Histone Deacetylase Inhibitors as Immunomodulators in Cancer Therapeutics

References

• Xu WS , ParmigianiRB , MarksPA . Histone deacetylase inhibitors: molecular mechanisms of action . Oncogene26 ( 37 ), 5541 – 5552 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Yang XJ , SetoE . HATs and HDACs: from structure, function and regulation to novel strategies for therapy and prevention . Oncogene26 ( 37 ), 5310 – 5318 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Gao Z , HeQ , PengB , ChiaoPJ , YeJ . Regulation of nuclear translocation of HDAC3 by IkappaBalpha is required for tumor necrosis factor inhibition of peroxisome proliferator-activated receptor gamma function . J. Biol. Chem.281 ( 7 ), 4540 – 4547 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Houtkooper RH , PirinenE , AuwerxJ . Sirtuins as regulators of metabolism and healthspan . Nat. Rev. Mol. Cell Biol.13 ( 4 ), 225 – 238 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Schreiber RD , OldLJ , SmythMJ . Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion . Science331 ( 6024 ), 1565 – 1570 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Vesely MD , KershawMH , SchreiberRD , SmythMJ . Natural innate and adaptive immunity to cancer . Annu. Rev. Immunol.29 , 235 – 271 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Gajewski TF , FuertesM , SpaapenR , ZhengY , KlineJ . Molecular profiling to identify relevant immune resistance mechanisms in the tumor microenvironment . Curr. Opin. Immunol.23 ( 2 ), 286 – 292 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Von Boehmer L , MattleM , BodePet al. NY-ESO-1-specific immunological pressure and escape in a patient with metastatic melanoma . Cancer Immun.13 , 12 ( 2013 ).
   PubMedGoogle Scholar
• Bunt SK , SinhaP , ClementsVK , LeipsJ , Ostrand-RosenbergS . Inflammation induces myeloid-derived suppressor cells that facilitate tumor progression . J. Immunol.176 ( 1 ), 284 – 290 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Song X , KrelinY , DvorkinTet al. CD11b+/Gr-1+ immature myeloid cells mediate suppression of T cells in mice bearing tumors of IL-1beta-secreting cells . J. Immunol.175 ( 12 ), 8200 – 8208 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Shariat SF , ShalevM , Menesses-DiazAet al. Preoperative plasma levels of transforming growth factor beta1 (TGF-beta1) strongly predict progression in patients undergoing radical prostatectomy . J. Clin. Oncol.19 ( 11 ), 2856 – 2864 ( 2001 ).
   PubMed Web of Science ®Google Scholar
• Fong L , KwekSS , O’BrienSet al. Potentiating endogenous antitumor immunity to prostate cancer through combination immunotherapy with CTLA4 blockade and GM-CSF . Cancer Res.69 ( 2 ), 609 – 615 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Chen L . Co-inhibitory molecules of the B7-CD28 family in the control of T-cell immunity . Nat. Rev. Immunol.4 ( 5 ), 336 – 347 ( 2004 ).
   PubMed Web of Science ®Google Scholar
• Ceeraz S , NowakEC , NoelleRJ . B7 family checkpoint regulators in immune regulation and disease . Trends Immunol.34 ( 11 ), 556 – 563 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Grabiec AM , KrauszS , De JagerWet al. Histone deacetylase inhibitors suppress inflammatory activation of rheumatoid arthritis patient synovial macrophages and tissue . J. Immunol.184 ( 5 ), 2718 – 2728 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Zhang X , HanS , KangYet al. SAHA, an HDAC inhibitor, synergizes with tacrolimus to prevent murine cardiac allograft rejection . Cell Mol. Immunol.9 ( 5 ), 390 – 398 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Wagner JM , HackansonB , LubbertM , JungM . Histone deacetylase (HDAC) inhibitors in recent clinical trials for cancer therapy . Clin. Epigenetics1 ( 3–4 ), 117 – 136 ( 2010 ).
   PubMedGoogle Scholar
• Subramanian S , BatesSE , WrightJJ , Espinoza-DelgadoI , PiekarzRL . Clinical toxicities of histone deacetylase inhibitors . Pharmaceuticals3 ( 9 ), 17 ( 2010 ).
   Google Scholar
• Kato Y , YoshimuraK , ShinTet al. Synergistic in vivo antitumor effect of the histone deacetylase inhibitor MS-275 in combination with interleukin 2 in a murine model of renal cell carcinoma . Clin. Cancer Res.13 ( 15 ), 4538 – 4546 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Shen L , CiesielskiM , RamakrishnanSet al. Class I histone deacetylase inhibitor entinostat suppresses regulatory T cells and enhances immunotherapies in renal and prostate cancer models . PLoS ONE7 ( 1 ), e30815 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Christiansen AJ , WestA , BanksKMet al. Eradication of solid tumors using histone deacetylase inhibitors combined with immune-stimulating antibodies . Proc. Natl Acad. Sci. USA108 ( 10 ), 4141 – 4146 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Schug TT , XuQ , GaoHet al. Myeloid deletion of SIRT1 induces inflammatory signaling in response to environmental stress . Mol. Cell Biol.30 ( 19 ), 4712 – 4721 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Kawahara TL , MichishitaE , AdlerASet al. SIRT6 links histone H3 lysine 9 deacetylation to NF-kappaB-dependent gene expression and organismal life span . Cell136 ( 1 ), 62 – 74 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Fernandes CA , FievezL , NeyrinckAM , DelzenneNM , BureauF , VanbeverR . Sirtuin inhibition attenuates the production of inflammatory cytokines in lipopolysaccharide-stimulated macrophages . Biochem. Biophys. Res. Commun.420 ( 4 ), 857 – 861 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Heltweg B , GatbontonT , SchulerADet al. Antitumor activity of a small-molecule inhibitor of human silent information regulator 2 enzymes . Cancer Res.66 ( 8 ), 4368 – 4377 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Ota H , TokunagaE , ChangKet al. Sirt1 inhibitor, Sirtinol, induces senescence-like growth arrest with attenuated Ras-MAPK signaling in human cancer cells . Oncogene25 ( 2 ), 176 – 185 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Vo DD , PrinsRM , BegleyJLet al. Enhanced antitumor activity induced by adoptive T-cell transfer and adjunctive use of the histone deacetylase inhibitor LAQ824 . Cancer Res.69 ( 22 ), 8693 – 8699 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Murakami T , SatoA , ChunNAet al. Transcriptional modulation using HDACi depsipeptide promotes immune cell-mediated tumor destruction of murine B16 melanoma . J. Invest. Dermatol.128 ( 6 ), 1506 – 1516 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Khan AN , GregorieCJ , TomasiTB . Histone deacetylase inhibitors induce TAP, LMP, Tapasin genes and MHC class I antigen presentation by melanoma cells . Cancer Immunol. Immunother.57 ( 5 ), 647 – 654 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Magner WJ , KazimAL , StewartCet al. Activation of MHC class I, II, and CD40 gene expression by histone deacetylase inhibitors . J. Immunol.165 ( 12 ), 7017 – 7024 ( 2000 ).
   PubMed Web of Science ®Google Scholar
• Maeda T , TowatariM , KosugiH , SaitoH . Up-regulation of costimulatory/adhesion molecules by histone deacetylase inhibitors in acute myeloid leukemia cells . Blood96 ( 12 ), 3847 – 3856 ( 2000 ).
   PubMed Web of Science ®Google Scholar
• Mehta NT , TruaxAD , BoydNH , GreerSF . Early epigenetic events regulate the adaptive immune response gene CIITA . Epigenetics6 ( 4 ), 516 – 525 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Cycon KA , MulvaneyK , RimszaLM , PerskyD , MurphySP . Histone deacetylase inhibitors activate CIITA and MHC class II antigen expression in diffuse large B-cell lymphoma . Immunology140 ( 2 ), 259 – 272 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Gialitakis M , KretsovaliA , SpilianakisCet al. Coordinated changes of histone modifications and HDAC mobilization regulate the induction of MHC class II genes by Trichostatin A . Nucleic Acids Res.34 ( 3 ), 765 – 772 ( 2006 ).
   PubMed Web of Science ®Google Scholar
• Cinatl J Jr , CinatlJ , ScholzMet al. Antitumor activity of sodium valproate in cultures of human neuroblastoma cells . Anticancer Drugs7 ( 7 ), 766 – 773 ( 1996 ).
   PubMed Web of Science ®Google Scholar
• Armeanu S , BitzerM , LauerUMet al. Natural killer cell-mediated lysis of hepatoma cells via specific induction of NKG2D ligands by the histone deacetylase inhibitor sodium valproate . Cancer Res.65 ( 14 ), 6321 – 6329 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Skov S , PedersenMT , AndresenL , StratenPT , WoetmannA , OdumN . Cancer cells become susceptible to natural killer cell killing after exposure to histone deacetylase inhibitors due to glycogen synthase kinase-3-dependent expression of MHC class I-related chain A and B . Cancer Res.65 ( 23 ), 11136 – 11145 ( 2005 ).
   PubMed Web of Science ®Google Scholar
• Yang H , LanP , HouZet al. Histone deacetylase inhibitor SAHA epigenetically regulates miR-17–92 cluster and MCM7 to upregulate MICA expression in hepatoma . Br. J. Cancer112 ( 1 ), 112 – 121 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Chen WY , BaileyEC , MccuneSL , DongJY , TownesTM . Reactivation of silenced, virally transduced genes by inhibitors of histone deacetylase . Proc. Natl Acad. Sci. USA94 ( 11 ), 5798 – 5803 ( 1997 ).
   PubMed Web of Science ®Google Scholar
• Dion LD , GoldsmithKT , TangDC , EnglerJA , YoshidaM , GarverRIJr . Amplification of recombinant adenoviral transgene products occurs by inhibition of histone deacetylase . Virology231 ( 2 ), 201 – 209 ( 1997 ).
   PubMed Web of Science ®Google Scholar
• Otsuki A , PatelA , KasaiKet al. Histone deacetylase inhibitors augment antitumor efficacy of herpes-based oncolytic viruses . Mol. Ther.16 ( 9 ), 1546 – 1555 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Lai MD , ChenCS , YangCRet al. An HDAC inhibitor enhances the antitumor activity of a CMV promoter-driven DNA vaccine . Cancer Gene Ther.17 ( 3 ), 203 – 211 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Ogbomo H , MichaelisM , KreuterJ , DoerrHW , CinatlJJr . Histone deacetylase inhibitors suppress natural killer cell cytolytic activity . FEBS Lett.581 ( 7 ), 1317 – 1322 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Rossi LE , AvilaDE , SpallanzaniRGet al. Histone deacetylase inhibitors impair NK cell viability and effector functions through inhibition of activation and receptor expression . J. Leukoc. Biol.91 ( 2 ), 321 – 331 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Alvarez-Breckenridge CA , YuJ , PriceRet al. The histone deacetylase inhibitor valproic acid lessens NK cell action against oncolytic virus-infected glioblastoma cells by inhibition of STAT5/T-BET signaling and generation of gamma interferon . J. Virol.86 ( 8 ), 4566 – 4577 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Zhu S , DenmanCJ , CobanogluZSet al. The narrow-spectrum HDAC inhibitor entinostat enhances NKG2D expression without NK cell toxicity, leading to enhanced recognition of cancer cells . Pharm. Res.32 ( 3 ), 779 – 792 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Akimova T , BeierUH , LiuY , WangL , HancockWW . Histone/protein deacetylases and T-cell immune responses . Blood119 ( 11 ), 2443 – 2451 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Chang S , CollinsPL , AuneTM . T-bet dependent removal of Sin3A-histone deacetylase complexes at the Ifng locus drives Th1 differentiation . J. Immunol.181 ( 12 ), 8372 – 8381 ( 2008 ).
   PubMed Web of Science ®Google Scholar
• Chuang C , LinSH , HuangF , PanJ , JosicD , Yu-LeeLY . Acetylation of RNA processing proteins and cell cycle proteins in mitosis . J. Proteome Res.9 ( 9 ), 4554 – 4564 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Moreira JM , ScheipersP , SorensenP . The histone deacetylase inhibitor Trichostatin A modulates CD4+ T cell responses . BMC Cancer3 , 30 ( 2003 ).
   PubMed Web of Science ®Google Scholar
• Jones RB , O’connorR , MuellerSet al. Histone deacetylase inhibitors impair the elimination of HIV-infected cells by cytotoxic T-lymphocytes . PLoS Pathog.10 ( 8 ), e1004287 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Cao K , WangG , LiWet al. Histone deacetylase inhibitors prevent activation-induced cell death and promote anti-tumor immunity . Oncogene34 ( 49 ), 5960 – 5970 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Glauben R , SonnenbergE , WetzelM , MascagniP , SiegmundB . Histone deacetylase inhibitors modulate interleukin 6-dependent CD4+ T cell polarization in vitro and in vivo . J. Biol. Chem.289 ( 9 ), 6142 – 6151 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Lisiero DN , SotoH , EversonRG , LiauLM , PrinsRM . The histone deacetylase inhibitor, LBH589, promotes the systemic cytokine and effector responses of adoptively transferred CD8+ T cells . J. Immunother. Cancer2 , 8 ( 2014 ).
   PubMedGoogle Scholar
• Lee Sc , BottaroA , InselRA . Activation of terminal B cell differentiation by inhibition of histone deacetylation . Mol. Immunol.39 ( 15 ), 923 – 932 ( 2003 ).
   PubMed Web of Science ®Google Scholar
• Kienzler AK , RizziM , ReithM , NuttSL , EibelH . Inhibition of human B-cell Development into plasmablasts by histone deacetylase inhibitor valproic acid . J. Allergy Clin. Immunol.131 ( 6 ), 1695 – 1699 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Tao R , De ZoetenEF , OzkaynakEet al. Deacetylase inhibition promotes the generation and function of regulatory T cells . Nat. Med.13 ( 11 ), 1299 – 1307 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Lucas JL , MirshahpanahP , Haas-StapletonE , AsadullahK , ZollnerTM , NumerofRP . Induction of Foxp3+ regulatory T cells with histone deacetylase inhibitors . Cell Immunol.257 ( 1–2 ), 97 – 104 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Van Loosdregt J , VercoulenY , GuichelaarTet al. Regulation of Treg functionality by acetylation-mediated Foxp3 protein stabilization . Blood115 ( 5 ), 965 – 974 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• De Zoeten EF , WangL , ButlerKet al. Histone deacetylase 6 and heat shock protein 90 control the functions of Foxp3(+) T-regulatory cells . Mol. Cell Biol.31 ( 10 ), 2066 – 2078 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• De Zoeten EF , WangL , SaiH , DillmannWH , HancockWW . Inhibition of HDAC9 increases T regulatory cell function and prevents colitis in mice . Gastroenterology138 ( 2 ), 583 – 594 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Akimova T , GeG , GolovinaTet al. Histone/protein deacetylase inhibitors increase suppressive functions of human FOXP3+ Tregs . Clin. Immunol.136 ( 3 ), 348 – 363 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Shen L , PiliR . Class I histone deacetylase inhibition is a novel mechanism to target regulatory T cells in immunotherapy . Oncoimmunology1 ( 6 ), 948 – 950 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Wang L , LiuY , HanRet al. FOXP3+ regulatory T cell development and function require histone/protein deacetylase 3 . J. Clin. Invest.125 ( 3 ), 1111 – 1123 ( 2015 ).
   PubMed Web of Science ®Google Scholar
• Leoni F , ZalianiA , BertoliniGet al. The antitumor histone deacetylase inhibitor suberoylanilide hydroxamic acid exhibits antiinflammatory properties via suppression of cytokines . Proc. Natl Acad. Sci. USA99 ( 5 ), 2995 – 3000 ( 2002 ).
   PubMed Web of Science ®Google Scholar
• Reddy P , MaedaY , HotaryKet al. Histone deacetylase inhibitor suberoylanilide hydroxamic acid reduces acute graft-versus-host disease and preserves graft-versus-leukemia effect . Proc. Natl Acad. Sci. USA101 ( 11 ), 3921 – 3926 ( 2004 ).
   PubMed Web of Science ®Google Scholar
• Mishra N , ReillyCM , BrownDR , RuizP , GilkesonGS . Histone deacetylase inhibitors modulate renal disease in the MRL-lpr/lpr mouse . J. Clin. Invest.111 ( 4 ), 539 – 552 ( 2003 ).
   PubMed Web of Science ®Google Scholar
• Nencioni A , BeckJ , WerthDet al. Histone deacetylase inhibitors affect dendritic cell differentiation and immunogenicity . Clin. Cancer. Res.13 ( 13 ), 3933 – 3941 ( 2007 ).
   PubMed Web of Science ®Google Scholar
• Song W , TaiYT , TianZet al. HDAC inhibition by LBH589 affects the phenotype and function of human myeloid dendritic cells . Leukemia25 ( 1 ), 161 – 168 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Chauvistre H , KustermannC , RehageNet al. Dendritic cell development requires histone deacetylase activity . Eur. J. Immunol.44 ( 8 ), 2478 – 2488 ( 2014 ).
   PubMed Web of Science ®Google Scholar
• Villagra A , ChengF , WangHWet al. The histone deacetylase HDAC11 regulates the expression of interleukin 10 and immune tolerance . Nat. Immunol.10 ( 1 ), 92 – 100 ( 2009 ).
   PubMed Web of Science ®Google Scholar
• Barneda-Zahonero B , Roman-GonzalezL , CollazoOet al. HDAC7 is a repressor of myeloid genes whose downregulation is required for transdifferentiation of pre-B cells into macrophages . PLoS Genet.9 ( 5 ), e1003503 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Mombelli M , LugrinJ , RubinoIet al. Histone deacetylase inhibitors impair antibacterial defenses of macrophages . J. Infect. Dis.204 ( 9 ), 1367 – 1374 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Roger T , LugrinJ , LE RoyDet al. Histone deacetylase inhibitors impair innate immune responses to Toll-like receptor agonists and to infection . Blood117 ( 4 ), 1205 – 1217 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Mullican SE , GaddisCA , AlenghatTet al. Histone deacetylase 3 is an epigenomic brake in macrophage alternative activation . Genes Dev.25 ( 23 ), 2480 – 2488 ( 2011 ).
   PubMed Web of Science ®Google Scholar
• Halili MA , AndrewsMR , LabzinLIet al. Differential effects of selective HDAC inhibitors on macrophage inflammatory responses to the Toll-like receptor 4 agonist LPS . J. Leukoc. Biol.87 ( 6 ), 1103 – 1114 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Rosborough BR , CastellanetaA , NatarajanS , ThomsonAW , TurnquistHr . Histone deacetylase inhibition facilitates GM-CSF-mediated expansion of myeloid-derived suppressor cells in vitro and in vivo . J. Leukoc. Biol.91 ( 5 ), 701 – 709 ( 2012 ).
   PubMed Web of Science ®Google Scholar
• Tran K , RisingsongR , RoyceDBet al. The combination of the histone deacetylase inhibitor vorinostat and synthetic triterpenoids reduces tumorigenesis in mouse models of cancer . Carcinogenesis34 ( 1 ), 199 – 210 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• US FDA . FDA approves Farydak for treatment of multiple myeloma ( 2015 ). www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm435296.htm .
   Google Scholar
• Tan J , CangS , MaY , PetrilloRl , LiuD . Novel histone deacetylase inhibitors in clinical trials as anti-cancer agents . J. Hematol. Oncol.3 , 5 ( 2010 ).
   PubMed Web of Science ®Google Scholar
• Qiu T , ZhouL , ZhuWet al. Effects of treatment with histone deacetylase inhibitors in solid tumors: a review based on 30 clinical trials . Future Oncol.9 ( 2 ), 255 – 269 ( 2013 ).
   PubMed Web of Science ®Google Scholar
• Bridle BW , ChenL , LemayCGet al. HDAC inhibition suppresses primary immune responses, enhances secondary immune responses, and abrogates autoimmunity during tumor immunotherapy . Mol. Ther.21 ( 4 ), 887 – 894 ( 2013 ).
   PubMed Web of Science ®Google Scholar