DNA methylation inhibition increases T cell KIR expression through effects on both promoter methylation and transcription factors

Clinical Immunology

Volumn 130, Issue 2, 2009, Pages 213-224

  Liu, Ying ^a   Kuick, Rork ^b   Hanash, Samir ^c   Richardson, Bruce ^a,d  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN COMPREHENSIVE CANCER CENTER   (United States)

^c Fred Hutchinson Cancer Research Center   (United States)

^d VA ANN ARBOR HEALTHCARE SYSTEM   (United States)

Author keywords

DNA methylation; ; Epigenetics; KIR genes; ; T cells;

Indexed keywords

KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL1; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL4; TRANSCRIPTION FACTOR ETS 1; TRANSCRIPTION FACTOR RUNX; TRANSCRIPTION FACTOR SP1;

ARTICLE; CHROMATIN STRUCTURE; COMPETITIVE INHIBITION; CONTROLLED STUDY; DEMETHYLATION; DNA METHYLATION; EPIGENETICS; GENE ACTIVATION; GENE EXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROMOTER REGION; REPORTER GENE; T LYMPHOCYTE;

AZACITIDINE; DNA METHYLATION; ENZYME INHIBITORS; EPIGENESIS, GENETIC; HUMANS; MICROARRAY ANALYSIS; PROMOTER REGIONS, GENETIC; PROTEIN BIOSYNTHESIS; RECEPTORS, KIR2DL4; RECEPTORS, KIR3DL2; RNA, MESSENGER; T-LYMPHOCYTES; TRANS-ACTIVATORS;

EID: 58049132791     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2008.08.009     Document Type: Article

References (35)

1. Feinberg A.P. Phenotypic plasticity and the epigenetics of human disease. Nature 447 (2007) 433-440
2. Lu Q., Wu A., Tesmer L., Ray D., Yousif N., and Richardson B. Demethylation of CD40LG on the inactive X in T cells from women with lupus. J. Immunol. 179 (2007) 6352-6358
3. Bird A.P. Gene number, noise reduction and biological complexity. Trends Genet. 11 (1995) 94-100
4. Blom B., and Spits H. Development of human lymphoid cells. Annu. Rev. Immunol. 24 (2006) 287-320
5. Cantrell D. T cell antigen receptor signal transduction pathways. Annu. Rev. Immunol. 14 (1996) 259-274
6. Lu Q., Wu A., Ray D., Deng C., Attwood J., Hanash S., Pipkin M., Lichtenheld M., and Richardson B. DNA methylation and chromatin structure regulate T cell perforin gene expression. J. Immunol. 170 (2003) 5124-5132
7. Sanders V.M. Epigenetic regulation of Th1 and Th2 cell development. Brain Behav. Immun. 20 (2006) 317-324
8. Golbus J., Palella T.D., and Richardson B.C. Quantitative changes in T cell DNA methylation occur during differentiation and ageing. Eur. J. Immunol. 20 (1990) 1869-1872
9. Richardson B., Scheinbart L., Strahler J., Gross L., Hanash S., and Johnson M. Evidence for impaired T cell DNA methylation in systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum. 33 (1990) 1665-1673
10. Richardson B. Primer: epigenetics of autoimmunity. Nat. Clin. Pract. Rheumatol. 3 (2007) 521-527
11. Cornacchia E., Golbus J., Maybaum J., Strahler J., Hanash S., and Richardson B. Hydralazine and procainamide inhibit T cell DNA methylation and induce autoreactivity. J. Immunol. 140 (1988) 2197-2200
12. Shedden K., Chen W., Kuick R., Ghosh D., Macdonald J., Cho K.R., Giordano T.J., Gruber S.B., Fearon E.R., Taylor J.M., and Hanash S. Comparison of seven methods for producing affymetrix expression scores based on false discovery rates in disease profiling data. BMC Bioinformatics 6 (2005) 26
13. Uhrberg M., Valiante N.M., Shum B.P., Shilling H.G., Lienert-Weidenbach K., Corliss B., Tyan D., Lanier L.L., and Parham P. Human diversity in killer cell inhibitory receptor genes. Immunity 7 (1997) 753-763
14. Lu Q., Wu A., and Richardson B.C. Demethylation of the same promoter sequence increases CD70 expression in lupus T cells and T cells treated with lupus-inducing drugs. J. Immunol. 174 (2005) 6212-6219
15. Lu Q., and Richardson B. Methods for analyzing the role of DNA methylation and chromatin structure in regulating T lymphocyte gene expression. Biol. Proced. Online 6 (2004) 189-203
16. Trowsdale J., Barten R., Haude A., Stewart C.A., Beck S., and Wilson M.J. The genomic context of natural killer receptor extended gene families. Immunol. Rev. 181 (2001) 20-38
17. Xu J., Vallejo A.N., Jiang Y., Weyand C.M., and Goronzy J.J. Distinct transcriptional control mechanisms of killer immunoglobulin-like receptors in natural killer (NK) and in T cells. J. Biol. Chem. 280 (2005) 24277-24285
18. Hsu K.C., Chida S., Geraghty D.E., and Dupont B. The killer cell immunoglobulin-like receptor (KIR) genomic region: gene-order, haplotypes and allelic polymorphism. Immunol. Rev. 190 (2002) 40-52
19. Chan H.W., Miller J.S., Moore M.B., and Lutz C.T. Epigenetic control of highly homologous killer Ig-like receptor gene alleles. J. Immunol. 175 (2005) 5966-5974
20. Rajagopalan S., Fu J., and Long E.O. Cutting edge: induction of IFN-gamma production but not cytotoxicity by the killer cell Ig-like receptor KIR2DL4 (CD158d) in resting NK cells. J. Immunol. 167 (2001) 1877-1881
21. Khakoo S.I., Rajalingam R., Shum B.P., Weidenbach K., Flodin L., Muir D.G., Canavez F., Cooper S.L., Valiante N.M., Lanier L.L., and Parham P. Rapid evolution of NK cell receptor systems demonstrated by comparison of chimpanzees and humans. Immunity 12 (2000) 687-698
22. Valiante N.M., Uhrberg M., Shilling H.G., Lienert-Weidenbach K., Arnett K.L., D'Andrea A., Phillips J.H., Lanier L.L., and Parham P. Functionally and structurally distinct NK cell receptor repertoires in the peripheral blood of two human donors. Immunity 7 (1997) 739-751
23. Single R.M., Martin M.P., Gao X., Meyer D., Yeager M., Kidd J.R., Kidd K.K., and Carrington M. Global diversity and evidence for coevolution of KIR and HLA. Nat. Genet. 39 (2007) 1114-1119
24. van Bergen J., Thompson A., van der Slik A., Ottenhoff T.H., Gussekloo J., and Koning F. Phenotypic and functional characterization of CD4 T cells expressing killer Ig-like receptors. J. Immunol. 173 (2004) 6719-6726
25. Kikuchi-Maki A., Yusa S., Catina T.L., and Campbell K.S. KIR2DL4 is an IL-2-regulated NK cell receptor that exhibits limited expression in humans but triggers strong IFN-gamma production. J. Immunol. 171 (2003) 3415-3425
26. Young H.A. Regulation of interferon-gamma gene expression. J. Interferon. Cytokine Res. 16 (1996) 563-568
27. Anfossi N., Doisne J.M., Peyrat M.A., Ugolini S., Bonnaud O., Bossy D., Pitard V., Merville P., Moreau J.F., Delfraissy J.F., Dechanet-Merville J., Bonneville M., Venet A., and Vivier E. Coordinated expression of Ig-like inhibitory MHC class I receptors and acquisition of cytotoxic function in human CD8+ T cells. J. Immunol. 173 (2004) 7223-7229
28. Weyand C.M., Fulbright J.W., and Goronzy J.J. Immunosenescence, autoimmunity, and rheumatoid arthritis. Exp. Gerontol. 38 (2003) 833-841
29. Goodridge J.P., Witt C.S., Christiansen F.T., and Warren H.S. KIR2DL4 (CD158d) genotype influences expression and function in NK cells. J. Immunol. 171 (2003) 1768-1774
30. Santourlidis S., Trompeter H.I., Weinhold S., Eisermann B., Meyer K.L., Wernet P., and Uhrberg M. Crucial role of DNA methylation in determination of clonally distributed killer cell Ig-like receptor expression patterns in NK cells. J. Immunol. 169 (2002) 4253-4261
31. Trompeter H.I., Gomez-Lozano N., Santourlidis S., Eisermann B., Wernet P., Vilches C., and Uhrberg M. Three structurally and functionally divergent kinds of promoters regulate expression of clonally distributed killer cell Ig-like receptors (KIR), of KIR2DL4, and of KIR3DL3. J. Immunol. 174 (2005) 4135-4143
32. Jaenisch R., and Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 33 Suppl. (2003) 245-254
33. Grewal S.I., and Moazed D. Heterochromatin and epigenetic control of gene expression. Science 301 (2003) 798-802
34. Stewart C.A., Van Bergen J., and Trowsdale J. Different and divergent regulation of the KIR2DL4 and KIR3DL1 promoters. J. Immunol. 170 (2003) 6073-6081
35. Nakajima T., Goek O., Zhang X., Kopecky S.L., Frye R.L., Goronzy J.J., and Weyand C.M. De novo expression of killer immunoglobulin-like receptors and signaling proteins regulates the cytotoxic function of CD4 T cells in acute coronary syndromes. Circ. Res. 93 (2003) 106-113