Identification of natural killer cell receptor genes in the genome of the marsupial Tasmanian devil (Sarcophilus harrisii)

Immunogenetics

Volumn 65, Issue 1, 2013, Pages 25-35

  Van Der Kraan, Lauren E ^a   Wong, Emily S W ^a   Lo, Nathan ^a   Ujvari, Beata ^a   Belov, Katherine ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Evolution; LRC; Marsupial; Natural killer cell receptors; NKC; Tasmanian devil

Indexed keywords

CD69 ANTIGEN; CLEC1A PROTEIN; CLEC1B PROTEIN; CLEC4E PROTEIN; IMMUNOGLOBULIN; KLRK1 PROTEIN; LEUKOCYTE RECEPTOR COMPLEX; LYMPHOCYTE RECEPTOR; NATURAL KILLER CELL RECEPTOR; NATURAL KILLER CELL RECEPTOR NKG2D; UNCLASSIFIED DRUG;

ARTICLE; CHROMOSOME 5; CHROMOSOME ANALYSIS; GENE FUNCTION; GENE IDENTIFICATION; GENOME ANALYSIS; MARSUPIAL; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN STRUCTURE; SARCOPHILUS HARRISII; SEQUENCE ANALYSIS;

ANIMALS; BASE SEQUENCE; EVOLUTION, MOLECULAR; GENOME; MARSUPIALIA; NEOPLASMS; PHYLOGENY; RECEPTORS, NATURAL KILLER CELL; SEQUENCE ALIGNMENT;

DIDELPHIDAE; EUTHERIA; MAMMALIA; METATHERIA; SARCOPHILUS HARRISII;

EID: 84872343411     PISSN: 00937711     EISSN: 14321211     Source Type: Journal    
DOI: 10.1007/s00251-012-0643-z     Document Type: Article

References (61)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403-410
2. Anderson KJ, Allen RL (2009) Regulation of T-cell immunity by leucocyte immunoglobulin-like receptors: innate immune receptors for self on antigen-presenting cells. Immunology 127:8-17
3. Barrow A, Trowsdale J (2008) The extended human leukocyte receptor complex: diverse ways of modulating immune responses. Immunol Rev 224:98-123
4. Belov K, Sanderson CE, Deakin JE, Wong ESW, 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 17:982-991
5. Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A (2007) The delayed rise of present-day mammals. Nature 446:507-512
6. Blasioli J, Paust S, Thomas ML (1999) Definition of the sites of interaction between the protein tyrosine phosphatase SHP-1 and CD22. J Biol Chem 274:2303-2307
7. Brown GK, Kreiss A, Lyons AB, Woods GM (2011) Natural killer cell mediated cytotoxic responses in the Tasmanian devil. PLoS One 6:e24475
8. Burgess SJ, Maasho K, Masilamani M, Narayanan S, Borrego F, Coligan JE (2008) The NKG2D receptor: immunobiology and clinical implications. Immunol Res 40:18-34
9. Cao H, de Bono B, Belov K, Wong E, Trowsdale J, Barrow A (2009) Comparative genomics indicates the mammalian CD33rSiglec locus evolved by an ancient large-scale inverse duplication and suggests all Siglecs share a common ancestral region. Immunogenetics 61:401-417
10. Chiang H-I, Zhou H, Raudsepp T, Jesudhasan P, Zhu J (2007) Chicken CD69 and CD94/NKG2-like genes in a chromosomal region syntenic to mammalian natural killer gene complex. Immunogenetics 59:603-611
11. Colonna M, Samaridis J, Angman L (2000) Molecular characterization of two novel C-type lectin-like receptors, one of which is selectively expressed in human dendritic cells. Eur J Immunol 30:697-704
12. Cummings RD, McEver RP (2009) C-type lectins. In: Varki A, Cummings R, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME (eds) Essentials of glycobiology, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
13. Desai S, Heffelfinger A, Orcutt T, Litman G, Yoder J (2008) The medaka novel immune-type receptor (NITR) gene clusters reveal an extraordinary degree of divergence in variable domains. BMC Evol Biol 8:177
14. Eagle RA, Trowsdale J (2007) Promiscuity and the single receptor: NKG2D. Nat Rev Immunol 7:737-744
15. Edgar R (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinforma 5:113
16. Flornes LM, Bryceson YT, Spurkland A, Lorentzen JC, Dissen E, Fossum S (2004) Identification of lectin-like receptors expressed by antigen presenting cells and neutrophils and their mapping to a novel gene complex. Immunogenetics 56:506-517
17. Gay LJ, Felding-Habermann B (2011) Contribution of platelets to tumour metastasis. Nat Rev Cancer 11:123-134
18. Hall TA (1999) BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95-98
19. 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 103:3192-3197
20. Hedges SB, Dudley J, Kumar S (2006) TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22:2971-2972
21. Holz P (2008) Dasyurids. In: Vogelnest V, Woods R (eds) Medicine of Australian mammals. CSIRO Publishing, Melbourne, pp 359-382
22. Kammerer R, Zimmermann W (2010) Coevolution of activating and inhibitory receptors within mammalian carcinoembryonic antigen families. BMC Biol 8:12
23. Kelley J, Walter L, Trowsdale J (2005) Comparative genomics of natural killer cell receptor gene clusters. PLoS Genet 1:e27
24. Kirsch JAW, Springer MS, Lapointe FJ (1997) DNA-hybridisation studies of marsupials and their implications for metatherian classification. Aust J Zool 45:211-280
25. 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:e73
26. Martin AM, Kulski JK, Witt C, Pontarotti P, Christiansen FT (2002) Leukocyte Ig-like receptor complex (LRC) in mice and men. Trends Immunol 23:81-88
27. Martin P, Gomez M, Lamana A, Cruz-Adalia A, Ramirez-Huesca M, Ursa MA, Yanez-Mo M, Sanchez-Madrid F (2010) CD69 association with Jak3/Stat5 proteins regulates Th17 cell differentiation. Mol Cell Biol 30:4877-4889
28. McIntire RH, Sifers T, Platt JS, Ganacias KG, Langat DK, Hunt JS (2008) Novel HLA-G-binding leukocyte immunoglobulin-like Receptor (LILR) expression patterns in human placentas and umbilical cords. Placenta 29:631-638
29. Miller W, Hayes VM, Ratan A, Petersen DC, Wittekindt NE, Miller J, Walenz B, Knight J, Qi J, Zhao F, Wang Q, Bedoya-Reina OC, Katiyar N, Tomsho LP, Kasson LM, Hardie R-A, Woodbridge P, Tindall EA, Bertelsen MF, Dixon D, Pyecroft S, Helgen KM, Lesk AM, Pringle TH, Patterson N, Zhang Y, Kreiss A, Woods GM, Jones ME, Schuster SC (2011) Genetic diversity and population structure of the endangered marsupial Sarcophilus harrisii (Tasmanian devil). Proc Natl Acad Sci 108:12348-12353
30. Murchison EP, Schulz-Trieglaff OB, Ning Z, Alexandrov LB, Bauer MJ, Fu B, Hims M, Ding Z, Ivakhno S, Stewart C, Ng BL, Wong W, Aken B, White S, Alsop A, Becq J, Bignell GR, Cheetham RK, Cheng W, Connor TR, Cox AJ, Feng Z-P, Gu Y, Grocock RJ, Harris SR, Khrebtukova I, Kingsbury Z, Kowarsky M, Kreiss A, Luo S, Marshall J, McBride DJ, Murray L, Pearse A-M, Raine K, Rasolonjatovo I, Shaw R, Tedder P, Tregidgo C, Vilella AJ, Wedge DC, Woods GM, Gormley N, Humphray S, Schroth G, Smith G, Hall K, Searle SMJ, Carter NP, Papenfuss AT, Futreal PA, Campbell PJ, Yang F, Bentley DR, Evers DJ, Stratton MR (2012) Genome sequencing and analysis of the Tasmanian devil and its transmissible cancer. Cell 148:780-791
31. Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39:121-152
32. Nieswandt B, Watson SP (2003) Platelet-collagen interaction: is GPVI the central receptor? Blood 102:449-461
33. Nylenna Ø, Naper C, Vaage JT, Woon PY, Gauguier D, Dissen E, Ryan JC, Fossum S (2005) The genes and gene organization of the Ly49 region of the rat natural killer cell gene complex. Eur J Immunol 35:261-272
34. Ozaki Y, Suzuki-Inoue K, Inoue O (2009) Novel interactions in platelet biology: CLEC-2/podoplanin and laminin/GPVI. J Thromb Haemost 7:191-194
35. Pearse AM, Swift K (2006) Allograft theory: transmission of devil facial-tumour disease. Nature 439:549
36. Renfree M, Papenfuss A, Deakin J, Lindsay J, Heider T, Belov K, Rens W, Waters P, Pharo E, Shaw G, Wong E, Lefevre C, Nicholas K, Kuroki Y, Wakefield M, Zenger K, Wang C, Ferguson-Smith M, Nicholas F, Hickford D, Yu H, Short K, Siddle H, Frankenberg S, Chew K, Menzies B, Stringer J, Suzuki S, Hore T, Delbridge M (2011) Genome sequence of an Australian kangaroo, Macropus eugenii, provides insight into the evolution of mammalian reproduction and development. Genome Biol 12:414
37. Rogers SL, Göbel 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 174:3475-3483
38. Sanderson CE (2009) Immune genes: genomic and diversity studies in marsupials and monotremes. Dissertation, University of Sydney
39. 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 100:7779-7784
40. Séverin S, Pollitt AY, Navarro-Nuñez L, Nash CA, Mourão-Sá D, Eble JA, Senis YA, Watson SP (2011) Syk-dependent phosphorylation of CLEC-2. J Biol Chem 286:4107-4116
41. Sloane DE, Tedla N, Awoniyi M, MacGlashan DW, Borges L, Austen KF, Arm JP (2004) Leukocyte immunoglobulin-like receptors: novel innate receptors for human basophil activation and inhibition. Blood 104:2832-2839
42. Sobanov Y, Bernreiter A, Derdak S, Mechtcheriakova D, Schweighofer B, Düchler M, Kalthoff F, Hofer E (2001) A novel cluster of lectin-like receptor genes expressed in monocytic, dendritic and endothelial cells maps close to the NK receptor genes in the human NK gene complex. Eur J Immunol 31:3493-3503
43. Suzuki-Inoue K, Fuller GLJ, García Á, Eble JA, Pöhlmann S, Inoue O, Gartner TK, Hughan SC, Pearce AC, Laing GD, Theakston RDG, Schweighoffer E, Zitzmann N, Morita T, Tybulewicz VLJ, Ozaki Y, Watson SP (2006) A novel Syk-dependent mechanism of platelet activation by the C-type lectin receptor CLEC-2. Blood 107:542-549
44. Takahashi T, Yawata M, Raudsepp T, Lear TL, Chowdhary BP, Antczak DF, Kasahara M (2004) Natural killer cell receptors in the horse: evidence for the existence of multiple transcribed Ly49 genes. Eur J Immunol 34:773-784
45. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739
46. Thebault P, Lhermite N, Tilly G, Le Texier L, Quillard T, Heslan M, Anegon I, Soulillou J-P, Brouard S, Charreau B, Cuturi M-C, Chiffoleau E (2009) The C-type lectin-like receptor CLEC-1, expressed by myeloid cells and endothelial cells, is up-regulated by immunoregulatory mediators and moderates T cell activation. J Immunol 183:3099-3108
47. Varki A, Crocker PR (2009) I-type lectins. In: Varki A, Cummings R, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME (eds) Essentials of glycobiology, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
48. Viertlboeck BC, Habermann FA, Schmitt R, Groenen MAM, Du Pasquier L, Göbel TW (2005) The chicken leukocyte receptor complex: a highly diverse multigene family encoding at least six structurally distinct receptor types. J Immunol 175:385-393
49. Walker JA, Smith KGC (2008) CD22: an inhibitory enigma. Immunology 123:314-325
50. Wong ES, Sanderson CE, Deakin JE, Whittington CM, Papenfuss AT, Belov K (2009) Identification of natural killer cell receptor clusters in the platypus genome reveals an expansion of C-type lectin genes. Immunogenetics 61:565-579
51. Wong E, Papenfuss A, Belov K (2011) Immunome database for marsupials and monotremes. BMC Immunol 12:48
52. Woods G, Kreiss A, Belov K, Siddle H, Obendorf D, Muller H (2007) The immune response of the Tasmanian devil (Sarcophilus harrisii) and devil facial tumour disease. Ecohealth 4:338-345
53. Yamasaki S, Ishikawa E, Sakuma M, Hara H, Ogata K, Saito T (2008) Mincle is an ITAM-coupled activating receptor that senses damaged cells. Nat Immunol 9:1179-1188
54. Yamasaki S, Matsumoto M, Takeuchi O, Matsuzawa T, Ishikawa E, Sakuma M, Tateno H, Uno J, Hirabayashi J, Mikami Y, Takeda K, Akira S, Saito T (2009) C-type lectin Mincle is an activating receptor for pathogenic fungus, Malassezia. Proc Natl Acad Sci 106:1897-1902
55. Yoder JA (2004) Investigating the morphology, function and genetics of cytotoxic cells in bony fish. Comp Biochem Physiol 138:271-280
56. Yoder J, Litman G (2011) The phylogenetic origins of natural killer receptors and recognition: relationships, possibilities, and realities. Immunogenetics 63:123-141
57. Yoder J, Cannon J, Litman R, Murphy C, Freeman J, Litman G (2008) Evidence for a transposition event in a second NITR gene cluster in zebrafish. Immunogenetics 60:257-265
58. Zelensky AN, Gready JE (2003) Comparative analysis of structural properties of the C-type-lectin-like domain (CTLD). Protein Struct Funct Bioinform 52:466-477
59. Zelensky A, Gready J (2004) C-type lectin-like domains in Fugu rubripes. BMC Genomics 5:51
60. Zelensky AN, Gready JE (2005) The C-type lectin-like domain superfamily. FEBS J 272:6179-6217
61. Ziegler SF, Ramsdell F, Hjerrild KA, Armitage RJ, Grabstein KH, Hennen KB, Farrah T, Fanslow WC, Shevach EM, Alderson MR (1993) Molecular characterization of the early activation antigen CD69: a type II membrane glycoprotein related to a family of natural killer cell activation antigens. Eur J Immunol 23:1643-1648