Login Register Cart 0
Generic placeholder image

Current Topics in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1568-0266
ISSN (Online): 1873-4294

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Research Advances in the Use of Histone Deacetylase Inhibitors for Epigenetic Targeting of Cancer

Author(s): Yu Bai, Daid Ahmad, Ting Wang*, Guihua Cui and Wenliang Li*

Volume 19, Issue 12, 2019

Page: [995 - 1004] Pages: 10

DOI: 10.2174/1568026619666190125145110

Price: $65

Abstract

The causes and progression of cancer are controlled by epigenetic processes. The mechanisms involved in epigenetic regulation of cancer development, gene expression, and signaling pathways have been studied. Histone deacetylases (HDACs) have a major impact on chromatin remodeling and epigenetics, making their inhibitors a very interesting area of cancer research. This review comprehensively summarizes the literature regarding HDAC inhibitors (HDACis) as an anticancer treatment published in the past few years. In addition, we explain the mechanisms of their therapeutic effects on cancer. An analysis of the beneficial characteristics and drawbacks of HDACis also is presented, which will assist preclinical and clinical researchers in the design of future experiments to improve the therapeutic efficacy of these drugs and circumvent the challenges in the path of successful epigenetic therapy. Future therapeutic strategies may include a combination of HDACis and chemotherapy or other inhibitors to target multiple oncogenic signaling pathways.

Keywords: Histone deacetylase (HDAC) Inhibitors, Cancer, Mechanisms, Histone deacetylases, Epigenetic therapy, Signaling pathways.

« Previous Next »
[1]
Arnedos, M.; Vicier, C.; Loi, S.; Lefebvre, C.; Michiels, S.; Bonnefoi, H.; Andre, F. Precision medicine for metastatic breast cancer--limitations and solutions. Nat. Rev. Clin. Oncol., 2015, 12(12), 693-704. [http://dx.doi.org/10.1038/nrclinonc.2015.123]. [PMID: 26196250].
[2]
Darshan, M.S.; Loftus, M.S.; Thadani-Mulero, M.; Levy, B.P.; Escuin, D.; Zhou, X.K.; Gjyrezi, A.; Chanel-Vos, C.; Shen, R.; Tagawa, S.T.; Bander, N.H.; Nanus, D.M.; Giannakakou, P. Taxane-induced blockade to nuclear accumulation of the androgen receptor predicts clinical responses in metastatic prostate cancer. Cancer Res., 2011, 71(18), 6019-6029. [http://dx.doi.org/10.1158/0008-5472.CAN-11-1417]. [PMID: 21799031].
[3]
Peng, Z.; Zhou, W.; Zhang, C.; Liu, H.; Zhang, Y. Curcumol controls choriocarcinoma stem-like cells self-renewal via repression of DNA methyltransferase (DNMT)- and histone deacetylase (HDAC)-mediated epigenetic regulation. Med. Sci. Monit., 2018, 24, 461-472. [http://dx.doi.org/10.12659/MSM.908430]. [PMID: 29363667].
[4]
Suraweera, A.; O’Byrne, K.J.; Richard, D.J. Combination therapy with histone deacetylase inhibitors (HDACi) for the treatment of cancer: Achieving the full therapeutic potential of HDACi. Front. Oncol., 2018, 8, 92. [http://dx.doi.org/10.3389/fonc.2018.00092]. [PMID: 29651407].
[5]
Heimburg, T.; Kolbinger, F.R.; Zeyen, P.; Ghazy, E.; Herp, D.; Schmidtkunz, K.; Melesina, J.; Shaik, T.B.; Erdmann, F.; Schmidt, M.; Romier, C.; Robaa, D.; Witt, O.; Oehme, I.; Jung, M.; Sippl, W. Structure-based design and biological characterization of selective histone deacetylase 8 (HDAC8) inhibitors with anti-neuroblastoma activity. J. Med. Chem., 2017, 60(24), 10188-10204. [http://dx.doi.org/10.1021/acs.jmedchem.7b01447]. [PMID: 29190092].
[6]
Garmpis, N.; Damaskos, C.; Garmpi, A.; Kalampokas, E.; Kalampokas, T.; Spartalis, E.; Daskalopoulou, A.; Valsami, S.; Kontos, M.; Nonni, A.; Kontzoglou, K.; Perrea, D.; Nikiteas, N.; Dimitroulis, D. Histone Deacetylases as new therapeutic targets in triple-negative breast cancer: progress and promises. Cancer Genomics Proteomics, 2017, 14(5), 299-313. [PMID: 28870998].
[7]
Guarasci, F.; D’Aquila, P.; Mandalà, M.; Garasto, S.; Lattanzio, F.; Corsonello, A.; Passarino, G.; Bellizzi, D. Aging and nutrition induce tissue-specific changes on global DNA methylation status in rats. Mech. Ageing Dev., 2018, 174, 47-54. [http://dx.doi.org/10.1016/j.mad.2018.02.001]. [PMID: 29427568].
[8]
Duca, R.C.; Grova, N.; Ghosh, M.; Do, J.M.; Hoet, P.H.M.; Vanoirbeek, J.A.J.; Appenzeller, B.M.R.; Godderis, L. Exposure to polycyclic aromatic hydrocarbons leads to non-monotonic modulation of DNA and RNA (hydroxy)methylation in a Rat Model. Sci. Rep., 2018, 8(1), 10577. [http://dx.doi.org/10.1038/s41598-018-28911-y]. [PMID: 30002487].
[9]
Rifaï, K.; Judes, G.; Idrissou, M.; Daures, M.; Bignon, Y.J.; Penault-Llorca, F.; Bernard-Gallon, D. SIRT1-dependent epigenetic regulation of H3 and H4 histone acetylation in human breast cancer. Oncotarget, 2018, 9(55), 30661-30678. [http://dx.doi.org/10.18632/oncotarget.25771]. [PMID: 30093977].
[10]
Bove, R.M.; Patrick, E.; Aubin, C.M.; Srivastava, G.; Schneider, J.A.; Bennett, D.A.; De Jager, P.L.; Chibnik, L.B. Reproductive period and epigenetic modifications of the oxidative phosphorylation pathway in the human prefrontal cortex. PLoS One, 2018, 13(7)e0199073 [http://dx.doi.org/10.1371/journal.pone.0199073]. [PMID: 30052629].
[11]
Nucifora, F.C., Jr; Nucifora, L.G.; Ng, C.H.; Arbez, N.; Guo, Y.; Roby, E.; Shani, V.; Engelender, S.; Wei, D.; Wang, X.F.; Li, T.; Moore, D.J.; Pletnikova, O.; Troncoso, J.C.; Sawa, A.; Dawson, T.M.; Smith, W.; Lim, K.L.; Ross, C.A. Ubiqutination via K27 and K29 chains signals aggregation and neuronal protection of LRRK2 by WSB1. Nat. Commun., 2016, 7, 11792. [http://dx.doi.org/10.1038/ncomms11792]. [PMID: 27273569].
[12]
Zhou, L.; Zhang, W.; Sun, Y.; Jia, L. Protein neddylation and its alterations in human cancers for targeted therapy. Cell. Signal., 2018, 44, 92-102. [http://dx.doi.org/10.1016/j.cellsig.2018.01.009]. [PMID: 29331584].
[13]
Pérez-Garrastachu, M.; Arluzea, J.; Andrade, R.; Díez-Torre, A.; Urtizberea, M.; Silió, M.; Aréchaga, J. Nucleoporins redistribute inside the nucleus after cell cycle arrest induced by histone deacetylases inhibition. Nucleus, 2017, 8(5), 515-533. [http://dx.doi.org/10.1080/19491034.2017.1320001]. [PMID: 28696859].
[14]
Gaisina, I.N.; Tueckmantel, W.; Ugolkov, A.; Shen, S.; Hoffen, J.; Dubrovskyi, O.; Mazar, A.; Schoon, R.A.; Billadeau, D.; Kozikowski, A.P. Identification of HDAC6-selective inhibitors of low cancer cell cytotoxicity. ChemMedChem, 2016, 11(1), 81-92. [http://dx.doi.org/10.1002/cmdc.201500456]. [PMID: 26592932].
[15]
Hayashi, A.; Horiuchi, A.; Kikuchi, N.; Hayashi, T.; Fuseya, C.; Suzuki, A.; Konishi, I.; Shiozawa, T. Type-specific roles of histone deacetylase (HDAC) overexpression in ovarian carcinoma: HDAC1 enhances cell proliferation and HDAC3 stimulates cell migration with downregulation of E-cadherin. Int. J. Cancer, 2010, 127(6), 1332-1346. [http://dx.doi.org/10.1002/ijc.25151]. [PMID: 20049841].
[16]
Chen, Y.; Sprung, R.; Tang, Y.; Ball, H.; Sangras, B.; Kim, S.C.; Falck, J.R.; Peng, J.; Gu, W.; Zhao, Y. Lysine propionylation and butyrylation are novel post-translational modifications in histones. Mol. Cell. Proteomics, 2007, 6(5), 812-819. [http://dx.doi.org/10.1074/mcp.M700021-MCP200]. [PMID: 17267393].
[17]
McClure, J.J.; Inks, E.S.; Zhang, C.; Peterson, Y.K.; Li, J.; Chundru, K.; Lee, B.; Buchanan, A.; Miao, S.; Chou, C.J. Comparison of the deacylase and deacetylase activity of zinc-dependent HDACs. ACS Chem. Biol., 2017, 12(6), 1644-1655. [http://dx.doi.org/10.1021/acschembio.7b00321]. [PMID: 28459537].
[18]
Wei, W.; Liu, X.; Chen, J.; Gao, S.; Lu, L.; Zhang, H.; Ding, G.; Wang, Z.; Chen, Z.; Shi, T.; Li, J.; Yu, J.; Wong, J. Class I histone deacetylases are major histone decrotonylases: evidence for critical and broad function of histone crotonylation in transcription. Cell Res., 2017, 27(7), 898-915. [http://dx.doi.org/10.1038/cr.2017.68]. [PMID: 28497810].
[19]
Tang, F.; Choy, E.; Tu, C.; Hornicek, F.; Duan, Z. Therapeutic applications of histone deacetylase inhibitors in sarcoma. Cancer Treat. Rev., 2017, 59(59), 33-45. [http://dx.doi.org/10.1016/j.ctrv.2017.06.006]. [PMID: 28732326].
[20]
Zhu, Q.; Yu, X.; Shen, Q.; Zhang, Q.; Su, M.; Zhou, Y.; Li, J.; Chen, Y.; Lu, W. A series of camptothecin prodrugs exhibit HDAC inhibition activity. Bioorg. Med. Chem., 2018, 26(16), 4706-4715. [http://dx.doi.org/10.1016/j.bmc.2018.08.008]. [PMID: 30115492].
[21]
Brindisi, M.; Senger, J.; Cavella, C.; Grillo, A.; Chemi, G.; Gemma, S.; Cucinella, D.M.; Lamponi, S.; Sarno, F.; Iside, C.; Nebbioso, A.; Novellino, E.; Shaik, T.B.; Romier, C.; Herp, D.; Jung, M.; Butini, S.; Campiani, G.; Altucci, L.; Brogi, S. Novel spiroindoline HDAC inhibitors: Synthesis, molecular modelling and biological studies. Eur. J. Med. Chem., 2018, 157, 127-138. [http://dx.doi.org/10.1016/j.ejmech.2018.07.069]. [PMID: 30092367].
[22]
Gatla, H.R.; Zou, Y.; Uddin, M.M.; Singha, B.; Bu, P.; Vancura, A.; Vancurova, I. Histone deacetylase (HDAC) inhibition induces IκB kinase (IKK)-dependent Interleukin-8/CXCL8 expression in ovarian cancer cells. J. Biol. Chem., 2017, 292(12), 5043-5054. [http://dx.doi.org/10.1074/jbc.M116.771014]. [PMID: 28167529].
[23]
Patel, M.M.; Patel, B.M. Repurposing of sodium valproate in colon cancer associated with diabetes mellitus: Role of HDAC inhibition. Eur. J. Pharm. Sci., 2018, 121, 188-199. [http://dx.doi.org/10.1016/j.ejps.2018.05.026]. [PMID: 29852291].
[24]
West, A.C.; Johnstone, R.W. New and emerging HDAC inhibitors for cancer treatment. J. Clin. Invest., 2014, 124(1), 30-39. [http://dx.doi.org/10.1172/JCI69738]. [PMID: 24382387].
[25]
De Souza, C.; Chatterji, B.P. HDAC inhibitors as novel anti-cancer therapeutics. Recent Patents Anticancer Drug Discov., 2015, 10(2), 145-162. [http://dx.doi.org/10.2174/1574892810666150317144511]. [PMID: 25782916].
[26]
Schmauss, C. An HDAC-dependent epigenetic mechanism that enhances the efficacy of the antidepressant drug fluoxetine. Sci. Rep., 2015, 5, 8171.
[27]
Rauzan, M.; Chuah, C.T.; Ko, T.K.; Ong, S.T. The HDAC inhibitor SB939 overcomes resistance to BCR-ABL kinase Inhibitors conferred by the BIM deletion polymorphism in chronic myeloid leukemia. PLoS One, 2017, 12(3)e0174107 [http://dx.doi.org/10.1371/journal.pone.0174107]. [PMID: 28301600].
[28]
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].
[29]
Wang, J.; Yang, D.; Luo, Q.; Qiu, M.; Zhang, L.; Li, B.; Chen, H.; Yi, H.; Yan, X.; Li, S.; Sun, J. APG-1252-12A induces mitochondria-dependent apoptosis through inhibiting the antiapoptotic proteins Bcl-2/Bcl-xl in HL-60 cells. Int. J. Oncol., 2017, 51(2), 563-572. [http://dx.doi.org/10.3892/ijo.2017.4028]. [PMID: 28586007].
[30]
He, L.; Torres-Lockhart, K.; Forster, N.; Ramakrishnan, S.; Greninger, P.; Garnett, M.J.; McDermott, U.; Rothenberg, S.M.; Benes, C.H.; Ellisen, L.W. Mcl-1 and FBW7 control a dominant survival pathway underlying HDAC and Bcl-2 inhibitor synergy in squamous cell carcinoma. Cancer Discov., 2013, 3(3), 324-337. [http://dx.doi.org/10.1158/2159-8290.CD-12-0417]. [PMID: 23274910].
[31]
Lemke, J.; von Karstedt, S.; Zinngrebe, J.; Walczak, H. Getting TRAIL back on track for cancer therapy. Cell Death Differ., 2014, 21(9), 1350-1364. [http://dx.doi.org/10.1038/cdd.2014.81]. [PMID: 24948009].
[32]
Zhou, W.; Feng, X.; Han, Han. Guo, S.; Wang, G. Synergistic effects of combined treatment with histone deacetylase inhibitor suberoylanilide hydroxamic acid and TRAIL on human breast cancer cells. Sci. Rep., 2016, 6, 28004. [http://dx.doi.org/10.1038/srep28004]. [PMID: 27292433].
[33]
Chen, S.; Ye, J.; Chen, X.; Shi, J.; Wu, W.; Lin, W.; Lin, W.; Li, Y.; Fu, H.; Li, S. Valproic acid attenuates traumatic spinal cord injury-induced inflammation via STAT1 and NF-κB pathway dependent of HDAC3. J. Neuroinflammation, 2018, 15(1), 150. [http://dx.doi.org/10.1186/s12974-018-1193-6]. [PMID: 29776446].
[34]
Rajashekar Reddy, C.B.; Rajasekhara Reddy, S.; Suthindhiran, K.; Sivakumar, A. HDAC and NF-κB mediated cytotoxicity induced by novel N-Chloro β-lactams and benzisoxazole derivatives. Chem. Biol. Interact., 2016, 246, 69-76. [http://dx.doi.org/10.1016/j.cbi.2016.01.010]. [PMID: 26776669].
[35]
Cheng, M.H.; Wong, Y.H.; Chang, C.M.; Yang, C.C.; Chen, S.H.; Yuan, C.L.; Kuo, H.M.; Yang, C.Y.; Chiu, H.F. B1, a novel HDAC inhibitor, induces apoptosis through the regulation of STAT3 and NF-κB. Int. J. Mol. Med., 2017, 39(5), 1137-1148. [http://dx.doi.org/10.3892/ijmm.2017.2946]. [PMID: 28393178].
[36]
Zhou, W.; Zhu, W.; Ma, L.; Xiao, F.; Qian, W. Proteasome inhibitor MG-132 enhances histone deacetylase inhibitor SAHA-induced cell death of chronic myeloid leukemia cells by an ROS-mediated mechanism and downregulation of the Bcr-Abl fusion protein. Oncol. Lett., 2015, 10(5), 2899-2904. [http://dx.doi.org/10.3892/ol.2015.3665]. [PMID: 26722260].
[37]
Chiao, M.T.; Cheng, W.Y.; Yang, Y.C.; Shen, C.C.; Ko, J.L. Suberoylanilide hydroxamic acid (SAHA) causes tumor growth slowdown and triggers autophagy in glioblastoma stem cells. Autophagy, 2013, 9(10), 1509-1526. [http://dx.doi.org/10.4161/auto.25664]. [PMID: 23962875].
[38]
Booth, L.; Roberts, J.L.; Poklepovic, A.; Dent, P. [pemetrexed + sildenafil], via autophagy-dependent HDAC downregulation, enhances the immunotherapy response of NSCLC cells. Cancer Biol. Ther., 2017, 18(9), 705-714. [http://dx.doi.org/10.1080/15384047.2017.1362511]. [PMID: 28812434].
[39]
Mahalingam, D.; Mita, M.; Sarantopoulos, J.; Wood, L.; Amaravadi, R.K.; Davis, L.E.; Mita, A.C.; Curiel, T.J.; Espitia, C.M.; Nawrocki, S.T.; Giles, F.J.; Carew, J.S. Combined autophagy and HDAC inhibition: A phase I safety, tolerability, pharmacokinetic, and pharmacodynamic analysis of hydroxychloroquine in combination with the HDAC inhibitor vorinostat in patients with advanced solid tumors. Autophagy, 2014, 10(8), 1403-1414. [http://dx.doi.org/10.4161/auto.29231]. [PMID: 24991835].
[40]
Koeneke, E.; Witt, O.; Oehme, I. HDAC family members intertwined in the regulation of autophagy: A druggable vulnerability in aggressive tumor entities. Cells, 2015, 4(2), 135-168. [http://dx.doi.org/10.3390/cells4020135]. [PMID: 25915736].
[41]
Liu, Y.L.; Yang, P.M.; Shun, C.T.; Wu, M.S.; Weng, J.R.; Chen, C.C. Autophagy potentiates the anti-cancer effects of the histone deacetylase inhibitors in hepatocellular carcinoma. Autophagy, 2010, 6(8), 1057-1065. [http://dx.doi.org/10.4161/auto.6.8.13365]. [PMID: 20962572].
[42]
Hanke, N.T.; Garland, L.L.; Baker, A.F. Carfilzomib combined with suberanilohydroxamic acid (SAHA) synergistically promotes endoplasmic reticulum stress in non-small cell lung cancer cell lines. J. Cancer Res. Clin. Oncol., 2016, 142(3), 549-560. [http://dx.doi.org/10.1007/s00432-015-2047-6]. [PMID: 26385374].
[43]
To, M.; Swallow, E.B.; Akashi, K.; Haruki, K.; Natanek, S.A.; Polkey, M.I.; Ito, K.; Barnes, P.J. Reduced HDAC2 in skeletal muscle of COPD patients. Respir. Res., 2017, 18(1), 99. [http://dx.doi.org/10.1186/s12931-017-0588-8]. [PMID: 28526090].
[44]
Lai, F1.; Guo, S.T.; Jin, L.; Jiang, C.C.; Wang, C.Y.; Croft, A.; Chi, M.N.; Tseng, H.Y.; Farrelly, M.; Atmadibrata, B.; Norman, J.; Liu, T.; Hersey, P.; Zhang, X.D. Cotargeting histone deacetylases and oncogenic BRAF synergistically kills human melanoma cells by necrosis independently of RIPK1 and RIPK3. Cell Death Dis., 2013, 4e655
[45]
Hagiwara, K.; Kunishima, S.; Iida, H.; Miyata, Y.; Naoe, T.; Nagai, H. The synergistic effect of BCR signaling inhibitors combined with an HDAC inhibitor on cell death in a mantle cell lymphoma cell line. Apoptosis, 2015, 20(7), 975-985. [http://dx.doi.org/10.1007/s10495-015-1125-1]. [PMID: 25835755].
[46]
Kikuchi, S.; Suzuki, R.; Ohguchi, H.; Yoshida, Y.; Lu, D.; Cottini, F.; Jakubikova, J.; Bianchi, G.; Harada, T.; Gorgun, G.; Tai, Y.T.; Richardson, P.G.; Hideshima, T.; Anderson, K.C. Class IIa HDAC inhibition enhances ER stress-mediated cell death in multiple myeloma. Leukemia, 2015, 29(9), 1918-1927. [http://dx.doi.org/10.1038/leu.2015.83]. [PMID: 25801913].
[47]
Kolbinger, F.R.; Koeneke, E.; Ridinger, J.; Heimburg, T.; Müller, M.; Bayer, T.; Sippl, W.; Jung, M.; Gunkel, N.; Miller, A.K.; Westermann, F.; Witt, O.; Oehme, I. The HDAC6/8/10 inhibitor TH34 induces DNA damage-mediated cell death in human high-grade neuroblastoma cell lines. Arch. Toxicol., 2018, 92(8), 2649-2664. [http://dx.doi.org/10.1007/s00204-018-2234-8]. [PMID: 29947893].
[48]
Cedeno-Laurent, F.; Singer, E.M.; Wysocka, M.; Benoit, B.M.; Vittorio, C.C.; Kim, E.J.; Yosipovitch, G.; Rook, A.H. Improved pruritus correlates with lower levels of IL-31 in CTCL patients under different therapeutic modalities. Clin. Immunol., 2015, 158(1), 1-7. [http://dx.doi.org/10.1016/j.clim.2015.02.014]. [PMID: 25762519].
[49]
Bae, J.; Hideshima, T.; Tai, Y.T.; Song, Y.; Richardson, P.; Raje, N.; Munshi, N.C.; Anderson, K.C. Histone deacetylase (HDAC) inhibitor ACY241 enhances anti-tumor activities of antigen-specific central memory cytotoxic T lymphocytes against multiple myeloma and solid tumors. Leukemia, 2018, 32(9), 1932-1947. [http://dx.doi.org/10.1038/s41375-018-0062-8]. [PMID: 29487385].
[50]
Pickering, C.R.; Myers, J.N. Bcl-2 inhibition or FBXW7 mutation sensitizes solid tumor cells to HDAC inhibition in vitro but could prove difficult to validate in patients. Cancer Discov., 2013, 3(3), 258-259. [http://dx.doi.org/10.1158/2159-8290.CD-13-0019]. [PMID: 23475877].
[51]
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].
[52]
Deming, D.A.; Ninan, J.; Bailey, H.H.; Kolesar, J.M.; Eickhoff, J.; Reid, J.M.; Ames, M.M.; McGovern, R.M.; Alberti, D.; Marnocha, R.; Espinoza-Delgado, I.; Wright, J.; Wilding, G.; Schelman, W.R. A Phase I study of intermittently dosed vorinostat in combination with bortezomib in patients with advanced solid tumors. Invest. New Drugs, 2014, 32(2), 323-329. [http://dx.doi.org/10.1007/s10637-013-0035-8]. [PMID: 24114123].
[53]
Coiffier, B.; Pro, B.; Prince, H.M.; Foss, F.; Sokol, L.; Greenwood, M.; Caballero, D.; Morschhauser, F.; Wilhelm, M.; Pinter-Brown, L.; Padmanabhan Iyer, S.; Shustov, A.; Nielsen, T.; Nichols, J.; Wolfson, J.; Balser, B.; Horwitz, S. Romidepsin for the treatment of relapsed/refractory peripheral T-cell lymphoma: pivotal study update demonstrates durable responses. J. Hematol. Oncol., 2014, 7, 11. [http://dx.doi.org/10.1186/1756-8722-7-11]. [PMID: 24456586].
[54]
Bailey, H.; McPherson, J.P.; Bailey, E.B.; Werner, T.L.; Gupta, S.; Batten, J.; Reddy, G.; Bhat, G.; Sharma, S.; Agarwal, N. A phase I study to determine the pharmacokinetics and urinary excretion of belinostat and metabolites in patients with advanced solid tumors. Cancer Chemother. Pharmacol., 2016, 78(5), 1059-1071. [http://dx.doi.org/10.1007/s00280-016-3167-7]. [PMID: 27744565].
[55]
Maly, J.J.; Christian, B.A.; Zhu, X.; Wei, L.; Sexton, J.L.; Jaglowski, S.M.; Devine, S.M.; Fehniger, T.A.; Wagner-Johnston, N.D.; Phelps, M.A.; Bartlett, N.L.; Blum, K.A. A Phase I/II trial of panobinostat in combination with lenalidomide in patients with relapsed or refractory hodgkin lymphoma. Clin. Lymphoma Myeloma Leuk., 2017, 17(6), 347-353. [http://dx.doi.org/10.1016/j.clml.2017.05.008]. [PMID: 28622959].
[56]
De Souza, C.; Chatterji, B.P. HDAC inhibitors as novel anti-cancer therapeutics. Recent Patents Anticancer Drug Discov., 2015, 10(2), 145-162. [http://dx.doi.org/10.2174/1574892810666150317144511]. [PMID: 25782916].
[57]
Fedele, P.; Orlando, L.; Cinieri, S. Targeting triple negative breast cancer with histone deacetylase inhibitors. Expert Opin. Investig. Drugs, 2017, 26(11), 1199-1206. [http://dx.doi.org/10.1080/13543784.2017.1386172]. [PMID: 28952409].
[58]
Amemiya, S.; Yamaguchi, T.; Hashimoto, Y.; Noguchi-Yachide, T. Synthesis and evaluation of novel dual BRD4/HDAC inhibitors. Bioorg. Med. Chem., 2017, 25(14), 3677-3684. [DOI: 10.1016/j.bmc.2017.04.043]. [ PMID: 28549889].
[59]
Hosford, S.R.; Miller, T.W. Clinical potential of novel therapeutic targets in breast cancer: CDK4/6, Src, JAK/STAT, PARP, HDAC, and PI3K/AKT/mTOR pathways. Pharm. Genomics Pers. Med., 2014, 7, 203-215. [PMID: 25206307].
[60]
Kularatne, R.N.; Washington, K.E.; Bulumulla, C.; Calubaquib, E.L.; Biewer, M.C.; Oupicky, D.; Stefan, M.C. Histone deacetylase inhibitor (HDACi) conjugated polycaprolactone for combination cancer therapy. Biomacromolecules, 2018, 19(3), 1082-1089. [http://dx.doi.org/10.1021/acs.biomac.8b00221]. [PMID: 29485283].
[61]
Lauschke, V.M.; Barragan, I.; Ingelman-Sundberg, M. Pharmacoepigenetics and toxicoepigenetics: Novel mechanistic insights and therapeutic opportunities. Annu. Rev. Pharmacol. Toxicol., 2018, 58, 161-185. [http://dx.doi.org/10.1146/annurev-pharmtox-010617-053021]. [PMID: 29029592].
[62]
Mazzone, R.; Zwergel, C.; Mai, A.; Valente, S. Epi-drugs in combination with immunotherapy: A new avenue to improve anticancer efficacy. Clin. Epigenetics, 2017, 9, 59. [http://dx.doi.org/10.1186/s13148-017-0358-y]. [PMID: 28572863].
[63]
Lapinska, K.; Housman, G.; Byler, S.; Heerboth, S.; Willbanks, A.; Oza, A.; Sarkar, S. The effects of histone deacetylase inhibitor and calpain inhibitor combination therapies on ovarian cancer cells. Anticancer Res., 2016, 36(11), 5731-5742. [http://dx.doi.org/10.21873/anticanres.11156]. [PMID: 27793894].
[64]
Ganai, S.A. Histone deacetylase inhibitor pracinostat in doublet therapy: a unique strategy to improve therapeutic efficacy and to tackle herculean cancer chemoresistance. Pharm. Biol., 2016, 54(9), 1926-1935. [http://dx.doi.org/10.3109/13880209.2015.1135966]. [PMID: 26853619].
[65]
Damaskos, C.; Garmpis, N.; Karatzas, T.; Nikolidakis, L.; Kostakis, I.D.; Garmpi, A.; Karamaroudis, S.; Boutsikos, G.; Damaskou, Z.; Kostakis, A.; Kouraklis, G. Histone deacetylase (HDAC) inhibitors: Current evidence for therapeutic activities in pancreatic cancer. Anticancer Res., 2015, 35(6), 3129-3135. [PMID: 26026072].
[66]
Feng, W.; Cai, D.; Zhang, B.; Lou, G.; Zou, X. Combination of HDAC inhibitor TSA and silibinin induces cell cycle arrest and apoptosis by targeting survivin and cyclinB1/Cdk1 in pancreatic cancer cells. Biomed. Pharmacother., 2015, 74, 257-264. [http://dx.doi.org/10.1016/j.biopha.2015.08.017]. [PMID: 26349994].
[67]
Karagiannis, T.C.; El-Osta, A. Clinical potential of histone deacetylase inhibitors as stand alone therapeutics and in combination with other chemotherapeutics or radiotherapy for cancer. Epigenetics, 2006, 1(3), 121-126. [http://dx.doi.org/10.4161/epi.1.3.3328]. [PMID: 17965606].
[68]
Valdez, B.C.; Li, Y.; Murray, D.; Brammer, J.E.; Liu, Y.; Hosing, C.; Nieto, Y.; Champlin, R.E.; Andersson, B.S. Differential effects of histone deacetylase inhibitors on cellular drug transporters and their implications for using epigenetic modifiers in combination chemotherapy. Oncotarget, 2016, 7(39), 63829-63838. [http://dx.doi.org/10.18632/oncotarget.11561]. [PMID: 27564097].
[69]
Willoughby, C.E.; Reeves, H.L. Combination PARP and HDAC inhibition as a therapeutic strategy targeting liver cancer stem cells? Linchuang Zhongliuxue Zazhi, 2016, 5(5), 60. [http://dx.doi.org/10.21037/cco.2016.03.21]. [PMID: 27164859].
[70]
Kala, R.; Tollefsbol, T.O. A novel combinatorial epigenetic therapy using resveratrol and pterostilbene for restoring estrogen receptor-α (ERα) expression in erα-negative breast cancer cells. PLoS One, 2016, 11(5)e0155057 [http://dx.doi.org/10.1371/journal.pone.0155057]. [PMID: 27159275].
[71]
Rundall, B.K.; Denlinger, C.E.; Jones, D.R. Suberoylanilide hydroxamic acid combined with gemcitabine enhances apoptosis in non-small cell lung cancer. Surgery, 2005, 138(2), 360-367. [http://dx.doi.org/10.1016/j.surg.2005.06.016]. [PMID: 16153448].
[72]
Kurz, E.U.; Wilson, S.E.; Leader, K.B.; Sampey, B.P.; Allan, W.P.; Yalowich, J.C.; Kroll, D.J. The histone deacetylase inhibitor sodium butyrate induces DNA topoisomerase II alpha expression and confers hypersensitivity to etoposide in human leukemic cell lines. Mol. Cancer Ther., 2001, 1(2), 121-131. [PMID: 12467229].
[73]
Maggio, S.C.; Rosato, R.R.; Kramer, L.B.; Dai, Y.; Rahmani, M.; Paik, D.S.; Czarnik, A.C.; Payne, S.G.; Spiegel, S.; Grant, S. The histone deacetylase inhibitor MS-275 interacts synergistically with fludarabine to induce apoptosis in human leukemia cells. Cancer Res., 2004, 64(7), 2590-2600. [http://dx.doi.org/10.1158/0008-5472.CAN-03-2631]. [PMID: 15059916].
[74]
Singh, P.; Tomar, R.S.; Rath, S.K. Anticancer potential of the histone deacetylase inhibitor-like effects of flavones, a subclass of polyphenolic compounds: A review. Mol. Biol. Rep., 2015, 42(11), 1515-1531. [http://dx.doi.org/10.1007/s11033-015-3881-y]. [PMID: 26033434].
[75]
Bruserud, Ø.; Stapnes, C.; Tronstad, K.J.; Ryningen, A.; Anensen, N.; Gjertsen, B.T. Protein lysine acetylation in normal and leukaemic haematopoiesis: HDACs as possible therapeutic targets in adult AML. Expert Opin. Ther. Targets, 2006, 10(1), 51-68. [http://dx.doi.org/10.1517/14728222.10.1.51]. [PMID: 16441228].
[76]
Schwarz, K.; Romanski, A.; Puccetti, E.; Wietbrauk, S.; Vogel, A.; Keller, M.; Scott, J.W.; Serve, H.; Bug, G. The deacetylase inhibitor LAQ824 induces notch signalling in haematopoietic progenitor cells. Leuk. Res., 2011, 35(1), 119-125. [http://dx.doi.org/10.1016/j.leukres.2010.06.024]. [PMID: 20674020].
[77]
Androutsopoulos, V.P.; Spandidos, D.A. Antiproliferative effects of TSA, PXD 101 and MS 275 in A2780 and MCF7 cells: Acetylated histone H4 and acetylated tubulin as markers for HDACi potency and selectivity. Oncol. Rep., 2017, 38(6), 3412-3418. [http://dx.doi.org/10.3892/or.2017.6015]. [PMID: 29039546].
[78]
Wilson-Edell, K.A.; Yevtushenko, M.A.; Rothschild, D.E.; Rogers, A.N.; Benz, C.C. mTORC1/C2 and pan-HDAC inhibitors synergistically impair breast cancer growth by convergent AKT and polysome inhibiting mechanisms. Breast Cancer Res. Treat., 2014, 144(2), 287-298. [http://dx.doi.org/10.1007/s10549-014-2877-y]. [PMID: 24562770].
[79]
Hegde, A.N.; Upadhya, S.C. Role of ubiquitin-proteasome-mediated proteolysis in nervous system disease. Biochim. Biophys. Acta, 2011, 1809(2), 128-140. [http://dx.doi.org/10.1016/j.bbagrm.2010.07.006]. [PMID: 20674814].
[80]
Gandolfi, S.; Laubach, J.P.; Hideshima, T.; Chauhan, D.; Anderson, K.C.; Richardson, P.G. The proteasome and proteasome inhibitors in multiple myeloma. Cancer Metastasis Rev., 2017, 36(4), 561-584. [http://dx.doi.org/10.1007/s10555-017-9707-8]. [PMID: 29196868].
[81]
Zhu, L.; Wu, K.; Ma, S.; Zhang, S. HDAC inhibitors: A new radiosensitizer for non-small-cell lung cancer. Tumori, 2015, 101(3), 257-262. [http://dx.doi.org/10.5301/tj.5000347]. [PMID: 25953446].
[82]
Hesham, H.M.; Lasheen, D.S.; Abouzid, K.A.M. Chimeric HDAC inhibitors: Comprehensive review on the HDAC-based strategies developed to combat cancer. Med. Res. Rev., 2018, 38(6), 2058-2109. [http://dx.doi.org/10.1002/med.21505]. [PMID: 29733427].
[83]
Kunami, N.; Katsuya, H.; Nogami, R.; Ishitsuka, K.; Tamura, K. Promise of combining a Bcl-2 family inhibitor with bortezomib or SAHA for adult T-cell leukemia/lymphoma. Anticancer Res., 2014, 34(10), 5287-5294. [PMID: 25275021].
[84]
Liu, Y.; Qin, X.Q.; Weber, H.C.; Xiang, Y.; Liu, C.; Liu, H.J.; Yang, H.; Jiang, J.; Qu, X. Bombesin receptor-activated protein (BRAP) modulates NF-κB activation in bronchial epithelial cells by enhancing HDAC activity. J. Cell. Biochem., 2016, 117(5), 1069-1077. [http://dx.doi.org/10.1002/jcb.25406]. [PMID: 26460487].
[85]
Nakshatri, H.; Appaiah, H.N.; Anjanappa, M.; Gilley, D.; Tanaka, H.; Badve, S.; Crooks, P.A.; Mathews, W.; Sweeney, C.; Bhat-Nakshatri, P. NF-κB-dependent and -independent epigenetic modulation using the novel anti-cancer agent DMAPT. Cell Death Dis., 2015, 6e1608 [http://dx.doi.org/10.1038/cddis.2014.569]. [PMID: 25611383].
[86]
Kim, M.; Lu, F.; Zhang, Y. Loss of HDAC-mediated repression and gain of NF-κB activation underlie cytokine induction in ARID1A- and PIK3CA-mutation-driven ovarian cancer. Cell Rep., 2016, 17(1), 275-288. [http://dx.doi.org/10.1016/j.celrep.2016.09.003]. [PMID: 27681437].
[87]
Rafii, S.; Roda, D.; Geuna, E.; Jimenez, B.; Rihawi, K.; Capelan, M.; Yap, T.A.; Molife, L.R.; Kaye, S.B.; de Bono, J.S.; Banerji, U. Higher Risk of Infections with PI3K-AKT-mTOR Pathway Inhibitors in Patients with Advanced Solid Tumors on Phase I Clinical Trials. Clin. Cancer Res., 2015, 21(8), 1869-1876. [http://dx.doi.org/10.1158/1078-0432.CCR-14-2424]. [PMID: 25649020].
[88]
Wang, H.; Zhou, W.; Zheng, Z.; Zhang, P.; Tu, B.; He, Q.; Zhu, W.G. The HDAC inhibitor depsipeptide transactivates the p53/p21 pathway by inducing DNA damage. DNA Repair (Amst.), 2012, 11(2), 146-156. [http://dx.doi.org/10.1016/j.dnarep.2011.10.014]. [PMID: 22112863].
[89]
Sabnis, G.J.; Goloubeva, O.G.; Kazi, A.A.; Shah, P.; Brodie, A.H. HDAC inhibitor entinostat restores responsiveness of letrozole-resistant MCF-7Ca xenografts to aromatase inhibitors through modulation of Her-2. Mol. Cancer Ther., 2013, 12(12), 2804-2816. [http://dx.doi.org/10.1158/1535-7163.MCT-13-0345]. [PMID: 24092810].
[90]
Giommarelli, C.; Zuco, V.; Favini, E.; Pisano, C.; Dal Piaz, F.; De Tommasi, N.; Zunino, F. The enhancement of antiproliferative and proapoptotic activity of HDAC inhibitors by curcumin is mediated by Hsp90 inhibition. Cell. Mol. Life Sci., 2010, 67(6), 995-1004. [http://dx.doi.org/10.1007/s00018-009-0233-x]. [PMID: 20039095].
[91]
Meng, Q.; Chen, X.; Sun, L.; Zhao, C.; Sui, G.; Cai, L. Carbamazepine promotes Her-2 protein degradation in breast cancer cells by modulating HDAC6 activity and acetylation of Hsp90. Mol. Cell. Biochem., 2011, 348(1-2), 165-171. [http://dx.doi.org/10.1007/s11010-010-0651-y]. [PMID: 21082217].
[92]
Ryhänen, T.; Viiri, J.; Hyttinen, J.M.; Uusitalo, H.; Salminen, A.; Kaarniranta, K. Influence of Hsp90 and HDAC inhibition and tubulin acetylation on perinuclear protein aggregation in human retinal pigment epithelial cells. J. Biomed. Biotechnol., 2011, 2011798052 [http://dx.doi.org/10.1155/2011/798052]. [PMID: 20981255].
[93]
Singh, T.R.; Shankar, S.; Srivastava, R.K. HDAC inhibitors enhance the apoptosis-inducing potential of TRAIL in breast carcinoma. Oncogene, 2005, 24(29), 4609-4623. [http://dx.doi.org/10.1038/sj.onc.1208585]. [PMID: 15897906].
[94]
Fröhlich, L.F.; Mrakovcic, M.; Smole, C.; Lahiri, P.; Zatloukal, K. Epigenetic silencing of apoptosis-inducing gene expression can be efficiently overcome by combined SAHA and TRAIL treatment in uterine sarcoma cells. PLoS One, 2014, 9(3)e91558 [http://dx.doi.org/10.1371/journal.pone.0091558]. [PMID: 24618889].
[95]
Duong, V.; Bret, C.; Altucci, L.; Mai, A.; Duraffourd, C.; Loubersac, J.; Harmand, P.O.; Bonnet, S.; Valente, S.; Maudelonde, T.; Cavailles, V.; Boulle, N. Specific activity of class II histone deacetylases in human breast cancer cells. Mol. Cancer Res., 2008, 6(12), 1908-1919. [http://dx.doi.org/10.1158/1541-7786.MCR-08-0299]. [PMID: 19074835].
[96]
Facchetti, F.; Previdi, S.; Ballarini, M.; Minucci, S.; Perego, P.; La Porta, C.A. Modulation of pro- and anti-apoptotic factors in human melanoma cells exposed to histone deacetylase inhibitors. Apoptosis, 2004, 9(5), 573-582. [http://dx.doi.org/10.1023/B:APPT.0000038036.31271.50]. [PMID: 15314285].
[97]
Mohr, A.; Yu, R.; Zwacka, R.M. TRAIL-receptor preferences in pancreatic cancer cells revisited: Both TRAIL-R1 and TRAIL-R2 have a licence to kill. BMC Cancer, 2015, 15, 494. [http://dx.doi.org/10.1186/s12885-015-1508-2]. [PMID: 26138346].
[98]
Shi, X.Y.; Ding, W.; Li, T.Q.; Zhang, Y.X.; Zhao, S.C. Histone deacetylase (HDAC) inhibitor,suberoylanilide hydroxamic acid SAHA,inducesapoptosis in prostate cancer cell lines via the Akt/FOXO3a signaling pathway. Med. Sci. Monit., 2017, 23(12), 5793-5802. [http://dx.doi.org/10.12659/MSM.904597]. [PMID: 29211704].
[99]
Kong, L.R.; Tan, T.Z.; Ong, W.R.; Bi, C.; Huynh, H.; Lee, S.C.; Chng, W.J.; Eichhorn, P.J.A.; Goh, B.C. Belinostat exerts antitumor cytotoxicity through the ubiquitin-proteasome pathway in lung squamous cell carcinoma. Mol. Oncol., 2017, 11(8), 965-980. [http://dx.doi.org/10.1002/1878-0261.12064]. [PMID: 28397399].
[100]
Pathania, R.; Ramachandran, S.; Mariappan, G.; Thakur, P.; Shi, H.; Choi, J.H.; Manicassamy, S.; Kolhe, R.; Prasad, P.D.; Sharma, S.; Lokeshwar, B.L.; Ganapathy, V.; Thangaraju, M. Combined inhibition of DNMT and HDAC blocks the tumorigenicity of cancer stem-like cells and attenuates mammary tumor growth. Cancer Res., 2016, 76(11), 3224-3235. [http://dx.doi.org/10.1158/0008-5472.CAN-15-2249]. [PMID: 27197203].
[101]
Lopez, G.; Braggio, D.; Zewdu, A.; Casadei, L.; Batte, K.; Bid, H.K.; Koller, D.; Yu, P.; Iwenofu, O.H.; Strohecker, A.; Choy, E.; Lev, D.; Pollock, R. Mocetinostat combined with gemcitabine for the treatment of leiomyosarcoma: Preclinical correlates. PLoS One, 2017, 12(11)e0188859 [http://dx.doi.org/10.1371/journal.pone.0188859]. [PMID: 29186204].
[102]
Ni, M.; Esposito, E.; Raj, V.P.; Muzi, L.; Zunino, F.; Zuco, V.; Cominetti, D.; Penco, S.; Dal Pozzo, A. New macrocyclic analogs of the natural histone deacetylase inhibitor FK228; design, synthesis and preliminary biological evaluation. Bioorg. Med. Chem., 2015, 23(21), 6785-6793. [http://dx.doi.org/10.1016/j.bmc.2015.10.004]. [PMID: 26481659].
[103]
Wang, S.H.; Lin, P.Y.; Chiu, Y.C.; Huang, J.S.; Kuo, Y.T.; Wu, J.C.; Chen, C.C. Curcumin-mediated HDAC inhibition suppresses the DNA damage response and contributes to increased DNA damage sensitivity. PLoS One, 2015, 10(7)e0134110 [http://dx.doi.org/10.1371/journal.pone.0134110]. [PMID: 26218133].

Rights & Permissions Print Cite
Article Metrics
60
10
1
1
© 2024 Bentham Science Publishers | Privacy Policy