Advertisement

Immunogenetics

, Volume 61, Issue 8, pp 565–579 | Cite as

Identification of natural killer cell receptor clusters in the platypus genome reveals an expansion of C-type lectin genes

  • Emily S. W. Wong
  • Claire E. Sanderson
  • Janine E. Deakin
  • Camilla M. Whittington
  • Anthony T. Papenfuss
  • Katherine BelovEmail author
Original Paper

Abstract

Natural killer (NK) cell receptors belong to two unrelated, but functionally analogous gene families: the immunoglobulin superfamily, situated in the leukocyte receptor complex (LRC) and the C-type lectin superfamily, located in the natural killer complex (NKC). Here, we describe the largest NK receptor gene expansion seen to date. We identified 213 putative C-type lectin NK receptor homologs in the genome of the platypus. Many have arisen as the result of a lineage-specific expansion. Orthologs of OLR1, CD69, KLRE, CLEC12B, and CLEC16p genes were also identified. The NKC is split into at least two regions of the genome: 34 genes map to chromosome 7, two map to a small autosome, and the remainder are unanchored in the current genome assembly. No NK receptor genes from the LRC were identified. The massive C-type lectin expansion and lack of Ig-domain-containing NK receptors represents the most extreme polarization of NK receptors found to date. We have used this new data from platypus to trace the possible evolutionary history of the NK receptor clusters.

Keywords

NKC Platypus Natural killer receptors Evolution Gene expansion Immune 

Notes

Acknowledgments

This work was carried out as part of the Platypus Genome Project. We thank Wes Warren and his team at Washington University, St. Louis, for giving us the opportunity to work on such an exciting project. We thank Kaighan McColl for bioinformatics support. E.W. and C.S. receive scholarships from the Jean Walker Trust and the ARC Center for Kangaroo Genomics.

Supplementary material

251_2009_386_MOESM1_ESM.doc (755 kb)
ESM 1 Includes detailed information on the identification of Ig domains, specifically pertaining to the identification of OSCAR, SIGLEC and Fc receptor genes, FISH data and accession numbers for all non-platypus sequences used in phylogenetic analyses (DOC 755 kb)

References

  1. Alsop AE, Miethke P, Rofe R, Koina E, Sankovic N, Deakin JE, Haines H, Rapkins RW, Marshall Graves JA (2005) Characterizing the chromosomes of the Australian model marsupial Macropus eugenii (tammar wallaby). Chromosome Res 13:627–636PubMedCrossRefGoogle Scholar
  2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  3. Angata T, Tabuchi Y, Nakamura K, Nakamura M (2007) Siglec-15: an immune system Siglec conserved throughout vertebrate evolution. Glycobiology 17:838–846PubMedCrossRefGoogle Scholar
  4. Belov K, Deakin JE, Papenfuss AT, Baker ML, Melman SD, Siddle HV, Gouin N, Goode DL, Sargeant TJ, Robinson MD, Wakefield MJ, Mahony S, Cross JG, Benos PV, Samollow PB, Speed TP, Graves JA, Miller RD (2006) Reconstructing an ancestral mammalian immune supercomplex from a marsupial major histocompatibility complex. PLoS Biol 4:e46PubMedCrossRefGoogle Scholar
  5. Belov K, Sanderson CE, Deakin JE, Wong ES, Assange D, McColl KA, Gout A, de Bono B, Barrow AD, Speed TP, Trowsdale J, Papenfuss AT (2007) Characterization of the opossum immune genome provides insights into the evolution of the mammalian immune system. Genome Res 17:982PubMedCrossRefGoogle Scholar
  6. Bernal A, Crammer K, Hatzigeorgiou A, Pereira F (2007) Global discriminative learning for higher-accuracy computational gene prediction. PLoS Comput Biol 3:e54PubMedCrossRefGoogle Scholar
  7. Bina M, Crowely E (2001) Sequence patterns defining the 5' boundary of human genes. Biopolymers 59:347–355PubMedCrossRefGoogle Scholar
  8. Blery M, Kubagawa H, Chen CC, Vely F, Cooper MD, Vivier E (1998) The paired Ig-like receptor PIR-B is an inhibitory receptor that recruits the protein-tyrosine phosphatase SHP-1. Proc Natl Acad Sci U S A 95:2446–2451PubMedCrossRefGoogle Scholar
  9. Blery M, Olcese L, Vivier E (2000) Early signaling via inhibitory and activating NK receptors. Hum Immunol 61:51–64PubMedCrossRefGoogle Scholar
  10. Butcher S, Arney KL, Cook GP (1998) MAFA-L, an ITIM-containing receptor encoded by the human NK cell gene complex and expressed by basophils and NK cells. Eur J Immunol 28:3755–3762PubMedCrossRefGoogle Scholar
  11. Cambiaggi C, Scupoli MT, Cestari T, Gerosa F, Carra G, Tridente G, Accolla RS (1992) Constitutive expression of CD69 in interspecies T-cell hybrids and locus assignment to human chromosome 12. Immunogenetics 36:117–120PubMedCrossRefGoogle Scholar
  12. Carrington M, Cullen M (2004) Justified chauvinism: advances in defining meiotic recombination through sperm typing. Trends Genet 20:196–205PubMedCrossRefGoogle Scholar
  13. Chiang HI, Zhou H, Raudsepp T, Jesudhasan PR, Zhu JJ (2007) Chicken CD69 and CD94/NKG2-like genes in a chromosomal region syntenic to mammalian natural killer gene complex. Immunogenetics 59:603–611PubMedCrossRefGoogle Scholar
  14. Crocker PR, Paulson JC, Varki A (2007) Siglecs and their roles in the immune system. Nat Rev Immunol 7:255–266PubMedCrossRefGoogle Scholar
  15. Davis RS, Dennis G Jr, Odom MR, Gibson AW, Kimberly RP, Burrows PD, Cooper MD (2002) Fc receptor homologs: newest members of a remarkably diverse Fc receptor gene family. Immunol Rev 190:123–136PubMedCrossRefGoogle Scholar
  16. DeFranco AL, Locksley RM, Robertson M (2007) Immunity: the immune response in infectious and inflammatory disease. New Science, U.SGoogle Scholar
  17. DeLano WL (2002) The PyMOL molecular graphics systemGoogle Scholar
  18. Dennis G Jr, Kubagawa H, Cooper MD (2000) Paired Ig-like receptor homologs in birds and mammals share a common ancestor with mammalian Fc receptors. Proc Natl Acad Sci U S A 97:13245–13250PubMedCrossRefGoogle Scholar
  19. Dohm JC, Tsend-Ayush E, Reinhardt R, Grutzner F, Himmelbauer H (2007) Disruption and pseudoautosomal localization of the major histocompatibility complex in monotremes. Genome Biol 8:R175PubMedCrossRefGoogle Scholar
  20. Eagle RA, Trowsdale J (2007) Promiscuity and the single receptor: NKG2D. Nat Rev Immunol 7:737–744PubMedCrossRefGoogle Scholar
  21. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797PubMedCrossRefGoogle Scholar
  22. Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723PubMedCrossRefGoogle Scholar
  23. Hao L, Nei M (2005) Rapid expansion of killer cell immunoglobulin-like receptor genes in primates and their coevolution with MHC Class I genes. Gene 347:149–159PubMedCrossRefGoogle Scholar
  24. Hao L, Klein J, Nei M (2006) Heterogeneous but conserved natural killer receptor gene complexes in four major orders of mammals. Proc Natl Acad Sci U S A 103:3192–3197PubMedCrossRefGoogle Scholar
  25. Hoffmann SC, Schellack C, Textor S, Konold S, Schmitz D, Cerwenka A, Pflanz S, Watzl C (2007) Identification of CLEC12B, an inhibitory receptor on myeloid cells. J Biol Chem 282:22370–22375PubMedCrossRefGoogle Scholar
  26. Kelley J, Trowsdale J (2005) Features of MHC and NK gene clusters. Transpl Immunol 14:129–134PubMedCrossRefGoogle Scholar
  27. Kelley J, Walter L, Trowsdale J (2005) Comparative genomics of natural killer cell receptor gene clusters. PLoS Genet 1:129–139PubMedCrossRefGoogle Scholar
  28. 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
  29. Kumar S, Hedges SB (1998) A molecular timescale for vertebrate evolution. Nature 392:917–920PubMedCrossRefGoogle Scholar
  30. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  31. Laun K, Coggill P, Palmer S, Sims S, Ning Z, Ragoussis J, Volpi E, Wilson N, Beck S, Ziegler A, Volz A (2006) The leukocyte receptor complex in chicken is characterized by massive expansion and diversification of immunoglobulin-like Loci. PLoS Genet 2:e73PubMedCrossRefGoogle Scholar
  32. Messer M, Weiss AS, Shaw DC, Westerman M (1998) Evolution of the monotremes: phylogenetic relationship to marsupials and eutherians, and estimation of divergence dates based on a-lactalbumin amino acid sequences. J Mamm Evol 5:95–105CrossRefGoogle Scholar
  33. Munday BL, Whittington RJ, Stewart NJ (1998) Disease conditions and subclinical infections of the platypus (Ornithorhynchus anatinus). Philos Trans R Soc Lond B Biol Sci 353:1093–1099PubMedCrossRefGoogle Scholar
  34. Nikolaidis N, Klein J, Nei M (2005) Origin and evolution of the Ig-like domains present in mammalian leukocyte receptors: insights from chicken, frog, and fish homologues. Immunogenetics 57:151–157PubMedCrossRefGoogle Scholar
  35. Panagos PG, Dobrinski KP, Chen X, Grant AW, Traver D, Djeu JY, Wei S, Yoder JA (2006) Immune-related, lectin-like receptors are differentially expressed in the myeloid and lymphoid lineages of zebrafish. Immunogenetics 58:31–40PubMedCrossRefGoogle Scholar
  36. Pyz E, Marshall AS, Gordon S, Brown GD (2006) C-type lectin-like receptors on myeloid cells. Ann Med 38:242–251PubMedCrossRefGoogle Scholar
  37. Reid DM, Montoya M, Taylor PR, Borrow P, Gordon S, Brown GD, Wong SY (2004) Expression of the beta-glucan receptor, Dectin-1, on murine leukocytes in situ correlates with its function in pathogen recognition and reveals potential roles in leukocyte interactions. J Leukoc Biol 76:86–94PubMedCrossRefGoogle Scholar
  38. 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 55:100–108Google Scholar
  39. 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
  40. Saether PC, Westgaard IH, Hoelsbrekken SE, Benjamin J, Lanier LL, Fossum S, Dissen E (2008) KLRE/I1 and KLRE/I2: a novel pair of heterodimeric receptors that inversely regulate NK cell cytotoxicity. J Immunol 181:3177–3182PubMedGoogle Scholar
  41. Sambrook JG, Beck S (2007) Evolutionary vignettes of natural killer cell receptors. Curr Opin Immunol 19:553–560PubMedCrossRefGoogle Scholar
  42. 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
  43. Sawamura T, Kume N, Aoyama T, Moriwaki H, Hoshikawa H, Aiba Y, Tanaka T, Miwa S, Katsura Y, Kita T, Masaki T (1997) An endothelial receptor for oxidized low-density lipoprotein. Nature 386:73–77PubMedCrossRefGoogle Scholar
  44. Stet RJ, Hermsen T, Westphal AH, Jukes J, Engelsma M, Lidy Verburg-van Kemenade BM, Dortmans J, Aveiro J, Savelkoul HF (2005) Novel immunoglobulin-like transcripts in teleost fish encode polymorphic receptors with cytoplasmic ITAM or ITIM and a new structural Ig domain similar to the natural cytotoxicity receptor NKp44. Immunogenetics 57:77–89PubMedCrossRefGoogle Scholar
  45. Taylor PR, Brown GD, Reid DM, Willment JA, Martinez-Pomares L, Gordon S, Wong SY (2002) The beta-glucan receptor, dectin-1, is predominantly expressed on the surface of cells of the monocyte/macrophage and neutrophil lineages. J Immunol 169:3876–3882PubMedGoogle Scholar
  46. Tormo J, Natarajan K, Margulies DH, Mariuzza RA (1999) Crystal structure of a lectin-like natural killer cell receptor bound to its MHC class I ligand. Nature 402:623–631PubMedCrossRefGoogle Scholar
  47. Viertlboeck BC, Habermann FA, Schmitt R, Groenen MA, Du Pasquier L, Gobel TW (2005) The chicken leukocyte receptor complex: a highly diverse multigene family encoding at least six structurally distinct receptor types. J Immunol 175:385–393PubMedGoogle Scholar
  48. Warren WC, Hillier LW, Graves JAM, Birney E, Ponting CP, Grutzner F, Belov K, Miller W, Clarke L, Chinwalla AT et al (2008) Genome analysis of the platypus reveals unique signatures of evolution. Nature 453:175PubMedCrossRefGoogle Scholar
  49. Wernersson R, Pedersen AG (2003) RevTrans: multiple alignment of coding DNA from aligned amino acid sequences. Nucleic Acids Res 31:3537–3539PubMedCrossRefGoogle Scholar
  50. Willment JA, Marshall AS, Reid DM, Williams DL, Wong SY, Gordon S, Brown GD (2005) The human beta-glucan receptor is widely expressed and functionally equivalent to murine Dectin-1 on primary cells. Eur J Immunol 35:1539–1547PubMedCrossRefGoogle Scholar
  51. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555–556PubMedGoogle Scholar
  52. Yoder JA, Mueller MG, Wei S, Corliss BC, Prather DM, Willis T, Litman RT, Djeu JY, Litman GW (2001) Immune-type receptor genes in zebrafish share genetic and functional properties with genes encoded by the mammalian leukocyte receptor cluster. Proc Natl Acad Sci U S A 98:6771–6776PubMedCrossRefGoogle Scholar
  53. Yoder JA, Litman RT, Mueller MG, Desai S, Dobrinski KP, Montgomery JS, Buzzeo MP, Ota T, Amemiya CT, Trede NS, Wei S, Djeu JY, Humphray S, Jekosch K, Hernandez Prada JA, Ostrov DA, Litman GW (2004) Resolution of the novel immune-type receptor gene cluster in zebrafish. Proc Natl Acad Sci U S A 101:15706–15711PubMedCrossRefGoogle Scholar
  54. Yoshimura C, Yamaguchi M, Iikura M, Izumi S, Kudo K, Nagase H, Ishii A, Walls AF, Ra C, Iwata T, Igarashi T, Yamamoto K, Hirai K (2002) Activation markers of human basophils: CD69 expression is strongly and preferentially induced by IL-3. J Allergy Clin Immunol 109:817–823PubMedCrossRefGoogle Scholar
  55. Yusa S, Catina TL, Campbell KS (2002) SHP-1- and phosphotyrosine-independent inhibitory signaling by a killer cell Ig-like receptor cytoplasmic domain in human NK cells. J Immunol 168:5047–5057PubMedGoogle Scholar
  56. Zelensky AN, Gready JE (2003) Comparative analysis of structural properties of the C-type-lectin-like domain (CTLD). Proteins 52:466–477PubMedCrossRefGoogle Scholar
  57. Zelensky AN, Gready JE (2005) The C-type lectin-like domain superfamily. Febs J 272:6179–6217PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Emily S. W. Wong
    • 1
  • Claire E. Sanderson
    • 1
  • Janine E. Deakin
    • 2
  • Camilla M. Whittington
    • 1
  • Anthony T. Papenfuss
    • 3
  • Katherine Belov
    • 1
    Email author
  1. 1.Faculty of Veterinary ScienceUniversity of SydneySydneyAustralia
  2. 2.Research School of Biological SciencesAustralian National UniversityCanberraAustralia
  3. 3.Bioinformatics DivisionThe Walter and Eliza Hall Institute for Medical ResearchParkvilleAustralia

Personalised recommendations