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Venom and Antivenom of the Redback Spider (Latrodectus Hasseltii) in Japan

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Venom and Antivenom of the Redback Spider (Latrodectus Hasseltii) in Japan Jpn. J. Infect. Dis., 71, 116–121, 2018 Original Article Venom and Antivenom of the Redback Spider (Latrodectus hasseltii) in Japan. Part I. Venom Extraction, Preparation, and Laboratory Testing Takayuki Matsumura1, Reona Mashiko2, Tomomi Sato2, Kentaro Itokawa2, Yoshihide Maekawa2, Kohei Ogawa2, Haruhiko Isawa2, Akihiko Yamamoto3, Shigemi Mori4, Akira Horita4, Akihiro Ginnaga4, Yoshinobu Miyatsu4, Motohide Takahashi5, Hisashi Taki6, Toru Hifumi7, Kyoko Sawabe2†, and Manabu Ato1*† 1Department of Immunology, National Institute of Infectious Diseases; 2Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo 162-8640; 3Division of Biosafety Control and Research, National Institute of Infectious Diseases, Tokyo 208-0011; 4The Chemo-Sero-Therapeutic Research Institute (Kaketsuken), Kumamoto 860-8568; 5Pharmaceuticals and Medical Devices Agency, Tokyo 100-0013; 6Ministry of Health, Labour and Welfare, Tokyo 100-8916; and 7Kagawa University Hospital Emergency Medical Center, Kagawa 761-0793, Japan SUMMARY: The redback spider (Latrodectus hasseltii Thorell) reportedly invaded Japan in September 1995. To date, 84 redback spider bite cases have been reported; 7 of these cases employed the antivenom. Antivenom has been imported from Australia in the past, but because of restrictions on exportation it was evident that nearly all of the antivenom present in Japan would expire during 2014. In 2014, a plan was proposed to experimentally manufacture and stockpile a horse antiserum for ourselves, using redback spiders indigenous to Japan. A total of 11,403 female spiders were captured alive: 1,217 from the vicinity of Nishinomiya City, Hyogo prefecture, and 10,186 from Osaka prefecture. Of these, 10,007 females were dissected, and the venom was extracted from the venom glands of individuals and subjected to crude purification to yield 4 lots, of which the majority was α-latrotoxin. Among them, a large amount of single lots with an estimated protein content of 236 mg is subsequently scheduled to be used for immunizing horses. We also determined lethal toxicity of the venom (LD50: 9.17 μg per mouse), and established the assay for the determination of an anti-lethal titer of antivenom in mice. in recent years, importation from Australia has been INTRODUCTION limited. As a result, it became clear that nearly all of the In September 1995 the redback spider (Latrodectus antivenom present in Japan would expire during 2014. hasseltii Thorell) was first discovered in Takaishi City, A plan for experimental production and stockpiling Osaka prefecture (1, 2), in Yokkaichi City, Mie prefecture of a horse antiserum in Japan was implemented using the following November, and in Miyakojima City, redback spiders indigenous to Japan. We captured Okinawa prefecture that December (3). The distribution redback spiders, extracted their venom glands, and of redback spiders in Japan has since expanded. It has crudely purified the venom. We then performed been shown to be established in a total of 43 prefectures characterization analysis, determined the lethal toxicity in Japan until 2016 (4). The possibility that the of the venom (LD50), and established the assay for the distribution of this spider will continue expanding and determination of anti-lethal titer of antivenom in mice. that the population will continue increasing are causes for concern. MATERIALS AND METHODS Since 1996, 84 redback spider bite cases have been reported (14 of these cases were reported in 2009), and Capture of redback spiders: A total of 11,403 7 of these cases employed antivenom (5 and T. Hifumi, female redback spiders were captured alive: 1,217 in unpublished data). Native to Australia, the redback the vicinity of Nishinomiya City, Hyogo prefecture, and spider is known as a venomous species; there are 3,000 10,186 in Osaka prefecture (Fig. 1A and 1B). From June to 5,000 bite cases every year (6), and an antivenom is through December 2014, female spiders were captured also used for the treatment. The antivenom produced in alive in several sites close to Nishinomiya City and in Australia has been imported for use in Japan. However, 480 sites in Osaka prefecture. Every effort was made to capture individuals alive by hand using tweezers or with Received June 29,2017. Accepted November 6, 2017. gloves. Pesticides were not used during capture, and J-STAGE Advance Publication February 28, 2018. specimens were killed by freezing at –20°C. The redback DOI: 10.7883/yoken.JJID.2017.291 spiders stored in the freezer were transported frozen in * Corresponding author: Mailing address: Department of various batches to the National Institute of Infectious Immunology, National Institute of Infectious Diseases, Diseases (NIID), Tokyo, Japan. Dry ice was used during 1-23-1 Toyama, Shinjuku-ku, Tokyo 162-8640, Japan. Tel: transport to prevent specimens from thawing. +81-3-5285-1111, Fax: +81-3-5285-1147, E-mail: ato@ Removal of the redback spider venom glands and nih.go.jp crude purification of the venom: Because the venom †These authors contributed equally to this work. gland is covered with a thick layer of muscle, the fangs 116 Venom of Redback Spider in Japan B A Hyogo Tokyo Osaka 3,403 2,223 Takaishi City 1,217 N 20 km 0 or not inves gated 1 - 100 101 - 1,000 1,001 < N 20 km Fig. 1. Map of Hyogo (A) and Osaka (B) prefectures showing locations of the collection sites of redback spiders and their density for the entire survey period. Over 1,000 of redback spiders were captured from the black area, 101–1,000 spiders from the gray area, 1–100 spiders from the silver area and no spider was captured or not investigated at the white area. were gently seized and extracted from each spider determined using a Pierce Bicinchoninic acid (BCA) using sterilized forceps on a hole slide glass under a protein assay kit (Thermo Fisher Scientific, Rockford, stereomicroscope according to the previously described IL, USA). The neurotoxin α-Latrotoxin from Latrodectus method (7). The venom glands were individually tredecimguttatus was used as a positive control and was removed from the body and transferred to a glass slide obtained from Enzo Life Sciences (Farmingdale, NY, with wells filled with cold physiological saline (Otsuka USA). Equal amounts of protein were suspended in Pharmaceutical Co., Ltd., Tokyo, Japan). One-hundred an SDS sample buffer. The lysates (0.5 μg of positive pairs of venom glands were collected in a tube (2 ml control or 10 µg protein per lane) were boiled for 5 min protein adsorbing controlled cryopreservation tubes, then separated by SDS-PAGE and either visualized with Assist Co., Ltd., Tokyo, Japan) containing 1 ml of an Imperial protein stain kit (Thermo Fisher Scientific,) physiological saline, and stored in a freezer at –80°C or transferred to polyvinylidene fluoride membranes until use. (Millipore, Bedford, MA, USA). The membranes were All venom glands were removed, and after collection blocked with Tris-buffered saline containing 5% bovine into approximately 100 tubes, 3 zirconia beads 4 mm in serum albumin and 0.1% Tween 20 and incubated with diameter were put into each tube, and were homogenized anti-α-latrotoxin polyclonal Ab, which was developed using a high-speed mechanical homogenizer (Tissue- in rabbits using highly purified α-latrotoxin from Lyser II, QIAGEN N.V., Venlo, The Netherlands) for Latrodectus tredecimguttatus (8) (Sigma-Aldrich 30 s at 25.0 cycles per second. The tubes containing the Corp., St. Louis, MO, USA). The membranes were homogenized venom glands were centrifuged at 10,000 then incubated with anti-rabbit IgG Ab linked to HRP rpm (KUBOTA 3740, KUBOTA Co., Tokyo, Japan) (GE Healthcare Life Sciences, Buckinghamshire, UK). for 3 min, and the supernatant was then recovered and Immunoreactive proteins were visualized with an ECL poured into a 50 ml tube (Proteosave® SS centrifuge detection system (Thermo Fisher Scientific,) and were tube, Sumitomo Bakelite Co., Ltd., Tokyo, Japan). One analyzed by a chemiluminescence image analyzer, milliliter of cold physiological saline was added to each Image Quant LAS-4000 (GE Healthcare Life Sciences,). residue, and the mixture was again homogenized for Mice: All animal experiments were performed 30 s at 25.0 cycles per second and centrifuged for 15 according to institutional guidelines and with the min at 14,000 rpm (KUBOTA 3740). The supernatant approval of the NIID Animal Care and Use Committee from each sample was recovered as described above (Permit Numbers: 114097 and 115035). Female outbred and mixed in a 50 ml tube (mentioned above). The tube ddY mice (4-week-old) were purchased from Japan SLC containing the recovered venom was placed on ice to Inc.,(Shizuoka, Japan). Animals were maintained under minimize the activity of protease. The venom solution specific pathogen-free conditions. was stored at –80°C to avoid unnecessary freeze-thaw Assay for the determination of lethal toxicity in cycles. mouse (LD50): The assay was performed on 5 groups Quantification of protein, protein gel staining, (5 mice per group) for diluted solutions. The venom and immunoblotting: Quantification of protein was was diluted with 0.2% gelatin-phosphate buffered saline 117 (GPBS) in final concentrations of 144 (group 1), 120 September 2,595; October 2,280; November 2,144, and (group 2), 100 (group 3), 83 (group 4), and 69 µg/ December 1,283. Redback spiders are distributed widely ml (group 5). Aliquots of 0.1 ml of each dilution were throughout Osaka prefecture; 3,403 and 2,223 spiders injected into each mouse by intravenous route via the were captured in Toyonaka and Daito cities, respectively. tail. Subsequently, the number of deaths per group was A total of 11,403 redback spiders were captured from recorded for 10 d. LD50 was determined using the Probit both areas. method. Removal of redback spider venom glands and Assay for the determination of anti-lethal titer in crude purification of the venom: Of the 11,403 mouse: The assay was performed on 5 groups (3 mice captured redback spiders 10,007 females were dissected per group) for diluted solutions.
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