3867-z Parasites & Vectors RESEARCH Open Access Molecular and physiological characterization of the chitin synthase B gene isolated from Culex pipiens pallens (Diptera: Culicidae) Xiaoshan Yang, Qi Yin, Yang Xu, Xixi Li, Yan Sun, Lei Ma, Dan Zhou* and Bo Shen* Abstract Background: The growth and development of insects is strictly dependent on the precise regulation of chitin syn- thase (CHS), which is absent in vertebrates and plants. Therefore, CHS represents an attractive target for insecticides. At present, the research on the CHS gene in mosquitoes, especially its biological functions, remains limited. Results: The full-length cDNA of the chitin synthase B gene in Culex pipiens pallens (CpCHSB) was prepared and consists of 5158 nucleotides with an open reading frame (ORF) of 4722 nucleotides encoding a protein of 1573 amino acid residues. Among diferent tissues, CpCHSB gene is mainly expressed in the midgut tissue with the highest expres- sion in adult mosquitoes. Knockdown of CpCHSB in the larval stage signifcantly lowered the chitin content (16.5%) decreased body size (reduced by 25.6% in the larval stage and by 25.6% in the adult stage), and diminished reproduc- tion (20%). Injecting siCHSB into adult mosquito mainly decreased reproduction (27%). Conclusions: CpCHSB plays essential roles in growth and development, by severely reducing larval chitin content, midgut permeability, and reducing the number of female mosquito ofspring. These results indicate that CHSB may serve as a potential novel target for exploring biosafe insecticides. Keywords: Culex pipiens pallens, Insecticide resistance, Chitin synthase, RNA interference Background more classes [1]. In addition, since chemical insecticides Mosquitoes are among the most dangerous vectors for accumulate in the environment, they may have adverse many severe diseases including malaria, dengue fever, efects on non-target organisms, including humans Zika fever, yellow fever and chikungunya [1–3]. Tese [4]. New and more accurately targeted tools are indeed mosquito-borne diseases cause serious public health needed [5–7]. problems and large economic losses in tropical and sub- Chitin, a linear polymer of β-(1,4)-N-acetyl-d- tropical areas. At present, mosquito control programmes glucosamine (GlcNAc), is the second most abundant mainly rely on the application of chemical insecticides, natural polysaccharide after cellulose [8]. It is widely but their widespread and improper use leads to the devel- distributed in arthropods, nematodes and fungi, but is opment of resistance in vectors. Of the 80 countries in absent in vertebrates and plants. In insects, chitin is the which malaria is endemic that provided data for 2010– key structural component of the cuticular exoskeleton, 2017, 68 have reported resistance to at least one class of trachea, head capsule, cuticular lining of the foregut, insecticide, and 57 of those reported resistance to two or hindgut, and peritrophic membrane (PM) that lines the lumen of the midgut [9]. Chitin functions as a scafold material and plays an important role in protecting insects *Correspondence: [email protected]; [email protected] against external invasion and the abrasion of food [10]. Department of Pathogen Biology, Nanjing Medical University, Nanjing, China © The Author(s) 2019. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Yang et al. Parasites Vectors (2019) 12:614 Page 2 of 11 Terefore, chitin may be a potential selective target for we performed molecular characterization and expres- novel insect control strategies. sion profling of the CHSB gene in Cx. pipiens pallens Chitin synthase (CHS), an enzyme that transfers NDP- (CpCHSB) and explored the biological functions by gene acetylglucosamine (NAP-GlcNAc) to polymerise chitin silencing via microinjection experiments. [10], catalyses the last step of chitin synthesis. During development and metamorphosis, the chitin content Methods in insects fuctuates as a complex function of the activi- Mosquitoes ties of CHS. In general, insect CHS fall into two difer- Culex pipiens pallens larvae were reared at 28 1 °C in ent classes; CHSA and CHSB. Although both share some ± water supplemented with rat chow. Adult mosquitoes conserved motifs (DXD [hD(S/A)DT], EDR[E(D562E)R], were reared at 27 °C and 60–70% relative humidity with and QRRRW[(Q601N)RR(R604L)(W605Y)]) [6, 11] and unlimited access to water and 7% (w/v) sucrose solution have some basic properties in common, they are believed under a 16:8 h light:dark photoperiod. To allow females to have diferent functions during insect growth and to lay eggs, 3-day-old females were fed fresh mouse blood development. CHSA is responsible for chitin synthesis in [18, 19]. cuticle and trachea in Anopheles gambiae [12], Tribolium castaneum [13] and Locusta migratoria [14], whereas CHSB is mainly located in the midgut and is presum- CpCHSB cDNA cloning and sequencing ably responsible for synthesising chitin in the PM dur- Total RNA was isolated from 3-day-old female mos- ing the feeding stage in Anopheles gambiae [12], Ostrinia quitoes, 10 mosquitoes as a biological replicate using nubilalis [10] and L. migratoria [14]. Moreover, a recent RNAiso Plus reagent (TaKaRa, Tokyo, Japan) according study showed that both CHSA and CHSB proteins were to the manufacturer’s instructions. Te CpCHSB cDNA present in the newly formed compound eyes of Anoph- sequence was determined by sequencing six overlapping eles gambiae pupae according to immunohistochemical PCR fragments (Additional fle 1: Table S1), and primers analysis [12]. were designed based on the ORF of Culex quinquefascia- Previous functional analyses of the CHSB gene using tus (GenBank: XM_001846240.1). Te 5′- and 3′-RACE RNA interference (RNAi) in several diferent insect spe- ends were amplifed using a SMARTer RACE 5′/3′ Kit cies demonstrated its requirement for various physiologi- following the instructions of the manufacturer (TaKaRa). cal processes. In Bactrocera dorsalis, CHSB regulates the PCR was carried out with rTaq polymerase (TaKaRa) in chitin content of the midgut, and thereby afects growth a 50 μl reaction mixture containing 2.5 μl cDNA tem- and development. CHSB in Bombyx mori can afect the plates, 1 μl GSP (10 μM), 25 μl 2× SeqAmp bufer, 1.0 μl chitin synthesis-dependent form of the PM and is related SeqAmp DNA Polymerase, 5 μl 10× UPM and 15.5 μl to food intake and the molting process. Silencing of the ddH2O. Termal cycling involved 20 cycles of denatura- CHSB gene in Leptinotarsa decemlineata signifcantly tion at 95 °C for 30 s, annealing at 55–65 °C (based on the reduces food consumption, decreases chitin content and primer annealing temperature) for 30 s, and extension retards larval growth. Although the CHSB gene has been at 72 °C for 2–3 min (based on the size of the expected characterised in several mosquito species [12, 15], physi- fragment). Amplifed PCR products were analyzed on a ological functional information is rather limited. In Aedes 1% agarose gel and purifed using a Gel Extraction Mini aegypti, mature and immature larvae treated with dsRNA Kit (Tiangen, Beijing, China). Te product was placed targeting CHSB gene catalytic sites displayed decreased at −20 °C. Purifed DNA was ligated into the pMD18-T viability, and a few larval and adult survivors displayed vector and sequenced completely from both directions. altered morphology, including a reduction in chitinous bristles located on the abdominal segments and thorax Nucleotide and amino acid sequence analysis [4]. In addition, relatively high CHSB gene expression Te amino acid sequence of CpCHSB was translated occurs in the A. gambiae pupal stage compared with lar- using the ExPASy website (https ://web.expas y.org/trans val stages [12]. Tis fnding suggests that although CHSB late/). Similar sequences were searched using the non- may not be useful for PM-associated chitin development redundant protein sequence (nr) database of the National in pupae these enzymes may have other physiological Center for Biotechnology Information (NCBI) website roles, suggesting that further study is needed to under- (http://blast .ncbi.nlm.nih.gov/Blast .cgi). Prediction of stand the functions of the enzyme encoded by CHSB. molecular weight, isoelectric point and transmembrane Culex pipiens pallens is widely distributed in China helices was conducted using (http://cn.expas y.org/tools [16]. Tis species is the major vector of the Japanese /pi_tool.html), and N-glycosylation sites were also ana- encephalitis virus as well as Wuchereria bancrofti, the lyzed (http://www.cbs.dtu.dk/servi ces/NetNG lyc/) [20, causative agent of flariasis [17]. In the present study, 21]. Yang et al. Parasites Vectors (2019) 12:614 Page 3 of 11 Analysis of developmental stage and tissue‑specifc from at least four replicate experiments were combined expression of CpCHSB by real‑time quantitative PCR for statistical comparisons. All experiments included (RT‑qPCR) three biological replicates and at least four technical To assess developmental expression of CpCHSB, total replicates.
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