, Volume 59, Issue 7, pp 603–611 | Cite as

Chicken CD69 and CD94/NKG2-like genes in a chromosomal region syntenic to mammalian natural killer gene complex

  • Hsin-I Chiang
  • Huaijun Zhou
  • Terje Raudsepp
  • Palmy R. Jesudhasan
  • James J. Zhu
Brief Communication


In mammals, natural killer (NK) cell C-type lectin receptors were encoded in a gene cluster called natural killer gene complex (NKC). The NKC is not reported in chicken yet. Instead, NK receptor genes were found in the major histocompatibility complex. In this study, two novel chicken C-type lectin-like receptor genes were identified in a region on chromosome 1 that is syntenic to mammalian NKC region. The chromosomal locations were validated with fluorescent in situ hybridization. Based on 3D structure modeling, sequence homology, chromosomal location, and phlylogenetic analysis, one receptor is the orthologue of mammalian cluster of differentiation 69 (CD69), and the other is highly homologous to CD94 and NKG2. Like CD94/NKG2 gene found in teleostean fishes, chicken CD94/NKG2 has the features of both human CD94 and NKG2A. Unlike mammalian NKC, these two chicken C-type lectin receptors are not closely linked but separated by 42 million base pairs according to the chicken draft genome sequence. The arrangement of several other genes that are located outside the mammalian NKC is conserved among chicken, human, and mouse. The chicken NK C-type lectin-like receptors in the NKC syntenic region indicate that this chromosomal region existed before the divergence between mammals and aves.


Natural killer cells NKC Chicken C-type lectin-like receptor 

Supplementary material


  1. Boyington JC, Riaz AN, Patamawenu A, Coligan JE, Brooks AG, Sun PD (1999) Structure of CD94 reveals a novel C-type lectin fold: implications for the NK cell-associated CD94/NKG2 receptors. Immunity 10:75–82PubMedCrossRefGoogle Scholar
  2. Bumstead N (1998) Genomic mapping of resistance to Marek’s disease. Avian Pathol 27:S78–S81Google Scholar
  3. Christidis L (1983) Extensive chromosomal repatterning in two congeneric species: Pytilia melba, L. and Pytilia phoenicoptera Swainson (Estrildidae; Aves). Cytogenet Cell Genet 36:641–648PubMedGoogle Scholar
  4. Eisenberg D, Luthy R, Bowie JU (1997) VERIFY3D: assessment of protein models with three-dimensional profiles. Methods Enzymol 277:396–404PubMedCrossRefGoogle Scholar
  5. Hansen DS, Evans KJ, D’Ombrain MC, Bernard NJ, Sexton AC, Buckingham L, Scalzo AA, Schofield L (2005) The natural killer complex regulates severe malarial pathogenesis and influences acquired immune responses to Plasmodium berghei ANKA. Infect Immun 73:2288–2297PubMedCrossRefGoogle Scholar
  6. Ho EL, Heusel JW, Brown MG, Matsumoto K, Scalzo AA, Yokoyama WM (1998) Murine Nkg2d and Cd94 are clustered within the natural killer complex and are expressed independently in natural killer cells. Proc Natl Acad Sci USA 95:6320–6325PubMedCrossRefGoogle Scholar
  7. Kaufman J, Milne S, Gobel TW, Walker BA, Jacob JP, Auffray C, Zoorob R, Beck S (1999) The chicken B locus is a minimal essential major histocompatibility complex. Nature 401:923–925PubMedCrossRefGoogle Scholar
  8. Kikuno R, Sato A, Mayer WE, Shintani S, Aoki T, Klein J (2004) Clustering of C-type lectin natural killer receptor-like loci in the bony fish Oreochromis niloticus. Scand J Immunol 59:133–142PubMedCrossRefGoogle Scholar
  9. Koradi R, Billeter M, Wuthrich K (1996) MOLMOL: a program for display and analysis of macromolecular structures. Journal of Molecular Graphics 14:51PubMedCrossRefGoogle Scholar
  10. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  11. Ladjali-Mohammedi K, Bitgood JJ, Tixier-Boichard M, Ponce De Leon FA (1999) International system for standardized avian karyotypes (ISSAK): standardized banded karyotypes of the domestic fowl (Gallus domesticus). Cytogenet Cell Genet 86:271–276PubMedCrossRefGoogle Scholar
  12. Lanier LL (2005) NK cell recognition. Annu Rev Immunol 23:225–274PubMedCrossRefGoogle Scholar
  13. Letunic I, Copley RR, Schmidt S, Ciccarelli FD, Doerks T, Schultz J, Ponting CP, Bork P (2004) SMART 4.0: towards genomic data integration. Nucleic Acids Res 32:D142–D144PubMedCrossRefGoogle Scholar
  14. Puntervoll P, Linding R, Gemund C, Chabanis-Davidson S, Mattingsdal M, Cameron S, Martin DM, Ausiello G, Brannetti B, Costantini A, Ferre F, Maselli V, Via A, Cesareni G, Diella F, Superti-Furga G, Wyrwicz L, Ramu C, McGuigan C, Gudavalli R, Letunic I, Bork P, Rychlewski L, Kuster B, Helmer-Citterich M, Hunter WN, Aasland R, Gibson TJ (2003) ELM server: a new resource for investigating short functional sites in modular eukaryotic proteins. Nucleic Acids Res 31:3625–3630PubMedCrossRefGoogle Scholar
  15. Rogers S, Shaw I, Ross N, Nair V, Rothwell L, Kaufman J, Kaiser P (2003) Analysis of part of the chicken Rfp-Y region reveals two novel lectin genes, the first complete genomic sequence of a class I alpha-chain gene, a truncated class II beta-chain gene, and a large CR1 repeat. Immunogenetics 55:100–108PubMedGoogle Scholar
  16. Rogers SL, Gobel TW, Viertlboeck BC, Milne S, Beck S, Kaufman J (2005) Characterization of the chicken C-type lectin-like receptors B-NK and B-lec suggests that the NK complex and the MHC share a common ancestral region. J Immunol 174:3475–3483PubMedGoogle Scholar
  17. Sato A, Mayer WE, Overath P, Klein J (2003) Genes encoding putative natural killer cell C-type lectin receptors in teleostean fishes. Proc Natl Acad Sci U S A 100:7779–7784PubMedCrossRefGoogle Scholar
  18. Sawicki MW, Dimasi N, Natarajan K, Wang J, Margulies DH, Mariuzza RA (2001) Structural basis of MHC class I recognition by natural killer cell receptors. Immunol Rev 181:52–65PubMedCrossRefGoogle Scholar
  19. Scalzo AA, Manzur M, Forbes CA, Brown MG, Shellam GR (2005) NK gene complex haplotype variability and host resistance alleles to murine cytomegalovirus in wild mouse populations. Immunol Cell Biol 83:144–149PubMedCrossRefGoogle Scholar
  20. Shum BP, Flodin LR, Muir DG, Rajalingam R, Khakoo SI, Cleland S, Guethlein LA, Uhrberg M, Parham P (2002) Conservation and variation in human and common chimpanzee CD94 and NKG2 genes. J Immunol 168:240–252PubMedGoogle Scholar
  21. Testi R, D’Ambrosio D, De Maria R, Santoni A (1994) The CD69 receptor: a multipurpose cell-surface trigger for hematopoietic cells. Immunol Today 15:479–483PubMedCrossRefGoogle Scholar
  22. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  23. Trowsdale J, Barten R, Haude A, Stewart CA, Beck S, Wilson MJ (2001) The genomic context of natural killer receptor extended gene families. Immunol Rev 181:20–38PubMedCrossRefGoogle Scholar
  24. Vance BA, Bennett MJ, Ward Y, Gress RG, Kearse KP (1999) Distinct but dispensable N-glycosylation of human CD69 proteins. Arch Biochem Biophys 368:214–220PubMedCrossRefGoogle Scholar
  25. Yim D, Sotiriadis J, Kim KS, Shin SC, Jie HB, Rothschild MF, Kim YB (2002) Molecular cloning, expression pattern and chromosomal mapping of pig CD69. Immunogenetics 54:276–281PubMedCrossRefGoogle Scholar
  26. Yokoyama WM, Plougastel BF (2003) Immune functions encoded by the natural killer gene complex. Nat Rev Immunol 3:304–316PubMedCrossRefGoogle Scholar
  27. Yonash N, Kaiser MG, Heller ED, Cahaner A, Lamont SJ (1999) Major histocompatibility complex (MHC) related cDNA probes associated with antibody response in meat-type chickens. Anim Genet 30:92–101PubMedCrossRefGoogle Scholar
  28. Zhu JJ, Lillehoj HS, Allen PC, Van Tassell CP, Sonstegard TS, Cheng HH, Pollock D, Sadjadi M, Min W, Emara MG (2003) Mapping quantitative trait loci associated with resistance to coccidiosis and growth. Poult Sci 82:9–16PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Hsin-I Chiang
    • 1
  • Huaijun Zhou
    • 1
  • Terje Raudsepp
    • 2
  • Palmy R. Jesudhasan
    • 1
  • James J. Zhu
    • 1
  1. 1.Department of Poultry ScienceTexas A & M UniversityCollege StationUSA
  2. 2.Department of Veterinary Integrative BiosciencesTexas A & M UniversityCollege StationUSA
  3. 3.USDA-ARS, PIADCGreenportUSA

Personalised recommendations