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“Primordial Immune Complex”: Origins of MHC Class I and Antigen Receptors Revealed by Comparative Genomics

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“Primordial Immune Complex”: Origins of MHC Class I and Antigen Receptors Revealed by Comparative Genomics Inferring the ''Primordial Immune Complex'': Origins of MHC Class I and Antigen Receptors Revealed by Comparative Genomics This information is current as of September 29, 2021. Yuko Ohta, Masanori Kasahara, Timothy D. O'Connor and Martin F. Flajnik J Immunol published online 6 September 2019 http://www.jimmunol.org/content/early/2019/09/05/jimmun ol.1900597 Downloaded from Supplementary http://www.jimmunol.org/content/suppl/2019/09/06/jimmunol.190059 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 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 © 2019 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Published September 6, 2019, doi:10.4049/jimmunol.1900597 The Journal of Immunology Inferring the “Primordial Immune Complex”: Origins of MHC Class I and Antigen Receptors Revealed by Comparative Genomics Yuko Ohta,* Masanori Kasahara,† Timothy D. O’Connor,‡,x,{,‖ and Martin F. Flajnik* Comparative analyses suggest that the MHC was derived from a prevertebrate “primordial immune complex” (PIC). PIC duplicated twice in the well-studied two rounds of genome-wide duplications (2R) early in vertebrate evolution, generating four MHC paralogous regions (predominantly on human chromosomes [chr] 1, 6, 9, 19). Examining chiefly the amphibian Xenopus laevis, but also other vertebrates, we identified their MHC paralogues and mapped MHC class I, AgR, and “framework” genes. Most class I genes mapped to MHC paralogues, but a cluster of Xenopus MHC class Ib genes (xnc), which previously was mapped outside of the MHC paralogues, was surrounded by genes syntenic to mammalian CD1 genes, a region previously proposed as an Downloaded from MHC paralogue on human chr 1. Thus, this gene block is instead the result of a translocation that we call the translocated part of the MHC paralogous region (MHCtrans). Analyses of Xenopus class I genes, as well as MHCtrans, suggest that class I arose at 1R on the chr 6/19 ancestor. Of great interest are nonrearranging AgR-like genes mapping to three MHC paralogues; thus, PIC clearly contained several AgR precursor loci, predating MHC class I/II. However, all rearranging AgR genes were found on paralogues derived from the chr 19 precursor, suggesting that invasion of a variable (V) exon by the RAG transposon occurred after 2R. We propose models for the evolutionary history of MHC/TCR/Ig and speculate on the dichotomy between the jawless http://www.jimmunol.org/ (lamprey and hagfish) and jawed vertebrate adaptive immune systems, as we found genes related to variable lymphocyte receptors also map to MHC paralogues. The Journal of Immunology, 2019, 203: 000–000. he “2R hypothesis” has proposed that the early vertebrate (3, 4). Further analysis using the insulin/relaxin and neurotrophin/ genome experienced two rounds of genome-wide dupli- neurotrophin receptor family genes revealed that there are addi- T cations (1). Indeed, there are four paralogous clusters of tional regions containing paralogous genes in a similar order (5–7), genes in the genomes of all jawed vertebrates, first studied in humans and it has been suggested that the precursors of these regions and for homeobox and MHC genes (2, 3). When genes or genetic regions MHCpara were syntenic during the preduplication era, but some were are duplicated, some loci preserve their original function, whereas translocated over evolutionary time. These detached regions include by guest on September 29, 2021 others are modified (neofunctionalization or subfunctionalization) or sections of human chr 12, 14, and 15, and are generally shorter than may experience differential silencing. Other types of genome mod- the original regions; we refer to these detached regions as “minor ifications may occur, such as translocation of block regions, at times MHCpara,” and the original four regions as “major MHCpara.” blurring the origins of a particular genetic region. The MHC harbors many genes involved in adaptive and As mentioned, the MHC was one of the original gene clusters noted innate immunity (6, 8). Central to the adaptive immune system, for its paralogous regions (or “ohnologues”), found on human chro- the Ag-presenting MHC class I and class II molecules work in mosomes(chr)6(MHC),1,9,and19(MHCparalogues[MHCpara]) concert with Ag-processing (immunoproteasomes), peptide- transporting (TAP), peptide-editing (DM, TAPBP), and other *Department of Microbiology and Immunology, University of Maryland School molecules, to present antigenic peptides recognized by TCR. of Medicine, Baltimore, MD 21201; †Department of Pathology, Faculty of Med- Precursors of these genes were likely derived from the so-called icine and Graduate School of Medicine, Hokkaido University, Sapporo 060- 8638, Japan; ‡Institute for Genome Sciences, University of Maryland School primordial immune complex (PIC), predating the genome-wide of Medicine, Baltimore, MD, 21201; xProgram in Personalized and Genomic duplications in early vertebrates (9). Indeed, analysis of several in- Medicine, University of Maryland School of Medicine, Baltimore, MD, 21201; vertebrate deuterostome genomes [e.g., amphioxus (Branchiostoma {Marlene and Stewart Greenebaum Comprehensive Cancer Center, University of Maryland School of Medicine, Baltimore, MD, 21201; and ‖Department of Med- lanceolatum) (10), and a placozoan (Trichoplax adhaerens)(11)] icine, University of Maryland School of Medicine, Baltimore, MD 21201 revealed conserved synteny of proteasome and “framework” genes ORCID: 0000-0002-0276-1896 (T.D.O.). (i.e., nonimmune genes in MHC). To date, and unfortunately, no Received for publication May 23, 2019. Accepted for publication August 2, 2019. candidate class I/II genes have been detected in species derived from This project was supported by National Institutes of Health Grants AI140326-26 and ancestors predating the jawed vertebrates, and thus most genes AI02877 to Y.O. and M.F.F. strictly involved in adaptive immunity (based on MHC, Ig, TCR) Address correspondence and reprint requests to Dr. Martin F. Flajnik, University of seem to have appeared “suddenly” in a gnathostome ancestor. Be- Maryland, Baltimore, 655 West Baltimore Avenue, Room 3-056, Baltimore, MD cause both MHC and MHCpara are derived from a preduplicated 21201. E-mail address: mfl[email protected] precursor region in a common vertebrate ancestor (3, 6, 9), analysis The online version of this article contains supplemental material. of these regions from different extant vertebrates provides insight Abbreviations used in this article: chr, chromosome; FISH, fluorescence in situ hybrid- ization; huMHCpara,humanMHCpara; IgSF, Ig superfamily; L, long; LRR, leucine-rich into the evolutionary history of the MHC and its precursor. repeat; MHCpara,MHCparalogue;MHCtrans, translocated part of the MHC paralogous Previous work on the paralogous regions has focused only on region; NCBI, National Center for Biotechnology Information; NKC, NK complex; PIC, mammals. In this study, we took advantage of the published work in primordial immune complex; S, short; VLR, variable lymphocyte receptor. humans and focused on the genome of the amphibian Xenopus. Copyright Ó 2019 by The American Association of Immunologists, Inc. 0022-1767/19/$37.50 Previous studies showed that the Xenopus genome is relatively stable www.jimmunol.org/cgi/doi/10.4049/jimmunol.1900597 2 EMERGENCE OF Ag RECEPTORS AND MHC CLASS I INCLUDING CD1 and preserves some primordial features that were lost in other ver- content of the L chromosomes is most similar to the genome of tebrates (12), thus serving as a complementary model system to study the true diploid X. tropicalis. Although most housekeeping genome evolution. We used the true diploid Xenopus tropicalis (13) genes are present on both chromosomes, most class I (except a few and especially the tetraploid Xenopus laevis (14), in which the ge- class I–like genes), AgR, and AgR-like genes discussed in this report nomes have been recently sequenced and analyzed. In combination were diploidized and thus found only on the L chromosomes, and with comparative genomic analyses, we obtained evidence for the therefore we focused our analyses on the L chromosomes. timing of emergence of MHC class I/II and AgR genes. We further Xenopus MHC and identification of major and minor propose a model for the evolution of the human chr 1q21.1–23.3 MHCpara regions region, including the CD1 genes, and reflect on the dichotomy be- tween the jawed and jawless vertebrate adaptive immune systems. The Xenopus MHC was previously mapped by FISH to chr 8 (18) and now is precisely mapped to 8Lq21. To identify Xenopus MHCpara, we used sets of paralogous hallmark genes that were Materials and Methods originally used to identify the human MHCpara (huMHCpara) (3) Data mining (e.g., notch1, 2, 3, 4; pbx1, 2, 3, 4;
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