Histone/protein deacetylase inhibitors increase suppressive functions of human FOXP3+ Tregs

Clinical Immunology

Volumn 136, Issue 3, 2010, Pages 348-363

  Akimova, Tatiana ^a   Ge, Guanghui ^a   Golovina, Tatiana ^a   Mikheeva, Tatiana ^a   Wang, Liqing ^a   Riley, James L ^a   Hancock, Wayne W ^a  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

FOXP3; HDAC; Suppression; Therapy; Tregs

Indexed keywords

(N (2 AMINOPHENYL) N' PHENYL OCTANE DIAMIDE; BML 210; BUFEXAMAC; BUTYRIC ACID; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; DIAMIDE; HISTONE DEACETYLASE INHIBITOR; N (2 AMINOPHENYL) 4 (3 PYRIDINYLMETHOXYCARBONYLAMINOMETHYL)BENZAMIDE; TRANSCRIPTION FACTOR FOXP3; TUBACIN; UNCLASSIFIED DRUG; VALPROIC ACID; VORINOSTAT;

ANTIGEN EXPRESSION; ARTICLE; AUTOIMMUNITY; CELL ISOLATION; CONTROLLED STUDY; DRUG MECHANISM; EFFECTOR CELL; FEMALE; HUMAN; HUMAN CELL CULTURE; IN VITRO STUDY; LYMPHOCYTE FUNCTION; MALE; NORMAL HUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; TRANSPLANTATION;

EID: 77955277730     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2010.04.018     Document Type: Article

References (55)

1. Buckner J.H., Ziegler S.F. Functional analysis of FOXp3. Ann. N. Y. Acad. Sci. 2008, 1143:151-169.
2. Shevach E.M. Mechanisms of Foxp3+ T regulatory cell-mediated suppression. Immunity 2009, 30:636-645.
3. Lu L.F., Rudensky A. Molecular orchestration of differentiation and function of regulatory T cells. Genes Dev. 2009, 23:1270-1282.
4. Wing K., Sakaguchi S. Regulatory T cells exert checks and balances on self tolerance and autoimmunity. Nat. Immunol. 2010, 11:7-13.
5. Riley J.L., June C.H., Blazar B.R. Human T regulatory cell therapy: take a billion or so and call me in the morning. Immunity 2009, 30:656-665.
6. Trzonkowski P., Bieniaszewska M., Juscinska J., Dobyszuk A., Krzystyniak A., Marek N., Mysliwska J., Hellmann A. First-in-man clinical results of the treatment of patients with graft versus host disease with human ex vivo expanded CD4+CD25+CD127- T regulatory cells. Clin. Immunol. 2009, 133:22-26.
7. Koenen H.J., Smeets R.L., Vink P.M., Van Rijssen E., Boots A.M., Joosten I. Human Cd25highfoxp3pos regulatory T cells differentiate into IL-17-producing cells. Blood 2008, 112:2340-2352.
8. Duarte J.H., Zelenay S., Bergman M.L., Martins A.C., Demengeot J. Natural treg cells spontaneously differentiate into pathogenic helper cells in lymphopenic conditions. Eur. J. Immunol. 2009, 39:948-955.
9. Wu Y., Borde M., Heissmeyer V., Feuerer M., Lapan A.D., Stroud J.C., Bates D.L., Guo L., Han A., Ziegler S.F., Mathis D., Benoist C., Chen L., Rao A. Foxp3 controls regulatory T cell function through cooperation with NFAT. Cell 2006, 126:375-387.
10. Bettelli E., Dastrange M., Oukka M. Foxp3 interacts with nuclear factor of activated T cells and Nf-Kappa B to repress cytokine gene expression and effector functions of T helper cells. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:5138-5143.
11. Chen C., Rowell E.A., Thomas R.M., Hancock W.W., Hancock W.W., Wells A.D. Transcriptional regulation by Foxp3 is associated with direct promoter occupancy and modulation of histone acetylation. J. Biol. Chem. 2006, 281:36828-36834.
12. Li B., Samanta A., Song X., Iacono K.T., Bembas K., Tao R., Basu S., Riley J.L., Hancock W.W., Shen Y., Saouaf S.J., Greene M.I. FOXP3 interactions with histone acetyltransferase and class II histone deacetylases are required for repression. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:4571-4576.
13. Tao R., De Zoeten E.F., Ozkaynak E., Chen C., Wang L., Porrett P.M., Li B., Turka L.A., Olson E.N., Greene M.I., Wells A.D., Hancock W.W. Deacetylase inhibition promotes the generation and function of regulatory T cells. Nat. Med. 2007, 13:1299-1307.
14. De Zoeten E.F., Wang L., Sai H., Hancock W.W. Inhibition of HDAC9 increases T regulatory cell function and prevents colitis in mice. Gastroenterology 2010, 583-594.
15. De Zoeten E.F., Lee I., Wang L., Chen C., Ge G., Wells A.D., Hancock W.W., Ozkaynak E. Foxp3 processing by proprotein convertases and control of regulatory T cell function. J. Biol. Chem. 2009, 284:5709-5716.
16. Yang X.J., Seto E. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat. Rev. Mol. Cell Biol. 2008, 9:206-218.
17. Haberland M., Montgomery R.L., Olson E.N. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet. 2009, 10:32-42.
18. Johnstone R.W. Histone-deacetylase inhibitors: novel drugs for the treatment of cancer. Nat. Rev. Drug Discov. 2002, 1:287-299.
19. Wang L., De Zoeten E.F., Greene M.I., Hancock W.W. Immunomodulatory effects of deacetylase inhibitors: therapeutic targeting of FOXP3(+) regulatory T cells. Nat. Rev. Drug Discov. 2009, 8:969-981.
20. Tang H., Wang X.S., Huang X.P., Roth B.L., Butler K.V., Kozikowski A.P., Jung M., Tropsha A. Novel inhibitors of human histone deacetylase (HDAC) identified by QSAR modeling of known inhibitors, virtual screening, and experimental validation. J. Chem. Inf. Model. 2009, 49:461-476.
21. Blanchard F., Chipoy C. Histone deacetylase inhibitors: new drugs for the treatment of inflammatory diseases?. Drug Discov. Today 2005, 10:197-204.
22. Lucas J.L., Mirshahpanah P., Haas-Stapleton E., Asadullah K., Zollner T.M., Numerof R.P. Induction of Foxp3+ regulatory t cells with histone deacetylase inhibitors. Cell. Immunol. 2009, 257:97-104.
23. Tuovinen H., Laurinolli T.T., Rossi L.H., Pekkarinen P.T., Mattila I., Arstila T.P. Thymic production of human FOXP3(+) regulatory T cells is stable but does not correlate with peripheral FOXP3 expression. Immunol. Lett. 2008, 117:146-153.
24. Wang J., Ioan-Facsinay A., Van Der Voort E.I., Huizinga T.W., Toes R.E. Transient expression of FOXP3 in human activated nonregulatory CD4+ T cells. Eur. J. Immunol. 2007, 37:129-138.
25. Hori S., Nomura T., Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003, 299:1057-1061.
26. Yagi H., Nomura T., Nakamura K., Yamazaki S., Kitawaki T., Hori S., Maeda M., Onodera M., Uchiyama T., Fujii S., Sakaguchi S. Crucial role of FOXp3 in the development and function of human CD25+CD4+ regulatory T cells. Int. Immunol. 2004, 16:1643-1656.
27. Allan S.E., Passerini L., Bacchetta R., Crellin N., Dai M., Orban P.C., Ziegler S.F., Roncarolo M.G., Levings M.K. The role of 2 FOXP3 isoforms in the generation of human CD4+ Tregs. J. Clin. Invest. 2005, 115:3276-3284.
28. Zheng Y., Manzotti C.N., Burke F., Dussably L., Qureshi O., Walker L.S., Sansom D.M. Acquisition of suppressive function by activated human CD4+ CD25- T cells is associated with the expression of CTLA-4 not FoxP3. J. Immunol. 2008, 181:1683-1691.
29. Collison L.W., Workman C.J., Kuo T.T., Boyd K., Wang Y., Vignali K.M., Cross R., Sehy D., Blumberg R.S., Vignali D.A. The inhibitory cytokine IL-35 contributes to regulatory T-cell function. Nature 2007, 450:566-569.
30. Bardel E., Larousserie F., Charlot-Rabiega P., Coulomb-L'hermine A., Devergne O. Human CD4+ CD25+ Foxp3+ regulatory T cells do not constitutively express IL-35. J. Immunol. 2008, 181:6898-6905.
31. Suhoski M.M., Golovina T.N., Aqui N.A., Tai V.C., Varela-Rohena A., Milone M.C., Carroll R.G., Riley J.L., June C.H. Engineering artificial antigen-presenting cells to express a diverse array of co-stimulatory molecules. Mol. Ther. 2007, 15:981-988.
32. Golovina T.N., Mikheeva T., Suhoski M.M., Aqui N.A., Tai V.C., Shan X., Liu R., Balcarcel R.R., Fisher N., Levine B.L., Carroll R.G., Warner N., Blazar B.R., June C.H., Riley J.L. Cd28 costimulation is essential for human T regulatory expansion and function. J. Immunol. 2008, 181:2855-2868.
33. Moreira J.M., Scheipers P., Sorensen P. The histone deacetylase inhibitor trichostatin a modulates CD4+ T cell responses. BMC Cancer 2003, 3:30.
34. Grozinger C.M., Schreiber S.L. Deacetylase enzymes: biological functions and the use of small-molecule inhibitors. Chem. Biol. 2002, 9:3-16.
35. Guenther M.G., Lane W.S., Fischle W., Verdin E., Lazar M.A., Shiekhattar R. A core SMRT corepressor complex containing HDAC3 And TBL1, a WD40-repeat protein linked to deafness. Genes Dev. 2000, 14:1048-1057.
36. Lagger G., O'carroll D., Rembold M., Khier H., Tischler J., Weitzer G., Schuettengruber B., Hauser C., Brunmeir R., Jenuwein T., Seiser C. Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression. EMBO J. 2002, 21:2672-2681.
37. Montgomery R.L., Davis C.A., Potthoff M.J., Haberland M., Fielitz J., Qi X., Hill J.A., Richardson J.A., Olson E.N. Histone deacetylases 1 and 2 redundantly regulate cardiac morphogenesis, growth, and contractility. Genes Dev. 2007, 21:1790-1802.
38. Montgomery R.L., Potthoff M.J., Haberland M., Qi X., Matsuzaki S., Humphries K.M., Richardson J.A., Bassel-Duby R., Olson E.N. Maintenance of cardiac energy metabolism by histone deacetylase 3 in mice. J. Clin. Invest. 2008, 118:3588-3597.
39. Haberland M., Mokalled M.H., Montgomery R.L., Olson E.N. Epigenetic control of skull morphogenesis by histone deacetylase 8. Genes Dev. 2009, 23:1625-1630.
40. Dangond F., Gullans S.R. Differential expression of human histone deacetylase mrnas in response to immune cell apoptosis induction by trichostatin A and butyrate. Biochem. Biophys. Res. Commun. 1998, 247:833-837.
41. Ma P., Schultz R.M. Histone deacetylase 1 (HDAC1) regulates histone acetylation, development, and gene expression in preimplantation mouse embryos. Dev. Biol. 2008, 319:110-120.
42. Escaffit F., Vaute O., Chevillard-Briet M., Segui B., Takami Y., Nakayama T., Trouche D. Cleavage and cytoplasmic relocalization of histone deacetylase 3 are important for apoptosis progression. Mol. Cell. Biol. 2007, 27:554-567.
43. Balasubramanian S., Ramos J., Luo W., Sirisawad M., Verner E., Buggy J.J. A novel histone deacetylase 8 (HDAC8)-specific inhibitor PCI-34051 induces apoptosis in T-cell lymphomas. Leukemia 2008, 22:1026-1034.
44. Tao R., Hancock W.W. Resistance of Foxp3+ regulatory T cells to Nur77-induced apoptosis promotes allograft survival. PLoS ONE 2008, 3:E2321.
45. Vega R.B., Matsuda K., Oh J., Barbosa A.C., Yang X., Meadows E., Mcanally J., Pomajzl C., Shelton J.M., Richardson J.A., Karsenty G., Olson E.N. Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell 2004, 119:555-566.
46. Chang S., Young B.D., Li S., Qi X., Richardson J.A., Olson E.N. Histone deacetylase 7 maintains vascular integrity by repressing matrix metalloproteinase 10. Cell 2006, 126:321-334.
47. Dequiedt F., Kasler H., Fischle W., Kiermer V., Weinstein M., Herndier B.G., Verdin E. HDAC7, a thymus-specific class II histone deacetylase, regulates Nur77 transcription and TCR-mediated apoptosis. Immunity 2003, 18:687-698.
48. Wing K., Onishi Y., Prieto-Martin P., Yamaguchi T., Miyara M., Fehervari Z., Nomura T., Sakaguchi S. CTLA-4 control over Foxp3+ regulatory T cell function. Science 2008, 322:271-275.
49. Sakaguchi S., Wing K., Onishi Y., Prieto-Martin P., Yamaguchi T. Regulatory T cells: how do they suppress immune responses?. Int. Immunol. 2009, 21:1105-1111.
50. Wong J.C., Hong R., Schreiber S.L. Structural biasing elements for in-cell histone deacetylase paralog selectivity. J. Am. Chem. Soc. 2003, 125:5586-5587.
51. Hildmann C., Wegener D., Riester D., Hempel R., Schober A., Merana J., Giurato L., Guccione S., Nielsen T.K., Ficner R., Schwienhorst A. Substrate and inhibitor specificity of class 1 and class 2 histone deacetylases. J. Biotechnol. 2006, 124:258-270.
52. Marks P.A. Discovery and development of SAHA as an anticancer agent. Oncogene 2007, 26:1351-1356.
53. Hess-Stumpp H., Bracker T.U., Henderson D., Politz O. MS-275, a potent orally available inhibitor of histone deacetylases-the development of an anticancer agent. Int. J. Biochem. Cell Biol. 2007, 39:1388-1405.
54. Haggarty S.J., Koeller K.M., Wong J.C., Grozinger C.M., Schreiber S.L. Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:4389-4394.
55. Gurvich N., Tsygankova O.M., Meinkoth J.L., Klein P.S. Histone deacetylase is a target of valproic acid-mediated cellular differentiation. Cancer Res. 2004, 64:1079-1086.