HDAC5 controls the functions of Foxp3+ T-regulatory and CD8+ T cells

International Journal of Cancer

Volumn 138, Issue 10, 2016, Pages 2477-2486

  Xiao, Haiyan ^a   Jiao, Jing ^a   Wang, Liqing ^a   O'Brien, Shaun ^b   Newick, Kheng ^b   Wang, Liang Chuan S ^b   Falkensammer, Eva ^a   Liu, Yujie ^a   Han, Rongxiang ^a   Kapoor, Veena ^b   Hansen, Finn K ^c   Kurz, Thomas ^c   Hancock, Wayne W ^a   Beier, Ulf H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

cancer immunotherapy; Foxp3; HDAC; lung adenocarcinoma; Treg

Indexed keywords

GAMMA INTERFERON; HISTONE DEACETYLASE 5; MESSENGER RNA; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FOXP3; CYTOKINE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; HDAC5 PROTEIN, MOUSE; HISTONE DEACETYLASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; EFFECTOR CELL; GENE EXPRESSION; INTERFERON PRODUCTION; LUNG ADENOCARCINOMA; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; TH17 CELL; TUMOR ASSOCIATED LEUKOCYTE; ANIMAL; BIOSYNTHESIS; GENE DELETION; GENE TARGETING; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; NEOPLASM; T LYMPHOCYTE SUBPOPULATION; TUMOR CELL LINE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CYTOKINES; FORKHEAD TRANSCRIPTION FACTORS; GENE DELETION; GENE TARGETING; HISTONE DEACETYLASES; INTERFERON-GAMMA; LYMPHOCYTE ACTIVATION; MICE; MICE, KNOCKOUT; NEOPLASMS; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY;

EID: 84959934514     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.29979     Document Type: Article

References (46)

1. Barneda-Zahonero B, Parra M., Histone deacetylases and cancer. Mol Oncol 2012; 6: 579-89.
2. Fraga MF, Ballestar E, Villar-Garea A, et al., Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat Genet 2005; 37: 391-400.
3. Kuo MH, Allis CD., Roles of histone acetyltransferases and deacetylases in gene regulation. Bioessays 1998; 20: 615-26.
4. West AC, Johnstone RW., New and emerging HDAC inhibitors for cancer treatment. J Clin Invest 2014; 124: 30-9.
5. San-Miguel JF, Hungria VT, Yoon S-S, et al., Panobinostat plus bortezomib and dexamethasone versus placebo plus bortezomib and dexamethasone in patients with relapsed or relapsed and refractory multiple myeloma: a multicentre, randomised, double-blind phase 3 trial. Lancet Oncol 2014; 15: 1195-206.
6. Akimova T, Ge G, Golovina T, et al., Histone/protein deacetylase inhibitors increase suppressive functions of human FOXP3+ Tregs. Clin Immunol 2010; 136: 348-63.
7. Tao R, de Zoeten EF, Ozkaynak E, et al., Deacetylase inhibition promotes the generation and function of regulatory T cells. Nat Med 2007; 13: 1299-307.
8. Feuerer M, Hill JA, Mathis D, et al., Foxp3+ regulatory T cells: differentiation, specification, subphenotypes. Nat Immunol 2009; 10: 689-95.
9. Hori S, Nomura T, Sakaguchi S., Control of regulatory T cell development by the transcription factor Foxp3. Science 2003; 299: 1057-61.
10. Fontenot JD, Gavin MA, Rudensky AY., Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 2003; 4: 330-6.
11. Wang L, de Zoeten EF, Greene MI, et al., Immunomodulatory effects of deacetylase inhibitors: therapeutic targeting of FOXP3+ regulatory T cells. Nat Rev Drug Discov 2009; 8: 969-81.
12. Hanahan D, Weinberg RA., Hallmarks of cancer: the next generation. Cell 2011; 144: 646-74.
13. Kroesen M, Gielen P, Brok IC, et al., HDAC inhibitors and immunotherapy; a double edged sword? Oncotarget 2014; 5: 6558-72.
14. Nishikawa H, Sakaguchi S., Regulatory T cells in tumor immunity. Int J Cancer 2010; 127: 759-67.
15. Nguyen LT, Ohashi PS., Clinical blockade of PD1 and LAG3 [mdash] potential mechanisms of action. Nat Rev Immunol 2015; 15: 45-56.
16. Hodi FS, Butler M, Oble DA, et al., Immunologic and clinical effects of antibody blockade of cytotoxic T lymphocyte-associated antigen 4 in previously vaccinated cancer patients. Proc Natl Acad Sci USA 2008; 105: 3005-10.
17. van Loosdregt J, Coffer PJ., Post-translational modification networks regulating FOXP3 function. Trends Immunol 2014; 35: 368-78.
18. Beier UH, Akimova T, Liu Y, et al., Histone/protein deacetylases control Foxp3 expression and the heat shock response of T-regulatory cells. Curr Opin Immunol 2011; 23: 670-8.
19. Liu Y, Wang L, Han R, et al., Two lysines in the forkhead domain of foxp3 are key to T regulatory cell function. PloS One 2012; 7: e29035.
20. van Loosdregt J, Vercoulen Y, Guichelaar T, et al., Regulation of Treg functionality by acetylation-mediated Foxp3 protein stabilization. Blood 2010; 115: 965-74.
21. van Loosdregt J, Brunen D, Fleskens V, et al., Rapid temporal control of Foxp3 protein degradation by sirtuin-1. PloS One 2011; 6: e19047.
22. Liu Y, Wang L, Predina J, et al., Inhibition of p300 impairs Foxp3(+) T regulatory cell function and promotes antitumor immunity. Nat Med 2013; 19: 1173-7.
23. de Zoeten EF, Wang L, Sai H, et al., Inhibition of HDAC9 increases T regulatory cell function and prevents colitis in mice. Gastroenterology 2010; 138: 583-94.
24. de Zoeten EF, Wang L, Butler K, et al., Histone deacetylase 6 and heat shock protein 90 control the functions of Foxp3(+) T-regulatory cells. Mol Cell Biol 2011; 31: 2066-78.
25. Beier UH, Wang L, Bhatti TR, et al., Sirtuin-1 targeting promotes Foxp3+ T-regulatory cell function and prolongs allograft survival. Mol Cell Biol 2011; 31: 1022-9.
26. Chang S, McKinsey TA, Zhang CL, et al., Histone deacetylases 5 and 9 govern responsiveness of the heart to a subset of stress signals and play redundant roles in heart development. Mol Cell Biol 2004; 24: 8467-76.
27. Lin KY, Guarnieri FG, Staveley-O'Carroll KF, et al., Treatment of established tumors with a novel vaccine that enhances major histocompatibility class II presentation of tumor antigen. Cancer Res 1996; 56: 21-6.
28. Marek L, Hamacher A, Hansen FK, et al., Histone deacetylase (HDAC) inhibitors with a novel connecting unit linker region reveal a selectivity profile for HDAC4 and HDAC5 with improved activity against chemoresistant cancer cells. J Med Chem 2013; 56: 427-36.
29. Tao R, Wang L, Han R, et al., Differential effects of B and T lymphocyte attenuator and programmed death-1 on acceptance of partially versus fully MHC-mismatched cardiac allografts. J Immunol 2005; 175: 5774-82.
30. Akimova T, Levine MH, Beier UH, et al., Standardization, evaluation, and area-under-curve analysis of human and murine Treg suppressive function. Methods Mol Biol 2016; 1371: 43-78.
31. Thomas RM, Sai H, Wells AD., Conserved intergenic elements and DNA methylation cooperate to regulate transcription at the il17 locus. J Biol Chem 2012; 287: 25049-59.
32. Akimova T, Xiao H, Liu Y, et al., Targeting sirtuin-1 alleviates experimental autoimmune colitis by induction of Foxp3+ T-regulatory cells. Mucosal Immunol 2014; 7: 1209-20.
33. Beier UH, Wang L, Han R, et al., Histone deacetylases 6 and 9 and sirtuin-1 control Foxp3+ regulatory T cell function through shared and isoform-specific mechanisms. Sci Signal 2012; 5: ra45.
34. Haas AR, Sun J, Vachani A, et al., Cycloxygenase-2 inhibition augments the efficacy of a cancer vaccine. Clin Cancer Res 2006; 12: 214-22.
35. Mihaylova MM, Vasquez DS, Ravnskjaer K, et al., Class IIa histone deacetylases are hormone-activated regulators of FOXO and mammalian glucose homeostasis. Cell 2011; 145: 607-21.
36. Matsuzaki H, Daitoku H, Hatta M, et al., Acetylation of Foxo1 alters its DNA-binding ability and sensitivity to phosphorylation. Proc Natl Acad Sci USA 2005; 102: 11278-83.
37. Ouyang W, Beckett O, Ma Q, et al., Foxo proteins cooperatively control the differentiation of Foxp3+ regulatory T cells. Nat Immunol 2010; 11: 618-27.
38. Ouyang W, Liao W, Luo CT, et al., Novel Foxo1-dependent transcriptional programs control T(reg) cell function. Nature 2012; 491: 554-9.
39. Kerdiles YM, Stone EL, Beisner DR, et al., Foxo transcription factors control regulatory T cell development and function. Immunity 2010; 33: 890-904.
40. Gajewski TF, Schreiber H, Fu YX., Innate and adaptive immune cells in the tumor microenvironment. Nat Immunol 2013; 14: 1014-22.
41. Eom GH, Nam YS, Oh JG, et al., Regulation of acetylation of histone deacetylase 2 by p300/CBP-associated factor/histone deacetylase 5 in the development of cardiac hypertrophy. Circ Res 2014; 114: 1133-43.
42. Tsai SC, Seto E., Regulation of histone deacetylase 2 by protein kinase CK2. J Biol Chem 2002; 277: 31826-33.
43. Boucheron N, Tschismarov R, Goeschl L, et al., CD4(+) T cell lineage integrity is controlled by the histone deacetylases HDAC1 and HDAC2. Nat Immunol 2014; 15: 439-48.
44. Cruz-Guilloty F, Pipkin ME, Djuretic IM, et al., Runx3 and T-box proteins cooperate to establish the transcriptional program of effector CTLs. J Exp Med 2009; 206: 51-9.
45. Kitoh A, Ono M, Naoe Y, et al., Indispensable role of the Runx1-Cbfbeta transcription complex for in vivo-suppressive function of FoxP3+ regulatory T cells. Immunity 2009; 31: 609-20.
46. Klunker S, Chong MM, Mantel PY, et al., Transcription factors RUNX1 and RUNX3 in the induction and suppressive function of Foxp3+ inducible regulatory T cells. J Exp Med 2009; 206: 2701-15.