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Identification and Characterization of Differentially Expressed Cdnas of the Vector Mosquito, Anopheles Gambiae

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Identification and Characterization of Differentially Expressed Cdnas of the Vector Mosquito, Anopheles Gambiae Proc. Natl. Acad. Sci. USA Vol. 93, pp. 13066–13071, November 1996 Genetics Identification and characterization of differentially expressed cDNAs of the vector mosquito, Anopheles gambiae GEORGE DIMOPOULOS*†‡,ADAM RICHMAN‡,ALESSANDRA DELLA TORRE*§,FOTIS C. KAFATOS‡, AND CHRISTOS LOUIS*† *Institute of Molecular Biology and Biotechnology, Foundation of Research and Technology–Hellas, GR-711 10 Heraklion, Crete, Greece; †Department of Biology, University of Crete, GR-711 10 Heraklion, Crete, Greece; §Istituto di Parassitologia, Fondazione Cenci Bolognetti, Universita`degli Studi ‘‘La Sapienza,’’ I-00185 Rome, Italy; and ‡European Molecular Biology Laboratory, D-69117 Heidelberg, Germany Contributed by Fotis C. Kafatos, August 19, 1996 ABSTRACT The isolation and study of Anopheles gambiae More broadly, isolation of differentially expressed mosquito genes that are differentially expressed in development, notably genes should provide tools for analyzing development and phys- in tissues associated with the maturation and transmission of iology, potentially contributing to our understanding of how the the malaria parasite, is important for the elucidation of basic vector interacts with insect-specific stages of the malaria parasite. molecular mechanisms underlying vector–parasite interac- Until recently, the methods of choice for identification of tions. We have used the differential display technique to differentially expressed genes were construction of subtracted screen for mRNAs specifically expressed in adult males, cDNA libraries, or differential screening of ordinary genomic or females, and midgut tissues of blood-fed and unfed females. cDNA libraries. In both cases, the availability of sufficient starting We also screened for mRNAs specifically induced upon bac- material can represent a problem, as is often true for mosquito terial infection of larval stage mosquitoes. We have charac- studies. This problem has been circumvented by the use of terized 19 distinct cDNAs, most of which show developmen- PCR-based techniques that use primers of arbitrary sequence to tally regulated expression specificity during the mosquito life amplify, and subsequently isolate, differentially expressed mRNA cycle. The most interesting are six new sequences that are sequences. An adaptation of the random amplified polymorphic midgut-specific in the adult, three of which are also modulated DNA method of detecting DNA polymorphisms (5) uses a single by blood-feeding. The gut-specific sequences encode a maltase, arbitrary primer for both reverse transcription (RT) and the a V-ATPase subunit, a GTP binding protein, two different amplification of cDNAs (6). In a second method, oligo(dT) with lectins, and a nontrypsin serine protease. The latter sequence or without a partial anchor (7) is used to prime cDNAs, which are is also induced in larvae subjected to bacterial challenge. With then amplified using an arbitrary decanucleotide as the 59 primer. the exception of a mitochondrial DNA fragment, the other 18 In both cases, the radioactively labeled amplification products are sequences constitute expressed genomic sequence tags, 4 of resolved by electrophoresis on sequencing gels. In such ‘‘differ- which have been mapped cytogenetically. ential display’’ methods, comparison of samples processed in parallel permits rapid and easy identification of a set of candidate Blood feeding by female mosquitoes provides the means of tissue-specific or developmental stage-specific gene products. transmission for a variety of viral, protozoan, and metazoan Although these methods were developed using abundantly avail- able biological material, the use of PCR amplification can allow disease agents. Plasmodium, the protozoon causing malaria, identification of even rare mRNA sequences in tissues that are enters the mosquito midgut with the blood meal where it under- difficult to obtain. goes gametogenesis and fertilization, before developing into an In the present study we used a streamlined differential display ameboid cell (ookinete) that must traverse the epithelial cells. In technique, coupled with PCR-based verification assays, to isolate the midgut the developing parasite must resist attack by immu- mosquito cDNA sequences potentially expressed in a differential noreactive molecules and digestive enzymes, penetrate through manner. Six selected sequences are preferentially expressed in the the chitinous peritrophic membrane, and cross the gut wall to adult midgut, our primary target organ. We have isolated two reach the basal lamina (1). There it multiplies vegetatively as an additional sequences that are affected by blood feeding. Most of oocyst, unless it is blocked by melanotic encapsulation of unknown the sequences that were examined carefully show some stage origin, as occurs in certain genetic strains of mosquitoes selected specificity, while only four represent constitutive or housekeeping for refractoriness to the parasite (2). Thus, the midgut constitutes components, one is female specific, and one is induced by an important potential barrier to malaria transmission. bacterial infection of the larvae. We are studying the molecular genetics of the mosquito, Anopheles gambiae, one of the most important disease vectors in MATERIALS AND METHODS sub-Saharan Africa. Identification of the genes expressed in the Mosquito Colony and Infections. An. gambiae G3 and Suakoko digestive tract of the mosquito is of obvious importance for strains were reared at 288C, 75% humidity, with a 12-h lightydark elucidation of the mechanisms that permit parasite development cycle. Adults were maintained on 10% sucrose solution and and successful passage through the midgut wall. However, only a females were blood-fed on anesthetized rats. Larvae were exper- few midgut-specific genes have been isolated to date, largely those imentally infected by pricking with a needle dipped in a bacterial encoding digestive proteases (3). Other components involved in pellet of Escherichia coli (strain 1106) and Micrococcus luteus the development and physiology of the midgut, as well as immune (strain A270) and allowed to recover for varying time periods in effectors which might operate in the midgut environment, remain clean H20. to be identified and studied. Promoters of midgut-specific genes RNA Extraction and Differential Display. RNA was prepared are also of potential interest, because they may be used in the from midguts and remaining carcasses of adult female An. future for engineering new types of malaria-refractory mosqui- gambiae. The blood meal was removed from the fed guts prior to toes, specifically expressing Plasmodium-blocking agents (4). Abbreviation: RT–PCR, reverse transcription–PCR. The publication costs of this article were defrayed in part by page charge Data deposition: The sequences reported in this paper have been payment. This article must therefore be hereby marked ‘‘advertisement’’ in deposited in the GenBank data base (accession numbers are given in accordance with 18 U.S.C. §1734 solely to indicate this fact. Table 1). 13066 Downloaded by guest on September 29, 2021 Genetics: Dimopoulos et al. Proc. Natl. Acad. Sci. USA 93 (1996) 13067 RNA extraction. Total RNAs were extracted from these samples by heating to 958C for 5 min. Beads were rinsed and resuspended or entire animals at the indicated stages by using the RNaid PLUS in distilled water. One microliter of the cDNA template was used kit (Bio 101) according to the manufacturer’s instructions, fol- in 25 ml PCRs containing primer pairs specific for the various lowed by DNase I treatment. cDNAs (see below), 50 mM KCl, 10 mM TriszHCl (pH 8.3), 2 mM Differential display, G and S series. First-strand oligo(dT)- MgCl2, 20 pmol each primer, 100 mM dNTPs (Pharmacia), and primed cDNA synthesis was performed in 50 ml reactions 2.5 units Taq polymerase. Appropriate annealing temperatures consisting of 1 mg RNA, 50 mM TriszHCl (pH 8.3), 50 mM KCl, and cycle numbers were estimated empirically for each primer 4 mM MgC12, 0.1 mM each dNTP, 20 mM DTT, 6 mM pair separately. Reaction products were visualized on 1.4% oligo(dT) primer [59-CGGCCTCGAC(T)12-39], 20 units RNa- ethidium-stained agarose gels. Primers specific for ribosomal sin (Promega) and 40 units Moloney murine leukemia virus protein S7 (14) or actin (15) cDNAs were used as controls. The reverse transcriptase (Pharmacia). Reactions were incubated primers used for these experiments were as follows: G3A, 59- at 378C for 90 min and then heated to 608C for 10 min. The mix ACCTCAAAGTACAGCTTGCC-39 and G3B, 59-CTACGTG- was centrifuged through a Sephadex G-25 column (Pharmacia) AAGGTTGTCAAGG-39; G9A, 59-ATTAGGCAATAACTT- and adjusted to 100 ml. For PCR amplification, 2 mlofthe ATCCG-39 and G9B, 59-TGAACCATTTATTTTTTG-39; cDNA template was used in 25 ml reactions containing 10 mM G10A, 59-CCAACTTCATGGTTGTCG-39 and G10B, 59-GG- TriszHCl (pH 8.3), 25 mM KCl, 2 mM MgCl2, 0.1 mM each GAGAGGTTCAAAATAC-39; G11A, 59-ATAATGCGTTCT- dNTP, 0.5 mM decamer primer (Operon Technologies, Ala- TCTTTCCC-39 and G11B, 59-GACTCCGTTTCAAAATCC- meda, CA) and 0.5 mM oligo(dT) primer (as for first-strand AC-39; G13A, 59-GTCCTGGGGAGGTATTCC-39 and G13B, cDNA synthesis). Forty-five amplification cycles (1 min at 59- AGCACTTCATTTGAAGCC-39; G14A, 59-CGTATCCA- 948C, 1 min at 408C, 2 min at 728C) were performed in a CAGACCGATG-39 and G14B, 59-GTTCTTCAGCCCTTTC- Perkin–Elmer thermal cycler. Reaction products were re- TG-39; G18A, 59-ACTACACAGGAGAGTAAACC-39 and solved on a 1.4% agarose gel, visualized by ethidium
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