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Resembling Those of Antigen Receptors Receptor Family with A Hagfish Leukocytes Express a Paired Receptor Family with a Variable Domain Resembling Those of Antigen Receptors This information is current as Takashi Suzuki, Tadasu Shin-I, Asao Fujiyama, Yuji Kohara of September 29, 2021. and Masanori Kasahara J Immunol 2005; 174:2885-2891; ; doi: 10.4049/jimmunol.174.5.2885 http://www.jimmunol.org/content/174/5/2885 Downloaded from References This article cites 37 articles, 11 of which you can access for free at: http://www.jimmunol.org/content/174/5/2885.full#ref-list-1 http://www.jimmunol.org/ Why The JI? Submit online. • 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 by guest on September 29, 2021 *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 © 2005 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology Hagfish Leukocytes Express a Paired Receptor Family with a Variable Domain Resembling Those of Antigen Receptors1,2 Takashi Suzuki,* Tadasu Shin-I,§ Asao Fujiyama,†¶ʈ Yuji Kohara,‡§ and Masanori Kasahara3* Jawed vertebrates are equipped with TCR and BCR with the capacity to rearrange their V domains. By contrast, jawless vertebrates, represented by hagfish and lampreys, apparently lack such receptors. We describe in this study a family of hagfish genes carrying a single V-type domain resembling those of TCR/BCR. This multigene family, which we call agnathan paired receptors resembling Ag receptors (APAR), is expressed in leukocytes and predicted to encode a group of membrane glycoproteins with organizations characteristic of paired Ig-like receptors, consisting of activating and inhibitory forms. APAR has a J region in its V-type domain, and its V and J regions are encoded in a single exon. Thus, APAR is a member of the emerging families of diversified, innate immune-type receptors with TCR/BCR-like V-type domains and has many of the features expected for a primordial TCR/BCR-like receptor. The extracellular domain of APAR may be descended from a V-type domain postulated to Downloaded from have acquired recombination signal sequences in a jawed vertebrate lineage. The Journal of Immunology, 2005, 174: 2885–2891. wo types of Ag receptor, TCR and BCR, are central ele- call agnathan paired receptors resembling Ag receptors (APAR).4 ments of the adaptive immune system. Through recom- The overall domain organization of APAR resembles those of T bining V and J or V, D, and J gene fragments, they gen- novel immune-type receptors (NITR) (14) and signal-regulatory erate enormous variability in their Ag-binding regions (1, 2). proteins (SIRP) (15) in that it is a member of paired Ig-like re- http://www.jimmunol.org/ Although the strategies for generating BCR diversity differ in an- ceptor families carrying TCR/BCR-like, V-type domains. The imals in different taxa, all jawed vertebrates, including the most close structural similarity of the V-type domain of APAR to those phylogenetically primitive extant representatives, such as sharks, of TCR/BCR (and, to a lesser extent, those of NITR) reinforces an are equipped with both TCR and BCR (3–6). By sharp contrast, all evolutionary link between innate and adaptive immune receptors attempts to identify TCR, BCR, or MHC have been unsuccessful (16, 17) and raises the possibility that the V-type domain of APAR in jawless vertebrates and invertebrates (7–10), suggesting that is descended from a hypothetical V-type domain that, after inser- these molecules exist only in jawed vertebrates. Indeed, recent tion of recombination signal sequences (RSS), gave rise to the V work in the sea lamprey indicates that this jawless vertebrate regions of TCR/BCR in a jawed vertebrate lineage. mounts anticipatory immune responses by using a novel receptor by guest on September 29, 2021 structurally unrelated to TCR or BCR (11). Materials and Methods As the most advanced animals with no clear evidence for the Animals presence of TCR or BCR, the jawless fish represented by hagfish and lampreys offer unique opportunities for investigating the origin Adult hagfishes, E. burgeri, were captured in the Pacific Ocean off the coast of Misaki, Kanagawa Prefecture, Japan. of Ag receptors (12). As an initial step in understanding their im- mune systems, we recently conducted large-scale expressed se- Screening of the cDNA library quence tag analysis of leukocytes isolated from the inshore hag- A cDNA clone predicted to encode a TCR/BCR-like V-type domain was fish, Eptatretus burgeri (13). Although this survey yielded no identified in the course of expressed sequence tag analysis of hagfish leu- evidence for the existence of TCR, BCR, or MHC, we found a kocytes. Part of this clone (nt positions 86–426; GenBank accession no. cDNA clone predicted to encode a V-type Ig domain resembling AB177615) was used as a probe to screen the leukocyte cDNA library 5 those of TCR/BCR. In this study we show that this cDNA clone prepared from two individuals of adult hagfish (13). A total of 5 ϫ 10 encodes a member of the paired Ig-like receptor family, which we clones were screened with a digoxigenin (DIG)-labeled probe as previously described (18) following the instructions of the manufacturer (Roche). Hy- bridization was performed at 38°C in a DIG Easy Hyb solution (Roche). Final washing conditions were 1ϫ SSC/0.1% SDS at 50°C. *Department of Biosystems Science, School of Advanced Sciences, and Departments Southern blot analysis of †Informatics and ‡Genetics, School of Life Sciences, Graduate University for Ad- vanced Studies (Sokendai), Hayama, Japan; §Center for Genetic Resource Informa- Genomic DNAs digested by restriction enzymes were size-fractionated on tion and ¶Division of Theoretical Genetics, National Institute of Genetics, Mishima, a 0.8% agarose gel, blotted to a nylon membrane, and hybridized with Japan; and ʈInformation Research Division, National Institute of Informatics, Tokyo, DIG-labeled probes according to the instructions of the manufacturer Japan (Roche) as previously described (19). Hybridization was performed at Received for publication August 17, 2004. Accepted for publication December 3, 2004. 3 Address correspondence and reprint requests to Dr. Masanori Kasahara at his current ad- The costs of publication of this article were defrayed in part by the payment of page dress: Department of Pathology, Hokkaido University Graduate School of Medicine, North-15 charges. This article must therefore be hereby marked advertisement in accordance West-7, Sapporo 060-8638, Japan. E-mail address: [email protected] with 18 U.S.C. Section 1734 solely to indicate this fact. 4 Abbreviations used in this paper: APAR, agnathan paired receptor resembling Ag 1 This work was supported by a Grant-in-Aid for Scientific Research on Priority Areas receptor; BAC, bacterial artificial chromosome; CP, connecting peptide; CYT, cyto- (C) Genome Science from the Ministry of Education, Culture, Sports, Science, and plasmic tail; DIG, digoxigenin; NAR, nurse shark novel Ag receptor; NICIR, novel Technology of Japan. ITAM-containing Ig superfamily receptor; NITR, novel immune-type receptor; RSS, 2 Sequence data reported in this paper have been submitted to the DDBJ/EMBL/GenBank recombination signal sequence; SIRP, signal regulatory protein; TM, transmembrane; databases under accession numbers AB177610–AB177620. UTR, untranslated region; VCBP, V region-containing chitin-binding protein. Copyright © 2005 by The American Association of Immunologists, Inc. 0022-1767/05/$02.00 2886 AGNATHAN PAIRED RECEPTORS RESEMBLING Ag RECEPTORS 42°C in a DIG Easy Hyb solution. Final washing conditions were 2ϫ made up of six distinct sequences (B1–B6) and predicted type I SSC/0.1% SDS at 45°C. membrane proteins with a single extracellular V-type domain, fol- Real-time quantitative PCR lowed by the CP, the TM region without any charged residues, and the CYT containing an ITIM. Thus, the APAR gene family has Expression patterns of APAR were analyzed by real-time RT-PCR using a features characteristic of paired Ig-like receptors (14, 22, 23); GeneAmp 5700 sequence detection system (Applied Biosystems). Briefly, total cellular RNAs isolated from leukocytes and various organs of adult APAR-A molecules are likely to associate with an adaptor mole- hagfish were converted to cDNA with the Superscript II kit (Invitrogen cule with an ITAM and function as activating receptors. In con- Life Technologies). PCR was set up in triplicate on 2 ␮l (20 ng) of cDNA trast, APAR-B molecules are likely to function as inhibitory using a SYBR Green PCR kit (Applied Biosystems). Primer sequences receptors. were 5Ј-TCATCAGGAAATGGAAGATTGA-3Ј and 5Ј-AATACACAGT TGGGTTGCTGGA-3Ј for the activating form of APAR,5Ј-ACAGTCTT Signal peptides of 27 and 25 aa residues were predicted for GGTGTTTGCGAGA-3Ј and 5Ј-ATCTTCCAGTGTGCCATTTCC-3Ј for APAR-A and APAR-B, respectively. Thus, mature APAR-A pro- the inhibitory form of APAR, and 5Ј-AACCCATGGAAAATGGAAGG-3Ј teins would contain 238–264 aa, with a calculated molecular mass Ј Ј and 5 -GTCACGCTCCTGGAAAACTG-3 for GAPDH (a reference of 26,616–29,839; mature APAR-B proteins are predicted to have housekeeping gene). Cycling conditions were one cycle at 50°C for 2 min, one cycle at 95°C for 10 min, followed by 40 cycles of denaturation at 258–264 aa, with a calculated molecular mass of 28,315–29,078.
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