Genome-wide microarray expression analysis of CD4+ T cells from nonobese diabetic congenic mice identifies Cd55 (Daf1) and Acadl as candidate genes for type 1 diabetes

Journal of Immunology

Volumn 180, Issue 2, 2008, Pages 1071-1079

  Irie, Junichiro ^a   Reck, Brian ^b   Wu, Yuehong ^a   Wicker, Linda S ^c   Howlett, Sarah ^c   Rainbow, Daniel ^c   Feingold, Eleanor ^b   Ridgway, William M ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIBODY; DECAY ACCELERATING FACTOR; INTERLEUKIN 4; LONG CHAIN ACYL COENZYME A DEHYDROGENASE; MONOCLONAL ANTIBODY CD28; RNA; DECAY ACCELERATING FACTOR 1, MOUSE; DECAY-ACCELERATING FACTOR 1, MOUSE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL SURFACE; CHROMOSOME 1; CHROMOSOME 3; FEMALE; GENE EXPRESSION; GENE IDENTIFICATION; GENE LOCATION; GENOME; INSULIN DEPENDENT DIABETES MELLITUS; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; PATHOGENESIS; PRIORITY JOURNAL; TH1 CELL; UPREGULATION; ANIMAL; CONGENIC STRAIN; DNA MICROARRAY; DRUG EFFECT; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY;

ACYL-COA DEHYDROGENASE, LONG-CHAIN; ANIMALS; ANTIGENS, CD55; CD4-POSITIVE T-LYMPHOCYTES; DIABETES MELLITUS, TYPE 1; GENE EXPRESSION PROFILING; GENOME; INTERLEUKIN-4; MICE; MICE, CONGENIC; MICE, INBRED NOD; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TH1 CELLS; UP-REGULATION;

EID: 40449113829     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.2.1071     Document Type: Article

References (53)

1. The Wellcome Trust Case Control Consortium. 2007. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447: 661-678.
2. Easton, D. F., K. A. Pooley, A. M. Dunning, P. D. Pharoah, D. Thompson, D. G. Ballinger, J. P. Struewing, J. Morrison, H. Field, R. Luben, et al. 2007. Genome-wide association study identifies novel breast cancer susceptibility loci. Nature 447: 1087-1093.
3. Todd, J. A., N. M. Walker, J. D. Cooper, D. J. Smyth, K. Downes, V. Plagnol, R. Bailey, S. Nejentsev, S. F. Field, F. Payne, et al. 2007. Robust associations of four new chromosome regions from genome-wide analyses of type 1 diabetes. Nat. Genet. 39: 857-864.
4. Kissler, S., P. Stern, K. Takahashi, K. Hunter, L. B. Peterson, and L. S. Wicker. 2006. In vivo RNA interference demonstrates a role for Nramp1 in modifying susceptibility to type 1 diabetes. Nat. Genet. 38: 479-483.
5. Wicker, L. S., J. A. Todd, and L. B. Peterson. 1995. Genetic control of autoimmune diabetes in the NOD mouse. Annu. Rev. Immunol. 13: 179-200.
6. Ueda, H., J. M. Howson, L. Esposito, J. Heward, H. Snook, G. Chamberlain, D. B. Rainbow, K. M. Hunter, A. N. Smith, G. Di Genova, et al. 2003. Association of the T-cell regulatory gene CTLA4 with susceptibility to autoimmune disease. Nature 423: 506-511.
7. Vijayakrishnan, L., J. M. Slavik, Z. Illes, R. J. Greenwald, D. Rainbow, B. Greve, L. B. Peterson, D. A. Hafler, G. J. Freeman, A. H. Sharpe, et al. 2004. An autoimmune disease-associated CTLA-4 splice variant lacking the B7 binding domain signals negatively in T cells. Immunity 20: 563-575.
8. Wicker, L. S., G. Chamberlain, K. Hunter, D. Rainbow, S. Howlett, P. Tiffen, J. Clark, A. Gonzalez-Munoz, A. M. Cumiskey, R. L. Rosa, et al. 2004. Fine mapping, gene content, comparative sequencing, and expression analyses support Ctla4 and Nramp1 as candidates for Idd5.1 and Idd5.2 in the nonobese diabetic mouse. J. Immunol. 173: 164-173.
9. Lyons, P. A., N. Armitage, F. Argentina, P. Denny, N. J. Hill, C. J. Lord, M. B. Wilusz, L. B. Peterson, L. S. Wicker, and J. A. Todd. 2000. Congenic mapping of the type 1 diabetes locus, Idd3, to a 780-kb region of mouse chromosome 3: identification of a candidate segment of ancestral DNA by haplotype mapping. Genome Res. 10: 446-453.
10. Lyons, P. A., W. W. Hancock, P. Denny, C. J. Lord, N. J. Hill, N. Armitage, T. Siegmund, J. A. Todd, M. S. Phillips, J. F. Hess, et al. 2000. The NOD Idd9 genetic interval influences the pathogenicity of insulitis and contains molecular variants of Cd30, Tnfr2, and Cd137. Immunity 13: 107-115.
11. Olofsson, P., J. Holmberg, J. Tordsson, S. Lu, B. Akerstrom, and R. Holmdahl. 2003. Positional identification of Ncf1 as a gene that regulates arthritis severity in rats. Nat. Genet. 33: 25-32.
12. Todd, J. A., T. J. Aitman, R. J. Cornall, S. Ghosh, J. R. Hall, C. M. Hearne, A. M. Knight, J. M. Love, M. A. McAleer, J. B. Prins, et al. 1991. Genetic analysis of autoimmune type 1 diabetes mellitus in mice. Nature 351: 542-547.
13. Wicker, L. S., J. A. Todd, J. B. Prins, P. L. Podolin, R. J. Renjilian, and L. B.Peterson. 1994. Resistance alleles at two non-major histocompatibility complex-linked insulin-dependent diabetes loci on chromosome 3, Idd3 and Idd10, protect nonobese diabetic mice from diabetes. J. Exp. Med. 180: 1705-1713.
14. Cervino, A. C., M. Gosink, M. Fallahi, B. Pascal, C. Mader, and N. F. Tsinoremas. 2006. A comprehensive mouse IBD database for the efficient localization of quantitative trait loci. Mamm. Genome 17: 565-574.
15. Pease, A. C., D. Solas, E. J. Sullivan, M. T. Cronin, C. P. Holmes, and S. P. Fodor. 1994. Light-generated oligonucleotide arrays for rapid DNA sequence analysis. Proc. Natl. Acad. Sci. USA 91: 5022-5026.
16. Schena, M., D. Shalon, R. W. Davis, and P. O. Brown. 1995. Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270: 467-470.
17. Liu, K., C. Liang, Z. Liang, K. Tus, and E. K. Wakeland. 2005. Sle1ab mediates the aberrant activation of STAT3 and Ras-ERK signaling pathways in B lymphocytes. J. Immunol. 174: 1630-1637.
18. Rozzo, S. J., J. D. Allard, D. Choubey, T. J. Vyse, S. Izui, G. Peltz, and B. L. Kotzin. 2001. Evidence for an interferon-inducible gene, Ifi202, in the susceptibility to systemic lupus. Immunity 15: 435-443.
19. Eaves, I. A., L. S. Wicker, G. Ghandour, P. A. Lyons, L. B. Peterson, J. A. Todd, and R. J. Glynne. 2002. Combining mouse congenic strains and microarray gene expression analyses to study a complex trait: the NOD model of type 1 diabetes. Genome Res. 12: 232-243.
20. Wong, F. S., and C. A. Janeway, Jr. 1997. The role of CD4 and CD8 T cells in type I diabetes in the NOD mouse. Res. Immunol. 148: 327-332.
21. + T cells in autoimmune diabetes through the use of TCR transgenic mice. Immunol. Rev. 169: 55-65.
22. Anderson, M. S., and J. A. Bluestone. 2005. The NOD mouse: a model of immune dysregulation. Annu. Rev. Immunol. 23: 447-485.
23. Hill, N. J., P. A. Lyons, N. Armitage, J. A. Todd, L. S. Wicker, and L. B. Peterson. 2000. NOD Idd5 locus controls insulitis and diabetes and overlaps the orthologous CTLA4/IDDM12 and NRAMP1 loci in humans. Diabetes 49: 1744-1747.
24. Yamanouchi, J., D. Rainbow, P. Serra, S. Howlett, K. Hunter, V. E. Garner, A. Gonzalez-Munoz, J. Clark, R. Veijola, R. Cubbon, et al. 2007. Interleukin-2 gene variation impairs regulatory T cell function and causes autoimmunity. Nat. Genet. 39: 329-337.
25. Hunter, K., D. Rainbow, V. Plagnol, J. A. Todd, L. B. Peterson, and L. S. Wicker. 2007. Interactions between Idd5.1/Ctla4 and other type 1 diabetes genes. J. Immunol. 179: 8341-8349.
26. Ridgway, W. M., B. Healy, L. J. Smink, D. Rainbow, and L. S. Wicker. 2007. New tools for defining the "genetic background" of inbred mouse strains. Nat. Immunol. 8: 669-673.
27. Irizarry, R. A., B. Hobbs, F. Collin, Y. D. Beazer-Barclay, K. J. Antonellis, U. Scherf, and T. P. Speed. 2003. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
28. Gautier, L., L. Cope, B. M. Bolstad, and R. A. Irizarry. 2004. affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20: 307-315.
29. Bolstad, B. M., R. A. Irizarry, M. Astrand, and T. P. Speed. 2003. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193.
30. Lin, Y., P. Reynolds, and E. Feingold. 2003. An empirical Bayesian method for differential expression studies using one-channel microarray data. In Statistical Applications in Genetics and Molecular Biology, Vol. 2, No. 1, Article 8, pp. 1-18.
31. Tusher, V. G., R. Tibshirani, and G. Chu. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98: 5116-5121.
32. Matsubara, Y., Y. Indo, E. Naito, H. Ozasa, R. Glassberg, J. Vockley, Y. Ikeda, J. Kraus, and K. Tanaka. 1989. Molecular cloning and nucleotide sequence of cDNAs encoding the precursors of rat long chain acyl-coenzyme A, short chain acyl-coenzyme A, and isovaleryl-coenzyme A dehydrogenases: sequence homology of four enzymes of the acyl-CoA dehydrogenase family. J. Biol. Chem. 264: 16321-16331.
33. Fox, C. J., P. S. Hammerman, and C. B. Thompson. 2005. Fuel feeds function: energy metabolism and the T-cell response. Nat. Rev. Immunol. 5: 844-852.
34. Deberardinis, R. J., J. J. Lum, and C. B. Thompson. 2006. Phosphatidylinositol 3-kinase-dependent modulation of carnitine palmitoyltransferase 1A expression regulates lipid metabolism during hematopoietic cell growth. J. Biol. Chem. 281: 37372-37380.
35. Cordell, H. J., J. A. Todd, N. J. Hill, C. J. Lord, P. A. Lyons, L. B. Peterson, L. S. Wicker, and D. G. Clayton. 2001. Statistical modeling of interlocus interactions in a complex disease: rejection of the multiplicative model of epistasis in type 1 diabetes. Genetics 158: 357-367.
36. Hamann, J., B. Vogel, G. M. van Schijndel, and R. A. van Lier. 1996. The sevenspan transmembrane receptor CD97 has a cellular ligand (CD55, DAF). J. Exp. Med. 184: 1185-1189.
37. Gray, J. X., M. Haino, M. J. Roth, J. E. Maguire, P. N. Jensen, A. Yarme, M. A. Stetler-Stevenson, U. Siebenlist, and K. Kelly. 1996. CD97 is a processed, seven-transmembrane, heterodimeric receptor associated with inflammation. J. Immunol. 157: 5438-5447.
38. Hamann, J., C. Stortelers, E. Kiss-Toth, B. Vogel, W. Eichler, and R. A. van Lier. 1998. Characterization of the CD55 (DAF)-binding site on the seven-span transmembrane receptor CD97. Eur. J. Immunol. 28: 1701-1707.
39. Sogabe, H., M. Nangaku, Y. Ishibashi, T. Wada, T. Fujita, X. Sun, T. Miwa, M. P. Madaio, and W. C. Song. 2001. Increased susceptibility of decay-accelerating factor deficient mice to anti-glomerular basement membrane glomerulonephritis. J. Immunol. 167: 2791-2797.
40. Lin, F., S. N. Emancipator, D. J. Salant, and M. E. Medof. 2002. Decay-accelerating factor confers protection against complement-mediated podocyte injury in acute nephrotoxic nephritis. Lab. Invest. 82: 563-569.
41. Lin, F., H. J. Kaminski, B. M. Conti-Fine, W. Wang, C. Richmonds, and M. E. Medof. 2002. Markedly enhanced susceptibility to experimental autoimmune myasthenia gravis in the absence of decay-accelerating factor protection. J. Clin. Invest. 110: 1269-1274.
42. Liu, J., T. Miwa, B. Hilliard, Y. Chen, J. D. Lambris, A. D. Wells, and W. C. Song. 2005. The complement inhibitory protein DAF (CD55) suppresses T cell immunity in vivo. J. Exp. Med. 201: 567-577.
43. + T cells selected by I-Ag7 on a nonobese diabetic versus C57BL/6 genetic background. J. Immunol. 167: 1693-1702.
44. + T cell intrinsic and independent of APC genetic background. J. Immunol. 169: 6580-6587.
45. Katz, J. D., C. Benoist, and D. Mathis. 1995. T helper cell subsets in insulin-dependent diabetes. Science 268: 1185-1188.
46. Trembleau, S., G. Penna, E. Bosi, A. Mortara, M. K. Gately, and L. Adorini. 1995. Interleukin 12 administration induces T helper type 1 cells and accelerates autoimmune diabetes in NOD mice. J. Exp. Med. 181: 817-821.
47. Trembleau, S., G. Penna, S. Gregori, M. K. Gately, and L. Adorini. 1997. Deviation of pancreas-infiltrating cells to Th2 by interleukin-12 antagonist administration inhibits autoimmune diabetes. Eur. J. Immunol. 27: 2330-2339.
48. Trembleau, S., G. Penna, S. Gregori, H. D. Chapman, D. V. Serreze, J. Magram, and L. Adorini. 1999. Pancreas-infiltrating Th1 cells and diabetes develop in IL-12-deficient nonobese diabetic mice. J. Immunol. 163: 2960-2968.
49. Rabinovitch, A. 1994. Immunoregulatory and cytokine imbalances in the pathogenesis of IDDM: therapeutic intervention by immunostimulation? Diabetes 43: 613-621.
50. Rabinovitch, A., O. Sorensen, W. L. Suarez-Pinzon, R. F. Power, R. V. Rajotte, and R. C. Bleackley. 1994. Analysis of cytokine mRNA expression in syngeneic islet grafts of NOD mice: interleukin 2 and interferon γ mRNA expression correlate with graft rejection and interleukin 10 with graft survival. Diabetologia 37: 833-837.
51. Rabinovitch, A., W. L. Suarez-Pinzon, O. Sorensen, R. C. Bleackley, R. F. Power, and R. V. Rajotte. 1995. Combined therapy with interleukin-4 and interleukin-10 inhibits autoimmune diabetes recurrence in syngeneic islet-transplanted nonobese diabetic mice: analysis of cytokine mRNA expression in the graft. Transplantation 60: 368-374.
52. Fox, C. J., and J. S. Danska. 1997. IL-4 expression at the onset of islet inflammation predicts nondestructive insulitis in nonobese diabetic mice. J. Immunol. 158: 2414-2424.
53. Adorini, L., and S. Trembleau. 1997. Immune deviation towards Th2 inhibits Th-1-mediated autoimmune diabetes. Biochem. Soc. Trans. 25: 625-629.