Mouse Nkrp1-Clr Gene Cluster Sequence and Expression Analyses Reveal Conservation of Tissue-Specific MHC-Independent Immunosurveillance

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Zhang, Qiang ^a   Rahim, Mir Munir A ^a   Allan, David S J ^b   Tu, Megan M ^a   Belanger, Simon ^a   Abou Samra, Elias ^a   Ma, Jaehun ^b   Sekhon, Harman S ^c   Fairhead, Todd ^d   Zein, Haggag S ^a,e   Carlyle, James R ^b   Anderson, Stephen K ^f   Makrigiannis, Andrew P ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b Canada   (Canada)

^c UNIVERSITY OF OTTAWA   (Canada)

^d OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^e CAIRO UNIVERSITY   (Egypt)

^f SAIC FREDERICK INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL TYPE; CLR GENE; CONTROLLED STUDY; EPITHELIUM CELL; GENE; GENE CLUSTER; GENE EXPRESSION; GENE ORDER; GENE SEQUENCE; GENETIC POLYMORPHISM; GENETIC TRANSCRIPTION; HAPLOTYPE; HEMATOPOIETIC CELL; IMMUNOSURVEILLANCE; IN SITU HYBRIDIZATION; LEUKOCYTE; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR EVOLUTION; MOUSE; MOUSE STRAIN; MUSCLE CELL; NKRP1 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PSEUDOGENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; STEM CELL;

ALLELES; ANIMALS; BASE SEQUENCE; CHROMOSOMES, ARTIFICIAL, BACTERIAL; COMPARATIVE GENOMIC HYBRIDIZATION; DNA PRIMERS; HAPLOTYPES; MAJOR HISTOCOMPATIBILITY COMPLEX; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MULTIGENE FAMILY; POLYMERASE CHAIN REACTION; REPRESSOR PROTEINS; RNA, MESSENGER;

EID: 84870727260     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050561     Document Type: Article

References (48)

1. Lanier LL, (2005) NK cell recognition. Annu Rev Immunol 23: 225-274.
2. Gasser S, Orsulic S, Brown EJ, Raulet DH, (2005) The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 436: 1186-1190.
3. Carlyle JR, Mesci A, Fine JH, Chen P, Belanger S, et al. (2008) Evolution of the Ly49 and Nkrp1 recognition systems. Semin Immunol 20: 321-330.
4. Plougastel B, Dubbelde C, Yokoyama WM, (2001) Cloning of Clr, a new family of lectin-like genes localized between mouse Nkrp1a and Cd69. Immunogenetics 53: 209-214.
5. Plougastel B, Matsumoto K, Dubbelde C, Yokoyama WM, (2001) Analysis of a 1-Mb BAC contig overlapping the mouse Nkrp1 cluster of genes: cloning of three new Nkrp1 members, Nkrp1d, Nkrp1e, and Nkrp1f. Immunogenetics 53: 592-598.
6. Chen P, Belanger S, Aguilar OA, Zhang Q, St-Laurent A, et al. (2011) Analysis of the mouse 129-strain Nkrp1-Clr gene cluster reveals conservation of genomic organization and functional receptor-ligand interactions despite significant allelic polymorphism. Immunogenetics 63: 627-640.
7. Carlyle JR, Mesci A, Ljutic B, Belanger S, Tai LH, et al. (2006) Molecular and genetic basis for strain-dependent NK1.1 alloreactivity of mouse NK cells. J Immunol 176: 7511-7524.
8. 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.
9. Aust JG, Gays F, Mickiewicz KM, Buchanan E, Brooks CG, (2009) The expression and function of the NKRP1 receptor family in C57BL/6 mice. J Immunol 183: 106-116.
10. Iizuka K, Naidenko OV, Plougastel BF, Fremont DH, Yokoyama WM, (2003) Genetically linked C-type lectin-related ligands for the NKRP1 family of natural killer cell receptors. Nat Immunol 4: 801-807.
11. Ryan JC, Turck J, Niemi EC, Yokoyama WM, Seaman WE, (1992) Molecular cloning of the NK1.1 antigen, a member of the NKR-P1 family of natural killer cell activation molecules. J Immunol 149: 1631-1635.
12. Arase H, Arase N, Saito T, (1996) Interferon gamma production by natural killer (NK) cells and NK1.1+ T cells upon NKR-P1 cross-linking. J Exp Med 183: 2391-2396.
13. Carlyle JR, Jamieson AM, Gasser S, Clingan CS, Arase H, et al. (2004) Missing self-recognition of Ocil/Clr-b by inhibitory NKR-P1 natural killer cell receptors. Proc Natl Acad Sci U S A 101: 3527-3532.
14. Fine JH, Chen P, Mesci A, Allan DS, Gasser S, et al. (2010) Chemotherapy-induced genotoxic stress promotes sensitivity to natural killer cell cytotoxicity by enabling missing-self recognition. Cancer Res 70: 7102-7113.
15. Williams KJ, Wilson E, Davidson CL, Aguilar OA, Fu L, et al. (2012) Poxvirus Infection-Associated Downregulation of C-Type Lectin-Related-b Prevents NK Cell Inhibition by NK Receptor Protein-1B. J Immunol 188: 4980-4991.
16. Kveberg L, Dai KZ, Inngjerdingen M, Brooks CG, Fossum S, et al. (2011) Phylogenetic and functional conservation of the NKR-P1F and NKR-P1G receptors in rat and mouse. Immunogenetics 63: 429-436.
17. Rosen DB, Bettadapura J, Alsharifi M, Mathew PA, Warren HS, et al. (2005) Cutting edge: lectin-like transcript-1 is a ligand for the inhibitory human NKR-P1A receptor. J Immunol 175: 7796-7799.
18. Aldemir H, Prod'homme V, Dumaurier MJ, Retiere C, Poupon G, et al. (2005) Cutting edge: lectin-like transcript 1 is a ligand for the CD161 receptor. J Immunol 175: 7791-7795.
19. Vogler I, Steinle A, (2011) Vis-a-vis in the NKC: genetically linked natural killer cell receptor/ligand pairs in the natural killer gene complex (NKC). J Innate Immun 3: 227-235.
20. Carlyle JR, Martin A, Mehra A, Attisano L, Tsui FW, et al. (1999) Mouse NKR-P1B, a novel NK1.1 antigen with inhibitory function. J Immunol 162: 5917-5923.
21. Arase N, Arase H, Park SY, Ohno H, Ra C, et al. (1997) Association with FcRgamma is essential for activation signal through NKR-P1 (CD161) in natural killer (NK) cells and NK1.1+ T cells. J Exp Med 186: 1957-1963.
22. Ljutic B, Carlyle JR, Filipp D, Nakagawa R, Julius M, et al. (2005) Functional requirements for signaling through the stimulatory and inhibitory mouse NKR-P1 (CD161) NK cell receptors. J Immunol 174: 4789-4796.
23. Ryan JC, Seaman WE, (1997) Divergent functions of lectin-like receptors on NK cells. Immunol Rev 155: 79-89.
24. Higuchi DA, Cahan P, Gao J, Ferris ST, Poursine-Laurent J, et al. (2010) Structural variation of the mouse natural killer gene complex. Genes Immun 11: 637-648.
25. Lattin JE, Schroder K, Su AI, Walker JR, Zhang J, et al. (2008) Expression analysis of G Protein-Coupled Receptors in mouse macrophages. Immunome Res 4: 5.
26. Wu C, Orozco C, Boyer J, Leglise M, Goodale J, et al. (2009) BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol 10: R130.
27. Gregorieff A, Clevers H (2010) In situ hybridization to identify gut stem cells. Curr Protoc Stem Cell Biol Chapter 2: Unit.
28. Wilhelm BT, Gagnier L, Mager DL, (2002) Sequence analysis of the Ly49 cluster in C57BL/6 mice: a rapidly evolving multigene family in the immune system. Genomics 80: 646-661.
29. Makrigiannis AP, Patel D, Goulet ML, Dewar K, Anderson SK, (2005) Direct sequence comparison of two divergent class I MHC natural killer cell receptor haplotypes. Genes Immun 6: 71-83.
30. Belanger S, Tai LH, Anderson SK, Makrigiannis AP, (2008) Ly49 cluster sequence analysis in a mouse model of diabetes: an expanded repertoire of activating receptors in the NOD genome. Genes Immun 9: 509-521.
31. Zhou H, Kartsogiannis V, Hu YS, Elliott J, Quinn JM, et al. (2001) A novel osteoblast-derived C-type lectin that inhibits osteoclast formation. J Biol Chem 276: 14916-14923.
32. Tian W, Nunez R, Cheng S, Ding Y, Tumang J, et al. (2005) C-type lectin OCILRP2/Clr-g and its ligand NKRP1f costimulate T cell proliferation and IL-2 production. Cell Immunol 234: 39-53.
33. Zohar O, Reiter Y, Bennink JR, Lev A, Cavallaro S, et al. (2008) Cutting edge: MHC class I-Ly49 interaction regulates neuronal function. J Immunol 180: 6447-6451.
34. Heng TS, Painter MW, (2008) The Immunological Genome Project: networks of gene expression in immune cells. Nat Immunol 9: 1091-1094.
35. Blasius AL, Barchet W, Cella M, Colonna M, (2007) Development and function of murine B220+CD11c+NK1.1+ cells identify them as a subset of NK cells. J Exp Med 204: 2561-2568.
36. Vosshenrich CA, Lesjean-Pottier S, Hasan M, Richard-Le GO, Corcuff E, et al. (2007) CD11cloB220+ interferon-producing killer dendritic cells are activated natural killer cells. J Exp Med 204: 2569-2578.
37. Yokoyama WM, Ryan JC, Hunter JJ, Smith HR, Stark M, et al. (1991) cDNA cloning of mouse NKR-P1 and genetic linkage with LY-49. Identification of a natural killer cell gene complex on mouse chromosome 6. J Immunol 147: 3229-3236.
38. Brodin P, Lakshmikanth T, Johansson S, Karre K, Hoglund P, (2009) The strength of inhibitory input during education quantitatively tunes the functional responsiveness of individual natural killer cells. Blood 113: 2434-2441.
39. Joncker NT, Fernandez NC, Treiner E, Vivier E, Raulet DH, (2009) NK cell responsiveness is tuned commensurate with the number of inhibitory receptors for self-MHC class I: the rheostat model. J Immunol 182: 4572-4580.
40. Proteau M-F, Rousselle E, Makrigiannis AP, (2004) Mapping of the BALB/c Ly49 cluster defines a minimal natural killer cell receptor gene repertoire. Genomics 84: 669-677.
41. Stoye JP, (2012) Studies of endogenous retroviruses reveal a continuing evolutionary saga. Nat Rev Microbiol 10: 395-406.
42. Balada E, Vilardell-Tarres M, Ordi-Ros J, (2010) Implication of human endogenous retroviruses in the development of autoimmune diseases. Int Rev Immunol 29: 351-370.
43. Flornes LM, Nylenna O, Saether PC, Daws MR, Dissen E, et al. (2010) The complete inventory of receptors encoded by the rat natural killer cell gene complex. Immunogenetics 62: 521-530.
44. Voigt S, Mesci A, Ettinger J, Fine JH, Chen P, et al. (2007) Cytomegalovirus evasion of innate immunity by subversion of the NKR-P1B:Clr-b missing-self axis. Immunity 26: 617-627.
45. Kveberg L, Dai KZ, Westgaard IH, Daws MR, Fossum S, et al. (2009) Two major groups of rat NKR-P1 receptors can be distinguished based on chromosomal localization, phylogenetic analysis and Clr ligand binding. Eur J Immunol 39: 541-551.
46. Rosen DB, Cao W, Avery DT, Tangye SG, Liu YJ, et al. (2008) Functional consequences of interactions between human NKR-P1A and its ligand LLT1 expressed on activated dendritic cells and B cells. J Immunol 180: 6508-6517.
47. Germain C, Meier A, Jensen T, Knapnougel P, Poupon G, et al. (2011) Induction of lectin-like transcript 1 (LLT1) protein cell surface expression by pathogens and interferon-gamma contributes to modulate immune responses. J Biol Chem 286: 37964-37975.
48. de HS, Woltman AM, Trouw LA, Bakker AC, Kamerling SW, et al. (2005) Renal tubular epithelial cells modulate T-cell responses via ICOS-L and B7-H1. Kidney Int 68: 2091-2102.