Silencing of the Il2 gene transcription is regulated by epigenetic changes in anergic T cells

European Journal of Immunology

Volumn 42, Issue 9, 2012, Pages 2471-2483

  Bandyopadhyay, Sanmay ^a   Montagna, Cristina ^a   Macian, Fernando ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Anergy; CD4+ T cells; Epigenetic; Heterochromatin; Histone methylation

Indexed keywords

HETEROCHROMATIN PROTEIN 1; HISTONE H3; INTERLEUKIN 2; METHYLTRANSFERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CELL NUCLEUS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CLONAL ANERGY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEACETYLATION; EPIGENETICS; GENE SILENCING; GENETIC TRANSCRIPTION; HETEROCHROMATIN; HISTONE ACETYLATION; HISTONE METHYLATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION;

ANIMALS; CELLS, CULTURED; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA METHYLATION; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; GENE SILENCING; HETEROCHROMATIN; HISTONE DEACETYLASES; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; INTERLEUKIN-2; METHYLTRANSFERASES; MICE; MICE, INBRED C57BL; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; T-LYMPHOCYTES; TRANSCRIPTION, GENETIC;

EID: 84865728531     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201142307     Document Type: Article

References (64)

1. Jenkins, M. K., Chen, C. A., Jung, G., Mueller, D. L., and Schwartz, R. H., Inhibition of antigen-specific proliferation of type 1 murine T-cell clones after stimulation with immobilized anti-CD3 monoclonal antibody. J. Immunol. 1990. 144: 16-22.
2. Schwartz, R. H., T-cell anergy. Annu. Rev. Immunol. 2003. 21: 305-334.
3. Chappert, P. and Schwartz, R. H., Induction of T-cell anergy: integration of environmental cues and infectious tolerance. Curr. Opin. Immunol. 2010. 22: 552-559.
4. Bandyopadhyay, S., Soto-Nieves, N., and Macian, F., Transcriptional regulation of T-cell tolerance. Semin. Immunol. 2007. 19: 180-187.
5. Fields, P. E., Gajewski, T. F., and Fitch, F. W., Blocked Ras activation in anergic CD4+ T cells. Science 1996. 271: 1276-1278.
6. Li, W., Whaley, C. D., Mondino, A., and Mueller, D. L., Blocked signal transduction to the ERK and JNK protein kinases in anergic CD4+ T cells. Science 1996. 271: 1272-1276.
7. Baine, I., Abe, B. T., and Macian, F., Regulation of T-cell tolerance by calcium/NFAT signaling. Immunol. Rev. 2009. 231: 225-240.
8. Wells, A. D., New insights into the molecular basis of T-cell anergy: anergy factors, avoidance sensors, and epigenetic imprinting. J. Immunol. 2009. 182: 7331-7341.
9. Fathman, C. G. and Lineberry, N. B., Molecular mechanisms of CD4+ T-cell anergy. Nat. Rev. Immunol. 2007. 7: 599-609.
10. Macian, F., Garcia-Cozar, F., Im, S. H., Horton, H. F., Byrne, M. C., and Rao, A., Transcriptional mechanisms underlying lymphocyte tolerance. Cell 2002. 109: 719-731.
11. Soto-Nieves, N., Puga, I., Abe, B. T., Bandyopadhyay, S., Baine, I., Rao, A., and Macian, F., Transcriptional complexes formed by NFAT dimers regulate the induction of T-cell tolerance. J. Exp. Med. 2009. 206: 867-876.
12. Heissmeyer, V., Macian, F., Im, S. H., Varma, R., Feske, S., Venuprasad, K., Gu, H. et al., Calcineurin imposes T-cell unresponsiveness through targeted proteolysis of signaling proteins. Nat. Immunol. 2004. 5: 255-265.
13. Nurieva, R. I., Zheng, S., Jin, W., Chung, Y., Zhang, Y., Martinez, G. J., Reynolds, J. M. et al., The E3 ubiquitin ligase GRAIL regulates T-cell tolerance and regulatory T-cell function by mediating T-cell receptor-CD3 degradation. Immunity 2010. 32: 670-680.
14. Olenchock, B. A., Guo, R., Carpenter, J. H., Jordan, M., Topham, M. K., Koretzky, G. A., and Zhong, X. P., Disruption of diacylglycerol metabolism impairs the induction of T-cell anergy. Nat. Immunol. 2006. 7: 1174-1181.
15. Puga, I., Rao, A., and Macian, F., Targeted cleavage of signaling proteins by caspase 3 inhibits T-cell receptor signaling in anergic T cells. Immunity 2008. 29: 193-204.
16. Zha, Y., Marks, R., Ho, A. W., Peterson, A. C., Janardhan, S., Brown, I., Praveen, K. et al., T-cell anergy is reversed by active Ras and is regulated by diacylglycerol kinase-alpha. Nat. Immunol. 2006. 7: 1166-1173.
17. Bandyopadhyay, S., Dure, M., Paroder, M., Soto-Nieves, N., Puga, I., and Macian, F., Interleukin 2 gene transcription is regulated by Ikaros-induced changes in histone acetylation in anergic T cells. Blood 2007. 109: 2878-2886.
18. Thomas, R. M., Chunder, N., Chen, C., Umetsu, S. E., Winandy, S., and Wells, A. D., Ikaros enforces the costimulatory requirement for IL2 gene expression and is required for anergy induction in CD4+ T lymphocytes. J. Immunol. 2007. 179: 7305-7315.
19. Thomas, R. M., Saouaf, S. J., and Wells, A. D., Superantigen-induced CD4+ T-cell tolerance is associated with DNA methylation and histone hypo-acetylation at cytokine gene loci. Genes Immun. 2007. 8: 613-618.
20. Taniuchi, I., Ellmeier, W., and Littman, D. R., The CD4/CD8 lineage choice: new insights into epigenetic regulation during T-cell development. Adv. Immunol. 2004. 83: 55-89.
21. Avni, O., Lee, D., Macian, F., Szabo, S. J., Glimcher, L. H., and Rao, A., T(H) cell differentiation is accompanied by dynamic changes in histone acetylation of cytokine genes. Nat. Immunol. 2002. 3: 643-651.
22. Ward, S. B., Hernandez-Hoyos, G., Chen, F., Waterman, M., Reeves, R., and Rothenberg, E. V., Chromatin remodeling of the interleukin-2 gene: distinct alterations in the proximal versus distal enhancer regions. Nucl. Acids Res. 1998. 26: 2923-2934.
23. Thomas, R. M., Gao, L., and Wells, A. D., Signals from CD28 induce stable epigenetic modification of the IL-2 promoter. J. Immunol. 2005. 174: 4639-4646.
24. Barth, T. K. and Imhof, A., Fast signals and slow marks: the dynamics of histone modifications. Trends Biochem. Sci. 2010. 35: 618-626.
25. Bernstein, B. E., Kamal, M., Lindblad-Toh, K., Bekiranov, S., Bailey, D. K., Huebert, D. J., McMahon, S. et al., Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 2005. 120: 169-181.
26. Heintzman, N. D., Stuart, R. K., Hon, G., Fu, Y., Ching, C. W., Hawkins, R. D., Barrera, L. O. et al., Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 2007. 39: 311-318.
27. Wang, L., Kametani, Y., Katano, I., and Habu, S., T-cell specific enhancement of histone H3 acetylation in 5' flanking region of the IL-2 gene. Biochem. Biophys. Res. Commun. 2005. 331: 589-594.
28. Yui, M.A., Hernandez-Hoyos, G., and Rothenberg, E. V., A new regulatory region of the IL-2 locus that confers position-independent transgene expression. J. Immunol. 2001. 166: 1730-1739.
29. Bannister, A. J., Zegerman, P., Partridge, J. F., Miska, E. A., Thomas, J. O., Allshire, R. C., and Kouzarides, T., Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 2001. 410: 120-124.
30. Peters, A. H., O'Carroll, D., Scherthan, H., Mechtler, K., Sauer, S., Schofer, C., Weipoltshammer, K. et al., Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 2001. 107: 323-337.
31. du Chene, I., Basyuk, E., Lin, Y. L., Triboulet, R., Knezevich, A., Chable-Bessia, C., Mettling, C. et al., Suv39H1 and HP1gamma are responsible for chromatin-mediated HIV-1 transcriptional silencing and post-integration latency. EMBO J. 2007. 26: 424-435.
32. Reed-Inderbitzin, E., Moreno-Miralles, I., Vanden-Eynden, S. K., Xie, J., Lutterbach, B., Durst-Goodwin, K. L., Luce, K. S. et al., RUNX1 associates with histone deacetylases and SUV39H1 to repress transcription. Oncogene 2006. 25: 5777-5786.
33. Lachner, M., O'Carroll, D., Rea, S., Mechtler, K., and Jenuwein, T., Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 2001. 410: 116-120.
34. Lomberk, G., Wallrath, L., and Urrutia, R., The Heterochromatin protein 1 family. Genome Biol. 2006. 7. doi:10.1186/gb-2006-7-7-228.
35. Boussiotis, V. A., Barber, D. L., Nakarai, T., Freeman, G. J., Gribben, J. G., Bernstein, G. M., D'Andrea, A. D. et al., Prevention of T-cell anergy by signaling through the gamma c chain of the IL-2 receptor. Science 1994. 266: 1039-1042.
36. Grewal, S. I. and Jia, S., Heterochromatin revisited. Nat. Rev. Genet. 2007. 8: 35-46.
37. Bandyopadhyay, S., Dure, M., Paroder, M., Soto-Nieves, N., Puga, I., and Macian, F., Interleukin 2 gene transcription is regulated by Ikaros-induced changes in histone acetylation in anergic T cells. Blood 2006. 109: 2878-2886.
38. Lundgren, M., Chow, C. M., Sabbattini, P., Georgiou, A., Minaee, S., and Dillon, N., Transcription factor dosage affects changes in higher order chromatin structure associated with activation of a heterochromatic gene. Cell 2000. 103: 733-743.
39. Macian, F., Im, S. H., Garcia-Cozar, F. J., and Rao, A., T-cell anergy. Curr. Opin. Immunol. 2004. 16: 209-216.
40. Anandasabapathy, N., Ford, G.S., Bloom, D., Holness, C., Paragas, V., Seroogy, C., Skrenta, H. et al., GRAIL: an E3 ubiquitin ligase that inhibits cytokine gene transcription is expressed in anergic CD4+ T cells. Immunity 2003. 18: 535-547.
41. Kriegel, M.A., Rathinam, C., and Flavell, R. A., E3 ubiquitin ligase GRAIL controls primary T-cell activation and oral tolerance. Proc. Natl. Acad. Sci. USA 2009. 106: 16770-16775.
42. Jeon, M. S., Atfield, A., Venuprasad, K., Krawczyk, C., Sarao, R., Elly, C., Yang, C. et al., Essential role of the E3 ubiquitin ligase Cbl-b in T-cell anergy induction. Immunity 2004. 21: 167-177.
43. Safford, M., Collins, S., Lutz, M. A., Allen, A., Huang, C. T., Kowalski, J., Blackford, A. et al., Egr-2 and Egr-3 are negative regulators of T-cell activation. Nat. Immunol. 2005. 6: 472-480.
44. Sridharan, R. and Smale, S. T., Predominant interaction of both Ikaros and Helios with the NuRD complex in immature thymocytes. J. Biol. Chem. 2007. 282: 30227-30238.
45. Kim, J., Sif, S., Jones, B., Jackson, A., Koipally, J., Heller, E., Winandy, S. et al., Ikaros DNA-binding proteins direct formation of chromatin remodeling complexes in lymphocytes. Immunity 1999. 10: 345-355.
46. Lee, J. S., Smith, E., and Shilatifard, A., The language of histone crosstalk. Cell 2010. 142: 682-685.
47. Ruthenburg, A. J., Li, H., Patel, D. J., and Allis, C. D., Multivalent engagement of chromatin modifications by linked binding modules. Nat. Rev. Mol. Cel. Biol. 2007. 8: 983-994.
48. Schultz, D. C., Ayyanathan, K., Negorev, D., Maul, G.G., and Rauscher, F.J., 3rd, SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev. 2002. 16: 919-932.
49. Tachibana, M., Sugimoto, K., Fukushima, T., and Shinkai, Y., Set domain-containing protein, G9a, is a novel lysine-preferring mammalian histone methyltransferase with hyperactivity and specific selectivity to lysines 9 and 27 of histone H3. J. Biol. Chem. 2001. 276: 25309-25317.
50. Chestier, A. and Yaniv, M., Rapid turnover of acetyl groups in the four core histones of simian virus 40 minichromosomes. Proc. Natl. Acad. Sci. USA 1979. 76: 46-50.
51. Zee, B. M., Levin, R. S., Xu, B., LeRoy, G., Wingreen, N. S., and Garcia, B. A., In vivo residue-specific histone methylation dynamics. J. Biol. Chem. 2010. 285: 3341-3350.
52. Fuks, F., Hurd, P.J., Deplus, R., and Kouzarides, T., The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucl. Acids Res. 2003. 31: 2305-2312.
53. Wallrath, L. L. and Elgin, S. C., Position effect variegation in Drosophila is associated with an altered chromatin structure. Genes Dev. 1995. 9: 1263-1277.
54. Hewitt, S. L., High, F. A., Reiner, S. L., Fisher, A. G., and Merkenschlager, M., Nuclear repositioning marks the selective exclusion of lineage-inappropriate transcription factor loci during T helper cell differentiation. Eur. J. Immunol. 2004. 34: 3604-3613.
55. Brown, K. E., Guest, S. S., Smale, S. T., Hahm, K., Merkenschlager, M., and Fisher, A. G., Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell 1997. 91: 845-854.
56. Cobb, B. S., Morales-Alcelay, S., Kleiger, G., Brown, K. E., Fisher, A. G., and Smale, S. T., Targeting of Ikaros to pericentromeric heterochromatin by direct DNA binding. Genes Dev. 2000. 14: 2146-2160.
57. Thomas, R. M., Chen, C., Chunder, N., Ma, L., Taylor, J., Pearce, E. J., and Wells, A. D., Ikaros silences T-bet expression and interferon-gamma production during T helper 2 differentiation. J. Biol. Chem. 2010. 285: 2545-2553.
58. Villarino, A. V., Katzman, S. D., Gallo, E., Miller, O., Jiang, S., McManus, M. T., and Abbas, A. K., Posttranscriptional silencing of effector cytokine mRNA underlies the anergic phenotype of self-reactive T cells. Immunity 2011. 34: 50-60.
59. Bonasio, R., Tu, S., and Reinberg, D., Molecular signals of epigenetic states. Science 2010. 330: 612-616.
60. Naito, T., Gomez-Del Arco, P., Williams, C. J., and Georgopoulos, K., Antagonistic interactions between Ikaros and the chromatin remodeler Mi-2beta determine silencer activity and Cd4 gene expression. Immunity 2007. 27: 723-734.
61. Klose, R. J., Yamane, K., Bae, Y., Zhang, D., Erdjument-Bromage, H., Tempst, P., Wong, J. et al., The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36. Nature 2006. 442: 312-316.
62. Whetstine, J. R., Nottke, A., Lan, F., Huarte, M., Smolikov, S., Chen, Z., Spooner, E. et al., Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell 2006. 125: 467-481.
63. Dure, M. and Macian, F., IL-2 signaling prevents T-cell anergy by inhibiting the expression of anergy-inducing genes. Mol. Immunol. 2009. 46: 999-1006.
64. Montagna, C., Lyu, M. S., Hunter, K., Lukes, L., Lowther, W., Reppert, T., Hissong, B. et al., The Septin 9 (MSF) gene is amplified and overexpressed in mouse mammary gland adenocarcinomas and human breast cancer cell lines. Cancer Res. 2003. 63: 2179-2187.