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Genes NKG2 and CD94 Common Chimpanzee Conservation And Conservation and Variation in Human and Common Chimpanzee CD94 and NKG2 Genes This information is current as Benny P. Shum, Laura R. Flodin, David G. Muir, Raja of October 2, 2021. Rajalingam, Salim I. Khakoo, Sophia Cleland, Lisbeth A. Guethlein, Markus Uhrberg and Peter Parham J Immunol 2002; 168:240-252; ; doi: 10.4049/jimmunol.168.1.240 http://www.jimmunol.org/content/168/1/240 Downloaded from References This article cites 66 articles, 16 of which you can access for free at: http://www.jimmunol.org/content/168/1/240.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 October 2, 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 © 2002 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Conservation and Variation in Human and Common Chimpanzee CD94 and NKG2 Genes1 Benny P. Shum, Laura R. Flodin, David G. Muir, Raja Rajalingam, Salim I. Khakoo,2 Sophia Cleland, Lisbeth A. Guethlein, Markus Uhrberg,3 and Peter Parham4 To assess polymorphism and variation in human and chimpanzee NK complex genes, we determined the coding-region sequences for CD94 and NKG2A, C, D, E, and F from several human (Homo sapiens) donors and common chimpanzees (Pan troglodytes). CD94 is highly conserved, while the NKG2 genes exhibit some polymorphism. For all the genes, alternative mRNA splicing variants were frequent among the clones obtained by RT-PCR. Alternative splicing acts similarly in human and chimpanzee to produce the CD94B variant from the CD94 gene and the NKG2B variant from the NKG2A gene. Whereas single chimpanzee orthologs for CD94, NKG2A, NKG2E, and NKG2F were identified, two chimpanzee paralogs of the human NKG2C gene were defined. The chimpanzee Pt-NKG2CI gene encodes a protein similar to human NKG2C, whereas in the chimpanzee Pt-NKG2CII gene the Downloaded from translation frame changes near the beginning of the carbohydrate recognition domain, causing premature termination. Analysis of a panel of chimpanzee NK cell clones showed that Pt-NKG2CI and Pt-NKG2CII are independently and clonally expressed. Pt-NKG2CI and Pt-NKG2CII are equally diverged from human NKG2C, indicating that they arose by gene duplication subsequent to the divergence of chimpanzee and human ancestors. Genomic DNA from 80 individuals representing six primate species were typed for the presence of CD94 and NKG2. Each species gave distinctive typing patterns, with NKG2A and CD94 being most conserved. Seven different NK complex genotypes within the panel of 48 common chimpanzees were due to differences in Pt-NKG2C http://www.jimmunol.org/ and Pt-NKG2D genes. The Journal of Immunology, 2002, 168: 240–252. uman NK cell receptors specific for HLA class I molecules CD94:NKG2C heterodimer is a receptor with ligand specificity are encoded in two genetic complexes, both situated on similar to CD94:NKG2A, but which generates activating signals different chromosomes from the MHC on human chromo- within NK cells (22, 23). Human NKG2D is a homodimeric acti- H 5 some 6 (1, 2). The killer cell Ig-like receptors (KIRs) are encoded on vating receptor that interacts with MHC class I-like chain A (24, the leukocyte receptor complex or cluster (LRC) on human chromo- 25), a MHC class I-like protein with considerable polymorphism, some 19q13.4 (3–6) and the lectin-like CD94 and NKG2 receptors and with unique long binding proteins (ULBPs), newly identified are encoded within the NK complex (NKC) on human chromosome molecules distantly related to MHC class I (26). In NK cells, ac- by guest on October 2, 2021 12p12.3-p13.1 (7–12). In human, one CD94 and five NKG2 (A/B, C, tivating signals are conveyed via positively charged amino acid D, E/H, F) genes are located within the NKC (7–12). residues in the transmembrane domains of activating receptors The CD94 and NKG2A polypeptides form a heterodimeric re- (NKG2C, D) that interact with signal-transducing adaptor mole- ceptor (13, 14) that recognizes the MHC nonclassical class I cules such as DAP-10 and DAP-12 (27, 28). The exact roles of HLA-E ligand complexed with peptides derived from the leader human NKG2E and NKG2F are uncertain, but both encode a pos- sequences of certain classical HLA-A, B, C, and nonclassical itively charged lysine residue in the transmembrane domain, as HLA-G H chains (15–19). Ligand recognition transduces inhibi- does NKG2C. tory signals in NK cells via the immunomodulatory tyrosine-based The KIR genes of the human LRC encode receptors that are inhibition motifs on the cytoplasmic tail of NKG2A (20–22). The specific for polymorphic determinants of HLA-A, B, and C, and also for HLA-G (1, 29). Previous work from our laboratory re- vealed diversity of KIR haplotype in the human population, with Departments of Structural Biology and Microbiology and Immunology, Stanford Uni- versity School of Medicine, Stanford, CA 94305 respect to the number and content of KIR genes (30) and also Received for publication May 4, 2001. Accepted for publication October 22, 2001. allelic polymorphism at individual genes (31–34). Furthermore, The costs of publication of this article were defrayed in part by the payment of page comparison of human and chimpanzee KIR revealed many species- charges. This article must therefore be hereby marked advertisement in accordance specific features to the KIR gene systems (35, 36). Given the di- with 18 U.S.C. Section 1734 solely to indicate this fact. versity and rapid evolution of the KIR genes it became of particular 1 This work was supported by National Institutes of Health Grants AI17892 and interest to investigate intraspecies and interspecies diversity of AI31168 (to P.P.). S.I.K. was a fellow of the Cancer Research Institute of New York. M.U. was supported by the Ministerium fu¨r Schule und Weiterdildung, Wissenschaft NKC genes that encode NK cell receptors for MHC class I mol- und Forschung des Landes Nordrhein-Westfalen. ecules. Therefore, we have investigated the diversity and variation 2 Current address: Department of Cell and Molecular Medicine, Southampton General in the CD94 and NKG2 genes of humans and apes. Hospital, Southampton, U.K. 3 Current address: Institute for Transplantation Diagnostics and Cell Therapeutics, Materials and Methods Heinrich Heine University Medical Center, Dusseldorf, Germany. Source materials from humans and apes 4 Address correspondence to Dr. Peter Parham, Department of Structural Biology, Stan- ford University School of Medicine, 299 Campus Drive West, Sherman Fairchild Build- Healthy human donors recruited from our laboratory represent a variety of ing, D-157, Stanford, CA 94305-5126. E-mail address: [email protected] ethnic and racial backgrounds, as shown in Fig. 1. Tissue samples from 5 ␤ ␤ non-human primates were purchased from the Yerkes Regional Primate Abbreviations used in this paper: KIR, killer cell Ig-like receptor; 2m, 2-micro- globulin; CRD, carbohydrate recognition domain; LRC, leukocyte receptor complex Center at Emory University (Atlanta, GA) and from the Laboratory for or cluster; NKC, NK complex; ULBP, unique long binding protein. Experimental Medicine and Surgery in Primates (New York University Copyright © 2002 by The American Association of Immunologists 0022-1767/02/$02.00 The Journal of Immunology 241 Medical Center, Tuxedo, NY). Blood was drawn from animal subjects as cDNA analysis of CD94 and NKG2 genes part of routine health examinations. Total cytoplasmic RNA was prepared from PMBC isolated from human and chimpanzee donors. In addition, Total cytoplasmic RNA was isolated with the reagent RNAzol following RNA was extracted from NK cell clones NK1.3 and M1.1 established from manufacturer’s protocol (Tel-Test, Friendswood, TX). First-strand cDNA chimpanzees Cathy and Mason, respectively (35); a splenic sample from was prepared from total RNA using murine Moloney leukemia virus-re- the chimpanzee Edwina was also used as source material. Genomic DNA verse transcriptase (Life Technologies, Rockville, MD) by standard pro- of higher primates used for PCR typing analysis was isolated from previ- cedures (38). ously established EBV-transformed B cell lines (36, 37). These include cDNA was amplified by PCR in 1ϫ AmpliTaq buffer (Applied Biosys- samples from the family Hominidae: humans (Homo sapiens, n ϭ 11), tems, Foster City, CA), 0.25 mM of each dNTP, 0.8 pM each of a sense common chimpanzees (Pan troglodytes, n ϭ 48), pygmy chimpanzees or (forward) and antisense (reverse) primer, and1UofAmpliTaq DNA poly- bonobos (P. paniscus, n ϭ 11), gorillas (Gorilla gorilla, n ϭ 2), and or- merase (Applied Biosystems). The following PCR conditions were used: angutans (Pongo pygmaeus, n ϭ 5); and from the family Hylobatidae: initial denaturation at 96°C for 1 min; then 30 cycles of denaturation at common gibbons (Hylobates lar, n ϭ 3). 94°C for 30 s, primer annealing at 52–60°C for 30 s, and extension at Table
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