A locus on mouse chromosome 13 inversely regulates CD1d expression and the development of invariant natural killer T-cells

Genes and Immunity

Volumn 16, Issue 3, 2015, Pages 221-230

  Tsaih, S W ^a   Presa, M ^b   Khaja, S ^a   Ciecko, A E ^a   Serreze, D V ^b   Chen, Y G ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b JACKSON LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD1D ANTIGEN; CD150 ANTIGEN; CELL SURFACE RECEPTOR; LEUKOCYTE ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL CELL; ANTIGEN EXPRESSION; ANTIGENIC VARIATION; ARTICLE; BONE MARROW TRANSPLANTATION; CELL COMPARTMENTALIZATION; CELL MATURATION; CHROMOSOME 13; FEMALE; GENE FREQUENCY; GENE MAPPING; GENETIC REGULATION; HEMATOPOIETIC CELL; INBRED STRAIN; MALE; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; T LYMPHOCYTE SUBPOPULATION; THYMOCYTE; ANIMAL; ANIMAL MODEL; CELL DIFFERENTIATION; CHROMOSOMAL MAPPING; CHROMOSOME; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INSTITUTE FOR CANCER RESEARCH MOUSE; LYMPHOCYTE COUNT; METABOLISM; NONOBESE DIABETIC MOUSE; PHENOTYPE;

MUS;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD1D; CELL DIFFERENTIATION; CHROMOSOME MAPPING; CHROMOSOMES, MAMMALIAN; GENE EXPRESSION REGULATION; LYMPHOCYTE COUNT; MICE; MICE, INBRED ICR; MICE, INBRED NOD; MODELS, ANIMAL; NATURAL KILLER T-CELLS; PHENOTYPE; QUANTITATIVE TRAIT LOCI; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, CELL SURFACE; SIGNALING LYMPHOCYTIC ACTIVATION MOLECULE FAMILY MEMBER 1; THYMOCYTES;

EID: 84928582595     PISSN: 14664879     EISSN: 14765470     Source Type: Journal    
DOI: 10.1038/gene.2014.81     Document Type: Article

References (47)

1. Bendelac A, Savage PB, Teyton L. The biology of NKT cells. Annu Rev Immunol 2007; 25: 297-336.
2. Matsuda JL, Mallevaey T, Scott-Browne J, Gapin L. CD1d-restricted iNKT cells, the 'Swiss-Army knife' of the immune system. Curr Opin Immunol 2008; 20: 358-368.
3. Chen YG, Tsaih SW, Serreze DV. Genetic control of murine invariant natural killer T-cell development dynamically differs dependent on the examined tissue type. Genes Immun 2012; 13: 164-174.
4. Chan AC, Serwecinska L, Cochrane A, Harrison LC, Godfrey DI, Berzins SP. Immune characterization of an individual with an exceptionally high natural killer T cell frequency and her immediate family. Clin Exp Immunol 2009; 156: 238-245.
5. Montoya CJ, Pollard D, Martinson J, Kumari K, Wasserfall C, Mulder CB et al. Characterization of human invariant natural killer T subsets in health and disease using a novel invariant natural killer T cell-clonotypic monoclonal antibody, 6B11. Immunology 2007; 122: 1-14.
6. Kis J, Engelmann P, Farkas K, Richman G, Eck S, Lolley J et al. Reduced CD4+ subset and Th1 bias of the human iNKT cells in type 1 diabetes mellitus. J Leukoc Biol 2007; 81: 654-662.
7. Berzins SP, Cochrane AD, Pellicci DG, Smyth MJ, Godfrey DI. Limited correlation between human thymus and blood NKT cell content revealed by an ontogeny study of paired tissue samples. Eur J Immunol 2005; 35: 1399-1407.
8. Lee PT, Putnam A, Benlagha K, Teyton L, Gottlieb PA, Bendelac A. Testing the NKT cell hypothesis of human IDDM pathogenesis. J Clin Invest 2002; 110: 793-800.
9. Chen YG, Driver JP, Silveira PA, Serreze DV. Subcongenic analysis of genetic basis for impaired development of invariant NKT cells in NOD mice. Immunogenetics 2007; 59: 705-712.
10. Esteban LM, Tsoutsman T, Jordan MA, Roach D, Poulton LD, Brooks A et al. Genetic control of NKT cell numbers maps to major diabetes and lupus loci. J Immunol 2003; 171: 2873-2878.
11. Fletcher JM, Jordan MA, Snelgrove SL, Slattery RM, Dufour FD, Kyparissoudis K et al. Congenic analysis of the NKT cell control gene Nkt2 implicates the peroxisomal protein Pxmp4. J Immunol 2008; 181: 3400-3412.
12. Hammond KJ, Poulton LD, Palmisano LJ, Silveira PA, Godfrey DI, Baxter AG. alpha/beta-T cell receptor (TCR)+CD4-CD8-(NKT) thymocytes prevent insulin-dependent diabetes mellitus in nonobese diabetic (NOD)/Lt mice by the influence of interleukin (IL)-4 and/or IL-10. J Exp Med 1998; 187: 1047-1056.
13. Hong S, Wilson MT, Serizawa I, Wu L, Singh N, Naidenko OV et al. The natural killer T-cell ligand alpha-galactosylceramide prevents autoimmune diabetes in non-obese diabetic mice. Nat Med 2001; 7: 1052-1056.
14. Lehuen A, Lantz O, Beaudoin L, Laloux V, Carnaud C, Bendelac A et al. Overexpression of natural killer T cells protects Valpha14-Jalpha281 transgenic nonobese diabetic mice against diabetes. J Exp Med 1998; 188: 1831-1839.
15. Matsuki N, Stanic AK, Embers ME, Van Kaer L, Morel L, Joyce S. Genetic dissection of V alpha 14J alpha 18 natural T cell number and function in autoimmuneprone mice. J Immunol 2003; 170: 5429-5437.
16. Naumov YN, Bahjat KS, Gausling R, Abraham R, Exley MA, Koezuka Y et al. Activation of CD1d-restricted T cells protects NOD mice from developing diabetes by regulating dendritic cell subsets. Proc Natl Acad Sci USA 2001; 98: 13838-13843.
17. Sharif S, Arreaza GA, Zucker P, Mi QS, Sondhi J, Naidenko OV et al. Activation of natural killer T cells by alpha-galactosylceramide treatment prevents the onset and recurrence of autoimmune type 1 diabetes. Nat Med 2001; 7: 1057-1062.
18. Shi FD, Flodstrom M, Balasa B, Kim SH, Van Gunst K, Strominger JL et al. Germ line deletion of the CD1 locus exacerbates diabetes in the NOD mouse. Proc Natl Acad Sci USA 2001; 98: 6777-6782.
19. Ueno A, Wang J, Cheng L, Im JS, Shi Y, Porcelli SA et al. Enhanced early expansion and maturation of semi-invariant NK T cells inhibited autoimmune pathogenesis in congenic nonobese diabetic mice. J Immunol 2008; 181: 6789-6796.
20. Wang B, Geng YB, Wang CR., CD1-restricted NK. T cells protect nonobese diabetic mice from developing diabetes. J Exp Med 2001; 194: 313-320.
21. Zekavat G, Mozaffari R, Arias VJ, Rostami SY, Badkerhanian A, Tenner AJ et al. A novel CD93 polymorphism in non-obese diabetic (NOD) and NZB/W F1 mice is linked to a CD4+ iNKT cell deficient state. Immunogenetics 2010; 62: 397-407.
22. Leiter E, Atkinson M (eds). NOD Mice and Related Strains: Research Applications in Diabetes, AIDS, Cancer and Other Diseases. R.G. Landes Company: Austin, TX, USA, 1998.
23. Tsaih SW, Khaja S, Ciecko AE, MacKinney E, Chen YG. Genetic control of murine invariant natural killer T cells maps to multiple type 1 diabetes regions. Genes Immun 2013; 14: 380-386.
24. Griewank K, Borowski C, Rietdijk S, Wang N, Julien A, Wei DG et al. Homotypic interactions mediated by Slamf1 and Slamf6 receptors control NKT cell lineage development. Immunity 2007; 27: 751-762.
25. Hu T, Simmons A, Yuan J, Bender TP, Alberola-Ila J. The transcription factor c-Myb primes CD4+CD8+ immature thymocytes for selection into the iNKT lineage. Nat Immunol 2010; 11: 435-441.
26. Kageyama R, Cannons JL, Zhao F, Yusuf I, Lao C, Locci M et al. The receptor Ly108 functions as a SAP adaptor-dependent on-off switch for T cell help to B cells and NKT cell development. Immunity 2012; 36: 986-1002.
27. Dutta M, Kraus ZJ, Gomez-Rodriguez J, Hwang SH, Cannons JL, Cheng J et al. A role for Ly108 in the induction of promyelocytic zinc finger transcription factor in developing thymocytes. J Immunol 2013; 190: 2121-2128.
28. Sintes J, Cuenca M, Romero X, Bastos R, Terhorst C, Angulo A et al. Cutting edge: Ly9 (CD229), a SLAM family receptor, negatively regulates the development of thymic innate memory-like CD8+ T and invariant NKT cells. J Immunol 2013; 190: 21-26.
29. Jordan MA, Fletcher JM, Pellicci D, Baxter AG. Slamf1, the NKT cell control gene Nkt1. J Immunol 2007; 178: 1618-1627.
30. Jordan MA, Fletcher JM, Jose R, Chowdhury S, Gerlach N, Allison J et al. Role of SLAM in NKT cell development revealed by transgenic complementation in NOD mice. J Immunol 2011; 186: 3953-3965.
31. Bendelac A. Positive selection of mouse NK1+ T cells by CD1-expressing cortical thymocytes. J Exp Med 1995; 182: 2091-2096.
32. Coles MC, Raulet DH. NK1.1+ T cells in the liver arise in the thymus and are selected by interactions with class I molecules on CD4+CD8+ cells. J Immunol 2000; 164: 2412-2418.
33. Schumann J, Pittoni P, Tonti E, Macdonald HR, Dellabona P, Casorati G. Targeted expression of human CD1d in transgenic mice reveals independent roles for thymocytes and thymic APCs in positive and negative selection of Valpha14i NKT cells. J Immunol 2005; 175: 7303-7310.
34. Wei DG, Lee H, Park SH, Beaudoin L, Teyton L, Lehuen A et al. Expansion and longrange differentiation of the NKT cell lineage in mice expressing CD1d exclusively on cortical thymocytes. J Exp Med 2005; 202: 239-248.
35. Zimmer MI, Colmone A, Felio K, Xu H, Ma A, Wang CR. A cell-type specific CD1d expression program modulates invariant NKT cell development and function. J Immunol 2006; 176: 1421-1430.
36. Weinreich MA, Odumade OA, Jameson SC, Hogquist KA. T cells expressing the transcription factor PLZF regulate the development of memory-like CD8+ T cells. Nat Immunol 2010; 11: 709-716.
37. Lee YJ, Holzapfel KL, Zhu J, Jameson SC, Hogquist KA. Steady-state production of IL-4 modulates immunity in mouse strains and is determined by lineage diversity of iNKT cells. Nat Immunol 2013; 14: 1146-1154.
38. Honey K, Benlagha K, Beers C, Forbush K, Teyton L, Kleijmeer MJ et al. Thymocyte expression of cathepsin L is essential for NKT cell development. Nat Immunol 2002; 3: 1069-1074.
39. Borg ZD, Benoit PJ, Lilley GW, Aktan I, Chant A, DeVault VL et al. Polymorphisms in the CD1d promoter that regulate CD1d gene expression are associated with impaired NKT cell development. J Immunol 2014; 192: 189-199.
40. Zhang F, Liang ZY, Matsuki N, Van Kaer L, Joyce S, Wakeland EK et al. A murine locus on chromosome 18 controls NKT cell homeostasis and Th cell differentiation. J Immunol 2003; 171: 4613-4620.
41. Tsukamoto K, Ohtsuji M, Shiroiwa W, Lin Q, Nakamura K, Tsurui H et al. Aberrant genetic control of invariant TCR-bearing NKT cell function in New Zealand mouse strains: possible involvement in systemic lupus erythematosus pathogenesis. J Immunol 2008; 180: 4530-4539.
42. Chun T, Page MJ, Gapin L, Matsuda JL, Xu H, Nguyen H et al. CD1d-expressing dendritic cells but not thymic epithelial cells can mediate negative selection of NKT cells. J Exp Med 2003; 197: 907-918.
43. Wandstrat AE, Nguyen C, Limaye N, Chan AY, Subramanian S, Tian XH et al. Association of extensive polymorphisms in the SLAM/CD2 gene cluster with murine lupus. Immunity 2004; 21: 769-780.
44. Cox A, Ackert-Bicknell CL, Dumont BL, Ding Y, Bell JT, Brockmann GA et al. A new standard genetic map for the laboratory mouse. Genetics 2009; 182: 1335-1344.
45. Broman KW, Wu H, Sen S, Churchill GA. R/qtl: QTL mapping in experimental crosses. Bioinformatics 2003; 19: 889-890.
46. Sen S, Churchill GA. A statistical framework for quantitative trait mapping. Genetics 2001; 159: 371-387.
47. Wergedal JE, Ackert-Bicknell CL, Tsaih SW, Sheng MH, Li R, Mohan S et al. Femur mechanical properties in the F2 progeny of an NZB/B1NJ x RF/J cross are regulated predominantly by genetic loci that regulate bone geometry. J Bone Miner Res 2006; 21: 1256-1266.