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Ornithodoros Moubata (Acari: Argasidae)

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Ornithodoros Moubata (Acari: Argasidae) 1 Babesia parasites develop and are transmitted by the non-vector soft tick Ornithodoros moubata (Acari: Argasidae) B. BATTSETSEG1,T.MATSUO2,X.XUAN1,D.BOLDBAATAR1,S.H.CHEE1, R. UMEMIYA1,T.SAKAGUCHI1,T.HATTA1,J.ZHOU1,A.R.VERDIDA1, D. TAYLOR3 and K. FUJISAKI1* 1 National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan 2 Department of Infectious Diseases, Kyorin University, School of Medicine, Mitaka, Tokyo 181-8611, Japan 3 Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8577, Japan (Received 24 April 2006; revised 30 May 2006; accepted 2 June 2006; first published online 18 September 2006) SUMMARY Ornithodoros moubata ticks were fed on blood infected with Babesia equi. However, the parasites were quickly cleared as evidenced by the disappearance of B. equi-specific ribosomal RNA from the ticks. We hypothesized that if the Babesia parasite can escape midgut-associated barriers a non-vector tick can become infected with Babesia. To test this hypothesis, B. equi parasite-infected blood from in vitro culture was injected into the haemocoel of ticks. B. equi-specific rRNA was surprisingly detected 45 days after injection even in the eggs. Babesia-free dogs were infested with O. moubata ticks that were infected by inoculation with B. gibsoni-infected red blood cells. Parasitaemia and antibody production against Bg-TRAP of B. gibsoni increased gradually. These results indicate that O. moubata may be a useful vector model for Babesia parasites and also a very important tool for studies on tick immunity against Babesia parasites and tick-Babesia interactions. Key words: Babesia, Ornithodoros moubata, midgut-associated barrier, tick transmission, vertebrate host. INTRODUCTION glands. Sporozoites invade the salivary glands to be injected into a vertebrate host when the tick ingests Babesia are tick-transmitted protozoa that comprise an infected bloodmeal (Kuttler, 1988). For trans- some of the most ubiquitous and widespread para- mission to occur, therefore, the Babesia parasite must sites of erythrocytes in humans and a wide range complete an elaborate developmental programme in of wild and economically valuable domestic animals the hostile tick environment. However, the precise such as cattle and horses (Kuttler, 1988; Kjemtrup mechanisms by which ticks limit parasite develop- and Conrad, 2000; Homer et al. 2000; Wei et al. ment still remain to be elucidated. 2001). These single-celled organisms invade red In mosquito responses to midgut invasion by blood cells and cause fatigue, aches, fever, chills, malarial parasites, microvillar proteins, peritrophic sweating, dark urine, enlarged spleen and anaemia. matrix and mosquito digestive enzymes appear Infections can range from no serious symptoms to a important as barriers to parasite development fatal disease. The life-cycle of Babesia includes (Shen et al. 1999; Sinden and Billingsley, 2001; asexual and sexual stages in the vertebrate and tick Abraham and Jacobs-Lorena, 2004). Soft ticks also host, respectively. Ticks transfer Babesia sporozoites have a number of midgut barriers such as a peri- during feeding and the sporozoites invade the host trophic membrane (Grandjean, 1983), gut lysozymes red blood cells. When Babesia gametocytes are (Kopacek et al. 1999) and antimicrobial peptides ingested by a suitable tick host they develop into (Nakajima et al. 2002a, b) that limit or prevent gametes, fuse to form a motile zygote that penetrates invasion of parasites in non-vector species. The non- the peritrophic matrix (PM), enters the cells of the vector tick Ornithodoros moubata is easier to maintain intestinal epithelium and divides into kinetes. The and handle in laboratory experiments than vector kinetes break free, enter the body cavity (haemocoel) ticks like Haemaphysalis longicornis because they are by crossing the midgut and migrate to the salivary larger in size and have a short blood-feeding period. Therefore, if the Babesia parasite can develop in O. moubata, it may be useful for elucidating the * Corresponding author: National Research Center for genetic pathways involved in vector competence and Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido clarifying the importance of the midgut barrier for 080-8555, Japan. Tel: +81 155 49 5646. Fax: +81 155 development and transmission of Babesia parasites 49 5643. E-mail: [email protected] in ticks. Parasitology (2007), 134, 1–8. f 2006 Cambridge University Press doi:10.1017/S0031182006000916 Printed in the United Kingdom Downloaded from https://www.cambridge.org/core. University of Athens, on 05 Oct 2021 at 14:55:53, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0031182006000916 B. Battsetseg and others 2 MATERIALS AND METHODS thiocyanate solution (Chomczynski and Sacchi, Parasites 1987) from injected and artificially fed ticks. Then 1 mg of total RNA from each sample was applied to a The United States Department of Agriculture One Step RNA PCR kit (TAKARA, Otsu, Japan) (USDA) strain of Babesia equi was grown in horse according to the conditions recommended by the erythrocytes in vitro as described by Avarzed et al. manufacturer with the following primers. Primers (1997). A B. gibsoni strain isolated from a hunting designed from 18S ribosomal RNA of B. equi were dog in Hyougo Prefecture Japan, designated strain rE1F 5k-GTTTATTTGATGTTTGTTT-3k and NRCPD (Fukumoto et al. 2001a) was used for rE1R 5k-CCAAGCGCAGTCAACGAAA-3k and experimental infection of beagles. for O. moubata ribosomal protein 18S were rOM 5k-GTTCCTTCC TTGATTGTCATGAG-3k and Dogs rOM 5k-TCGGTTAGATGCACTGCTCGTCT-3k as a loading control. Tick and blood samples col- One-year-old female beagle dogs were confirmed to lected from dogs were lysed in 0.1 M Tris-HCl be free of natural B. gibsoni infection by detection of (pH 8.0) containing 1% SDS, 0.1 M NaCl and 10 mM specific antibody prior to use in the experiments. All EDTA and treated with proteinase K (100 mg/ml) animal experiments were conducted in accordance for 2 h at 55 xC. The DNA was extracted with with Standards for the Care and Management of phenol/chloroform and precipitated with ethanol, Experimental Animals promulgated by the National then dissolved in 25 ml of TE buffer and stored at Research Center for Protozoan Diseases, Obihiro 4 xC. PCR was performed with p18d3 and p18d4 University of Agriculture and Veterinary Medicine, oligonucleotide primers (5k-TCCGTTCCCACAA- Japan. CACCAGC-3k and 5k-CGAATGAGGATGATG- AGGAGGA-3k) as targets for the 182 bp fragment of Ticks B. gibsoni P18 gene (Fukumoto et al. 2001b). DNA products were run on an agarose gel, stained with Soft ticks, Ornithodoros moubata (Acari: Argasidae), ethidium bromide and photographed. were obtained from the National Institute of Animal Health (Tsukuba, Japan) and have been maintained at the National Research Center for Protozoan Transmission electron microscopy (TEM) Diseases, Obihiro University of Agriculture and The salivary glands and ovaries of ticks 7 days after Veterinary Medicine for several generations by injection with Babesia parasites were removed, fixed feeding on rabbits (Oryctolagus cunniculus) and with cold 3% glutaraldehyde in sodium cacodylate maintained at 27¡1 xC, 50–60% RH and total buffer (pH 7.4) overnight at 4 xC, post-fixed with 1% darkness. Feeding and rearing of ticks were per- OsO4 in the same buffer for 2 h at 4 xC after washing formed as described by Chinzei (1983). thoroughly with the same buffer, dehydrated in an ethanol series and embedded in quetol 651 resin (Nissin EM, Tokyo, Japan). Thin sections (ap- Artificial feeding proximately 80 nm thick) were cut on a Leica An artificial feeding study was used to introduce UCT ultramicrotome using a diamond knife and B. equi into the tick digestive tract. Adult female doubly stained with uranyl acetate and lead citrate O. moubata were fed by an artificial membrane sys- before examination with a Hitachi H-7500 electron tem using Parafilm M (Pechiney plastic packaging microscope. Menasha, WI 54952) similar to the Baudruche membrane described by Waladde et al. (1991) and Immuno-electron microscopy (IEM) Matsuo et al. (2004). The artificial meal consisted of B. equi-infected red blood cells with 12% para- The ovaries were removed from ticks injected with sitaemia suspended in the same volume of PBS. infected RBC of B. equi and B. gibsoni, fixed in 4% paraformaldehyde with 0.1% glutaraldehyde in PBS overnight at 4 xC, washed thoroughly in PBS and Tick injection embedded in 2% agarose. After dehydration with an Ticks were infected under the last coxa with 15 mlof ethanol series, the samples were embedded in LR B. equi-orB. gibsoni-infected RBC suspended in Gold resin (Polysciences Inc., USA). Thin sections PBS with a 27-gauge intravenous needle. (about 80 nm thick) were cut on a Leica UCT ultramicrotome using a diamond knife and placed on nickel grids. Sections were exposed at room tem- Reverse transcriptase-polymerase chain reaction perature (RT) for 30 min to 5% skim milk PBS as a analysis (RT-PCR) and PCR blocking agent then incubated with anti-B. equi Total RNA was extracted with solution D, prepared specific merozoite antigen 1 and EMA-1 (Kapp- by adding 2-mercaptoethanol to a stock guanidinium meyer et al. 1993) or EMA–2 (Knowles et al. 1997) Downloaded from https://www.cambridge.org/core. University of Athens, on 05 Oct 2021 at 14:55:53, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0031182006000916 O. moubata can transmit Babesia parasite 3 M12 345678 M123456789PN 357 bp 357 bp AB C D SB DMBS ER N 2 µm 2 µm Fig. 1. Detection of Babesia equi in Ornithodoros moubata ticks. (A) RT-PCR for detection of B.
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