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Leucine aminopeptidase,HlLAP, from the ixodid tick Haemaphysalis longicornis,plays vital roles in the development of oocytes
Authors:Takeshi Hatta  Naotoshi Tsuji  Takeharu Miyoshi  M. Khyrul Islam  M. Abdul Alim  Kayoko Yamaji  Kozo Fujisaki
Affiliation:1. National Institute of Animal Health, National Agriculture and Food Research Organization, 3-1-5 Kannondai, Tsukuba, Ibaraki 305-0856, Japan;2. National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan;3. Department of Frontier Veterinary Medicine, Kagoshima University, 1-21-24 Korimoto, Kagoshima 890-0065, Japan;1. National Institute of Livestock and Grassland Science, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-0901, Japan;2. National Institute of Animal Health, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-0856, Japan;3. Department of Frontier Veterinary Medicine, Kagoshima University, Korimoto, Kagoshima 890-0065, Japan;4. Department of Global Agricultural Sciences, Graduate School of Agriculture and Life Sciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan;1. National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-Cho, Obihiro 080-8555, Hokkaido, Japan;2. Laboratory of Emerging Infectious Diseases, Joint Faculty of Veterinary Medicine, Kagoshima University, Korimoto 1-21-24, Kagoshima 890-0065, Japan;3. National Institute of Animal Health, National Agricultural and Food Research Organization, Kannondai 3-1-5, Tsukuba 305-0856, Ibaraki, Japan;1. Laboratory of Emerging Infectious Diseases, Joint Faculty of Veterinary Medicine, Kagoshima University, Korimoto, Kagoshima 890-0065, Japan;2. Department of Pathological and Preventive Veterinary Science, The United Graduate School of Veterinary Science, Yamaguchi University, Yoshida, Yamaguchi 753-8515, Japan;3. Laboratory of Parasitology, Joint Faculty of Veterinary Medicine, Kagoshima University, Korimoto, Kagoshima 890-0065, Japan;4. National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan;5. National Agricultural and Food Research Organization, Kannondai, Tsukuba, Ibaraki 305-0856, Japan;1. Department of Veterinary Pharmacology and Toxicology, College of Veterinary and Animal Sciences, Pookode, Lakkidi, P. O., Wayanad, Kerala 673576, India;2. Department of Veterinary Anatomy, College of Veterinary and Animal Sciences, Pookode, Lakkidi, P. O., Wayanad, Kerala 673576, India;3. Department of Veterinary Parasitology, College of Veterinary and Animal Sciences, Pookode, Lakkidi, P. O., Wayanad, Kerala 673576, India;4. Division of Parasitology, Indian Veterinary Research Institute, Izatnagar, UP 243122, India;1. Laboratory of Infectious Diseases, Joint Faculty of Veterinary Medicine, Kagoshima University, Korimoto, 1-21-24 Korimoto, Kagoshima 890-0065, Japan;2. Department of Pathological and Preventive Veterinary Science, The United Graduate School of Veterinary Science, Yamaguchi University, Yoshida, Yamaguchi 753-8515, Japan;3. Department of Parasitology, Kitasato University School of Medicine, 1-15-1 Kitasato, Kitasato, Minami, Sagamihara, Kanagawa 252-0374, Japan;4. Department of Parasitology, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh 2202, Bangladesh;5. Laboratory of International Prevention of Epidemics, Graduate School of Life and Environmental Sciences, Osaka Prefecture University, Gakuen-cho, Nakaku, Sakai, Osaka 599-8531, Japan;6. National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada, Obihiro, Hokkaido 080-8555, Japan;1. Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, ?eské Budějovice, CZ 370 05, Czech Republic;2. Institute of Organic Chemistry and Biochemistry, Academy of Sciences of the Czech Republic, Prague, CZ 16610, Czech Republic;3. Center for Discovery and Innovation in Parasitic Diseases, Department of Pathology, University of California San Francisco, San Francisco, CA 94158, USA
Abstract:Female ixodid ticks are amazing invertebrate animals which efficiently convert a large amount of nutrients derived from their ingested blood meals into eggs. Although oocyte development (vitellogenesis) in ticks is triggered by a blood meal and is assumed to be supported by nutrition derived from ovarian cells connecting oocytes, little is known about the ovarian molecules processing nutrient materials for the vitellogenesis. In this study, we have suggested a putative function of leucine aminopeptidase (HlLAP) in the ovary of parthenogenetic adult ixodid tick Haemaphysalis longicornis regarding a negative output of reproduction following disruption of HlLAP gene by RNA interference. Endogenous HlLAP was shown to be localized in the ovarian cells, including ovarian epithelial and pedicel cells which were assumed to provide nutrients for the developing oocytes. Histological studies demonstrated that a majority of immature oocytes in HlLAP gene knockdown ticks were transformed into abnormal morpho-histological oocytes with vacuolated cytoplasm and/or condensed nucleus. Taken together, a reduction of the numbers of laid eggs in the HlLAP gene knockdown ticks may be due to the degeneration of immature oocytes following deprivation of nutrients such as amino acids supplied not only by midgut HlLAP but also by the ovarian HlLAP. Regulation of the tick molecules involved in nutrient metabolism for the reproduction, including blood digestion and vitellogenesis, would help in controlling the tick population and tick-borne pathogens.
Keywords:
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