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Molecular Pattern Recognition of A Hyperconservation of the N-Formyl Peptide Binding Site of M3: Evidence that M3 Is an Old Eutherian Molecule with Conserved Recognition of a Pathogen-Associated This information is current as Molecular Pattern of September 27, 2021. C. Kuyler Doyle, Beckley K. Davis, Richard G. Cook, Robert R. Rich and John R. Rodgers J Immunol 2003; 171:836-844; ; doi: 10.4049/jimmunol.171.2.836 Downloaded from http://www.jimmunol.org/content/171/2/836 References This article cites 63 articles, 25 of which you can access for free at: http://www.jimmunol.org/ http://www.jimmunol.org/content/171/2/836.full#ref-list-1 Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists by guest on September 27, 2021 • 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 © 2003 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology Hyperconservation of the N-Formyl Peptide Binding Site of M3: Evidence that M3 Is an Old Eutherian Molecule with Conserved Recognition of a Pathogen-Associated Molecular Pattern1 C. Kuyler Doyle, Beckley K. Davis, Richard G. Cook, Robert R. Rich,2 and John R. Rodgers3 The mouse MHC class I-b molecule H2-M3 has unique specificity for N-formyl peptides, derived from bacteria (and mitochon- dria), and is thus a pathogen-associated molecular pattern recognition receptor (PRR). To test whether M3 was selected for this PRR function, we studied M3 sequences from diverse murid species of murine genera Mus, Rattus, Apodemus, Diplothrix, Hybomys, Mastomys, and Tokudaia and of sigmodontine genera Sigmodon and Peromyscus. We found that M3 is highly conserved, and the Downloaded from 10 residues coordinating the N-formyl group are almost invariant. The ratio of nonsynonymous and synonymous substitution rates suggests the Ag recognition site of M3, unlike the Ag recognition site of class I-a molecules, is under strong negative (purifying) selection and has been for at least 50–65 million years. Consistent with this, M3 ␣1␣2 domains from Rattus norvegicus and Sigmodon hispidus and from the “null” allele H2-M3b specifically bound N-formyl peptides. The pattern of nucleotide substitution in M3 suggests M3 arose rapidly from murid I-a precursors by an evolutionary leap (“saltation”), perhaps involving intense selective pressure from bacterial pathogens. Alternatively, M3 arose more slowly but prior to the radiation of eutherian (placental) http://www.jimmunol.org/ mammals. Older dates for the emergence of M3, and the accepted antiquity of CD1, suggest that primordial class I MHC molecules could have evolved originally as monomorphic PRR, presenting pathogen-associated molecular patterns. Such MHC PRR mol- ecules could have been preadaptations for the evolution of acquired immunity during the early vertebrate radiation. The Journal of Immunology, 2003, 171: 836–844. he mouse class I-b molecule H2-M3 preferentially binds domain (12). In contrast to the minimal oligomorphism of class I-b N-formyl peptides (1, 2), pathogen-associated molecular genes (6), class I-a genes are extremely polymorphic, allowing patterns (PAMP)4 (3) also recognized by neutrophil che- presentation of diverse intracellular Ags to T cells (13). Polymor- T by guest on September 27, 2021 motactic receptors (4). Thus, M3 is a pattern-recognition receptor phism is pronounced especially in the Ag recognition site (ARS) (PRR). In this respect, M3 resembles CD1, which presents myco- and is thought to be generated through diversifying (positive) se- bacterial waxy lipids to T cells (5). M3 may be important for lection (13) evidenced by a high ratio of nonsynonymous to syn- protection against intracellular bacteria (6). Indeed, M3-restricted onymous substitutions in the ARS (14). CTL are protective in experimental infections by the intracellular The paucity of I-b orthologs shared among species of different pathogen Listeria monocytogenes (7–9). The laboratory of Fischer taxonomic orders led to the hypothesis that I-b genes are relatively Lindahl and colleagues (10) showed Norway rats have a gene young, formed by duplications of class I-a genes (15). Such du- nearly identical to H2-M3, suggesting that M3 has been conserved plicates are often redundant and may drift rapidly under neutral since the rat/mouse divergence ϳ14–40 million years ago (MYA). selection towards pseudogeny (15). Functional divergence of gene Like other class I-b genes, M3 is virtually monomorphic in Mus duplicates (16) probably requires positive selection (17). Phyloge- musculus (11). A minor allele, M3b, has been considered null be- netic analyses suggest that many mouse class I-b genes, such as cause it does not restrict lysis by known M3-specific CTL (11); Qa-2 (15) and H2-B1 (our unpublished observations) arose since null activity was mapped to a Leu95Gln substitution in the ␣2 the rat/mouse divergence from duplications of class I-a genes. Be- cause M3 has been unknown outside the murine genera Rattus and Baylor College of Medicine, Department of Immunology, Houston, TX 77030 Mus, it may also have evolved from murine or murid I-a genes. A contrasting model, similar to one proposed for H2-TL (18, 19), Received for publication December 23, 2002. Accepted for publication May 12, 2003. suggests that M3 arose before the mammalian radiation. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance The unique ligand specificity of M3 makes it especially inter- with 18 U.S.C. Section 1734 solely to indicate this fact. esting as a model to study how MHC specificities evolve, presum- 1 This work was supported by National Institutes of Heatlh RO1 Grants AI30036 (to ably in response to pathogen or other immune pressure. The mech- R. R. R. and R. G. C.) AI18882 (to R. R. R. and J. R. R.), and RO1 AI17897 (to anism of N-formyl specificity in M3 is well-studied (11). The R. G. C. and J. R. R.). crystal structure of M3a (20) indicated 10 amino acids coordinated 2 Current address: Emory University School of Medicine, Atlanta, GA 30322. N-formyl specificity, with a key contribution from histidine in po- 3 Address correspondence and reprint requests to Dr. John R. Rodgers, Department of 9 Immunology Room M929, Baylor College of Medicine, One Baylor Plaza, Houston, sition 9 (His ). Five of these residues are rarely found in other class TX 77030. E-mail address: [email protected] I molecules. However, our unpublished studies in which we trans- b 4 Abbreviations used in this paper: PAMP, pathogen-associated molecular pattern; planted these residues between M3 and H2-K suggested other ARS, Ag recognition site; NARS, non-ARS; MY, million years; MYA, MY ago; dN, residues are required to achieve N-formyl specificity. Moreover, rate of nonsynonymous substitution; dS, rate of synonymous substitution; indel, in- sertion and/or deletion; NJ, neighbor-joining; PRR, pattern recognition receptor; UP- the differences between M3 and murine class I-a molecules are not GMA, unweighted pair-group method with arithmetic means; cytb, cytochrome b. concentrated in the ARS but are spread throughout the ␣1 and ␣2 Copyright © 2003 by The American Association of Immunologists, Inc. 0022-1767/03/$02.00 The Journal of Immunology 837 domains. This raises the question of how M3 evolved from a class GTG GGA GTT (reverse); exon 3 primers were 5Ј-AAG CTT GAT CCA I-a gene. Identification of M3 orthologs from related species AAC CTG GCA GAT (forward) and 5Ј-CTC GAG CCT AAG GTT GAG should identify transitional forms, or “missing links,” between mu- GGA TTT (reverse). PCR using these primers discovered S. hispidus M3 not found with the original primer set. rine M3 and I-a genes. The phylogeny of Muridae, the largest extant rodent family, has Cloning PCR products been studied intensively. Four subgenera of Mus (Coelomys, shrew PCR products of the expected size were gel-purified using the Qiagen mice; Mus; Nannomys, African pygmy mice; and Pyromys, spiny (Valencia, CA) Qiaquick Gel Extraction kit and eluted products cloned mice) diverged ϳ9 MYA (21). The Old World subfamily Murinae with the Zero Blunt TOPO PCR Cloning kit (Invitrogen). Plasmids were includes Mus and Rattus, which diverged 14–40 MYA (22, 23). sequenced by Lone Star Labs (Houston, TX) or the DNA sequencing core Two genera of the New World subfamily Sigmodontinae, Sigmo- facility (Baylor College of Medicine) using an Applied Biosystems (Foster ϳ City, CA) ABI PRISM 377 DNA Sequencer. Most sequences were con- don (cotton rats) and Peromyscus (deer mice), diverged 12 MYA firmed from independent clones and/or sequencing in the reverse direction. (24). Subfamilies Murinae and Sigmodontinae diverged 50–65 M3 and cytb sequences have been deposited at GenBank with Accession MYA (22). We isolated 43 unique M3 sequences from 22 species nos. AY263509-AY263623. of these two subfamilies. We tested these for evidence of selective Phylogenetic trees pressures, and the most disparate members for N-formyl specific- ity. Finally, we asked whether the origins of M3 from class I-a A well-aligned database of exons 2 and 3 of 160 class I genes, including genes could be discerned by phylogenetic analysis.
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