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Analysis of the Chinese Alligator Tcrα/Δ Loci Reveals the Evolutionary Pattern of Atypical Tcrδ/Tcrµ in Tetrapods

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Analysis of the Chinese Alligator Tcrα/Δ Loci Reveals the Evolutionary Pattern of Atypical Tcrδ/Tcrµ in Tetrapods Analysis of the Chinese Alligator TCRα/δ Loci Reveals the Evolutionary Pattern of Atypical TCRδ/TCRµ in Tetrapods This information is current as Xifeng Wang, Jinwei Huang, Peng Wang, Renping Wang, of October 6, 2021. Chaolin Wang, Di Yu, Cuncun Ke, Tian Huang, Yu Song, Jianhui Bai, Kongpan Li, Liming Ren, Robert D. Miller, Haitang Han, Xin Zhou and Yaofeng Zhao J Immunol published online 26 June 2020 http://www.jimmunol.org/content/early/2020/06/25/jimmun ol.2000257 Downloaded from Supplementary http://www.jimmunol.org/content/suppl/2020/06/25/jimmunol.200025 Material 7.DCSupplemental 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 October 6, 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 © 2020 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Published June 26, 2020, doi:10.4049/jimmunol.2000257 The Journal of Immunology Analysis of the Chinese Alligator TCRa/d Loci Reveals the Evolutionary Pattern of Atypical TCRd/TCRm in Tetrapods Xifeng Wang,*,1 Jinwei Huang,†,1 Peng Wang,†,1 Renping Wang,‡ Chaolin Wang,‡ Di Yu,† Cuncun Ke,† Tian Huang,x Yu Song,† Jianhui Bai,† Kongpan Li,† Liming Ren,† Robert D. Miller,{ Haitang Han,† Xin Zhou,* and Yaofeng Zhao† Atypical TCRd found in sharks, amphibians, birds, and monotremes and TCRm found in monotremes and marsupials are TCR chains that use Ig or BCR-like variable domains (VHd/Vm) rather than conventional TCR V domains. These unconventional TCR are consistent with a scenario in which TCR and BCR, although having diverged from each other more than 400 million years ago, continue to exchange variable gene segments in generating diversity for Ag recognition. However, the process underlying this exchange and leading to the evolution of these atypical TCR receptor genes remains elusive. In this study, we identified a d a d d a two TCR / gene loci in the Chinese alligator (Alligator sinensis). In total, there were 144 V, 154 J , nine J , eight D , two C , Downloaded from and five Cd gene segments in the TCRa/d loci of the Chinese alligator, representing the most complicated TCRa/d gene system in both genomic structure and gene content in any tetrapod examined so far. A pool of 32 VHd genes divided into 18 subfamilies was found to be scattered over the two loci. Phylogenetic analyses revealed that these VHd genes could be related to bird VHd genes, VHd/Vm genes in platypus or opossum, or alligator VH genes. Based on these findings, a model explaining the evolutionary pattern of atypical TCRd/TCRm genes in tetrapods is proposed. This study sheds new light on the evolution of TCR and BCR genes, two of the most essential components of adaptive immunity. The Journal of Immunology, 2020, 205: 000–000. http://www.jimmunol.org/ cell receptors play a significant role in the specific rec- These have been found in all jawed vertebrates, with only the ognition of pathogen-associated epitopes (1). Four TCR squamate reptiles appearing to have lost the g/d TCR (2, 3). These T chains, called a, b, g, and d, are expressed as hetero- polypeptide chains are encoded by the TCRa, TCRb, TCRg, and dimers either as a with b on ab T cells or g with d on gd T cells. TCRd genes, respectively (4, 5). Generally, the TCRb and TCRg are encoded by their own loci present on separate chromosomes. The TCRd locus, in contrast, is nested within the TCRa locus at a *Beijing Advanced Innovation Center for Food Nutrition and Human Health, College separate chromosomal location (5, 6). of Plant Protection, China Agricultural University, Beijing 100193, People’s Repub- by guest on October 6, 2021 lic of China; †State Key Laboratory of Agrobiotechnology, College of Biological Like Igs, TCRs generate diverse binding specificities to Ags by Sciences, National Engineering Laboratory for Animal Breeding, China Agricultural undergoing somatic recombination of V(D)J segments (7, 8). The University, Beijing 100193, People’s Republic of China; ‡Administration Bureau of Alligator sinensis National Nature Reserve Protection, Anhui 242000, People’s Re- TCR and Ig genes share a common origin in jawed vertebrates; the public of China; xHenan Engineering Laboratory for Mammary Bioreactor, School of conventional variable domain genes (TCRV) are estimated to have Life Sciences, Henan University, Kaifeng 475004, Henan, People’s Republic of { diverged from IgV genes ∼400 million years ago, and the two are China; and Department of Biology, Center for Evolutionary and Theoretical Immu- nology, University of New Mexico, Albuquerque, NM 87131 readily distinguishable (9, 10). Interestingly, V genes, which are 1X.W., J.H., and P.W. contributed equally to this work. indistinguishable from IgH V genes (VH), have recently been ORCIDs: 0000-0001-8298-0177 (D.Y.); 0000-0002-8479-8819 (R.D.M.); 0000- identified within TCR gene loci of several vertebrates and are used 0002-1407-7952 (X.Z.); 0000-0003-4499-8610 (Y.Z.). in generating the TCR repertoire (10–16). Received for publication March 11, 2020. Accepted for publication May 22, 2020. Such atypical TCRV genes were first identified in an additional This work was supported by the National Natural Science Foundation of China TCR locus, named TCRm, found, so far, only in marsupials and (31472085 and 31772589), the Program of Introducing Talents of Discipline to Univer- monotremes (10, 12, 13, 17). TCRm genes are unlinked to those sities, Plan 111 (B12008), and funding from the Beijing Advanced Innovation Center for gene loci that encode conventional TCR chains and, in marsupials, Food Nutrition and Human Health, China Agricultural University. R.D.M. was supported in part by National Institute of General Medical Sciences of the National Institutes of are organized in tandem repeats of a core unit: Vm–Dmn–Jm–Vmj– Health Award P30 GM110907 and National Science Foundation Award IOS-13531232. Cm (12, 17). Most notably, the Cm genes related to Cd, whereas the The sequences presented in this article have been submitted to the National Center Vm genes are more related to VH genes than to conventional TCRV for Biotechnology Information GenBank (https://www.ncbi.nlm.nih.gov/genbank/) genes (12, 17). Furthermore, TCRm chains are predicted to have an under accession numbers MT081963 and MT081964. extracellular atypical structure, containing three extracellular IgSF Address correspondence and reprint requests to Dr. Haitang Han and Prof. Yaofeng Zhao or Prof. Xin Zhou, State Key Laboratory of Agrobiotechnology, College of Biological Sci- domains rather than conventional two due an extra V domain (12). ences, China Agricultural University, 2 Yuanmingyuan Western Road, Beijing 100193, The N-terminal V of marsupial TCRm (Vm) is encoded by somati- People’s Republic of China (H.H. and Y.Z.) or Beijing Advanced Innovation Center for cally recombined VDJ segments, whereas the C-proximal V domain Food Nutrition and Human Health, College of Plant Protection, China Agricultural Univer- sity, 2 Yuanmingyuan Western Road, Beijing 100193, People’s Republic of China (X.Z.). (Vmj) is encoded by an exon in which the V and J genes are already E-mail addresses: [email protected] (H.H.) and [email protected] (Y.Z.) or prejoined in the germline DNA, and it is relatively invariant (12, 13, [email protected] (X.Z.) 17). In the platypus, the C-proximal V domain still requires somatic The online version of this article contains supplemental material. recombination of a V and J segment (17). Abbreviations used in this article: BAC, bacterial artificial chromosome; RSS, re- So far, TCRm homologs have not been found in nonmammalian combination signal sequence. species (12, 13, 17). However, in primordial jawed vertebrates, such Copyright Ó 2020 by The American Association of Immunologists, Inc. 0022-1767/20/$37.50 as sharks and other cartilaginous fish, a TCR chain structurally www.jimmunol.org/cgi/doi/10.4049/jimmunol.2000257 2 ANALYSIS OF THE CHINESE ALLIGATOR TCRa/d LOCI similar to TCRm has been identified, called NAR-TCR. NAR- protocol. Various tissues of Chinese alligator were provided by the TCR also employs two V domains, each encoded by separate, Administration Bureau of Chinese Alligator National Nature Reserve somatically rearranging VDJ segments (11, 18). The distal V domain Protection of Anhui Province. Total RNA was extracted from the spleen and thymus using a TRIzol kit (TIAGEN Biotech, Beijing, China) of NAR-TCR is more closely related to the V domains of IgNAR according to the manufacturer’s instructions. Reverse transcription was than to the V domains of conventional TCR. IgNAR is an H chain conducted using Moloney Murine Leukemia Virus Reverse Transcrip- homodimer that is not associated with light chains and is found only tase (Promega, Madison, WI) with an oligo(dT) adapter primer. Our in cartilaginous fish (19, 20). It can be assumed that the structures of studieswereapprovedbytheAnimalCareandUseCommitteeofChina Agricultural University. TCRm and NAR-TCR may represent an ancient receptor system. However, phylogenetic analysis and structure are consistent with Bacterial artificial chromosome screening NAR-TCR and TCRm being more likely the results of convergent Based on the sequences of TCR Ca and TCR Cd derived from chicken evolution rather than being related by direct descent (10, 17).
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