HDAC-driven mechanisms in anticancer resistance: epigenetics and beyond

Martina Minisini , Martina Mascaro , Claudio Brancolini

Cancer Drug Resistance ›› 2024, Vol. 7 : 46

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Cancer Drug Resistance ›› 2024, Vol. 7 :46 DOI: 10.20517/cdr.2024.103
review-article

HDAC-driven mechanisms in anticancer resistance: epigenetics and beyond

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Abstract

The emergence of drug resistance leading to cancer recurrence is one of the challenges in the treatment of cancer patients. Several mechanisms can lead to drug resistance, including epigenetic changes. Histone deacetylases (HDACs) play a key role in chromatin regulation through epigenetic mechanisms and are also involved in drug resistance. The control of histone acetylation and the accessibility of regulatory DNA sequences such as promoters, enhancers, and super-enhancers are known mechanisms by which HDACs influence gene expression. Other targets of HDACs that are not histones can also contribute to resistance. This review describes the contribution of HDACs to the mechanisms that, in some cases, may determine resistance to chemotherapy or other cancer treatments.

Keywords

HDACs / chemotherapy / hormone deprivation / acetylation / palbociclib / PARP / DNA damage

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Martina Minisini, Martina Mascaro, Claudio Brancolini. HDAC-driven mechanisms in anticancer resistance: epigenetics and beyond. Cancer Drug Resistance, 2024, 7: 46 DOI:10.20517/cdr.2024.103

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References

[1]

World Bank Group. Metadata glossary. Cause of death, by injury (% of total). Available from: https://databank.worldbank.org/metadataglossary/world-development-indicators/series/SH.DTH.INJR.ZS. [Last accessed on 20 Nov 2024]

[2]

Sung H,Siegel RL.Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.CA Cancer J Clin2021;71:209-49

[3]

Collaborative and National Institute for Health Research Global Health Research Unit on Global Surgery. Global variation in postoperative mortality and complications after cancer surgery: a multicentre, prospective cohort study in 82 countries.Lancet2021;397:387-97

[4]

Mansoori B,Davudian S,Baradaran B.The different mechanisms of cancer drug resistance: a brief review.Adv Pharm Bull2017;7:339-48 PMCID:PMC5651054

[5]

Mollaei M,Khorshidi F.Chemotherapeutic drugs: cell death- and resistance-related signaling pathways. Are they really as smart as the tumor cells?.Transl Oncol2021;14:101056 PMCID:PMC7938256

[6]

Luria SE.Mutations of bacteria from virus sensitivity to virus resistance.Genetics1943;28:491-511 PMCID:PMC1209226

[7]

Goldie JH.A mathematic model for relating the drug sensitivity of tumors to their spontaneous mutation rate.Cancer Treat Rep1979;63:1727-33

[8]

Longley DB.Molecular mechanisms of drug resistance.J Pathol2005;205:275-92

[9]

Brancolini C,Minisini M.HDACs and the epigenetic plasticity of cancer cells: target the complexity.Pharmacol Ther2022;238:108190

[10]

Bahl S.Regulation of histone deacetylase activities and functions by phosphorylation and its physiological relevance.Cell Mol Life Sci2021;78:427-45 PMCID:PMC7854769

[11]

Kelly RDW,Watson PJ.Histone deacetylase (HDAC) 1 and 2 complexes regulate both histone acetylation and crotonylation in vivo.Sci Rep2018;8:14690 PMCID:PMC6168483

[12]

Zhao Y.Comprehensive catalog of currently documented histone modifications.Cold Spring Harb Perspect Biol2015;7:a025064 PMCID:PMC4563710

[13]

Porter NJ.Structure, mechanism, and inhibition of the zinc-dependent histone deacetylases.Curr Opin Struct Biol2019;59:9-18 PMCID:PMC6687579

[14]

Bantscheff M,Savitski MM.Chemoproteomics profiling of HDAC inhibitors reveals selective targeting of HDAC complexes.Nat Biotechnol2011;29:255-65

[15]

Millard CJ,Fairall L.Targeting class I histone deacetylases in a “complex” environment.Trends Pharmacol Sci2017;38:363-77

[16]

BioGRID4.4. Available from: https://thebiogrid.org. [Last accessed on 18 Nov 2024]

[17]

Di Giorgio E, Hancock WW, Brancolini C. MEF2 and the tumorigenic process, hic sunt leones.Biochim Biophys Acta Rev Cancer2018;1870:261-73

[18]

Di Giorgio E,Tolotto V.HDAC4 influences the DNA damage response and counteracts senescence by assembling with HDAC1/HDAC2 to control H2BK120 acetylation and homology-directed repair.Nucleic Acids Res2024;52:8218-40 PMCID:PMC11317144

[19]

Park SY,Hwang HJ.Structural basis of the specific interaction of SMRT corepressor with histone deacetylase 4.Nucleic Acids Res2018;46:11776-88 PMCID:PMC6294515

[20]

Lahm A,Pallaoro M.Unraveling the hidden catalytic activity of vertebrate class IIa histone deacetylases.Proc Natl Acad Sci U S A2007;104:17335-40 PMCID:PMC2077257

[21]

Zhang Y,Hanna AA.Evidence that HDAC7 acts as an epigenetic “reader” of AR acetylation through NCoR-HDAC3 dissociation.Cell Chem Biol2022;29:1162-73.e5 PMCID:PMC9450512

[22]

Di Giorgio E, Brancolini C. Regulation of class IIa HDAC activities: it is not only matter of subcellular localization.Epigenomics2016;8:251-69

[23]

Dai S,Dey R.Structural insights into the HDAC4-MEF2A-DNA complex and its implication in long-range transcriptional regulation.Nucleic Acids Res2024;52:2711-23 PMCID:PMC10954479

[24]

Biersack B,Höpfner M.Immunomodulatory properties of HDAC6 inhibitors in cancer diseases: new chances for sophisticated drug design and treatment optimization.Semin Cell Dev Biol2024;154:286-94

[25]

Pulya S,Adhikari N,Jha T.HDAC6 as privileged target in drug discovery: a perspective.Pharmacol Res2021;163:105274

[26]

Lambona C,Fioravanti R,Mai A.Histone deacetylase 10: a polyamine deacetylase from the crystal structure to the first inhibitors.Curr Opin Struct Biol2023;82:102668

[27]

Hai Y,Porter NJ.Histone deacetylase 10 structure and molecular function as a polyamine deacetylase.Nat Commun2017;8:15368 PMCID:PMC5454378

[28]

Sengupta N.Regulation of histone deacetylase activities.J Cell Biochem2004;93:57-67

[29]

Milazzo G,Di Muzio G.Histone deacetylases (HDACs): evolution, specificity, role in transcriptional complexes, and pharmacological actionability.Genes2020;11:E556 PMCID:PMC7288346

[30]

Li G,Zhu WG.The roles of histone deacetylases and their inhibitors in cancer therapy.Front Cell Dev Biol2020;8:576946 PMCID:PMC7552186

[31]

Emmett MJ.Integrative regulation of physiology by histone deacetylase 3.Nat Rev Mol Cell Biol2019;20:102-15 PMCID:PMC6347506

[32]

Ghosh S.Cisplatin: The first metal based anticancer drug.Bioorg Chem2019;88:102925

[33]

Song M,Liu K.Therapeutic strategies to overcome cisplatin resistance in ovarian cancer.Eur J Med Chem2022;232:114205

[34]

Spears N,Stefansdottir A.Ovarian damage from chemotherapy and current approaches to its protection.Hum Reprod Update2019;25:673-93 PMCID:PMC6847836

[35]

Galluzzi L,Vitale I.Molecular mechanisms of cisplatin resistance.Oncogene2012;31:1869-83

[36]

Zhang Z,Li L.SNP rs4971059 predisposes to breast carcinogenesis and chemoresistance via TRIM46-mediated HDAC1 degradation.EMBO J2021;40:e107974 PMCID:PMC8488578

[37]

Mylavarapu S,Roy M.Role of BRCA mutations in the modulation of response to platinum therapy.Front Oncol2018;8:16 PMCID:PMC5807680

[38]

Zhu Y,Zhang C.Tamoxifen-resistant breast cancer cells are resistant to DNA-damaging chemotherapy because of upregulated BARD1 and BRCA1.Nat Commun2018;9:1595 PMCID:PMC5913295

[39]

Ding S,Jiang Y.HDAC1 regulates the chemosensitivity of laryngeal carcinoma cells via modulation of interleukin-8 expression.Eur J Pharmacol2021;896:173923

[40]

Sun Y,Ren Y.Targeting HDAC/OAZ1 axis with a novel inhibitor effectively reverses cisplatin resistance in non-small cell lung cancer.Cell Death Dis2019;10:400 PMCID:PMC6534535

[41]

Kurian L,Gödderz D.Polyamine sensing by nascent ornithine decarboxylase antizyme stimulates decoding of its mRNA.Nature2011;477:490-4

[42]

Sun JM,Davie JR.Differential distribution of unmodified and phosphorylated histone deacetylase 2 in chromatin.J Biol Chem2007;282:33227-36

[43]

Huang R,Tse M.The role of HDAC2 in chromatin remodelling and response to chemotherapy in ovarian cancer.Oncotarget2016;7:4695-711 PMCID:PMC4826236

[44]

Wang H,Du J.Enhanced histone H3 acetylation of the PD-L1 promoter via the COP1/c-Jun/HDAC3 axis is required for PD-L1 expression in drug-resistant cancer cells.J Exp Clin Cancer Res2020;39:29 PMCID:PMC7003365

[45]

Stronach EA,Rama N.HDAC4-regulated STAT1 activation mediates platinum resistance in ovarian cancer.Cancer Res2011;71:4412-22 PMCID:PMC3130134

[46]

Spaety ME,Badie A.HDAC4 levels control sensibility toward cisplatin in gastric cancer via the p53-p73/BIK pathway.Cancers2019;11:1747 PMCID:PMC6896094

[47]

Brachova P,Leslie KK.The consequence of oncomorphic TP53 mutations in ovarian cancer.Int J Mol Sci2013;14:19257-75 PMCID:PMC3794832

[48]

Reles A,Schmider A.Correlation of p53 mutations with resistance to platinum-based chemotherapy and shortened survival in ovarian cancer.Clin Cancer Res2001;7:2984-97

[49]

Zhang X,Yin H.Interaction between p53 and Ras signaling controls cisplatin resistance via HDAC4- and HIF-1α-mediated regulation of apoptosis and autophagy.Theranostics2019;9:1096-114 PMCID:PMC6401400

[50]

Minisini M,Brancolini C.Acetylation and phosphorylation in the regulation of hypoxia-inducible factor activities: additional options to modulate adaptations to changes in oxygen levels.Life2023;14:20 PMCID:PMC10821055

[51]

Aydin B.Co-expression network analysis elucidated a core module in association with prognosis of non-functioning non-invasive human pituitary adenoma.Front Endocrinol2019;10:361 PMCID:PMC6563679

[52]

Guo C,Zhang Y.Mining TCGA data for key biomarkers related to immune microenvironment in endometrial cancer by immune score and weighted correlation network analysis.Front Mol Biosci2021;8:645388 PMCID:PMC8048410

[53]

Zhang Y,Jia XY.METTL3-mediated N6-methyladenosine modification and HDAC5/YY1 promote IFFO1 downregulation in tumor development and chemo-resistance.Cancer Lett2023;553:215971

[54]

Sucharov CC,Bristow M.Shuttling of HDAC5 in H9C2 cells regulates YY1 function through CaMKIV/PKD and PP2A.Am J Physiol Cell Physiol2006;291:C1029-37

[55]

Sucharov CC,McKinsey TA.YY1 protects cardiac myocytes from pathologic hypertrophy by interacting with HDAC5.Mol Biol Cell2008;19:4141-53 PMCID:PMC2555926

[56]

Qian S,Li M.Transcriptional factor Yin Yang 1 facilitates the stemness of ovarian cancer via suppressing miR-99a activity through enhancing its deacetylation level.Biomed Pharmacother2020;126:110085

[57]

Zhou L,Liu H.Prognosis analysis of histone deacetylases mRNA expression in ovarian cancer patients.J Cancer2018;9:4547-55 PMCID:PMC6277648

[58]

Li X,Xie Y.Deacetylation induced nuclear condensation of HP1γ promotes multiple myeloma drug resistance.Nat Commun2023;14:1290 PMCID:PMC9998874

[59]

Kumar A.Heterochromatin protein 1 (HP1): interactions with itself and chromatin components.Biophys Rev2020;12:387-400 PMCID:PMC7242596

[60]

Zeng W,Yokomori K.HP1: heterochromatin binding proteins working the genome.Epigenetics2010;5:287-92 PMCID:PMC3103764

[61]

Casale AM,Piacentini L.Unravelling HP1 functions: post-transcriptional regulation of stem cell fate.Chromosoma2021;130:103-11 PMCID:PMC8426308

[62]

Arcamone F,Fantini G.Adriamycin, 14-hydroxydaunomycin, a new antitumor antibiotic from S. peucetius var. caesius.Biotechnol Bioeng1969;11:1101-10

[63]

Cox J.Mechanisms of doxorubicin resistance in hepatocellular carcinoma.Hepat Oncol2016;3:57-9 PMCID:PMC4792121

[64]

Kim SJ,Seo YR.Understanding of ROS-inducing strategy in anticancer therapy.Oxid Med Cell Longev2019;2019:5381692 PMCID:PMC6939418

[65]

Long J,Chang L.Targeting HDAC3, a new partner protein of AKT in the reversal of chemoresistance in acute myeloid leukemia via DNA damage response.Leukemia2017;31:2761-70

[66]

Grandage VL,Linch DC.PI3-kinase/Akt is constitutively active in primary acute myeloid leukaemia cells and regulates survival and chemoresistance via NF-kappaB, mapkinase and p53 pathways.Leukemia2005;19:586-94

[67]

West KA,Dennis PA.Activation of the PI3K/Akt pathway and chemotherapeutic resistance.Drug Resist Updat2002;5:234-48

[68]

Fryknäs M,Oberg F.STAT1 signaling is associated with acquired crossresistance to doxorubicin and radiation in myeloma cell lines.Int J Cancer2007;120:189-95

[69]

Kaowinn S,Kim CS.Increased EGFR expression induced by a novel oncogene, CUG2, confers resistance to doxorubicin through Stat1-HDAC4 signaling.Cell Oncol2017;40:549-61

[70]

Drury AN.The physiological activity of adenine compounds with especial reference to their action upon the mammalian heart.J Physiol1929;68:213-37 PMCID:PMC1402863

[71]

Aumer T,Runtsch LS.Comprehensive comparison between azacytidine and decitabine treatment in an acute myeloid leukemia cell line.Clin Epigenetics2022;14:113 PMCID:PMC9465881

[72]

Wu HL,Ji P,Jiang YZ.Targeting nucleotide metabolism: a promising approach to enhance cancer immunotherapy.J Hematol Oncol2022;15:45 PMCID:PMC9044757

[73]

Beutel AK.Barriers and opportunities for gemcitabine in pancreatic cancer therapy.Am J Physiol Cell Physiol2023;324:C540-52 PMCID:PMC9925166

[74]

Meng XN,Liu YH.Dynamic genomic changes in methotrexate-resistant human cancer cell lines beyond DHFR amplification suggest potential new targets for preventing drug resistance.Br J Cancer2024;130:1819-27 PMCID:PMC11130306

[75]

Alnuqaydan AM,Almutary AG.Synergistic antitumor effect of 5-fluorouracil and withaferin-A induces endoplasmic reticulum stress-mediated autophagy and apoptosis in colorectal cancer cells.Am J Cancer Res2020;10:799-815 PMCID:PMC7136917

[76]

Wang M,Yuan Z.Long non-coding RNA H19 confers 5-Fu resistance in colorectal cancer by promoting SIRT1-mediated autophagy.Cell Death Dis2018;9:1149 PMCID:PMC6242979

[77]

Offer SM,Fossum C,Diasio RB.Phenotypic profiling of DPYD variations relevant to 5-fluorouracil sensitivity using real-time cellular analysis and in vitro measurement of enzyme activity.Cancer Res2013;73:1958-68 PMCID:PMC3602211

[78]

Hait NC,Maceyka M.Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate.Science2009;325:1254-7 PMCID:PMC2850596

[79]

Zhang YH,Wu SH.SphK2 confers 5-fluorouracil resistance to colorectal cancer via upregulating H3K56ac-mediated DPD expression.Oncogene2020;39:5214-27

[80]

Kiweler N,Nguyen A.The epigenetic modifier HDAC2 and the checkpoint kinase ATM determine the responses of microsatellite instable colorectal cancer cells to 5-fluorouracil.Cell Biol Toxicol2023;39:2401-19 PMCID:PMC10547618

[81]

Wen W,Sun W.Suppression of cyclin D1 by hypoxia-inducible factor-1 via direct mechanism inhibits the proliferation and 5-fluorouracil-induced apoptosis of A549 cells.Cancer Res2010;70:2010-9

[82]

Song B,Xi Y.Mechanism of chemoresistance mediated by miR-140 in human osteosarcoma and colon cancer cells.Oncogene2009;28:4065-74 PMCID:PMC2783211

[83]

Zhao L,Zhang Q,Hu H.ATF4-mediated microRNA-145/HDAC4/p53 axis affects resistance of colorectal cancer cells to 5-fluorouracil by regulating autophagy.Cancer Chemother Pharmacol2022;89:595-607

[84]

Zeng Y,Zhou J.MARK2 regulates chemotherapeutic responses through class IIa HDAC-YAP axis in pancreatic cancer.Oncogene2022;41:3859-75 PMCID:PMC9339507

[85]

Zhao S,Wang R.Mechanisms of cancer cell death induction by paclitaxel: an updated review.Apoptosis2022;27:647-67

[86]

Snyder JP,Cornett B,Nogales E.The binding conformation of Taxol in beta-tubulin: a model based on electron crystallographic density.Proc Natl Acad Sci U S A2001;98:5312-6 PMCID:PMC33206

[87]

Mosca L,Fazi F,Colotti G.Taxanes in cancer treatment: activity, chemoresistance and its overcoming.Drug Resist Updat2021;54:100742

[88]

Ismail U. Taxane toxicity. In: StatPearls. 2023. Available from: https://www.ncbi.nlm.nih.gov/books/NBK589655/. [Last accessed on 18 Nov 2024]

[89]

Holohan C,Longley DB.Cancer drug resistance: an evolving paradigm.Nat Rev Cancer2013;13:714-26

[90]

Liao D,Gupta P.Tetrandrine interaction with ABCB1 reverses multidrug resistance in cancer cells through competition with anti-cancer drugs followed by downregulation of ABCB1 expression.Molecules2019;24:4383 PMCID:PMC6930469

[91]

Wang L,Ren Y.Targeting HDAC with a novel inhibitor effectively reverses paclitaxel resistance in non-small cell lung cancer via multiple mechanisms.Cell Death Dis2016;7:e2063 PMCID:PMC4816165

[92]

Kadamb R,Bansal N,Saluja D.Sin3: insight into its transcription regulatory functions.Eur J Cell Biol2013;92:237-46

[93]

Merle NS,Fremeaux-Bacchi V.Complement system part I - molecular mechanisms of activation and regulation.Front Immunol2015;6:262 PMCID:PMC4451739

[94]

Merle NS,Halbwachs-Mecarelli L,Roumenina LT.Complement system part II: role in immunity.Front Immunol2015;6:257 PMCID:PMC4443744

[95]

Hollander MC.Genomic instability, centrosome amplification, cell cycle checkpoints and Gadd45a.Oncogene2002;21:6228-33

[96]

Wang X,Chen J.Nuclear complement C3b promotes paclitaxel resistance by assembling the SIN3A/HDAC1/2 complex in non-small cell lung cancer.Cell Death Dis2023;14:351 PMCID:PMC10250389

[97]

Broux M,Demeyer S.Suz12 inactivation cooperates with JAK3 mutant signaling in the development of T-cell acute lymphoblastic leukemia.Blood2019;134:1323-36 PMCID:PMC6888143

[98]

Conway E,Bracken AP.PRC2 mediated H3K27 methylations in cellular identity and cancer.Curr Opin Cell Biol2015;37:42-8

[99]

Jiang M,Zhang K.MARCKSL1-2 reverses docetaxel-resistance of lung adenocarcinoma cells by recruiting SUZ12 to suppress HDAC1 and elevate miR-200b.Mol Cancer2022;21:150 PMCID:PMC9306054

[100]

Chen DQ,Huang JY.HDAC 1/4-mediated silencing of microRNA-200b promotes chemoresistance in human lung adenocarcinoma cells.Oncotarget2014;5:3333-49 PMCID:PMC4102813

[101]

Narita N,Kimura Y.Suppression of histone deacetylase 3 (HDAC3) enhances apoptosis induced by paclitaxel in human maxillary cancer cells in vitro and in vivo.Biochem Biophys Res Commun2010;396:310-6

[102]

Jia J,Shi Q.Erratum: KLF5 downregulation desensitizes castration-resistant prostate cancer cells to docetaxel by increasing BECN1 expression and inducing cell autophagy: Erratum.Theranostics2023;13:2962-3 PMCID:PMC10240812

[103]

Brancolini C,Formisano L.Quis custodiet ipsos custodes (who controls the controllers)? Two decades of studies on HDAC9.Life2021;11:90 PMCID:PMC7912504

[104]

Lian B,Jiang YZ.Truncated HDAC9 identified by integrated genome-wide screen as the key modulator for paclitaxel resistance in triple-negative breast cancer.Theranostics2020;10:11092-109 PMCID:PMC7532680

[105]

Chudobová J.Microtubule affinity regulating kinase (MARK/Par1) isoforms differentially regulate Alzheimer-like TAU missorting and Aβ-mediated synapse pathology.Neural Regen Res2023;18:335-6 PMCID:PMC9396503

[106]

Natalia MA,Virginia TJ.MARK1 is a novel target for miR-125a-5p: implications for cell migration in cervical tumor cells.Microrna2018;7:54-61

[107]

Miki Y.Hormone-dependent cancers: new aspects on biochemistry and molecular pathology.Int J Mol Sci2023;24:10830 PMCID:PMC10341538

[108]

Mouridsen H,Patterson J.Tamoxifen in advanced breast cancer.Cancer Treat Rev1978;5:131-41

[109]

Kowalczyk W,Jach R.Steroid receptors in breast cancer: understanding of molecular function as a basis for effective therapy development.Cancers2021;13:4779 PMCID:PMC8507808

[110]

Murphy CG.Endocrine resistance in hormone-responsive breast cancer: mechanisms and therapeutic strategies.Endocr Relat Cancer2016;23:R337-52

[111]

Achinger-Kawecka J,Luu PL.Epigenetic reprogramming at estrogen-receptor binding sites alters 3D chromatin landscape in endocrine-resistant breast cancer.Nat Commun2020;11:320

[112]

Davis T,Chiew YE,deFazio A.Histone deacetylase inhibitors decrease proliferation and modulate cell cycle gene expression in normal mammary epithelial cells.Clin Cancer Res2000;6:4334-42

[113]

Vigushin DM,Pace PE.Trichostatin A is a histone deacetylase inhibitor with potent antitumor activity against breast cancer in vivo.Clin Cancer Res2001;7:971-6

[114]

Margueron R,Lazennec G,Cavaillès V.Oestrogen receptor alpha increases p21(WAF1/CIP1) gene expression and the antiproliferative activity of histone deacetylase inhibitors in human breast cancer cells.J Endocrinol2003;179:41-53

[115]

Alao JP,Lam EW,Vigushin DM.Histone deacetylase inhibitor, trichostatin A induces ubiquitin-dependent cyclin D1 degradation in MCF-7 breast cancer cells.Mol Cancer2006;5:8 PMCID:PMC1397858

[116]

Connolly RM,Miller KD.E2112: randomized phase III trial of endocrine therapy plus entinostat or placebo in hormone receptor-positive advanced breast cancer. A trial of the ECOG-ACRIN Cancer Research Group.J Clin Oncol2021;39:3171-81 PMCID:PMC8478386

[117]

Macaluso M,Russo G,Giordano A.pRb2/p130-E2F4/5-HDAC1-SUV39H1-p300 and pRb2/p130-E2F4/5-HDAC1-SUV39H1-DNMT1 multimolecular complexes mediate the transcription of estrogen receptor-alpha in breast cancer.Oncogene2003;22:3511-7

[118]

Liu XF.Recruitment of distinct chromatin-modifying complexes by tamoxifen-complexed estrogen receptor at natural target gene promoters in vivo.J Biol Chem2004;279:15050-8

[119]

Demirpence E,Oliva J.An estrogen-responsive element-targeted histone deacetylase enzyme has an antiestrogen activity that differs from that of hydroxytamoxifen.Cancer Res2002;62:6519-28

[120]

Konduri SD,Liu W.Mechanisms of estrogen receptor antagonism toward p53 and its implications in breast cancer therapeutic response and stem cell regulation.Proc Natl Acad Sci U S A2010;107:15081-6 PMCID:PMC2930589

[121]

Suzuki A,Miyawaki Y.Down-regulation of PROS1 gene expression by 17beta-estradiol via estrogen receptor alpha (ERalpha)-Sp1 interaction recruiting receptor-interacting protein 140 and the corepressor-HDAC3 complex.J Biol Chem2010;285:13444-53 PMCID:PMC2859504

[122]

Leong H,Nash PD.Recruitment of histone deacetylase 4 to the N-terminal region of estrogen receptor alpha.Mol Endocrinol2005;19:2930-42

[123]

Duong V,Altucci L.Specific activity of class II histone deacetylases in human breast cancer cells.Mol Cancer Res2008;6:1908-19 PMCID:PMC2810315

[124]

Malik S,Garee JP.Histone deacetylase 7 and FoxA1 in estrogen-mediated repression of RPRM.Mol Cell Biol2010;30:399-412 PMCID:PMC2798473

[125]

Kurtev V,Kroboth K,Cavailles V.Transcriptional regulation by the repressor of estrogen receptor activity via recruitment of histone deacetylases.J Biol Chem2004;279:24834-43

[126]

Zhou J,Wang Q.SERPINA3-ANKRD11-HDAC3 pathway induced aromatase inhibitor resistance in breast cancer can be reversed by HDAC3 inhibition.Commun Biol2023;6:695 PMCID:PMC10326080

[127]

Yang F,Liu Z.Glucocorticoid receptor:MegaTrans switching mediates the repression of an ERα-regulated transcriptional program.Mol Cell2017;66:321-31.e6 PMCID:PMC5510478

[128]

Emmett MJ,Jager J.Histone deacetylase 3 prepares brown adipose tissue for acute thermogenic challenge.Nature2017;546:544-8 PMCID:PMC5826652

[129]

Huang WT,Chen SH.HDAC2 and HDAC5 up-regulations modulate survivin and miR-125a-5p expressions and promote hormone therapy resistance in estrogen receptor positive breast cancer cells.Front Pharmacol2017;8:902 PMCID:PMC5736991

[130]

Xue Y,Zhi J.HDAC5-mediated deacetylation and nuclear localisation of SOX9 is critical for tamoxifen resistance in breast cancer.Br J Cancer2019;121:1039-49 PMCID:PMC6964674

[131]

Choi SR,Lee J.Network analysis identifies regulators of basal-like breast cancer reprogramming and endocrine therapy vulnerability.Cancer Res2022;82:320-33

[132]

Liu C,Chen X.Sox9 regulates self-renewal and tumorigenicity by promoting symmetrical cell division of cancer stem cells in hepatocellular carcinoma.Hepatology2016;64:117-29

[133]

Jeselsohn R,Pun M.Embryonic transcription factor SOX9 drives breast cancer endocrine resistance.Proc Natl Acad Sci U S A2017;114:E4482-91 PMCID:PMC5465894

[134]

Jin K,Teo WW.HOXB7 is an ERα cofactor in the activation of HER2 and multiple ER target genes leading to endocrine resistance.Cancer Discov2015;5:944-59 PMCID:PMC4560624

[135]

Linares A,Lapierre M.Increased expression of the HDAC9 gene is associated with antiestrogen resistance of breast cancers.Mol Oncol2019;13:1534-47 PMCID:PMC6599838

[136]

Ahmad A,Yin S,Reddy KB.Functional role of miR-10b in tamoxifen resistance of ER-positive breast cancer cells through down-regulation of HDAC4.BMC Cancer2015;15:540 PMCID:PMC4512090

[137]

Katsogiannou M,Karaki S,Henry de Villeneuve M.The hallmarks of castration-resistant prostate cancers.Cancer Treat Rev2015;41:588-97

[138]

Westaby D,Paschalis A.A new old target: androgen receptor signaling and advanced prostate cancer.Annu Rev Pharmacol Toxicol2022;62:131-53

[139]

Biersack B,Höpfner M.HDAC inhibitors with potential to overcome drug resistance in castration-resistant prostate cancer.Cancer Drug Resist2022;5:64-79 PMCID:PMC8992583

[140]

Welsbie DS,Chen Y.Histone deacetylases are required for androgen receptor function in hormone-sensitive and castrate-resistant prostate cancer.Cancer Res2009;69:958-66 PMCID:PMC3219545

[141]

McLeod AB,Wardell SE,Chang CY.Validation of histone deacetylase 3 as a therapeutic target in castration-resistant prostate cancer.Prostate2018;78:266-77

[142]

Jia L,Wang Y.Orphan nuclear receptor TLX contributes to androgen insensitivity in castration-resistant prostate cancer via its repression of androgen receptor transcription.Oncogene2018;37:3340-55 PMCID:PMC6013422

[143]

Liu P,Gan L,Huang H.A transcription-independent function of FOXO1 in inhibition of androgen-independent activation of the androgen receptor in prostate cancer cells.Cancer Res2008;68:10290-9

[144]

Li X,Deng S.Loss of SYNCRIP unleashes APOBEC-driven mutagenesis, tumor heterogeneity, and AR-targeted therapy resistance in prostate cancer.Cancer Cell2023;41:1427-49.e12 PMCID:PMC10530398

[145]

Yang Y,Li P.Inhibition of androgen receptor activity by histone deacetylase 4 through receptor SUMOylation.Oncogene2011;30:2207-18 PMCID:PMC3093431

[146]

Degirmenci U,Sim YRM,Hu J.Drug resistance in targeted cancer therapies with RAF inhibitors.Cancer Drug Resist2021;4:665-83 PMCID:PMC9094075

[147]

Rinne N,Ardasheva A.Targeting the PI3K/AKT/mTOR pathway in epithelial ovarian cancer, therapeutic treatment options for platinum-resistant ovarian cancer.Cancer Drug Resist2021;4:573-95 PMCID:PMC9019160

[148]

Zielli T,Del Grande M,Colombo I.The clinical challenges of homologous recombination proficiency in ovarian cancer: from intrinsic resistance to new treatment opportunities.Cancer Drug Resist2023;6:499-516 PMCID:PMC10571062

[149]

Wang Z,Lyu R.SETD5-coordinated chromatin reprogramming regulates adaptive resistance to targeted pancreatic cancer therapy.Cancer Cell2020;37:834-49.e13 PMCID:PMC8187079

[150]

Martinelli E,Troiani T.Cancer resistance to therapies against the EGFR-RAS-RAF pathway: the role of MEK.Cancer Treat Rev2017;53:61-9

[151]

Infante JR,Park JO.A randomised, double-blind, placebo-controlled trial of trametinib, an oral MEK inhibitor, in combination with gemcitabine for patients with untreated metastatic adenocarcinoma of the pancreas.Eur J Cancer2014;50:2072-81

[152]

Sun Y,Hatzivassiliou G.Metabolic and transcriptional profiling reveals pyruvate dehydrogenase kinase 4 as a mediator of epithelial-mesenchymal transition and drug resistance in tumor cells.Cancer Metab2014;2:20 PMCID:PMC4221711

[153]

Eichner LJ,Brun SN.HDAC3 is critical in tumor development and therapeutic resistance in Kras-mutant non-small cell lung cancer.Sci Adv2023;9:eadd3243 PMCID:PMC10022903

[154]

Iacovelli R,Escudier B.Emerging tyrosine kinase inhibitors for the treatment of renal cancer.Expert Opin Emerg Drugs2015;20:379-92

[155]

Makhov P,Ghatalia P,Uzzo RG.Resistance to systemic therapies in clear cell renal cell carcinoma: mechanisms and management strategies.Mol Cancer Ther2018;17:1355-64 PMCID:PMC6034114

[156]

Xiong W,Yu H,Yi L.RRM2 regulates sensitivity to sunitinib and PD-1 blockade in renal cancer by stabilizing ANXA1 and activating the AKT pathway.Adv Sci2021;8:e2100881 PMCID:PMC8456228

[157]

von Hagen F,Strick A.N6-Methyladenosine (m6 A) readers are dysregulated in renal cell carcinoma.Mol Carcinog2021;60:354-62

[158]

Li W,Li X.YTHDC1 is downregulated by the YY1/HDAC2 complex and controls the sensitivity of ccRCC to sunitinib by targeting the ANXA1-MAPK pathway.J Exp Clin Cancer Res2022;41:250 PMCID:PMC9382764

[159]

Abdelgalil AA,Al-Jenoobi FI.Chapter Four - Sorafenib. In: Profiles of drug substances, excipients, and related methodology. Elsevier; 2019. pp. 239-66.

[160]

Kudo M.A paradigm change in the treatment strategy for hepatocellular carcinoma.Liver Cancer2020;9:367-77 PMCID:PMC7506281

[161]

Tang W,Zhang W.The mechanisms of sorafenib resistance in hepatocellular carcinoma: theoretical basis and therapeutic aspects.Signal Transduct Target Ther2020;5:87 PMCID:PMC7292831

[162]

Grégoire S,Xiao L.Control of MEF2 transcriptional activity by coordinated phosphorylation and sumoylation.J Biol Chem2006;281:4423-33

[163]

Clocchiatti A,Viviani G.The MEF2-HDAC axis controls proliferation of mammary epithelial cells and acini formation in vitro.J Cell Sci2015;128:3961-76

[164]

Rudalska R,Longerich T.In vivo RNAi screening identifies a mechanism of sorafenib resistance in liver cancer.Nat Med2014;20:1138-46 PMCID:PMC4587571

[165]

Xu Y,Ma L.MicroRNA-122 confers sorafenib resistance to hepatocellular carcinoma cells by targeting IGF-1R to regulate RAS/RAF/ERK signaling pathways.Cancer Lett2016;371:171-81

[166]

Ma Q,Zhao J.Coupling HDAC4 with transcriptional factor MEF2D abrogates SPRY4-mediated suppression of ERK activation and elicits hepatocellular carcinoma drug resistance.Cancer Lett2021;520:243-54

[167]

Isaacs JT,Antony L.Third generation quinoline-3-carboxamide transcriptional disrupter of HDAC4, HIF-1α, and MEF-2 signaling for metastatic castration-resistant prostate cancer.Prostate2023;83:1470-93 PMCID:PMC10559933

[168]

Papadimitriou MC,Iliakopoulos K,Michalaki V.Resistance to CDK4/6 inhibition: mechanisms and strategies to overcome a therapeutic problem in the treatment of hormone receptor-positive metastatic breast cancer.Biochim Biophys Acta Mol Cell Res2022;1869:119346

[169]

Magge T,Brufsky AM.CDK4/6 inhibitors: the devil is in the detail.Curr Oncol Rep2024;26:665-78

[170]

Luo RX,Dean DC.Rb interacts with histone deacetylase to repress transcription.Cell1998;92:463-73

[171]

Sanidas I,Fella KA.A code of mono-phosphorylation modulates the function of RB.Mol Cell2019;73:985-1000.e6 PMCID:PMC6424368

[172]

Yu Z,Chen Y.Pharmacological modulation of RB1 activity mitigates resistance to neoadjuvant chemotherapy in locally advanced rectal cancer.Proc Natl Acad Sci U S A2024;121:e2304619121 PMCID:PMC10861914

[173]

Zhou Y,Ma J.HDAC5 loss impairs RB repression of pro-oncogenic genes and confers CDK4/6 inhibitor resistance in cancer.Cancer Res2021;81:1486-99

[174]

Marek L,Hansen FK.Histone deacetylase (HDAC) inhibitors with a novel connecting unit linker region reveal a selectivity profile for HDAC4 and HDAC5 with improved activity against chemoresistant cancer cells.J Med Chem2013;56:427-36

[175]

Di Giorgio E, Gagliostro E, Brancolini C. Selective class IIa HDAC inhibitors: myth or reality.Cell Mol Life Sci2015;72:73-86 PMCID:PMC11113455

[176]

Konstantinopoulos PA,Shapiro GI.Homologous recombination deficiency: exploiting the fundamental vulnerability of ovarian cancer.Cancer Discov2015;5:1137-54 PMCID:PMC4631624

[177]

Dibitetto D,Rottenberg S.PARPi, BRCA, and gaps: controversies and future research.Trends Cancer2024;10:857-69

[178]

Lu Z,Yang H.SIK2 inhibition enhances PARP inhibitor activity synergistically in ovarian and triple-negative breast cancers.J Clin Invest2022;132:e146471 PMCID:PMC9151707

[179]

Krumm A,Kücük P.Enhanced histone deacetylase activity in malignant melanoma provokes RAD51 and FANCD2-triggered drug resistance.Cancer Res2016;76:3067-77

[180]

Sun D,Li Y.Histone deacetylase 2 is involved in DNA damage-mediated cell death of human osteosarcoma cells through stimulation of the ATM/p53 pathway.FEBS Open Bio2019;9:478-89 PMCID:PMC6396148

[181]

Gupta VG,Petersen S.Entinostat, a selective HDAC1/2 inhibitor, potentiates the effects of olaparib in homologous recombination proficient ovarian cancer.Gynecol Oncol2021;162:163-72 PMCID:PMC8647995

[182]

Sun L,Guo X.Acetylation-dependent regulation of core spliceosome modulates hepatocellular carcinoma cassette exons and sensitivity to PARP inhibitors.Nat Commun2024;15:5209 PMCID:PMC11189467

[183]

Roos WP.The multifaceted influence of histone deacetylases on DNA damage signalling and DNA repair.Nucleic Acids Res2016;44:10017-30 PMCID:PMC5137451

[184]

Geng L,Fu A,Atadja PW.Histone deacetylase (HDAC) inhibitor LBH589 increases duration of gamma-H2AX foci and confines HDAC4 to the cytoplasm in irradiated non-small cell lung cancer.Cancer Res2006;66:11298-304

[185]

Marampon F,Camero S.HDAC4 and HDAC6 sustain DNA double strand break repair and stem-like phenotype by promoting radioresistance in glioblastoma cells.Cancer Lett2017;397:1-11

[186]

Cuttini E,Pellarin E,Brancolini C.HDAC4 in cancer: a multitasking platform to drive not only epigenetic modifications.Front Mol Biosci2023;10:1116660 PMCID:PMC9902726

[187]

Chen F,Qin Q.Salt-inducible kinase 2: an oncogenic signal transmitter and potential target for cancer therapy.Front Oncol2019;9:18 PMCID:PMC6349817

[188]

Walkinshaw DR,Kim GW.The tumor suppressor kinase LKB1 activates the downstream kinases SIK2 and SIK3 to stimulate nuclear export of class IIa histone deacetylases.J Biol Chem2013;288:9345-62 PMCID:PMC3611005

[189]

Liang T,Elhassan RM.Targeting histone deacetylases for cancer therapy: trends and challenges.Acta Pharm Sin B2023;13:2425-63 PMCID:PMC10326266

[190]

Shi MQ,Fu X.Advances in targeting histone deacetylase for treatment of solid tumors.J Hematol Oncol2024;17:37 PMCID:PMC11143662

[191]

Hontecillas-Prieto L,Silver A,Hajji N.Synergistic enhancement of cancer therapy using HDAC inhibitors: opportunity for clinical trials.Front Genet2020;11:578011 PMCID:PMC7516260

[192]

Moran B,Reynolds JV,Lysaght J.The impact of histone deacetylase inhibitors on immune cells and implications for cancer therapy.Cancer Lett2023;559:216121

[193]

Rutherford KA.PROTACs: current and future potential as a precision medicine strategy to combat cancer.Mol Cancer Ther2024;23:454-63 PMCID:PMC10985480

[194]

Noonan EJ,Pookot D.miR-449a targets HDAC-1 and induces growth arrest in prostate cancer.Oncogene2009;28:1714-24

[195]

Shen Q,Sun J.Downregulation of histone deacetylase 1 by microRNA-520h contributes to the chemotherapeutic effect of doxorubicin.FEBS Lett2014;588:184-91

[196]

Roccaro AM,Jia X.microRNA-dependent modulation of histone acetylation in Waldenstrom macroglobulinemia.Blood2010;116:1506-14 PMCID:PMC2938840

[197]

Li Y,Luo X.Epigenetic silencing of microRNA-193a contributes to leukemogenesis in t(8;21) acute myeloid leukemia by activating the PTEN/PI3K signal pathway.Blood2013;121:499-509

[198]

Kim Y,Park H.miR-326-histone deacetylase-3 feedback loop regulates the invasion and tumorigenic and angiogenic response to anti-cancer drugs.J Biol Chem2014;289:28019-39 PMCID:PMC4183832

[199]

Topper MJ,Chiappinelli KB.Epigenetic therapy ties MYC depletion to reversing immune evasion and treating lung cancer.Cell2017;171:1284-300.e21 PMCID:PMC5808406

[200]

Blagitko-Dorfs N,Greve G.Combination treatment of acute myeloid leukemia cells with DNMT and HDAC inhibitors: predominant synergistic gene downregulation associated with gene body demethylation.Leukemia2019;33:945-56

[201]

Scotto L,Douglass E.Targeting the T-cell lymphoma epigenome induces cell death, cancer testes antigens, immune-modulatory signaling pathways.Mol Cancer Ther2021;20:1422-30 PMCID:PMC8941846

[202]

Mazzu YZ,Nandakumar S.Methylation-associated miR-193b silencing activates master drivers of aggressive prostate cancer.Mol Oncol2019;13:1944-58 PMCID:PMC6717747

[203]

Chang Y,Li X.Development of a first-in-class DNMT1/HDAC inhibitor with improved therapeutic potential and potentiated antitumor immunity.J Med Chem2024;67:16480-504

[204]

Liu B,Han L.BRD4-directed super-enhancer organization of transcription repression programs links to chemotherapeutic efficacy in breast cancer.Proc Natl Acad Sci U S A2022;119:e2109133119 PMCID:PMC8832982

[205]

Wen S,Wang L.Aberrant activation of super enhancer and choline metabolism drive antiandrogen therapy resistance in prostate cancer.Oncogene2020;39:6556-71

[206]

Shang S,Jazaeri AA.Chemotherapy-induced distal enhancers drive transcriptional programs to maintain the chemoresistant state in ovarian cancer.Cancer Res2019;79:4599-611 PMCID:PMC6744966

[207]

Biehs B,Piskol R.A cell identity switch allows residual BCC to survive Hedgehog pathway inhibition.Nature2018;562:429-33

[208]

Lai TH,Gasparini P.HDAC1 regulates the chromatin landscape to control transcriptional dependencies in chronic lymphocytic leukemia.Blood Adv2023;7:2897-911 PMCID:PMC10285551

[209]

Nguyen TTT,Shang E.HDAC inhibitors elicit metabolic reprogramming by targeting super-enhancers in glioblastoma models.J Clin Invest2020;130:3699-716 PMCID:PMC7324177

[210]

Gryder BE,Woldemichael GM.Chemical genomics reveals histone deacetylases are required for core regulatory transcription.Nat Commun2019;10:3004 PMCID:PMC6614369

[211]

Di Giorgio E, Benetti R, Kerschbamer E, Xodo L, Brancolini C. Super-enhancer landscape rewiring in cancer: the epigenetic control at distal sites.Int Rev Cell Mol Biol2023;380:97-148

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