{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T20:14:35Z","timestamp":1790712875472,"version":"4.1.0"},"reference-count":43,"publisher":"Oxford University Press (OUP)","issue":"10","license":[{"start":{"date-parts":[[2017,5,1]],"date-time":"2017-05-01T00:00:00Z","timestamp":1493596800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2017,5,15]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>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 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\u2013binding fractions from fugu mucus. Using liquid chromatography\u2013tandem mass spectrometry analysis, proteins contained in the fraction were identified as d-mannose\u2013specific IgM with two d-mannose\u2013binding 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 d-mannose\u2013specific 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\u2013binding IgM in gill mucus were sufficient to induce deciliation in vitro, indicating that H. okamotoi parasites initially use host Abs to colonize host gills.<\/jats:p>","DOI":"10.4049\/jimmunol.1601996","type":"journal-article","created":{"date-parts":[[2017,4,13]],"date-time":"2017-04-13T00:40:15Z","timestamp":1492044015000},"page":"4107-4114","source":"Crossref","is-referenced-by-count":24,"title":["Mucosal IgM Antibody with <scp>d<\/scp>-Mannose Affinity in Fugu <i>Takifugu rubripes<\/i> Is Utilized by a Monogenean Parasite <i>Heterobothrium okamotoi<\/i> for Host Recognition"],"prefix":"10.1093","volume":"198","author":[{"given":"Kento","family":"Igarashi","sequence":"first","affiliation":[{"name":"School of Marine Biosciences, Kitasato University , Kanagawa 252-0373,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ryohei","family":"Matsunaga","sequence":"additional","affiliation":[{"name":"Fisheries Laboratory, The University of Tokyo , Shizuoka 431-0214,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sachi","family":"Hirakawa","sequence":"additional","affiliation":[{"name":"Faculty of Marine Bioscience, Fukui Prefectural University , Fukui 917-0003,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sho","family":"Hosoya","sequence":"additional","affiliation":[{"name":"Fisheries Laboratory, The University of Tokyo , Shizuoka 431-0214,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hiroaki","family":"Suetake","sequence":"additional","affiliation":[{"name":"Faculty of Marine Bioscience, Fukui Prefectural University , Fukui 917-0003,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kiyoshi","family":"Kikuchi","sequence":"additional","affiliation":[{"name":"Fisheries Laboratory, The University of Tokyo , Shizuoka 431-0214,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuzuru","family":"Suzuki","sequence":"additional","affiliation":[{"name":"Fisheries Laboratory, The University of Tokyo , Shizuoka 431-0214,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Osamu","family":"Nakamura","sequence":"additional","affiliation":[{"name":"School of Marine Biosciences, Kitasato University , Kanagawa 252-0373,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Toshiaki","family":"Miyadai","sequence":"additional","affiliation":[{"name":"Faculty of Marine Bioscience, Fukui Prefectural University , Fukui 917-0003,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Satoshi","family":"Tasumi","sequence":"additional","affiliation":[{"name":"Fisheries Laboratory, The University of Tokyo , Shizuoka 431-0214,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shigeyuki","family":"Tsutsui","sequence":"additional","affiliation":[{"name":"School of Marine Biosciences, Kitasato University , Kanagawa 252-0373,","place":["Japan"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2017,5,15]]},"reference":[{"key":"2025030615130960600_r1","doi-asserted-by":"crossref","first-page":"1346","DOI":"10.1016\/j.dci.2011.11.009","article-title":"Mucosal immunoglobulins and B cells of teleost fish","volume":"35","author":"Salinas","year":"2011","journal-title":"Dev. Comp. Immunol."},{"key":"2025030615130960600_r2","doi-asserted-by":"crossref","first-page":"6919","DOI":"10.1073\/pnas.0500027102","article-title":"Discovery of a unique Ig heavy-chain isotype (IgT) in rainbow trout: implications for a distinctive B cell developmental pathway in teleost fish","volume":"102","author":"Hansen","year":"2005","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2025030615130960600_r3","doi-asserted-by":"crossref","first-page":"5682","DOI":"10.4049\/jimmunol.178.9.5682","article-title":"A teleost polymeric Ig receptor exhibiting two Ig-like domains transports tetrameric IgM into the skin","volume":"178","author":"Hamuro","year":"2007","journal-title":"J. Immunol."},{"key":"2025030615130960600_r4","doi-asserted-by":"crossref","first-page":"13097","DOI":"10.1073\/pnas.1304319110","article-title":"Teleost skin, an ancient mucosal surface that elicits gut-like immune responses","volume":"110","author":"Xu","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2025030615130960600_r5","doi-asserted-by":"crossref","first-page":"12008","DOI":"10.1074\/jbc.272.18.12008","article-title":"Isolation and characterization of pleurocidin, an antimicrobial peptide in the skin secretions of winter flounder","volume":"272","author":"Cole","year":"1997","journal-title":"J. Biol. Chem."},{"key":"2025030615130960600_r6","doi-asserted-by":"crossref","first-page":"20882","DOI":"10.1074\/jbc.M301038200","article-title":"Lectins homologous to those of monocotyledonous plants in the skin mucus and intestine of pufferfish, Fugu rubripes","volume":"278","author":"Tsutsui","year":"2003","journal-title":"J. Biol. Chem."},{"key":"2025030615130960600_r7","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1016\/j.dci.2004.06.005","article-title":"Demonstration of the mucosal lectins in the epithelial cells of internal and external body surface tissues in pufferfish (Fugu rubripes)","volume":"29","author":"Tsutsui","year":"2005","journal-title":"Dev. Comp. Immunol."},{"key":"2025030615130960600_r8","doi-asserted-by":"crossref","first-page":"683","DOI":"10.1016\/j.fsi.2007.01.018","article-title":"Possible immune functions of congerin, a mucosal galectin, in the intestinal lumen of Japanese conger eel","volume":"23","author":"Nakamura","year":"2007","journal-title":"Fish Shellfish Immunol."},{"key":"2025030615130960600_r9","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/j.cbpc.2004.02.004","article-title":"Two novel muramidases from skin mucosa of rainbow trout (Oncorhynchus mykiss)","volume":"138","author":"Fernandes","year":"2004","journal-title":"Comp. Biochem. Physiol. B Biochem. Mol. Biol."},{"key":"2025030615130960600_r10","first-page":"388","article-title":"Redescription of Heterobothrium tetrodonis (Goto, 1894) (Monogenea: Diclidophoridae) and other related new species from puffers of the genus Takifigu (Teleost: Tetraodontidae)","volume":"40","author":"Ogawa","year":"1991","journal-title":"J. Parasitol."},{"key":"2025030615130960600_r11","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/j.ijpara.2006.09.005","article-title":"Involvement of host recognition by oncomiracidia and post-larval survivability in the host specificity of Heterobothrium okamotoi (Monogenea: Diclidophoridae)","volume":"37","author":"Ohhashi","year":"2007","journal-title":"Int. J. Parasitol."},{"key":"2025030615130960600_r12","first-page":"295","volume-title":"Monogenoidea.","author":"Roberts","year":"2009"},{"key":"2025030615130960600_r13","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1111\/j.1600-065X.2010.00990.x","article-title":"Invasion and intracellular survival by protozoan parasites","volume":"240","author":"Sibley","year":"2011","journal-title":"Immunol. Rev."},{"key":"2025030615130960600_r14","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1016\/j.pt.2012.07.002","article-title":"Sink or swim: lipid rafts in parasite pathogenesis","volume":"28","author":"Goldston","year":"2012","journal-title":"Trends Parasitol."},{"key":"2025030615130960600_r15","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1016\/j.sbi.2010.08.003","article-title":"Apicomplexan parasite adhesins: novel strategies for targeting host cell carbohydrates","volume":"20","author":"Boulanger","year":"2010","journal-title":"Curr. Opin. Struct. Biol."},{"key":"2025030615130960600_r16","doi-asserted-by":"crossref","first-page":"560","DOI":"10.1016\/j.sbi.2010.06.008","article-title":"Carbohydrate binding molecules in malaria pathology","volume":"20","author":"Brown","year":"2010","journal-title":"Curr. Opin. Struct. Biol."},{"key":"2025030615130960600_r17","doi-asserted-by":"crossref","first-page":"3086","DOI":"10.4049\/jimmunol.179.5.3086","article-title":"A galectin of unique domain organization from hemocytes of the Eastern oyster (Crassostrea virginica) is a receptor for the protistan parasite Perkinsus marinus","volume":"179","author":"Tasumi","year":"2007","journal-title":"J. Immunol."},{"key":"2025030615130960600_r18","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1038\/nrmicro2146","article-title":"Roles of galectins in infection","volume":"7","author":"Vasta","year":"2009","journal-title":"Nat. Rev. Microbiol."},{"key":"2025030615130960600_r19","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1007\/978-1-4614-0106-3_2","article-title":"Galectins as pattern recognition receptors: structure, function, and evolution","volume":"946","author":"Vasta","year":"2012","journal-title":"Adv. Exp. Med. Biol."},{"key":"2025030615130960600_r20","first-page":"214","article-title":"Attachment-inducing capacities of fish tissue extracts on oncomiracidia of Neobenedenia girellae (Monogenea, Capsalidae)","volume":"86","author":"Yoshinaga","year":"2000","journal-title":"J. Parasitol."},{"key":"2025030615130960600_r21","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1016\/S0020-7519(01)00339-3","article-title":"Attachment-inducing capacities of fish skin epithelial extracts on oncomiracidia of Benedenia seriolae (Monogenea: Capsalidae)","volume":"32","author":"Yoshinaga","year":"2002","journal-title":"Int. J. Parasitol."},{"key":"2025030615130960600_r22","doi-asserted-by":"crossref","first-page":"1483","DOI":"10.1016\/j.ijpara.2007.04.024","article-title":"Purification and identification of a glycoprotein that induces the attachment of oncomiracidia of Neobenedenia girellae (Monogenea, Capsalidae)","volume":"37","author":"Ohashi","year":"2007","journal-title":"Int. J. Parasitol."},{"key":"2025030615130960600_r23","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.dci.2016.01.007","article-title":"Identification and characterization of pufflectin from the grass pufferfish Takifugu niphobles and comparison of its expression with that of Takifugu rubripes","volume":"59","author":"Tasumi","year":"2016","journal-title":"Dev. Comp. Immunol."},{"key":"2025030615130960600_r24","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1093\/jb\/mvv033","article-title":"Fugu (Takifugu rubripes) serum GlcNAc-binding lectin is a kalliklectin but has different properties from those of a reported homologue","volume":"158","author":"Tsutsui","year":"2015","journal-title":"J. Biochem."},{"key":"2025030615130960600_r25","doi-asserted-by":"crossref","first-page":"215","DOI":"10.3147\/jsfp.35.215","article-title":"Standardized method for experimental infection of tiger puffer Takifugu rubripes with oncomiracidia of Heterobothrium okamotoi (Monogenea: Diclidophoridae) with some data on the oncomiracidial biology","volume":"35","author":"Chigasaki","year":"2000","journal-title":"Fish Pathol."},{"key":"2025030615130960600_r26","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.dci.2013.03.018","article-title":"Serum GlcNAc-binding IgM of fugu (Takifugu rubripes) suppresses the growth of fish pathogenic bacteria: a novel function of teleost antibody","volume":"41","author":"Tsutsui","year":"2013","journal-title":"Dev. Comp. Immunol."},{"key":"2025030615130960600_r27","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1016\/j.fsi.2004.03.005","article-title":"Monoclonal antibodies recognising serum immunoglobulins and surface immunoglobulin-positive cells of puffer fish, torafugu (Takifugu rubripes)","volume":"17","author":"Miyadai","year":"2004","journal-title":"Fish Shellfish Immunol."},{"key":"2025030615130960600_r28","doi-asserted-by":"crossref","first-page":"909","DOI":"10.1016\/j.ijpara.2013.06.006","article-title":"Genomic regions of pufferfishes responsible for host specificity of a monogenean parasite, Heterobothrium okamotoi","volume":"43","author":"Hosoya","year":"2013","journal-title":"Int. J. Parasitol."},{"key":"2025030615130960600_r29","doi-asserted-by":"crossref","first-page":"604","DOI":"10.1038\/356604a0","article-title":"Tumour necrosis factor \u03b1 restores granulomas and induces parasite egg-laying in schistosome-infected SCID mice","volume":"356","author":"Amiri","year":"1992","journal-title":"Nature"},{"key":"2025030615130960600_r30","doi-asserted-by":"crossref","first-page":"763","DOI":"10.1038\/312763a0","article-title":"The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus","volume":"312","author":"Dalgleish","year":"1984","journal-title":"Nature"},{"key":"2025030615130960600_r31","doi-asserted-by":"crossref","first-page":"66","DOI":"10.3389\/fimmu.2012.00066","article-title":"Protective roles of natural IgM antibodies","volume":"3","author":"Gr\u00f6nwall","year":"2012","journal-title":"Front. Immunol."},{"key":"2025030615130960600_r32","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1146\/annurev-immunol-032713-120140","article-title":"Natural antibody repertoires: development and functional role in inhibiting allergic airway disease","volume":"33","author":"Kearney","year":"2015","journal-title":"Annu. Rev. Immunol."},{"key":"2025030615130960600_r33","doi-asserted-by":"crossref","first-page":"6174","DOI":"10.1128\/jvi.71.8.6174-6178.1997","article-title":"Sensitization of rhabdo-, lenti-, and spumaviruses to human serum by galactosyl(alpha1-3)galactosylation","volume":"71","author":"Takeuchi","year":"1997","journal-title":"J. Virol."},{"key":"2025030615130960600_r34","doi-asserted-by":"crossref","first-page":"418","DOI":"10.1016\/j.dci.2011.08.012","article-title":"Serum carbohydrate-binding IgM are present in Vietnamese striped catfish (Pangasianodon hypophthalmus) but not in North African catfish (Clarias gariepinus)","volume":"36","author":"Giang","year":"2012","journal-title":"Dev. Comp. Immunol."},{"key":"2025030615130960600_r35","doi-asserted-by":"crossref","first-page":"851","DOI":"10.1038\/nmeth803","article-title":"Evanescent-field fluorescence-assisted lectin microarray: a new strategy for glycan profiling","volume":"2","author":"Kuno","year":"2005","journal-title":"Nat. Methods"},{"key":"2025030615130960600_r36","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1111\/j.1600-065X.1998.tb01258.x","article-title":"Varied redox forms of teleost IgM: an alternative to isotypic diversity?","volume":"166","author":"Kaattari","year":"1998","journal-title":"Immunol. Rev."},{"key":"2025030615130960600_r37","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/S0020-7519(01)00332-0","article-title":"Interactions between monogenean parasites and their fish hosts","volume":"32","author":"Buchmann","year":"2002","journal-title":"Int. J. Parasitol."},{"key":"2025030615130960600_r38","doi-asserted-by":"crossref","first-page":"623","DOI":"10.1093\/molbev\/msn283","article-title":"Explosive speciation of Takifugu: another use of fugu as a model system for evolutionary biology","volume":"26","author":"Yamanoue","year":"2009","journal-title":"Mol. Biol. Evol."},{"key":"2025030615130960600_r39","doi-asserted-by":"crossref","first-page":"590","DOI":"10.1111\/j.1558-5646.2012.01781.x","article-title":"The genetic architecture of growth rate in juvenile Takifugu species","volume":"67","author":"Hosoya","year":"2013","journal-title":"Evolution"},{"key":"2025030615130960600_r40","doi-asserted-by":"crossref","first-page":"1301","DOI":"10.1126\/science.1072104","article-title":"Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes","volume":"297","author":"Aparicio","year":"2002","journal-title":"Science"},{"key":"2025030615130960600_r41","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1534\/genetics.105.042051","article-title":"A genetic linkage map for the tiger pufferfish, Takifugu rubripes","volume":"171","author":"Kai","year":"2005","journal-title":"Genetics"},{"key":"2025030615130960600_r42","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1093\/gbe\/evr041","article-title":"Integration of the genetic map and genome assembly of fugu facilitates insights into distinct features of genome evolution in teleosts and mammals","volume":"3","author":"Kai","year":"2011","journal-title":"Genome Biol. Evol."},{"key":"2025030615130960600_r43","doi-asserted-by":"crossref","first-page":"2039","DOI":"10.1534\/genetics.106.069278","article-title":"The sex-determining locus in the tiger pufferfish, Takifugu rubripes","volume":"175","author":"Kikuchi","year":"2007","journal-title":"Genetics"}],"container-title":["The Journal of Immunology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/jimmunol\/article-pdf\/198\/10\/4107\/61449619\/1601996.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jimmunol\/article-pdf\/198\/10\/4107\/61449619\/1601996.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,3,6]],"date-time":"2025-03-06T17:31:02Z","timestamp":1741282262000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jimmunol\/article\/198\/10\/4107\/7954949"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,5]]},"references-count":43,"journal-issue":{"issue":"10","published-print":{"date-parts":[[2017,5,15]]}},"URL":"https:\/\/doi.org\/10.4049\/jimmunol.1601996","relation":{},"ISSN":["0022-1767","1550-6606"],"issn-type":[{"value":"0022-1767","type":"print"},{"value":"1550-6606","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2017,5]]},"published":{"date-parts":[[2017,5]]}}}