Histone Deacetylase Inhibitors in Tumor Immunotherapy

Page: [2990 - 3008] Pages: 19

  • * (Excluding Mailing and Handling)

Abstract

Background: With an increasing understanding of the antitumor immune response, considerable progress has been made in the field of tumor immunotherapy in the last decade. Inhibition of histone deacetylases represents a new strategy in tumor therapy and histone deacetylase inhibitors have been recently developed and validated as potential antitumor drugs. In addition to the direct antitumor effects, histone deacetylase inhibitors have been found to have the ability to improve tumor recognition by immune cells that may contribute to their antitumor activity. These immunomodolutory effects are desirable, and their in-depth comprehension will facilitate the design of novel regimens with improved clinical efficacy.

Objective: Our goal here is to review recent developments in the application of histone deacetylase inhibitors as immune modulators in cancer treatment.

Methods: Systemic compilation of the relevant literature in this field.

Results & Conclusion: In this review, we summarize recent advances in the understanding of how histone deacetylase inhibitors alter immune process and discuss their effects on various cytokines. We also discuss the challenges to optimize the use of these inhibitors as immune modulators in cancer treatment. Information gained from this review will be valuable to this field and may be helpful for designing tumor immunotherapy trials involving histone deacetylase inhibitors.

Keywords: Tumor immunotherapy, HDAC, HDAC inhibitors, antitumor, immune response, cytokine.

[1]
Zarour, H.M.; Ferrone, S. Cancer immunotherapy: Progress and challenges in the clinical setting. Eur. J. Immunol., 2011, 41(6), 1510-1515.
[http://dx.doi.org/10.1002/eji.201190035] [PMID: 21618503]
[2]
Galluzzi, L.; Buqué, A.; Kepp, O.; Zitvogel, L.; Kroemer, G. Immunological effects of conventional chemotherapy and targeted anticancer agents. Cancer Cell, 2015, 28(6), 690-714.
[http://dx.doi.org/10.1016/j.ccell.2015.10.012] [PMID: 26678337]
[3]
Monneret, C. Histone deacetylase inhibitors. Eur. J. Med. Chem., 2005, 40(1), 1-13.
[http://dx.doi.org/10.1016/j.ejmech.2004.10.001] [PMID: 15642405]
[4]
Pontiki, E.; Hadjipavlou-Litina, D. Histone deacetylase inhibitors (HDACIs). Structure--activity relationships: history and new QSAR perspectives. Med. Res. Rev., 2012, 32(1), 1-165.
[http://dx.doi.org/10.1002/med.20200] [PMID: 20162725]
[5]
Kouzarides, T. Histone acetylases and deacetylases in cell proliferation. Curr. Opin. Genet. Dev., 1999, 9(1), 40-48.
[http://dx.doi.org/10.1016/S0959-437X(99)80006-9] [PMID: 10072350]
[6]
Muraoka, M.; Konishi, M.; Kikuchi-Yanoshita, R.; Tanaka, K.; Shitara, N.; Chong, J-M.; Iwama, T.; Miyaki, M. p300 gene alterations in colorectal and gastric carcinomas. Oncogene, 1996, 12(7), 1565-1569.
[PMID: 8622873]
[7]
Lin, R.J.; Nagy, L.; Inoue, S.; Shao, W.; Miller, W.H., Jr; Evans, R.M. Role of the histone deacetylase complex in acute promyelocytic leukaemia. Nature, 1998, 391(6669), 811-814.
[http://dx.doi.org/10.1038/35895] [PMID: 9486654]
[8]
Grignani, F.; De Matteis, S.; Nervi, C.; Tomassoni, L.; Gelmetti, V.; Cioce, M.; Fanelli, M.; Ruthardt, M.; Ferrara, F.F.; Zamir, I.; Seiser, C.; Grignani, F.; Lazar, M.A.; Minucci, S.; Pelicci, P.G. Fusion proteins of the retinoic acid receptor-α recruit histone deacetylase in promyelocytic leukaemia. Nature, 1998, 391(6669), 815-818.
[http://dx.doi.org/10.1038/35901] [PMID: 9486655]
[9]
Leder, A.; Orkin, S.; Leder, P. Differentiation of erythroleukemic cells in the presence of inhibitors of DNA synthesis. Science, 1975, 190(4217), 893-894.
[http://dx.doi.org/10.1126/science.1059262] [PMID: 1059262]
[10]
Leder, A.; Leder, P. Butyric acid, a potent inducer of erythroid differentiation in cultured erythroleukemic cells. Cell, 1975, 5(3), 319-322.
[http://dx.doi.org/10.1016/0092-8674(75)90107-5] [PMID: 1056809]
[11]
Riggs, M.G.; Whittaker, R.G.; Neumann, J.R.; Ingram, V.M. n-Butyrate causes histone modification in HeLa and Friend erythroleukaemia cells. Nature, 1977, 268(5619), 462-464.
[http://dx.doi.org/10.1038/268462a0] [PMID: 268489]
[12]
Prasad, K.N. Butyric acid: a small fatty acid with diverse biological functions. Life Sci., 1980, 27(15), 1351-1358.
[http://dx.doi.org/10.1016/0024-3205(80)90397-5] [PMID: 7003281]
[13]
Marks, P.; Rifkind, R.A.; Richon, V.M.; Breslow, R.; Miller, T.; Kelly, W.K. Histone deacetylases and cancer: causes and therapies. Nat. Rev. Cancer, 2001, 1(3), 194-202.
[http://dx.doi.org/10.1038/35106079] [PMID: 11902574]
[14]
Miller, T.A.; Witter, D.J.; Belvedere, S. Histone deacetylase inhibitors. J. Med. Chem., 2003, 46(24), 5097-5116.
[http://dx.doi.org/10.1021/jm0303094] [PMID: 14613312]
[15]
Paris, M.; Porcelloni, M.; Binaschi, M.; Fattori, D. Histone deacetylase inhibitors: from bench to clinic. J. Med. Chem., 2008, 51(6), 1505-1529.
[http://dx.doi.org/10.1021/jm7011408] [PMID: 18247554]
[16]
Kalin, J.H.; Bergman, J.A. Development and therapeutic implications of selective histone deacetylase 6 inhibitors. J. Med. Chem., 2013, 56(16), 6297-6313.
[http://dx.doi.org/10.1021/jm4001659] [PMID: 23627282]
[17]
Mottamal, M.; Zheng, S.; Huang, T.L.; Wang, G. Histone deacetylase inhibitors in clinical studies as templates for new anticancer agents. Molecules, 2015, 20(3), 3898-3941.
[http://dx.doi.org/10.3390/molecules20033898] [PMID: 25738536]
[18]
Richardson, P.G.; Mitsiades, C.S.; Laubach, J.P.; Hajek, R.; Spicka, I.; Dimopoulos, M.A.; Moreau, P.; Siegel, D.S.; Jagannath, S.; Anderson, K.C. Preclinical data and early clinical experience supporting the use of histone deacetylase inhibitors in multiple myeloma. Leuk. Res., 2013, 37(7), 829-837.
[http://dx.doi.org/10.1016/j.leukres.2013.03.006] [PMID: 23582718]
[19]
Manal, M.; Chandrasekar, M.J.; Gomathi Priya, J.; Nanjan, M.J. Inhibitors of histone deacetylase as antitumor agents: A critical review. Bioorg. Chem., 2016, 67, 18-42.
[http://dx.doi.org/10.1016/j.bioorg.2016.05.005] [PMID: 27239721]
[20]
Tedjaseputra, A.; Galli, S.; Ibrahim, M.; Harrison, C.; McLornan, D. Histone deacetylase inhibitors in myeloproliferative neoplasms: current roles and future prospects. Expert Opin. Orphan Drugs, 2016, 4, 417-427.
[http://dx.doi.org/10.1517/21678707.2016.1149467]
[21]
Shyamasundar, S.; Dheen, S.T.; Bay, B.H. Histone modifications as molecular targets in nasopharyngeal cancer. Curr. Med. Chem., 2016, 23(2), 186-197.
[http://dx.doi.org/10.2174/0929867323666151106125631] [PMID: 26549431]
[22]
Park, J.; Thomas, S.; Munster, P.N. Epigenetic modulation with histone deacetylase inhibitors in combination with immunotherapy. Epigenomics, 2015, 7(4), 641-652.
[http://dx.doi.org/10.2217/epi.15.16] [PMID: 26111034]
[23]
Shen, L.; Orillion, A.; Pili, R. Histone deacetylase inhibitors as immunomodulators in cancer therapeutics. Epigenomics, 2016, 8(3), 415-428.
[http://dx.doi.org/10.2217/epi.15.118] [PMID: 26950532]
[24]
Kim, H.J.; Bae, S.C. Histone deacetylase inhibitors: molecular mechanisms of action and clinical trials as anti-cancer drugs. Am. J. Transl. Res., 2011, 3(2), 166-179.
[PMID: 21416059]
[25]
Gore, S.D.; Carducci, M.A. Modifying histones to tame cancer: clinical development of sodium phenylbutyrate and other histone deacetylase inhibitors. Expert Opin. Investig. Drugs, 2000, 9(12), 2923-2934.
[http://dx.doi.org/10.1517/13543784.9.12.2923] [PMID: 11093362]
[26]
DeWoskin, V.A.; Million, R.P. The epigenetics pipeline. Nat. Rev. Drug Discov., 2013, 12(9), 661-662.
[http://dx.doi.org/10.1038/nrd4091] [PMID: 23989788]
[27]
Beckers, T.; Burkhardt, C.; Wieland, H.; Gimmnich, P.; Ciossek, T.; Maier, T.; Sanders, K. Distinct pharmacological properties of second generation HDAC inhibitors with the benzamide or hydroxamate head group. Int. J. Cancer, 2007, 121(5), 1138-1148.
[http://dx.doi.org/10.1002/ijc.22751] [PMID: 17455259]
[28]
Rajak, H.; Singh, A.; Raghuwanshi, K.; Kumar, R.; Dewangan, P.K.; Veerasamy, R.; Sharma, P.C.; Dixit, A.; Mishra, P. A structural insight into hydroxamic acid based histone deacetylase inhibitors for the presence of anticancer activity. Curr. Med. Chem., 2014, 21(23), 2642-2664.
[http://dx.doi.org/10.2174/09298673113209990191] [PMID: 23895688]
[29]
Chalret du Rieu, Q.; Fouliard, S.; Jacquet-Bescond, A.; Robert, R.; Kloos, I.; Depil, S.; Chatelut, E.; Chenel, M. Application of hematological toxicity modeling in clinical development of abexinostat (S-78454, PCI-24781), a new histone deacetylase inhibitor. Pharm. Res., 2013, 30(10), 2640-2653.
[http://dx.doi.org/10.1007/s11095-013-1089-1] [PMID: 23737346]
[30]
Choy, E.; Flamand, Y.; Balasubramanian, S.; Butrynski, J.E.; Harmon, D.C.; George, S.; Cote, G.M.; Wagner, A.J.; Morgan, J.A.; Sirisawad, M.; Mani, C.; Hornicek, F.J.; Duan, Z.; Demetri, G.D. Phase 1 study of oral abexinostat, a histone deacetylase inhibitor, in combination with doxorubicin in patients with metastatic sarcoma. Cancer, 2015, 121(8), 1223-1230.
[http://dx.doi.org/10.1002/cncr.29175] [PMID: 25536954]
[31]
Buggy, J.J.; Cao, Z.A.; Bass, K.E.; Verner, E.; Balasubramanian, S.; Liu, L.; Schultz, B.E.; Young, P.R.; Dalrymple, S.A. CRA-024781: a novel synthetic inhibitor of histone deacetylase enzymes with antitumor activity in vitro and in vivo. Mol. Cancer Ther., 2006, 5(5), 1309-1317.
[http://dx.doi.org/10.1158/1535-7163.MCT-05-0442] [PMID: 16731764]
[32]
Yang, C.; Choy, E.; Hornicek, F.J.; Wood, K.B.; Schwab, J.H.; Liu, X.; Mankin, H.; Duan, Z. Histone deacetylase inhibitor (HDACI) PCI-24781 potentiates cytotoxic effects of doxorubicin in bone sarcoma cells. Cancer Chemother. Pharmacol., 2011, 67(2), 439-446.
[http://dx.doi.org/10.1007/s00280-010-1344-7] [PMID: 20461381]
[33]
Banuelos, C.A.; Banáth, J.P.; MacPhail, S.H.; Zhao, J.; Reitsema, T.; Olive, P.L. Radiosensitization by the histone deacetylase inhibitor PCI-24781. Clin. Cancer Res., 2007, 13(22 Pt 1), 6816-6826.
[http://dx.doi.org/10.1158/1078-0432.CCR-07-1126] [PMID: 18006784]
[34]
Bhalla, S.; Balasubramanian, S.; David, K.; Sirisawad, M.; Buggy, J.; Mauro, L.; Prachand, S.; Miller, R.; Gordon, L.I.; Evens, A.M. PCI-24781 induces caspase and reactive oxygen species-dependent apoptosis through NF-kappaB mechanisms and is synergistic with bortezomib in lymphoma cells. Clin. Cancer Res., 2009, 15(10), 3354-3365.
[http://dx.doi.org/10.1158/1078-0432.CCR-08-2365] [PMID: 19417023]
[35]
Sholler, G.S.; Currier, E.A.; Dutta, A.; Slavik, M.A.; Illenye, S.A.; Mendonca, M.C.; Dragon, J.; Roberts, S.S.; Bond, J.P. PCI-24781 (abexinostat), a novel histone deacetylase inhibitor, induces reactive oxygen species-dependent apoptosis and is synergistic with bortezomib in neuroblastoma. J. Cancer Ther. Res., 2013, 2, 21.
[http://dx.doi.org/10.7243/2049-7962-2-21] [PMID: 25520806]
[36]
Rashidi, A.; Cashen, A.F. Belinostat for the treatment of relapsed or refractory peripheral T-cell lymphoma. Future Oncol., 2015, 11(11), 1659-1664.
[http://dx.doi.org/10.2217/fon.15.62] [PMID: 26043217]
[37]
Plumb, J.A.; Finn, P.W.; Williams, R.J.; Bandara, M.J.; Romero, M.R.; Watkins, C.J.; La Thangue, N.B.; Brown, R. Pharmacodynamic response and inhibition of growth of human tumor xenografts by the novel histone deacetylase inhibitor PXD101. Mol. Cancer Ther., 2003, 2(8), 721-728.
[PMID: 12939461]
[38]
Steele, N.L.; Plumb, J.A.; Vidal, L.; Tjørnelund, J.; Knoblauch, P.; Rasmussen, A.; Ooi, C.E.; Buhl-Jensen, P.; Brown, R.; Evans, T.R.; DeBono, J.S. A phase 1 pharmacokinetic and pharmacodynamic study of the histone deacetylase inhibitor belinostat in patients with advanced solid tumors. Clin. Cancer Res., 2008, 14(3), 804-810.
[http://dx.doi.org/10.1158/1078-0432.CCR-07-1786] [PMID: 18245542]
[39]
Lee, H.Z.; Kwitkowski, V.E.; Del Valle, P.L.; Ricci, M.S.; Saber, H.; Habtemariam, B.A.; Bullock, J.; Bloomquist, E.; Li , Shen. Y.; Chen, X.H.; Brown, J.; Mehrotra, N.; Dorff, S.; Charlab, R.; Kane, R.C.; Kaminskas, E.; Justice, R.; Farrell, A.T.; Pazdur, R. FDA approval: Belinostat for the treatment of patients with relapsed or refractory peripheral T-cell lymphoma. Clin. Cancer Res., 2015, 21(12), 2666-2670.
[http://dx.doi.org/10.1158/1078-0432.CCR-14-3119] [PMID: 25802282]
[40]
Poole, R.M. Belinostat: first global approval. Drugs, 2014, 74(13), 1543-1554.
[http://dx.doi.org/10.1007/s40265-014-0275-8] [PMID: 25134672]
[41]
Karin, M. Nuclear factor-kappaB in cancer development and progression. Nature, 2006, 441(7092), 431-436.
[http://dx.doi.org/10.1038/nature04870] [PMID: 16724054]
[42]
Beg, A.A.; Baltimore, D. An essential role for NF-kappaB in preventing TNF-α-induced cell death. Science, 1996, 274(5288), 782-784.
[http://dx.doi.org/10.1126/science.274.5288.782] [PMID: 8864118]
[43]
She, Q.B.; Halilovic, E.; Ye, Q.; Zhen, W.; Shirasawa, S.; Sasazuki, T.; Solit, D.B.; Rosen, N. 4E-BP1 is a key effector of the oncogenic activation of the AKT and ERK signaling pathways that integrates their function in tumors. Cancer Cell, 2010, 18(1), 39-51.
[http://dx.doi.org/10.1016/j.ccr.2010.05.023] [PMID: 20609351]
[44]
Moschetta, M.; Reale, A.; Marasco, C.; Vacca, A.; Carratù, M.R. Therapeutic targeting of the mTOR-signalling pathway in cancer: benefits and limitations. Br. J. Pharmacol., 2014, 171(16), 3801-3813.
[http://dx.doi.org/10.1111/bph.12749] [PMID: 24780124]
[45]
Chien, W.; Lee, D.H.; Zheng, Y.; Wuensche, P.; Alvarez, R.; Wen, D.L.; Aribi, A.M.; Thean, S.M.; Doan, N.B.; Said, J.W.; Koeffler, H.P. Growth inhibition of pancreatic cancer cells by histone deacetylase inhibitor belinostat through suppression of multiple pathways including HIF, NFkB, and mTOR signaling in vitro and in vivo. Mol. Carcinog., 2014, 53(9), 722-735.
[http://dx.doi.org/10.1002/mc.22024] [PMID: 23475695]
[46]
Thomas, A.; Rajan, A.; Szabo, E.; Tomita, Y.; Carter, C.A.; Scepura, B.; Lopez-Chavez, A.; Lee, M-J.; Redon, C.E.; Frosch, A.; Peer, C.J.; Chen, Y.; Piekarz, R.; Steinberg, S.M.; Trepel, J.B.; Figg, W.D.; Schrump, D.S.; Giaccone, G. A phase I/II trial of belinostat in combination with cisplatin, doxorubicin, and cyclophosphamide in thymic epithelial tumors: a clinical and translational study. Clin. Cancer Res., 2014, 20(21), 5392-5402.
[http://dx.doi.org/10.1158/1078-0432.CCR-14-0968] [PMID: 25189481]
[47]
Sakuishi, K.; Apetoh, L.; Sullivan, J.M.; Blazar, B.R.; Kuchroo, V.K.; Anderson, A.C. Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. J. Exp. Med., 2010, 207(10), 2187-2194.
[http://dx.doi.org/10.1084/jem.20100643] [PMID: 20819927]
[48]
Remiszewski, S.W. The discovery of NVP-LAQ824: from concept to clinic. Curr. Med. Chem., 2003, 10(22), 2393-2402.
[http://dx.doi.org/10.2174/0929867033456675] [PMID: 14529481]
[49]
Cho, Y.S.; Whitehead, L.; Li, J.; Chen, C.H.; Jiang, L.; Vögtle, M.; Francotte, E.; Richert, P.; Wagner, T.; Traebert, M.; Lu, Q.; Cao, X.; Dumotier, B.; Fejzo, J.; Rajan, S.; Wang, P.; Yan-Neale, Y.; Shao, W.; Atadja, P.; Shultz, M. Conformational refinement of hydroxamate-based histone deacetylase inhibitors and exploration of 3-piperidin-3-ylindole analogues of dacinostat (LAQ824). J. Med. Chem., 2010, 53(7), 2952-2963.
[http://dx.doi.org/10.1021/jm100007m] [PMID: 20205394]
[50]
Shultz, M.D.; Cao, X.; Chen, C.H.; Cho, Y.S.; Davis, N.R.; Eckman, J.; Fan, J.; Fekete, A.; Firestone, B.; Flynn, J.; Green, J.; Growney, J.D.; Holmqvist, M.; Hsu, M.; Jansson, D.; Jiang, L.; Kwon, P.; Liu, G.; Lombardo, F.; Lu, Q.; Majumdar, D.; Meta, C.; Perez, L.; Pu, M.; Ramsey, T.; Remiszewski, S.; Skolnik, S.; Traebert, M.; Urban, L.; Uttamsingh, V.; Wang, P.; Whitebread, S.; Whitehead, L.; Yan-Neale, Y.; Yao, Y.M.; Zhou, L.; Atadja, P. Optimization of the in vitro cardiac safety of hydroxamate-based histone deacetylase inhibitors. J. Med. Chem., 2011, 54(13), 4752-4772.
[http://dx.doi.org/10.1021/jm200388e] [PMID: 21650221]
[51]
Remiszewski, S.W.; Sambucetti, L.C.; Bair, K.W.; Bontempo, J.; Cesarz, D.; Chandramouli, N.; Chen, R.; Cheung, M.; Cornell-Kennon, S.; Dean, K.; Diamantidis, G.; France, D.; Green, M.A.; Howell, K.L.; Kashi, R.; Kwon, P.; Lassota, P.; Martin, M.S.; Mou, Y.; Perez, L.B.; Sharma, S.; Smith, T.; Sorensen, E.; Taplin, F.; Trogani, N.; Versace, R.; Walker, H.; Weltchek-Engler, S.; Wood, A.; Wu, A.; Atadja, P. N-hydroxy-3-phenyl-2-propenamides as novel inhibitors of human histone deacetylase with in vivo antitumor activity: discovery of (2E)-N-hydroxy-3-[4-[[(2-hydroxyethyl)[2-(1H-indol-3-yl)ethyl]amino]methyl] phen-yl]-2-propenamide (NVP-LAQ824). J. Med. Chem., 2003, 46(21), 4609-4624.
[http://dx.doi.org/10.1021/jm030235w] [PMID: 14521422]
[52]
Khan, N.; Jeffers, M.; Kumar, S.; Hackett, C.; Boldog, F.; Khramtsov, N.; Qian, X.; Mills, E.; Berghs, S.C.; Carey, N.; Finn, P.W.; Collins, L.S.; Tumber, A.; Ritchie, J.W.; Jensen, P.B.; Lichenstein, H.S.; Sehested, M. Determination of the class and isoform selectivity of small-molecule histone deacetylase inhibitors. Biochem. J., 2008, 409(2), 581-589.
[http://dx.doi.org/10.1042/BJ20070779] [PMID: 17868033]
[53]
Grant, S. The novel histone deacetylase inhibitor NVP-LAQ824: an addition to the therapeutic armamentarium in leukemia? Leukemia, 2004, 18(12), 1931-1933.
[http://dx.doi.org/10.1038/sj.leu.2403522] [PMID: 15496978]
[54]
Fuino, L.; Bali, P.; Wittmann, S.; Donapaty, S.; Guo, F.; Yamaguchi, H.; Wang, H.G.; Atadja, P.; Bhalla, K. Histone deacetylase inhibitor LAQ824 down-regulates Her-2 and sensitizes human breast cancer cells to trastuzumab, taxotere, gemcitabine, and epothilone B. Mol. Cancer Ther., 2003, 2(10), 971-984.
[PMID: 14578462]
[55]
Hsieh, C.L.; Chen, D.S.; Hwang, L.H. Tumor-induced immunosuppression: a barrier to immunotherapy of large tumors by cytokine-secreting tumor vaccine. Hum. Gene Ther., 2000, 11(5), 681-692.
[http://dx.doi.org/10.1089/10430340050015581] [PMID: 10757348]
[56]
Vo, D.D.; Prins, R.M.; Begley, J.L.; Donahue, T.R.; Morris, L.F.; Bruhn, K.W.; de la Rocha, P.; Yang, M.Y.; Mok, S.; Garban, H.J.; Craft, N.; Economou, J.S.; Marincola, F.M.; Wang, E.; Ribas, A. Enhanced antitumor activity induced by adoptive T-cell transfer and adjunctive use of the histone deacetylase inhibitor LAQ824. Cancer Res., 2009, 69(22), 8693-8699.
[http://dx.doi.org/10.1158/0008-5472.CAN-09-1456] [PMID: 19861533]
[57]
Groux, H.; Bigler, M.; de Vries, J.E.; Roncarolo, M.G. Interleukin-10 induces a long-term antigen-specific anergic state in human CD4+ T cells. J. Exp. Med., 1996, 184(1), 19-29.
[http://dx.doi.org/10.1084/jem.184.1.19] [PMID: 8691133]
[58]
Wang, H.; Cheng, F.; Woan, K.; Sahakian, E.; Merino, O.; Rock-Klotz, J.; Vicente-Suarez, I.; Pinilla-Ibarz, J.; Wright, K.L.; Seto, E.; Bhalla, K.; Villagra, A.; Sotomayor, E.M. Histone deacetylase inhibitor LAQ824 augments inflammatory responses in macrophages through transcriptional regulation of IL-10. J. Immunol., 2011, 186(7), 3986-3996.
[http://dx.doi.org/10.4049/jimmunol.1001101] [PMID: 21368229]
[59]
Suzuki, T.; Ando, T.; Tsuchiya, K.; Fukazawa, N.; Saito, A.; Mariko, Y.; Yamashita, T.; Nakanishi, O. Synthesis and histone deacetylase inhibitory activity of new benzamide derivatives. J. Med. Chem., 1999, 42(15), 3001-3003.
[http://dx.doi.org/10.1021/jm980565u] [PMID: 10425110]
[60]
Saito, A.; Yamashita, T.; Mariko, Y.; Nosaka, Y.; Tsuchiya, K.; Ando, T.; Suzuki, T.; Tsuruo, T.; Nakanishi, O. A synthetic inhibitor of histone deacetylase, MS-27-275, with marked in vivo antitumor activity against human tumors. Proc. Natl. Acad. Sci. USA, 1999, 96(8), 4592-4597.
[http://dx.doi.org/10.1073/pnas.96.8.4592] [PMID: 10200307]
[61]
Jaboin, J.; Wild, J.; Hamidi, H.; Khanna, C.; Kim, C.J.; Robey, R.; Bates, S.E.; Thiele, C.J. MS-27-275, an inhibitor of histone deacetylase, has marked in vitro and in vivo antitumor activity against pediatric solid tumors. Cancer Res., 2002, 62(21), 6108-6115.
[PMID: 12414635]
[62]
Lucas, D.M.; Davis, M.E.; Parthun, M.R.; Mone, A.P.; Kitada, S.; Cunningham, K.D.; Flax, E.L.; Wickham, J.; Reed, J.C.; Byrd, J.C.; Grever, M.R. The histone deacetylase inhibitor MS-275 induces caspase-dependent apoptosis in B-cell chronic lymphocytic leukemia cells. Leukemia, 2004, 18(7), 1207-1214.
[http://dx.doi.org/10.1038/sj.leu.2403388] [PMID: 15116122]
[63]
Qian, D.Z.; Wei, Y.F.; Wang, X.; Kato, Y.; Cheng, L.; Pili, R. Antitumor activity of the histone deacetylase inhibitor MS-275 in prostate cancer models. Prostate, 2007, 67(11), 1182-1193.
[http://dx.doi.org/10.1002/pros.20611] [PMID: 17520666]
[64]
Juergens, R.A.; Wrangle, J.; Vendetti, F.P.; Murphy, S.C.; Zhao, M.; Coleman, B.; Sebree, R.; Rodgers, K.; Hooker, C.M.; Franco, N.; Lee, B.; Tsai, S.; Delgado, I.E.; Rudek, M.A.; Belinsky, S.A.; Herman, J.G.; Baylin, S.B.; Brock, M.V.; Rudin, C.M. Combination epigenetic therapy has efficacy in patients with refractory advanced non-small cell lung cancer. Cancer Discov., 2011, 1(7), 598-607.
[http://dx.doi.org/10.1158/2159-8290.CD-11-0214] [PMID: 22586682]
[65]
Lee, P.; Murphy, B.; Miller, R.; Menon, V.; Banik, N.L.; Giglio, P.; Lindhorst, S.M.; Varma, A.K.; Vandergrift, W.A., III; Patel, S.J.; Das, A. Mechanisms and clinical significance of histone deacetylase inhibitors: epigenetic glioblastoma therapy. Anticancer Res., 2015, 35(2), 615-625.
[PMID: 25667438]
[66]
Frys, S.; Simons, Z.; Hu, Q.; Barth, M.J.; Gu, J.J.; Mavis, C.; Skitzki, J.; Song, L.; Czuczman, M.S.; Hernandez-Ilizaliturri, F.J. Entinostat, a novel histone deacetylase inhibitor is active in B-cell lymphoma and enhances the anti-tumour activity of rituximab and chemotherapy agents. Br. J. Haematol., 2015, 169(4), 506-519.
[http://dx.doi.org/10.1111/bjh.13318] [PMID: 25712263]
[67]
Curiel, T.J.; Coukos, G.; Zou, L.; Alvarez, X.; Cheng, P.; Mottram, P.; Evdemon-Hogan, M.; Conejo-Garcia, J.R.; Zhang, L.; Burow, M.; Zhu, Y.; Wei, S.; Kryczek, I.; Daniel, B.; Gordon, A.; Myers, L.; Lackner, A.; Disis, M.L.; Knutson, K.L.; Chen, L.; Zou, W. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med., 2004, 10(9), 942-949.
[http://dx.doi.org/10.1038/nm1093] [PMID: 15322536]
[68]
Shen, L.; Ciesielski, M.; Ramakrishnan, S.; Miles, K.M.; Ellis, L.; Sotomayor, P.; Shrikant, P.; Fenstermaker, R.; Pili, R. Class I histone deacetylase inhibitor entinostat suppresses regulatory T cells and enhances immunotherapies in renal and prostate cancer models. PLoS One, 2012, 7(1), e30815.
[http://dx.doi.org/10.1371/journal.pone.0030815] [PMID: 22303460]
[69]
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(11), 1299-1307.
[http://dx.doi.org/10.1038/nm1652] [PMID: 17922010]
[70]
Vire, B.; de Walque, S.; Restouin, A.; Olive, D.; Van Lint, C.; Collette, Y. Anti-leukemia activity of MS-275 histone deacetylase inhibitor implicates 4-1BBL/4-1BB immunomodulatory functions. PLoS One, 2009, 4(9), e7085.
[http://dx.doi.org/10.1371/journal.pone.0007085] [PMID: 19759901]
[71]
Cooper, M.A.; Fehniger, T.A.; Turner, S.C.; Chen, K.S.; Ghaheri, B.A.; Ghayur, T.; Carson, W.E.; Caligiuri, M.A. Human natural killer cells: a unique innate immunoregulatory role for the CD56(bright) subset. Blood, 2001, 97(10), 3146-3151.
[http://dx.doi.org/10.1182/blood.V97.10.3146] [PMID: 11342442]
[72]
Zhu, S.; Denman, C.J.; Cobanoglu, Z.S.; Kiany, S.; Lau, C.C.; Gottschalk, S.M.; Hughes, D.P.; Kleinerman, E.S.; Lee, D.A. The narrow-spectrum HDAC inhibitor entinostat enhances NKG2D expression without NK cell toxicity, leading to enhanced recognition of cancer cells. Pharm. Res., 2015, 32(3), 779-792.
[http://dx.doi.org/10.1007/s11095-013-1231-0] [PMID: 24203492]
[73]
Cycon, K.A.; Mulvaney, K.; Rimsza, L.M.; Persky, D.; Murphy, S.P. Histone deacetylase inhibitors activate CIITA and MHC class II antigen expression in diffuse large B-cell lymphoma. Immunology, 2013, 140(2), 259-272.
[http://dx.doi.org/10.1111/imm.12136] [PMID: 23789844]
[74]
Figdor, C.G.; de Vries, I.J.; Lesterhuis, W.J.; Melief, C.J. Dendritic cell immunotherapy: mapping the way. Nat. Med., 2004, 10(5), 475-480.
[http://dx.doi.org/10.1038/nm1039] [PMID: 15122249]
[75]
Nencioni, A.; Beck, J.; Werth, D.; Grünebach, F.; Patrone, F.; Ballestrero, A.; Brossart, P. Histone deacetylase inhibitors affect dendritic cell differentiation and immunogenicity. Clin. Cancer Res., 2007, 13(13), 3933-3941.
[http://dx.doi.org/10.1158/1078-0432.CCR-06-2903] [PMID: 17606727]
[76]
Leoni, F.; Fossati, G.; Lewis, E.C.; Lee, J.K.; Porro, G.; Pagani, P.; Modena, D.; Moras, M.L.; Pozzi, P.; Reznikov, L.L.; Siegmund, B.; Fantuzzi, G.; Dinarello, C.A.; Mascagni, P. The histone deacetylase inhibitor ITF2357 reduces production of pro-inflammatory cytokines in vitro and systemic inflammation. in vivo. Mol. Med., 2005, 11(1-12), 1- 15.
[http://dx.doi.org/10.2119/2006-00005.Dinarello] [PMID: 16557334]
[77]
Pathil, A.; Armeanu, S.; Venturelli, S.; Mascagni, P.; Weiss, T.S.; Gregor, M.; Lauer, U.M.; Bitzer, M. HDAC inhibitor treatment of hepatoma cells induces both TRAIL-independent apoptosis and restoration of sensitivity to TRAIL. Hepatology, 2006, 43(3), 425-434.
[http://dx.doi.org/10.1002/hep.21054] [PMID: 16583461]
[78]
Armeanu, S.; Pathil, A.; Venturelli, S.; Mascagni, P.; Weiss, T.S.; Göttlicher, M.; Gregor, M.; Lauer, U.M.; Bitzer, M. Apoptosis on hepatoma cells but not on primary hepatocytes by histone deacetylase inhibitors valproate and ITF2357. J. Hepatol., 2005, 42(2), 210-217.
[http://dx.doi.org/10.1016/j.jhep.2004.10.020] [PMID: 15664246]
[79]
Rambaldi, A.; Dellacasa, C.M.; Finazzi, G.; Carobbio, A.; Ferrari, M.L.; Guglielmelli, P.; Gattoni, E.; Salmoiraghi, S.; Finazzi, M.C.; Di Tollo, S.; D’Urzo, C.; Vannucchi, A.M.; Barosi, G.; Barbui, T. A pilot study of the Histone-Deacetylase inhibitor Givinostat in patients with JAK2V617F positive chronic myeloproliferative neoplasms. Br. J. Haematol., 2010, 150(4), 446-455.
[PMID: 20560970]
[80]
Finazzi, G.; Vannucchi, A.M.; Martinelli, V.; Ruggeri, M.; Nobile, F.; Specchia, G.; Pogliani, E.M.; Olimpieri, O.M.; Fioritoni, G.; Musolino, C.; Cilloni, D.; Sivera, P.; Barosi, G.; Finazzi, M.C.; Di Tollo, S.; Demuth, T.; Barbui, T.; Rambaldi, A. A phase II study of Givinostat in combination with hydroxycarbamide in patients with polycythaemia vera unresponsive to hydroxycarbamide monotherapy. Br. J. Haematol., 2013, 161(5), 688-694.
[http://dx.doi.org/10.1111/bjh.12332] [PMID: 23573950]
[81]
Carta, S.; Tassi, S.; Semino, C.; Fossati, G.; Mascagni, P.; Dinarello, C.A.; Rubartelli, A. Histone deacetylase inhibitors prevent exocytosis of interleukin-1β-containing secretory lysosomes: role of microtubules. Blood, 2006, 108(5), 1618-1626.
[http://dx.doi.org/10.1182/blood-2006-03-014126] [PMID: 16684958]
[82]
Faraco, G.; Pittelli, M.; Cavone, L.; Fossati, S.; Porcu, M.; Mascagni, P.; Fossati, G.; Moroni, F.; Chiarugi, A. Histone deacetylase (HDAC) inhibitors reduce the glial inflammatory response in vitro and in vivo. Neurobiol. Dis., 2009, 36(2), 269-279.
[http://dx.doi.org/10.1016/j.nbd.2009.07.019] [PMID: 19635561]
[83]
Lewis, E.C.; Blaabjerg, L.; Størling, J.; Ronn, S.G.; Mascagni, P.; Dinarello, C.A.; Mandrup-Poulsen, T. The oral histone deacetylase inhibitor ITF2357 reduces cytokines and protects islet β cells in vivo and in vitro. Mol. Med., 2011, 17(5-6), 369-377.
[http://dx.doi.org/10.2119/molmed.2010.00152] [PMID: 21193899]
[84]
Golay, J.; Cuppini, L.; Leoni, F.; Micò, C.; Barbui, V.; Domenghini, M.; Lombardi, L.; Neri, A.; Barbui, A.M.; Salvi, A.; Pozzi, P.; Porro, G.; Pagani, P.; Fossati, G.; Mascagni, P.; Introna, M.; Rambaldi, A. The histone deacetylase inhibitor ITF2357 has anti-leukemic activity in vitro and in vivo and inhibits IL-6 and VEGF production by stromal cells. Leukemia, 2007, 21(9), 1892-1900.
[http://dx.doi.org/10.1038/sj.leu.2404860] [PMID: 17637810]
[85]
Sirohi, B.; Powles, R. Multiple myeloma. Lancet, 2004, 363(9412), 875-887.
[http://dx.doi.org/10.1016/S0140-6736(04)15736-X] [PMID: 15031034]
[86]
Podar, K.; Anderson, K.C. The pathophysiologic role of VEGF in hematologic malignancies: therapeutic implications. Blood, 2005, 105(4), 1383-1395.
[http://dx.doi.org/10.1182/blood-2004-07-2909] [PMID: 15471951]
[87]
Galimberti, S.; Canestraro, M.; Savli, H.; Palumbo, G.A.; Tibullo, D.; Nagy, B.; Piaggi, S.; Guerrini, F.; Cine, N.; Metelli, M.R.; Petrini, M. ITF2357 interferes with apoptosis and inflammatory pathways in the HL-60 model: a gene expression study. Anticancer Res., 2010, 30(11), 4525-4535.
[PMID: 21115902]
[88]
Glauben, R.; Sonnenberg, E.; Wetzel, M.; Mascagni, P.; Siegmund, B. Histone deacetylase inhibitors modulate interleukin 6-dependent CD4+ T cell polarization in vitro and in vivo. J. Biol. Chem., 2014, 289(9), 6142-6151.
[http://dx.doi.org/10.1074/jbc.M113.517599] [PMID: 24421314]
[89]
Regna, N.L.; Chafin, C.B.; Hammond, S.E.; Puthiyaveetil, A.G.; Caudell, D.L.; Reilly, C.M. Class I and II histone deacetylase inhibition by ITF2357 reduces SLE pathogenesis in vivo. Clin. Immunol., 2014, 151(1), 29-42.
[http://dx.doi.org/10.1016/j.clim.2014.01.002] [PMID: 24503172]
[90]
Zhou, N.; Moradei, O.; Raeppel, S.; Leit, S.; Frechette, S.; Gaudette, F.; Paquin, I.; Bernstein, N.; Bouchain, G.; Vaisburg, A.; Jin, Z.; Gillespie, J.; Wang, J.; Fournel, M.; Yan, P.T.; Trachy-Bourget, M-C.; Kalita, A.; Lu, A.; Rahil, J.; MacLeod, A.R.; Li, Z.; Besterman, J.M.; Delorme, D. Discovery of N-(2-aminophenyl)-4-[(4-pyridin-3-ylpyrimidin-2-ylamino)methyl]benzamide (MGCD0103), an orally active histone deacetylase inhibitor. J. Med. Chem., 2008, 51(14), 4072-4075.
[http://dx.doi.org/10.1021/jm800251w] [PMID: 18570366]
[91]
Fournel, M.; Bonfils, C.; Hou, Y.; Yan, P.T.; Trachy-Bourget, M-C.; Kalita, A.; Liu, J.; Lu, A-H.; Zhou, N.Z.; Robert, M-F.; Gillespie, J.; Wang, J.J.; Ste-Croix, H.; Rahil, J.; Lefebvre, S.; Moradei, O.; Delorme, D.; Macleod, A.R.; Besterman, J.M.; Li, Z. MGCD0103, a novel isotype-selective histone deacetylase inhibitor, has broad spectrum antitumor activity in vitro and in vivo. Mol. Cancer Ther., 2008, 7(4), 759-768.
[http://dx.doi.org/10.1158/1535-7163.MCT-07-2026] [PMID: 18413790]
[92]
Boumber, Y.; Younes, A.; Garcia-Manero, G. Mocetinostat (MGCD0103): a review of an isotype-specific histone deacetylase inhibitor. Expert Opin. Investig. Drugs, 2011, 20(6), 823-829.
[http://dx.doi.org/10.1517/13543784.2011.577737] [PMID: 21554162]
[93]
Revill, P.; Mealy, N.; Serradell, N.; Bolos, J.; Rosa, E. Panobinostat: histone deacetylase (HDAC) inhibitor apoptosis inducer oncolytic drugs. Future, 2007, 32, 315-322.
[http://dx.doi.org/10.1358/dof.2007.032.04.1094476]
[94]
Ganai, S.A. Panobinostat: The small molecule metalloenzyme inhibitor with marvelous anticancer activity. Curr. Top. Med. Chem., 2016, 16(4), 427-434.
[http://dx.doi.org/10.2174/1568026615666150813145800] [PMID: 26268342]
[95]
Atadja, P. Development of the pan-DAC inhibitor panobinostat (LBH589): successes and challenges. Cancer Lett., 2009, 280(2), 233-241.
[http://dx.doi.org/10.1016/j.canlet.2009.02.019] [PMID: 19344997]
[96]
Garnock-Jones, K.P. Panobinostat: first global approval. Drugs, 2015, 75(6), 695-704.
[http://dx.doi.org/10.1007/s40265-015-0388-8] [PMID: 25837990]
[97]
Klein, J.M.; Henke, A.; Sauer, M.; Bessler, M.; Reiners, K.S.; Engert, A.; Hansen, H.P.; von Strandmann, E.P. The histone deacetylase inhibitor LBH589 (panobinostat) modulates the crosstalk of lymphocytes with Hodgkin lymphoma cell lines. PLoS One, 2013, 8(11), e79502.
[http://dx.doi.org/10.1371/journal.pone.0079502] [PMID: 24278143]
[98]
Woods, D.M.; Woan, K.; Cheng, F.; Wang, H.; Perez-Villarroel, P.; Lee, C.; Lienlaf, M.; Atadja, P.; Seto, E.; Weber, J.; Sotomayor, E.M.; Villagra, A. The antimelanoma activity of the histone deacetylase inhibitor panobinostat (LBH589) is mediated by direct tumor cytotoxicity and increased tumor immunogenicity. Melanoma Res., 2013, 23(5), 341-348.
[http://dx.doi.org/10.1097/CMR.0b013e328364c0ed] [PMID: 23963286]
[99]
Oki, Y.; Buglio, D.; Zhang, J.; Ying, Y.; Zhou, S.; Sureda, A.; Ben-Yehuda, D.; Zinzani, P.L.; Prince, H.M.; Harrison, S.J.; Kirschbaum, M.; Johnston, P.B.; Shen, A.; von Tresckow, B.; Younes, A.; Younes, A. Immune regulatory effects of panobinostat in patients with Hodgkin lymphoma through modulation of serum cytokine levels and T-cell PD1 expression. Blood Cancer J., 2014, 4, e236.
[http://dx.doi.org/10.1038/bcj.2014.58] [PMID: 25105535]
[100]
Lisiero, D.N.; Soto, H.; Everson, R.G.; Liau, L.M.; Prins, R.M. The histone deacetylase inhibitor, LBH589, promotes the systemic cytokine and effector responses of adoptively transferred CD8+ T cells. J. Immunother. Cancer, 2014, 2, 8.
[http://dx.doi.org/10.1186/2051-1426-2-8] [PMID: 25054063]
[101]
Song, W.; Tai, Y-T.; Tian, Z.; Hideshima, T.; Chauhan, D.; Nanjappa, P.; Exley, M.A.; Anderson, K.C.; Munshi, N.C. HDAC inhibition by LBH589 affects the phenotype and function of human myeloid dendritic cells. Leukemia, 2011, 25(1), 161-168.
[http://dx.doi.org/10.1038/leu.2010.244] [PMID: 21102427]
[102]
Wong, D.J.; Rao, A.; Avramis, E.; Matsunaga, D.R.; Komatsubara, K.M.; Atefi, M.S.; Escuin-Ordinas, H.; Chodon, T.; Koya, R.C.; Ribas, A.; Comin-Anduix, B. Exposure to a histone deacetylase inhibitor has detrimental effects on human lymphocyte viability and function. Cancer Immunol. Res., 2014, 2(5), 459-468.
[http://dx.doi.org/10.1158/2326-6066.CIR-13-0188] [PMID: 24795358]
[103]
Ramakrishnan, V.; Kimlinger, T.; Timm, M.; Haug, J.; Rajkumar, S.V.; Kumar, S. Multiple mechanisms contribute to the synergistic anti-myeloma activity of the pan-histone deacetylase inhibitor LBH589 and the rapalog RAD001. Leuk. Res., 2014, 38(11), 1358-1366.
[http://dx.doi.org/10.1016/j.leukres.2014.09.004] [PMID: 25282334]
[104]
Waibel, M.; Christiansen, A.J.; Hibbs, M.L.; Shortt, J.; Jones, S.A.; Simpson, I.; Light, A.; O’Donnell, K.; Morand, E.F.; Tarlinton, D.M.; Johnstone, R.W.; Hawkins, E.D. Manipulation of B-cell responses with histone deacetylase inhibitors. Nat. Commun., 2015, 6, 6838.
[http://dx.doi.org/10.1038/ncomms7838] [PMID: 25913720]
[105]
Ueda, H.; Nakajima, H.; Hori, Y.; Fujita, T.; Nishimura, M.; Goto, T.; Okuhara, M. FR901228, a novel antitumor bicyclic depsipeptide produced by Chromobacterium violaceum No. 968. I. Taxonomy, fermentation, isolation, physico-chemical and biological properties, and antitumor activity. J. Antibiot. , 1994, 47(3), 301-310.
[http://dx.doi.org/10.7164/antibiotics.47.301] [PMID: 7513682]
[106]
VanderMolen, K.M.; McCulloch, W.; Pearce, C.J.; Oberlies, N.H. Romidepsin (Istodax, NSC 630176, FR901228, FK228, depsipeptide): a natural product recently approved for cutaneous T-cell lymphoma. J. Antibiot. , 2011, 64(8), 525-531.
[http://dx.doi.org/10.1038/ja.2011.35] [PMID: 21587264]
[107]
Prince, H.M.; Dickinson, M.; Khot, A. Romidepsin for cutaneous T-cell lymphoma. Future Oncol., 2013, 9(12), 1819-1827.
[http://dx.doi.org/10.2217/fon.13.220] [PMID: 24295412]
[108]
Furumai, R.; Matsuyama, A.; Kobashi, N.; Lee, K.H.; Nishiyama, M.; Nakajima, H.; Tanaka, A.; Komatsu, Y.; Nishino, N.; Yoshida, M.; Horinouchi, S. FK228 (depsipeptide) as a natural prodrug that inhibits class I histone deacetylases. Cancer Res., 2002, 62(17), 4916-4921.
[PMID: 12208741]
[109]
Murakami, T.; Sato, A.; Chun, N.A.; Hara, M.; Naito, Y.; Kobayashi, Y.; Kano, Y.; Ohtsuki, M.; Furukawa, Y.; Kobayashi, E. Transcriptional modulation using HDACi depsipeptide promotes immune cell-mediated tumor destruction of murine B16 melanoma. J. Invest. Dermatol., 2008, 128(6), 1506-1516.
[http://dx.doi.org/10.1038/sj.jid.5701216] [PMID: 18185535]
[110]
Zheng, H.; Zhao, W.; Yan, C.; Watson, C.C.; Massengill, M.; Xie, M.; Massengill, C.; Noyes, D.R.; Martinez, G.V.; Afzal, R.; Chen, Z.; Ren, X.; Antonia, S.J.; Haura, E.B.; Ruffell, B.; Beg, A.A. HDAC inhibitors enhance T-cell chemokine expression and augment response to PD-1 immunotherapy in lung adenocarcinoma. Clin. Cancer Res., 2016, 22(16), 4119-4132.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-2584] [PMID: 26964571]
[111]
Tsuji, N.; Kobayashi, M.; Nagashima, K.; Wakisaka, Y.; Koizumi, K. A new antifungal antibiotic, trichostatin. J. Antibiot. , 1976, 29(1), 1-6.
[http://dx.doi.org/10.7164/antibiotics.29.1] [PMID: 931784]
[112]
Codd, R.; Braich, N.; Liu, J.; Soe, C.Z.; Pakchung, A.A. Zn(II)-dependent histone deacetylase inhibitors: suberoylanilide hydroxamic acid and trichostatin A. Int. J. Biochem. Cell Biol., 2009, 41(4), 736-739.
[http://dx.doi.org/10.1016/j.biocel.2008.05.026] [PMID: 18725319]
[113]
Yoshida, M.; Kijima, M.; Akita, M.; Beppu, T. Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. J. Biol. Chem., 1990, 265(28), 17174-17179.
[PMID: 2211619]
[114]
Vanhaecke, T.; Papeleu, P.; Elaut, G.; Rogiers, V. Trichostatin A-like hydroxamate histone deacetylase inhibitors as therapeutic agents: toxicological point of view. Curr. Med. Chem., 2004, 11(12), 1629-1643.
[http://dx.doi.org/10.2174/0929867043365099] [PMID: 15180568]
[115]
Best, J.D.; Carey, N. Epigenetic opportunities and challenges in cancer. Drug Discov. Today, 2010, 15(1-2), 65-70.
[http://dx.doi.org/10.1016/j.drudis.2009.10.010] [PMID: 19897050]
[116]
Cao, K.; Wang, G.; Li, W.; Zhang, L.; Wang, R.; Huang, Y.; Du, L.; Jiang, J.; Wu, C.; He, X.; Roberts, A.I.; Li, F.; Rabson, A.B.; Wang, Y.; Shi, Y. Histone deacetylase inhibitors prevent activation-induced cell death and promote anti-tumor immunity. Oncogene, 2015, 34(49), 5960-5970.
[http://dx.doi.org/10.1038/onc.2015.46] [PMID: 25745993]
[117]
Khan, A.N.; Magner, W.J.; Tomasi, T.B. An epigenetically altered tumor cell vaccine. Cancer Immunol. Immunother., 2004, 53(8), 748-754.
[http://dx.doi.org/10.1007/s00262-004-0513-0] [PMID: 14997346]
[118]
Khan, A.N.; Magner, W.J.; Tomasi, T.B. An epigenetic vaccine model active in the prevention and treatment of melanoma. J. Transl. Med., 2007, 5, 64.
[http://dx.doi.org/10.1186/1479-5876-5-64] [PMID: 18070359]
[119]
Khan, A.N.; Gregorie, C.J.; Tomasi, T.B. Histone deacetylase inhibitors induce TAP, LMP, Tapasin genes and MHC class I antigen presentation by melanoma cells. Cancer Immunol. Immunother., 2008, 57(5), 647-654.
[http://dx.doi.org/10.1007/s00262-007-0402-4] [PMID: 18046553]
[120]
Manning, J.; Indrova, M.; Lubyova, B.; Pribylova, H.; Bieblova, J.; Hejnar, J.; Simova, J.; Jandlova, T.; Bubenik, J.; Reinis, M. Induction of MHC class I molecule cell surface expression and epigenetic activation of antigen-processing machinery components in a murine model for human papilloma virus 16-associated tumours. Immunology, 2008, 123(2), 218-227.
[PMID: 17725605]
[121]
Setiadi, A.F.; Omilusik, K.; David, M.D.; Seipp, R.P.; Hartikainen, J.; Gopaul, R.; Choi, K.B.; Jefferies, W.A. Epigenetic enhancement of antigen processing and presentation promotes immune recognition of tumors. Cancer Res., 2008, 68(23), 9601-9607.
[http://dx.doi.org/10.1158/0008-5472.CAN-07-5270] [PMID: 19047136]
[122]
Chou, S.D.; Khan, A.N.; Magner, W.J.; Tomasi, T.B. Histone acetylation regulates the cell type specific CIITA promoters, MHC class II expression and antigen presentation in tumor cells. Int. Immunol., 2005, 17(11), 1483-1494.
[http://dx.doi.org/10.1093/intimm/dxh326] [PMID: 16210330]
[123]
Höring, E.; Podlech, O.; Silkenstedt, B.; Rota, I.A.; Adamopoulou, E.; Naumann, U. The histone deacetylase inhibitor trichostatin a promotes apoptosis and antitumor immunity in glioblastoma cells. Anticancer Res., 2013, 33(4), 1351-1360.
[PMID: 23564772]
[124]
Rossi, L.E.; Avila, D.E.; Spallanzani, R.G.; Ziblat, A.; Fuertes, M.B.; Lapyckyj, L.; Croci, D.O.; Rabinovich, G.A.; Domaica, C.I.; Zwirner, N.W. Histone deacetylase inhibitors impair NK cell viability and effector functions through inhibition of activation and receptor expression. J. Leukoc. Biol., 2012, 91(2), 321-331.
[http://dx.doi.org/10.1189/jlb.0711339] [PMID: 22124136]
[125]
Fiegler, N.; Textor, S.; Arnold, A.; Rölle, A.; Oehme, I.; Breuhahn, K.; Moldenhauer, G.; Witzens-Harig, M.; Cerwenka, A. Downregulation of the activating NKp30 ligand B7-H6 by HDAC inhibitors impairs tumor cell recognition by NK cells. Blood, 2013, 122(5), 684-693.
[http://dx.doi.org/10.1182/blood-2013-02-482513] [PMID: 23801635]
[126]
Roger, T.; Lugrin, J.; Le Roy, D.; Goy, G.; Mombelli, M.; Koessler, T.; Ding, X.C.; Chanson, A.L.; Reymond, M.K.; Miconnet, I.; Schrenzel, J.; François, P.; Calandra, T. Histone deacetylase inhibitors impair innate immune responses to Toll-like receptor agonists and to infection. Blood, 2011, 117(4), 1205-1217.
[http://dx.doi.org/10.1182/blood-2010-05-284711] [PMID: 20956800]
[127]
Kim, H-J.; Bae, S-C. Histone deacetylase inhibitors: molecular mechanisms of action and clinical trials as anti-cancer drugs. Am. J. Transl. Res., 2011, 3(2), 166-179.
[PMID: 21416059]
[128]
Garcia-Manero, G.; Yang, H.; Bueso-Ramos, C.; Ferrajoli, A.; Cortes, J.; Wierda, W.G.; Faderl, S.; Koller, C.; Morris, G.; Rosner, G.; Loboda, A.; Fantin, V.R.; Randolph, S.S.; Hardwick, J.S.; Reilly, J.F.; Chen, C.; Ricker, J.L.; Secrist, J.P.; Richon, V.M.; Frankel, S.R.; Kantarjian, H.M. Phase 1 study of the histone deacetylase inhibitor vorinostat (suberoylanilide hydroxamic acid [SAHA]) in patients with advanced leukemias and myelodysplastic syndromes. Blood, 2008, 111(3), 1060-1066.
[http://dx.doi.org/10.1182/blood-2007-06-098061] [PMID: 17962510]
[129]
Vansteenkiste, J.; Van Cutsem, E.; Dumez, H.; Chen, C.; Ricker, J.L.; Randolph, S.S.; Schöffski, P. Early phase II trial of oral vorinostat in relapsed or refractory breast, colorectal, or non-small cell lung cancer. Invest. New Drugs, 2008, 26(5), 483-488.
[http://dx.doi.org/10.1007/s10637-008-9131-6] [PMID: 18425418]
[130]
Galanis, E.; Jaeckle, K.A.; Maurer, M.J.; Reid, J.M.; Ames, M.M.; Hardwick, J.S.; Reilly, J.F.; Loboda, A.; Nebozhyn, M.; Fantin, V.R.; Richon, V.M.; Scheithauer, B.; Giannini, C.; Flynn, P.J.; Moore, D.F., Jr; Zwiebel, J.; Buckner, J.C. Phase II trial of vorinostat in recurrent glioblastoma multiforme: a north central cancer treatment group study. J. Clin. Oncol., 2009, 27(12), 2052-2058.
[http://dx.doi.org/10.1200/JCO.2008.19.0694] [PMID: 19307505]
[131]
Marks, P.A. Discovery and development of SAHA as an anticancer agent. Oncogene, 2007, 26(9), 1351-1356.
[http://dx.doi.org/10.1038/sj.onc.1210204] [PMID: 17322921]
[132]
Buglio, D.; Georgakis, G.V.; Hanabuchi, S.; Arima, K.; Khaskhely, N.M.; Liu, Y-J.; Younes, A. Vorinostat inhibits STAT6-mediated TH2 cytokine and TARC production and induces cell death in Hodgkin lymphoma cell lines. Blood, 2008, 112(4), 1424-1433.
[http://dx.doi.org/10.1182/blood-2008-01-133769] [PMID: 18541724]
[133]
May, R.D.; Fung, M. Strategies targeting the IL-4/IL-13 axes in disease. Cytokine, 2015, 75(1), 89-116.
[http://dx.doi.org/10.1016/j.cyto.2015.05.018] [PMID: 26255210]
[134]
Skinnider, B.F.; Elia, A.J.; Gascoyne, R.D.; Patterson, B.; Trumper, L.; Kapp, U.; Mak, T.W. Signal transducer and activator of transcription 6 is frequently activated in Hodgkin and Reed-Sternberg cells of Hodgkin lymphoma. Blood, 2002, 99(2), 618-626.
[http://dx.doi.org/10.1182/blood.V99.2.618] [PMID: 11781246]
[135]
Kortylewski, M.; Yu, H. Stat3 as a potential target for cancer immunotherapy. J. Immunother., 2007, 30(2), 131-139.
[http://dx.doi.org/10.1097/01.cji.0000211327.76266.65] [PMID: 17471161]
[136]
Lee, S-C.; Min, H-Y.; Jung, H.J.; Park, K.H.; Hyun, S.Y.; Cho, J.; Woo, J.K.; Kwon, S.J.; Lee, H-J.; Johnson, F.M.; Lee, H-Y. Essential role of insulin-like growth factor 2 in resistance to histone deacetylase inhibitors. Oncogene, 2016, 35(42), 5515-5526.
[http://dx.doi.org/10.1038/onc.2016.92] [PMID: 27086926]
[137]
Muldoon, L.L.; Soussain, C.; Jahnke, K.; Johanson, C.; Siegal, T.; Smith, Q.R.; Hall, W.A.; Hynynen, K.; Senter, P.D.; Peereboom, D.M.; Neuwelt, E.A. Chemotherapy delivery issues in central nervous system malignancy: a reality check. J. Clin. Oncol., 2007, 25(16), 2295-2305.
[http://dx.doi.org/10.1200/JCO.2006.09.9861] [PMID: 17538176]
[138]
Sonnemann, J.; Gressmann, S.; Becker, S.; Wittig, S.; Schmudde, M.; Beck, J.F. The histone deacetylase inhibitor vorinostat induces calreticulin exposure in childhood brain tumour cells in vitro. Cancer Chemother. Pharmacol., 2010, 66(3), 611-616.
[http://dx.doi.org/10.1007/s00280-010-1302-4] [PMID: 20221600]
[139]
Hockly, E.; Richon, V.M.; Woodman, B.; Smith, D.L.; Zhou, X.; Rosa, E.; Sathasivam, K.; Ghazi-Noori, S.; Mahal, A.; Lowden, P.A.; Steffan, J.S.; Marsh, J.L.; Thompson, L.M.; Lewis, C.M.; Marks, P.A.; Bates, G.P. Suberoylanilide hydroxamic acid, a histone deacetylase inhibitor, ameliorates motor deficits in a mouse model of Huntington’s disease. Proc. Natl. Acad. Sci. USA, 2003, 100(4), 2041-2046.
[http://dx.doi.org/10.1073/pnas.0437870100] [PMID: 12576549]
[140]
Luu, T.H.; Morgan, R.J.; Leong, L.; Lim, D.; McNamara, M.; Portnow, J.; Frankel, P.; Smith, D.D.; Doroshow, J.H.; Wong, C.; Aparicio, A.; Gandara, D.R.; Somlo, G. A phase II trial of vorinostat (suberoylanilide hydroxamic acid) in metastatic breast cancer: a California Cancer Consortium study. Clin. Cancer Res., 2008, 14(21), 7138-7142.
[http://dx.doi.org/10.1158/1078-0432.CCR-08-0122] [PMID: 18981013]
[141]
Traynor, A.M.; Dubey, S.; Eickhoff, J.C.; Kolesar, J.M.; Schell, K.; Huie, M.S.; Groteluschen, D.L.; Marcotte, S.M.; Hallahan, C.M.; Weeks, H.R.; Wilding, G.; Espinoza-Delgado, I.; Schiller, J.H. Vorinostat (NSC# 701852) in patients with relapsed non-small cell lung cancer: a Wisconsin Oncology Network phase II study. J. Thorac. Oncol., 2009, 4(4), 522-526.
[http://dx.doi.org/10.1097/JTO.0b013e3181952478] [PMID: 19347984]
[142]
Ding, L.; Zhang, Z.; Liang, G.; Yao, Z.; Wu, H.; Wang, B.; Zhang, J.; Tariq, M.; Ying, M.; Yang, B. SAHA triggered MET activation contributes to SAHA tolerance in solid cancer cells. Cancer Lett., 2015, 356(2 Pt B), 828-836.
[http://dx.doi.org/10.1016/j.canlet.2014.10.034] [PMID: 25449774]
[143]
Zeng, H.; Qu, J.; Jin, N.; Xu, J.; Lin, C.; Chen, Y.; Yang, X.; He, X.; Tang, S.; Lan, X.; Yang, X.; Chen, Z.; Huang, M.; Ding, J.; Geng, M. Feedback activation of leukemia inhibitory factor receptor limits response to histone deacetylase inhibitors in breast cancer. Cancer Cell, 2016, 30(3), 459-473.
[http://dx.doi.org/10.1016/j.ccell.2016.08.001] [PMID: 27622335]
[144]
Tran, T.H.; Ramasamy, T.; Truong, D.H.; Shin, B.S.; Choi, H-G.; Yong, C.S.; Kim, J.O. Development of vorinostat-loaded solid lipid nanoparticles to enhance pharmacokinetics and efficacy against multidrug-resistant cancer cells. Pharm. Res., 2014, 31(8), 1978-1988.
[http://dx.doi.org/10.1007/s11095-014-1300-z] [PMID: 24562809]
[145]
Christiansen, A.J.; West, A.; Banks, K-M.; Haynes, N.M.; Teng, M.W.; Smyth, M.J.; Johnstone, R.W. Eradication of solid tumors using histone deacetylase inhibitors combined with immune-stimulating antibodies. Proc. Natl. Acad. Sci. USA, 2011, 108(10), 4141-4146.
[http://dx.doi.org/10.1073/pnas.1011037108] [PMID: 21368108]
[146]
Huang, Z.; Peng, S.; Knoff, J.; Lee, S.Y.; Yang, B.; Wu, T-C.; Hung, C-F. Combination of proteasome and HDAC inhibitor enhances HPV16 E7-specific CD8+ T cell immune response and antitumor effects in a preclinical cervical cancer model. J. Biomed. Sci., 2015, 22, 7.
[http://dx.doi.org/10.1186/s12929-014-0111-1] [PMID: 25591912]
[147]
West, A.C.; Smyth, M.J.; Johnstone, R.W. The anticancer effects of HDAC inhibitors require the immune system. OncoImmunology, 2014, 3(1), e27414.
[http://dx.doi.org/10.4161/onci.27414] [PMID: 24701376]
[148]
Yang, H.; Lan, P.; Hou, Z.; Guan, Y.; Zhang, J.; Xu, W.; Tian, Z.; Zhang, C. Histone deacetylase inhibitor SAHA epigenetically regulates miR-17-92 cluster and MCM7 to upregulate MICA expression in hepatoma. Br. J. Cancer, 2015, 112(1), 112-121.
[http://dx.doi.org/10.1038/bjc.2014.547] [PMID: 25393367]
[149]
Ritter, C.; Fan, K.; Paulson, K.G.; Nghiem, P.; Schrama, D.; Becker, J.C. Reversal of epigenetic silencing of MHC class I chain-related protein A and B improves immune recognition of Merkel cell carcinoma. Sci. Rep., 2016, 6, 21678.
[http://dx.doi.org/10.1038/srep21678] [PMID: 26902929]
[150]
West, A.C.; Mattarollo, S.R.; Shortt, J.; Cluse, L.A.; Christiansen, A.J.; Smyth, M.J.; Johnstone, R.W. An intact immune system is required for the anticancer activities of histone deacetylase inhibitors. Cancer Res., 2013, 73(24), 7265-7276.
[http://dx.doi.org/10.1158/0008-5472.CAN-13-0890] [PMID: 24158093]
[151]
Schmudde, M.; Friebe, E.; Sonnemann, J.; Beck, J.F.; Bröker, B.M. Histone deacetylase inhibitors prevent activation of tumour-reactive NK cells and T cells but do not interfere with their cytolytic effector functions. Cancer Lett., 2010, 295(2), 173-181.
[http://dx.doi.org/10.1016/j.canlet.2010.02.024] [PMID: 20346580]
[152]
Yoon, S.; Eom, G.H. HDAC and HDAC Inhibitor: From cancer to cardiovascular diseases. Chonnam Med. J., 2016, 52(1), 1-11.
[http://dx.doi.org/10.4068/cmj.2016.52.1.1] [PMID: 26865995]
[153]
Wightman, F.; Ellenberg, P.; Churchill, M.; Lewin, S.R. HDAC inhibitors in HIV. Immunol. Cell Biol., 2012, 90(1), 47-54.
[http://dx.doi.org/10.1038/icb.2011.95] [PMID: 22083528]
[154]
Dickinson, M.; Johnstone, R.W.; Prince, H.M. Histone deacetylase inhibitors: potential targets responsible for their anti-cancer effect. Invest. New Drugs, 2010, 28(Suppl. 1), S3-S20.
[http://dx.doi.org/10.1007/s10637-010-9596-y] [PMID: 21161327]
[155]
de Visser, K.E.; Eichten, A.; Coussens, L.M. Paradoxical roles of the immune system during cancer development. Nat. Rev. Cancer, 2006, 6(1), 24-37.
[http://dx.doi.org/10.1038/nrc1782] [PMID: 16397525]
[156]
Raaijmakers, M.I.; Rozati, S.; Goldinger, S.M.; Widmer, D.S.; Dummer, R.; Levesque, M.P. Melanoma immunotherapy: historical precedents, recent successes and future prospects. Immunotherapy, 2013, 5(2), 169-182.
[http://dx.doi.org/10.2217/imt.12.162] [PMID: 23413908]
[157]
Mellman, I.; Coukos, G.; Dranoff, G. Cancer immunotherapy comes of age. Nature, 2011, 480(7378), 480-489.
[http://dx.doi.org/10.1038/nature10673] [PMID: 22193102]