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Mucosal Igm Antibody with D-Mannose Affinity in Fugu Takifugu

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Mucosal Igm Antibody with D-Mannose Affinity in Fugu Takifugu Mucosal IgM Antibody with d-Mannose Affinity in Fugu Takifugu rubripes Is Utilized by a Monogenean Parasite Heterobothrium okamotoi for Host Recognition This information is current as of October 5, 2021. Kento Igarashi, Ryohei Matsunaga, Sachi Hirakawa, Sho Hosoya, Hiroaki Suetake, Kiyoshi Kikuchi, Yuzuru Suzuki, Osamu Nakamura, Toshiaki Miyadai, Satoshi Tasumi and Shigeyuki Tsutsui J Immunol 2017; 198:4107-4114; Prepublished online 12 Downloaded from April 2017; doi: 10.4049/jimmunol.1601996 http://www.jimmunol.org/content/198/10/4107 http://www.jimmunol.org/ Supplementary http://www.jimmunol.org/content/suppl/2017/04/12/jimmunol.160199 Material 6.DCSupplemental References This article cites 42 articles, 10 of which you can access for free at: http://www.jimmunol.org/content/198/10/4107.full#ref-list-1 Why The JI? Submit online. by guest on October 5, 2021 • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2017 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology Mucosal IgM Antibody with D-Mannose Affinity in Fugu Takifugu rubripes Is Utilized by a Monogenean Parasite Heterobothrium okamotoi for Host Recognition Kento Igarashi,* Ryohei Matsunaga,† Sachi Hirakawa,‡ Sho Hosoya,† Hiroaki Suetake,‡ Kiyoshi Kikuchi,† Yuzuru Suzuki,† Osamu Nakamura,* Toshiaki Miyadai,‡ Satoshi Tasumi,† and Shigeyuki Tsutsui* How parasites recognize their definitive hosts is a mystery; however, parasitism is reportedly initiated by recognition of certain molecules on host surfaces. Fish ectoparasites make initial contact with their hosts at body surfaces, such as skin and gills, which are covered with mucosa that are similar to those of mammalian guts. Fish are among the most primitive vertebrates with immune systems that are equivalent to those in mammals, and they produce and secrete IgM into mucus. In this study, we showed that the Downloaded from monogenean parasite Heterobothrium okamotoi utilizes IgM to recognize its host, fugu Takifugu rubripes. Oncomiracidia are infective larvae of H. okamotoi that shed their cilia and metamorphose into juveniles when exposed to purified D-mannose–binding fractions from fugu mucus. Using liquid chromatography–tandem mass spectrometry analysis, proteins contained in the fraction were identified as D-mannose–specific IgM with two D-mannose–binding lectins. However, although deciliation was significantly induced by IgM and was inhibited by D-mannose or a specific Ab against fugu IgM, other lectins had no effect, and IgM without D-mannose affinity induced deciliation to a limited degree. Subsequent immunofluorescent staining experiments showed that fugu http://www.jimmunol.org/ D-mannose–specific IgM binds ciliated epidermal cells of oncomiracidium. These observations suggest that deciliation is triggered by binding of fugu IgM to cell surface Ags via Ag binding sites. Moreover, concentrations of D-mannose–binding IgM in gill mucus were sufficient to induce deciliation in vitro, indicating that H. okamotoi parasites initially use host Abs to colonize host gills. The Journal of Immunology, 2017, 198: 4107–4114. ish were the first animals to emerge with functional adap- lectins, lysozymes, and antimicrobial peptides (5–9). Hence, tive immune systems equivalent to those in mammals. The teleost pathogens require strategies for breaching mucosal gills, skin, and digestive tracts are covered with mucous barriers. F by guest on October 5, 2021 membranes that are similar to those in mammalian guts. Tele- The monogenean ectoparasite Heterobothrium okamotoi colo- ost mucus contains Igs, such as IgM and IgT (1), the latter of nizes external surfaces of the Tetraodontiformes teleost fugu which was recently discovered as being unique to teleosts (2). Takifugu rubripes (10) and has high host specificity; no report has The epithelial poly-IgR transports mucosal IgM in teleosts in a shown parasitism on any species other than T. rubripes (11). This similar way to the mammalian counterpart that carries mucosal species has a monoxenous life cycle that is initiated as oncomir- IgA (3). Thus, external surfaces of teleosts could be regarded as acidia, which are free-swimming larvae with cilia that attach to ancient mucosal surfaces that elicit intestine-like immune external host surfaces and grow at the gills for ∼30 d. Subse- responses of higher vertebrates (4). In addition, external mu- quently, oncomiracidia move to branchial cavity walls of their cosa of teleosts contains various defense molecules, including hosts, where they mature and spawn eggs. Oncomiracidia make initial contact with mucosal surfaces of the gills or the skin and *School of Marine Biosciences, Kitasato University, Kanagawa 252-0373, Japan; rapidly shed their ciliated epidermal cells like other monogeneans †Fisheries Laboratory, The University of Tokyo, Shizuoka 431-0214, Japan; and ‡ (12). Although it remains unclear how these parasites recognize Faculty of Marine Bioscience, Fukui Prefectural University, Fukui 917-0003, Japan their hosts and avoid attack by host defenses, they distinguish Received for publication November 28, 2016. Accepted for publication March 13, 2017. physical, physiological, and/or chemical characteristics of their host from nonhosts, including other Takifugu species. This work was supported by Grant-in-Aids for Scientific Research from the Ministry of Education, Science, Sports, and Culture of Japan (26450267 to S. Tsutsui and Several protein–protein (13), protein–lipid (14), and protein– 22780171 to S. Tasumi). S. Tasumi was also funded by the Towa Foundation for Food carbohydrate (13, 15, 16) interactions have been shown to mediate Research and the Lotte Shigemitsu Prize. host–parasite relationships. Among these, carbohydrate interac- Address correspondence and reprint requests to Dr. Satoshi Tasumi or Dr. Shigeyuki tions are known to trigger parasitism in some marine parasites. For Tsutsui, The University of Tokyo, Shizuoka 431-0214, Japan (S. Tasumi) or Kitasato University, 1-15-1 Kitasato, Kanagawa 252-0373, Japan (S. Tsutsui). E-mail ad- example, a tandem-repeat galectin that is produced by hemocytes dresses: [email protected] (S. Tasumi) or [email protected] of the eastern oyster Crassostrea virginica is used as an entry (S. Tsutsui) receptor by the protozoa Perkinsus marinus (17–19). Similarly, The online version of this article contains supplemental material. oncomiracidia of the monogenean species Neobenedenia girellae Abbreviations used in this article: CBB, Coomassie Brilliant Blue; FSW, filtration- Benedenia seriolae sterilized seawater; LC-MS/MS, liquid chromatography–tandem mass spectrometry; and are likely to recognize glycoproteins of ms-IgM, D-mannose-specific IgM; non-ms–IgM, IgM without D-mannose affinity; their hosts, as indicated by suppression of parasite attachment- QTL, quantitative trait locus; TBS (+), 25 mM Tris-HCl buffer (pH 7.5) containing inducing capacities of skin mucus extract by plant lectins (20, 150 mM NaCl, 10 mM CaCl , and 10 mM MgCl . 2 2 21). Furthermore, N. girellae reportedly recognizes T. rubripes Copyright Ó 2017 by The American Association of Immunologists, Inc. 0022-1767/17/$30.00 skin mucosa using the glycoprotein Wap65-2 (22). Hence, www.jimmunol.org/cgi/doi/10.4049/jimmunol.1601996 4108 A PARASITE UTILIZING HOST IgM FOR HOST RECOGNITION interactions via carbohydrates may be central to T. rubripes host recognition by H. okamotoi. In our previous studies, we identified two D-mannose–specific lectins in gill and skin mucus of T. rubripes.Amongthese,the 13-kDa lily-type lectin pufflectin binds adult H. okamotoi (6). Moreover, pufflectin protein and mRNA expression in gills is much higher in T. rubripes than in the closely related species T. niphobles (23), which is resistant to this parasite, suggesting participation of this lectin in parasitism. The other mucus lectin kalliklectin is homologous to the H chain of mammalian plasma kallikrein (24), although its role has not yet been clarified. Thus, in the current study, we focused on the D-mannose–binding fraction of fugu mucus and hypothesized that FIGURE 2. Effects of the purified D-mannose–binding fraction on it participates in the host recognition of H. okamotoi. Initially, we deciliation of H. okamotoi oncomiracidia and SDS-PAGE patterns of the determined whether oncomiracidia cause deciliation when exposed to fraction. (A) The D-mannose–binding fraction was purified from fugu the fraction and then identified the molecules involved. In these ex- mucus using D-mannose affinity chromatography. FSW or the purified periments, the D-mannose–binding fraction induced the deciliation of D-mannose–binding fraction was added to wells containing ∼10 oncomir- oncomiracidia, but the deciliation-inducing protein was a D-mannose- acidia, and percentages of deciliated individuals were calculated. Values specific IgM
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