Natural Bioactive Compounds Targeting Histone Deacetylases in Human Cancers: Recent Updates
Abstract
:1. Introduction
2. Epigenetic Regulation and Cancer
2.1. Cancer and DNA Methylation
2.2. Oncohistones and Histone Changes
2.2.1. Histone Methylation and Cancer
2.2.2. Histone Acetylation/Deacetylation and Cancer
2.2.3. Phosphorylation, Ubiquitination, SUMOylation, and Cancer
2.2.4. Epigenetic Regulation by miRNAs and Cancer
3. The Role of HDAC in Cancer
3.1. HDAC in Different Cancer Stages
3.1.1. Cell Cycle Progression and Apoptosis
3.1.2. Differentiation
3.1.3. DNA Damage Response
3.1.4. Metastasis
3.1.5. Angiogenesis
3.1.6. Autophagy
4. Natural Bioactive Compounds Targeting HDAC in Human Cancers
4.1. Flavonoids
4.1.1. Epigallocatechin Gallate
4.1.2. Apigenin
4.1.3. Galangin
4.1.4. Genistein
4.1.5. Silibinin and Kaempferol
4.1.6. Quercetin
4.2. Alkaloids
4.3. Terpenoids
4.3.1. Corosolic Acid
4.3.2. Cucurbitacin B
4.3.3. Ursolic Acid
4.4. Fatty Acids
4.4.1. Butyrate
4.4.2. Butyric Acid and Eicosapentaenoic Acid
4.5. Isothiocyanate
4.5.1. Phenethyl Isothiocyanate (PEITC)
4.5.2. Sulforaphane (SFN)
4.6. Quinones
4.6.1. Naphthazarin
4.6.2. Thymoquinone
4.7. Stilbenes
4.7.1. Resveratrol
4.7.2. Curcumin
4.7.3. Calebin-A
4.7.4. Pterostilbene
4.8. Steroids
4.8.1. Guggulsterone
4.8.2. Withaferin A (WFA)
4.9. Phenolic Acids, Secoiridoids, Tannins, and Tanshinones
4.9.1. Phenolic Acids: Caffeic Acid Chlorogenic Acid
4.9.2. Secoiridoids: Oleacein
4.9.3. Secoiridoids: Ellagic Acid
4.9.4. Tanshinones: Tanshinone IIA
4.10. Other Molecules Targeting HDAC in Human Cancers
4.10.1. Arsenic Trioxide
4.10.2. Curcumol
4.10.3. Selenium
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Molecules (Origins) | Used Models | Methods | Key Findings | Ref. |
---|---|---|---|---|
(−)-Epigallocatechin-3-gallate (EGCG) (Purchased) | MCF-7 and MDA-MB-231 (Breast cancer cells) | Flow cytometry (apoptosis assay) RT-PCR and real-time PCR (Quantification of hTERT expression) DNMTs, HDACs, and HATs activity assays ChIP assay Western blot analysis | Inhibited the transcription of hTERT through epigenetic mechanisms in estrogen receptor (ER)-positive MCF-7 and ER-negative MDA-MB-231 cells. Inhibited the activities of DNMT and histone acetyltransferase (HAT). Remodelled the chromatin structures of the hTERT promoter by decreasing the level of acetyl-H3, acetyl-H3K9, and acetyl-H4 in the hTERT promoter. Induced chromatin alterations that facilitated the binding of many hTERT repressors such as MAD1 and E2F-1 to the hTERT regulatory region. | [189] |
(−)-Epigallocatechin-3-gallate (EGCG) (Purchased) | A431 (Human skin cancer) | DNA methylation assay HDAC activity assay Western blot analysis Cell lysates | Decreased global DNA methylation levels in A431 cells in a dose-dependent manner. Decreased the HDAC activity. Increased the levels of acetylated lysine 9 and 14 on histone H3 (H3-Lys 9 and 14) and acetylated lysine 5, 12, and 16 on histone H4. Re-expressed the mRNA and proteins of silenced tumor suppressor genes, p16INK4a and Cip1/p21. | [190] |
(−)-Epigallocatechin-3-gallate (EGCG) (Purchased) | HT-29 and HCT 116 (Human colon cancer cell lines) | Western blot analysis RNA extraction Real-time PCR | Reduced HDAC and DNMT protein expression. Decreased HDAC2 and HDAC3 expressions. Decreased association between UHRF1 and DNMT3. Decreased association between UHRF1 and HDAC3 in only the HCT 116 cell line. | [187] |
(−)-Epigallocatechin-3-gallate (EGCG) (Purchased) | MCF7 and MDA MB 231 (Breast cancer cells) | RT-PCR Western blot analysis | Lowered the protein levels of DNMT1, HDAC1, and MeCP2. | [204] |
(−)-Epigallocatechin-3-gallate (EGCG) (Purchased) | HT29 (Human colon cancer cells) | HDAC enzyme activity Western blot | Inhibited the HDAC activity in intact HT29 cells. Decreased the HDAC1 protein level. | [188] |
(−)-Epigallocatechin-3-gallate (EGCG) (Not reported) | MCF-7 and MDA-MB-231 (Breast cancer cells) | RNA extraction RT PCR ChIP method Western blot analysis | Reduced levels of the enhancer of zeste homolog 2 (EZH2) and Class I HDAC proteins. | [205] |
(−)-Epigallocatechin-3-gallate (EGCG) (Purchased) | CRL-2577, HCT-116 and HT-29HTB-38 cells | Cell viability and apoptosis Real-time quantitative PCR HDAC activity assessment ChIP assay | Combinatorial effects of EGCG and NaB. Increased HDAC1 in RKO CRC cells. Inhibited the HDAC1, DNMT1, and survivin in all the three CRC cells tested. Affected the global DNA methylation. | [206] |
(−)-Epigallocatechin-3-gallate (EGCG) (Purchased) | HeLa cells | HDAC activity assessment Bisulfite modification MS-PCR RT-PCR | Decreased the HDAC activity time-dependently. Zn ion was taken to be the substrate-binding site of HDAC1. | [207] |
(−)-Epigallocatechin-3-gallate (EGCG) (Purchased) | A549/DDP cell line | Cell viability assay MTT assay RT- PCR Total HDAC activity and DNMT activity in vivo experiments | In vitro EGCG + cisplatin (DDP) treatment caused: Inhibition of DNMT and HDAC activities, reversal of hypermethylated status, and downregulation of the expression of GAS1, TIMP4, ICAM1, and WISP2 gene in A549/DDP cells. In vivo EGCG + DDP pre-treatment caused: Inhibition of tumors, a decrease in methylation levels of GAS1, TIMP4, ICAM, and WISP2, and an increase in their expression levels. | [208] |
(−)-Epigallocatechin-3-gallate (EGCG) (Not reported) | APL NB4 and HL-60 cells | RT-qPCR ChIP assay MSP and sequencing Western blot analysis | Downregulated the epigenetic modifiers HDAC1 and HDAC2 Downregulated the polycomb repressive complex 2 (PRC2) core components in gene and protein levels. Reduced gene-binding effect of core components of EZH2, SUZ12, and EED. | [209] |
(−)-Epigallocatechin-3-gallate (EGCG) (Not reported) | DUPRO and LNCaP (prostate cells) | RNA extraction RT– semi q-PCR Western blot analysis ChIP assay HDAC enzyme activity | Reduced the expression of both EZH2 enhancers and its catalytic product trimethylation of H3. Increased acetylation of histone H3K9/18. Reduced the activity of Class I HDACs, as well as EZH2 and H3K27me3 levels. | [210] |
(−)-Epigallocatechin-3-gallate (EGCG) (Not reported) | HMEC-1 and HUVECs cells | Cell proliferation assay RNA isolation Reverse transcription and RT- PCR Western blot analysis HDAC Activity Assay | Increased histone acetylation (H3K9/14ac, H3ac), as well as methylation of both active (H3K4me3) and repressive (H3K9me3) chromatin. Inhibited HDAC activity in both cellular and cell-free models. Altered epigenome modulator expression and activity (HDAC5 and 7, p300, CREBP, LSD1 or KMT2A). | [191] |
(−)-Epigallocatechin-3-gallate (EGCG) (Purchased) | Breast cancer cells | RNA extraction Protein extraction qRT-PCR Western blot analysis ChIP assay HDAC activity HMT (H3K27me3) activity | Induced changes in histone modifications. Resulted in an increased apoptosis. | [211] |
Delphinidin (Purchased) | JB6 P+ (Mouse epidermal cells) HepG2–C8 (hepatocellular cancer cells) | Western blot Quantitative real-time PCR Bisulfite genomic sequencing | Reduced DNMTs and HDACs protein expression. | [212] |
Apigenin (Purchased) | Human prostate cancer cell lines 22Rv1 and PC-3 (prostate cancer cells) | HDAC activity assessment RNA isolation RT-PCR and q-PCR Western blot analysis ChIP assay Tumor xenograft studies | Inhibited Class I HDACs in prostate cancer cells. Inhibited HDAC enzyme activity, particularly HDAC1 and HDAC3. Induced histone acetylation. Increased p21/waf1 protein and mRNA expression, as well as p21/waf1 mRNA expression. Reduced (in vivo) tumor development, HDAC activity, HDAC1, and HDAC3 protein expression. | [192] |
Apigenin (Purchased) | JB6 P+ (Skin cells) | RT-PCR Western blot analysis | Reduced some HDACs (1–8) and their expression levels. | [213] |
Apigenin (Purchased) | MDA-MB-231 (breast cancer cells) | Immunoblot analysis HDAC assay Nuclear extract preparation ChIP assay | Inhibited HDAC activity. Induced acetylation of histone H3. Increased the acetylation of histone. | [193] |
Galangin (Purchased) | Neuroblastoma cells | Flow cytometry ELISA RT-PCR and qPCR Western blot analysis ChIP assay DNA methylation analysis | Reduced the BACE1 at mRNA and protein levels. Reduced acetylated H3 in BACE1 promoter areas by increasing endogenous HDAC1-mediated deacetylation. | [194] |
Genistein (Purchased) | Human esophageal squamous cell carcinoma cell lines KYSE 510 and KYSE 150 cancer cells | Modification by bisulfite Methylation-specific PCR RT-PCR | Reversed DNA hypermethylation. Reactivated RARβ, p16INK4a, and MGMT in KYSE 510 cells. Reversed DNA hypermethylation and reactivated RARβ in KYSE 150 cells and prostate cancer LNCaP and PC3 cells. Activated RARβ. Inhibited the activity of HDAC. | [195] |
Genistein (Purchased) | MCF7 and MDA MB 231 (Breast cells) | Bisulfite conversion RT-PCR Western blot | Reduced HDAC1 and MeCP2 protein levels. | [204] |
Genistein (Purchased) | A498, ACHN, HEK-293 and HK-2 cells | RT-PCR Sodium bisulfite modification and sequencing HAT and HDAC analysis | Increased HAT activity and reduced HDAC activity. | [205] |
Genistein (Purchased) | LNCaP, PC3, and RWPE-1 (Prostate cells) | Quantitative RT-PCR Sodium bisulfite modification and sequencing ChIP analysis HAT and HDAC analysis | Increased the levels of acetylated histones 3, 4, histone three dimethylated at lysine 4, histone 3 trimethylated at lysine 4, and RNA polymerase II. Decreased DNA methyltransferase and methyl-binding domain protein 2 activity. Increased HAT activity. | [196] |
Genistein (Purchased) | HT29 (colon cancer cells) | HDAC enzyme activity Western blot analysis | Inhibited HDAC activity in intact HT29 cells. Reduced HDAC1 protein levels. | [188] |
Genistein (Purchased) | MCF-7, MDA-MB-231, and MDA-MB-157, HMECs cells, and two mouse models | MTT assay RT-PCR ChIP assay | Reduced the activity of HDAC, alone or in combination with TSA. Reduced binding to the ERα promoter, as well as gene expression for HDACs. Reduced HDAC1 protein and mRNA expression in both animal models studied. | [197] |
Genistein (Purchased) | Rat colon tissues | RNA isolation qPCR analysis ChIP analysis Bisulfite sequencing | In the post-AOM phase, there was a decrease in H3Ac at the promoter of Wnt5a, Sfrp5, and Sfrp2. Repressed histone H3 lysine 9 methylation and serine 10 phosphorylation at the promoters of Sfrp2, Sfrp5, and Wnt5a in the post-AOM period. In the post-AOM period, the nuclear level of HDAC3 protein was increased. After AOM induction, H3Ac was reduced in the same region of the Sfrp5 promoter. | [198] |
Genistein (Purchased) | MCF-7 and MDA-MB-231 cells | HDAC activity assay HMT activity | Inhibition of HDAC and HMT by GEN + SFN. Downregulation of HDAC2 and HDAC3 levels at the mRNA and protein levels. GEN + SFN downregulated the hTERT levels. | [214] |
Genistein (Purchased) | Human cervical cancer cells | DNMT and HDAC activity analysis In silico studies in the post-AOM period | Reduced the expression of HDAC and enzymatic activity in a time-dependent manner. Interacted with members of the DNMT and HDAC families. Reversed the tumor suppressor genes’ promoter region methylation, and their expression was restored. | [215] |
Genistein (Purchased) | HeLa cells | qPCR HDAC activity assay HMT-H3K9 activity Global DNA methylation | Altered HDACs, HMTs, demethylases, and histone phosphorylases’ expression. Reduced HDAC and HMT activity, as well as global DNA methylation levels. | [203] |
Kaempferol (Not reported) | HepG2, Hep3B, and HCT-116 cells | In silico docking analysis HDACi screening assay HDAC inhibition profiling Immunoblotting Real-time cell monitoring | Inhibited the activity of HDAC. Induced hyperacetylation of histone complex H3. Reduced cell viability and proliferation rate. | [201] |
Luteolin (Purchased) | MDA-MB231-1833, LNM35, HT29, HepG2, and MCF7/6 cells | HDAC assay and histone acetylation levels | Inhibited HDAC activity. | [216] |
Luteolin (Purchased) | HCT116 (Colorectal cells) | HDAC activity assay | Reduced levels of HDAC protein and enzyme activity. | [217] |
Pectolinarigenin (Purchased) | 143B, HOS, and MG63 (Osteosarcoma) | Western blot analysis RT-PCR ChIP assay MTS cell viability assay | Disrupted the development of the STAT3/DNMT1/HDAC1 complex. Caused an increase in SHP-1 expression in osteosarcoma. | [218] |
Pelargonidin (Purchased) | Skin epidermal JB6 (JB6 P+) cells | Western blot analysis RT-PCR Bisulfite genomic sequencing | Reduced protein levels of genes encoding HDACs. | [219] |
Silibinin (Not reported) | H1299 cells | HDAC activity RT- RT-PCR assay | Reduced the activity of HDAC in a dose-dependent manner. Reduced HDAC1, HDAC2, and HDAC3 protein levels, whereas HDAC1, HDAC6, SET domain proteins (SETD1A, D4, D6) and lysine-specific demethylases were upregulated (KDM 5B, 5C, 4A). | [199] |
Silibinin (Purchased) | SW480 and SW620 (Colon cells) | HDAC activity | No effect on the activity of HDACs. | [220] |
Silibinin (Purchased) | DU145 and PC3 (Prostate cells) | Western blot analysis RT-PCR HDACs assay | Reduced HDAC1-2 expression levels in a concentration-dependent manner. | [200] |
Taxifolin (Purchased) | HepG2 cells, skin epidermal JB6 P+ cells, and HepG2-C8 cells | Western blot analysis RNA extraction qRT-PCR assay Bisulfite genomic sequencing | Inhibited DNMT and HDAC protein expression. | [221] |
Quercetin (Purchased) | HL-60 (leukemia cells) | Western blot analysis RT-PCR HDAC assay HAT assay ChIP assay | Increased histone H3 acetylation, which promoted the production of FasL Activated HAT and inhibited HDAC. | [202] |
Quercetin (Purchased) | Hamster buccal pouch (HBP) carcinomas | Immunohistochemistry Western blot analysis RT-PCR | Inhibited HDAC-1 and DNMT1 activities. | [222] |
Quercetin (Purchased) | Eca9706 cells | MTT assay Immunoblotting MSP of p16INK4a gene promoter | Reduced the reverse expressions of global HDAC1. Quercetin + butyrate displayed a reverse effect targeting both altered DNA methylation and histone acetylation, acting as HDAC inhibitor mediated via epigenetic-NF-κB cascade signaling. | [223] |
Quercetin (Purchased) | HeLa cells | DNMT and HDAC activity assay HMT-H3K9 activity assay Molecular modeling qRT-PCR | Reduced the activity of HDAC activity. Reduced the activation of HMT-H3K9. Modified the expression of many chromatin modifiers, and lowered the activity of HDACs and HMTs. Several DNMTs and HDACs interacted with residues in their catalytic cavities (as a competitive inhibitor). | [203] |
Molecules (Origins) | Used Models | Methods | Key Findings | Ref. |
---|---|---|---|---|
Berberine (BBR) (Purchased) | U266, KG1-α, and HL-60 cells | Molecular Docking Growth inhibition assessment RT-PCR Western blot analysis | Affected the enzymes involved in histone acetylation and methylation. Induced cytotoxicity and apoptosis in HL-60/ADR and KG1-α cells. Upregulated histone acetyltransferase CREBBP and EP300, histone deacetylase SIRT3, histone demethylase KDM6A, as well as histone methyltransferase SETD7. Downregulated histone acetyltransferase HDAC8, histone methyltransferase WHSC1I, WHSC1II, and SMYD3. | [224] |
Isofistularin-3 (Iso-3) (Aplysina aerophoba) | RAJI, U-937, JURKAT, K-562, HL-60, MEG-01, cells | HDAC activity assessment Molecular docking study Western blot analysis | Modified the aryl hydrocarbon receptor (AHR) promoter methylation and increased the AHR expression in RAJI cells. | [225] |
Nicotinamide (NA) (Purchased) | Female mice skin | RT-PCR DNA bisulfite modification Western blot analysis | Downregulated the miR-203 levels at 16 weeks. Upregulated the HDAC, DNMT, and promoter methylation of miR-203 at 4 or 16 weeks. Prevented changed gene expression. | [226] |
Trichostatin A (TSA) (Purchased) | PANC-1, CAPAN (1 and 2), and KATO-III cells | RT-PCR siRNA Western blot analysis ChIP assay | TSA + 5-aza increased MUC4 expression in a cell-specific manner. MUC4 silencing was directly engaged by HDAC3, HDAC1, DNMT3B, and DNMT3A binding to its 5′-UTR in a cell-specific manner. Inhibited the histone deacetylation, associated with strong MUC4 repression in high-expressing cells | [227] |
Psammaplin (Jaspis sp. and Poecillastra wondoensis) | Ishikawa cancer cells | RT-PCR Western blot analysis | Induced accumulation of acetylated histones and reduced HDAC levels. Upregulated cyclin-dependent kinase inhibitor expression. | [228] |
Psammaplin (Pseudoceratina purpurea) | A549, MCF7, and W138 cells | HDAC Assay Immunoblotting | Inhibited HDAC1 activity. Exhibited significant cytotoxicity in A549, MCF7, and W138 cells. Increased acetylation of histones. | [229] |
Psammaplin (Pseudoceratina purpurea) | In vitro enzymatic assays | Cell proliferation assessment HDAC enzyme activity | Inhibited HDAC effectively. Induced weak cytotoxicity. | [230] |
TSA (Purchased) | MCF-7, MDA-MB-231, and MDA-MB-157 cells and mouse models | RT-PCR assay Western blot analysis ChIP assay | Reduced the activity of HDAC, either alone or in conjunction with GEN. | [197] |
TSA (Purchased) | SKOV3 (Ovarian cells) | Western blot analysis Histone immunoblots assay | TSA + decitabine reduced the DNMT and HDAC activities. TSA + decitabine increased acetylation of histone H3 and H4. TSA + decitabine inhibited the expression of lysine-specific demethylase-1. TSA + decitabine increased the transcription activity marker dimethylated-H3K4, while suppressing dimethylated-H3K9. | [231] |
Molecules (Origins) | Used Models | Methods | Key Findings | Ref. |
---|---|---|---|---|
Corosolic acid (Purchased) | TRAMP-C1 cells | RT-PCR DNA extraction HDAC activity assessment ChIP assay Western blot analysis | Increased the acetylation of histone H3 lysine 27 (H3K27ac). Reduced trimethylation of histone H3 lysine 27 (H3K27Me3) in the Nrf2 promoter region. Reduced the expression and activity of epigenetically modifying enzymes in TRAMP-C1 cells. | [232] |
Cucurbitacin B (L. graveolense Roxb.) | NSCLC cells | RT-PCR Western blot analysis HDAC activity Immunohistochemical staining | Altered histone modifications. | [233] |
Parthenolide (PTL) (Purchased) | ZR-75-1 and 293T cells | RT-PCR HDAC activity Western blot analysis ChIP assay | Depleted HDAC1 protein, without affecting Class I/II HDAC proteins. HDAC1 depletion and cell death were promoted by the mutant DNA-damage transducer ataxia telangiectasia. | [236] |
Parthenolide (PTL) (Purchased) | AML cells | Methylcellulose colony-forming Western blot analysis Flow cytometry | HDAC induced apoptosis was prevented in multiple human AML cells. Increased HDAC-induced lethality. PTL + HDACis caused apoptosis in MLL-ENL cells. PTL + HDACis triggered SAPK/JNK activation. | [237] |
Parthenolide (PTL) (Not reported) | JB6 cells | Western blot analysis ChIP method RT-PCR siRNA transfection HDAC activity | Modulated gene expression. | [238] |
Parthenolide (PTL) (Purchased) | MDA-MB231 cell line | Cell viability assessment ROS and GSH analysis Western blot analysis | PTL + HDACi induced GSH depletion, Cyt c release, activation of caspase 3 and apoptosis. PTL + HDACi sustained both HDACi-induced hyperacetylation of histones H3 and H4 and PTL-induced downregulation of DNMT1 expression PTL + HDACi boosted PTL’s cytotoxic impact. | [239] |
Ursolic acid (Purchased) | JB6 P+ cells | qPCR Western blot analysis HDAC activity assay | Reduced the expression of HDAC1, 2, 3, and 8 (Class I) enzymes and the activity of HDAC6 and 7 (Class II). | [240] |
Ursolic acid (Purchased) | Male Sprague-Dawley rats | mRNA expression measurement qPCR Development of PK/PD model | Inhibited the induction of epigenetic markers in leukocytes. | [232] |
Z-Ligustilide (LIG) (Purchased) | HS578t, MDA-MB-231 and MDA-MB-453 cells | Western blot analysis Luciferase assay ChIP assay Immunoprecipitation | Increased Ace-H3 (lys9/14) enrichment in the ER promoter. Downregulated the HDAC activity. | [241] |
Molecules (Origins) | Used Models | Methods | Key Findings | Ref. |
---|---|---|---|---|
Butyrate (Purchased) | Eca9706 cells | MTT assay Immunoblotting Methylation-specific PCR | Inhibited the development of human oesophageal cancer cells. Reduced NF-Bp65, DNMT1, HDAC1, and Cyclin D1 reverse expression. Increased caspase-3 and p16INK4 expression. Butyrate + quercetin acted as HDAC inhibitors through epigenetic-NF-κB cascade signaling. | [223] |
Butyrate (Purchased) | CRL-2577, HT-29, and HCT-116 cells | HDAC activity assessment CpG methylation ChIP assay | Inhibited survivin, DNMT1, and HDAC1. Affected chromatin structure and global DNA methylation. | [206] |
Butyric acid (Purchased) | Female mice skin | Bisulfite modification of DNA RT-PCR assay | Decreased miR-203 expression. Upregulated the methylation of DNMT, HDAC, and miR-203. | [226] |
Eicosapentaenoic acid (EPA) (Purchased) | McRH-7777 cells | Flow cytometry qRT-PCR Immunoblot analysis ChIP method | Reduced HDAC1 and DNMT activity and expression. Promoted tumor suppressor gene expression. Activated PPAR by inhibiting HDAC1 expression in hepatocarcinoma cells. Re-expressed the tumor suppressor gene Hic-1 in response to EPA-bound PPAR. | [243] |
Molecules (Origins) | Used Models | Methods | Key Finding | Ref. |
---|---|---|---|---|
Isothiocyanate | ||||
Phenethyl isothiocyanate (PEITC) (Not reported) | HCT116, SW480, and SW620 cells | Cell viability Western blot analysis Quantitative RT-PCR | Induced stable changes in the expression profile of epigenetic erasers/writers. Induced hypomethylation of PcG target genes, which are generally hypermethylated in cancer. | [244] |
Phenethyl isothiocyanate (PEITC) (Purchased) | HT29 (Colon cells) | Determination of HDAC1 levels | PEITC + LA reduced the amount of aberrant crypt foci, as well as DNMT1 and HDAC1 levels (in vivo). | [245] |
Sulforaphane (SFN) (Not reported) | MCF-7 and MDA-MB-231 | RT-PCR Western blot analysis HDAC and HAT activity Bisulfite sequencing analysis ChIP method | Inhibited hTERT in both cells. Reduced the trimethyl-H3K9 and trimethyl-H3K27 in active chromatin indicators in a dose-dependent manner. | [189] |
Sulforaphane (SFN) (Purchased) | HeLa cells | DNMT and HDAC activity assessment Molecular docking study Bisulfite Modification and MSP RT-PCR | Inhibited the activity of HDAC. Lowered the HDAC1 expression. Reactivated RAR, CDH1, DAPK1, and GSTP1 genes or elevated their expression. | [207] |
Sulforaphane (SFN) (Purchased) | A549 and H1299 (Lungs cells) | HDAC activity assay qRT-PCR Tumor xenografts | Inhibited the activity of HDAC in lung cancer cells. Increased histone (H4 and H3) acetylation. Suppressed the activity of HDAC in vivo. | [249] |
Sulforaphane (SFN) (Purchased) | MCF-7 and MDA-MB-231 | HDACs activity assay | SFN + WA decreased HDAC expression. | [250] |
Sulforaphane (SFN) (Purchased) | A549, HEK293, HT29 cells | Bisulfite genome sequencing RT-PCR Western blot analysis ChIP method HDAC and DNMT activity assessment | Reduced CpG methylation in the miR-9-3 promoter region. Increased H3K4me1 enrichment at the miR-9-3 promoter. Induced the expression of miR-9-3. Reduced the epigenetic modifying enzymes’ expression and activity. | [251] |
Sulforaphane (SFN) (Purchased) | Breast cancer cells | RT-PCR Western blot analysis HDACs activity Global histone H3 acetylation quantification RNA sequencing analysis | Increased gene transcription in tumor suppressor genes. Decreased the expression of tumor promoting genes. Decreased HDAC1 gene expression and enzymatic activity. Increased levels of histone acetylation. | [252] |
Sulforaphane (SFN) (Purchased) | HCT116 and RKO (Colon cells) | RT-PCR Western blot analysis HDAC activity | Reduced the oncogenic hTERT mRNA, HDAC, miR-21, protein, and enzyme levels. | [253] |
Sulforaphane (SFN) (Purchased) | MCF-7 and MDA-MB-231 | RT-PCR Western blot analysis HDAC activity | SFN + GEN suppressed HDAC and HMT. SFN + GEN inhibited the expression of hTERT. | [214] |
Sulforaphane (SFN) (Not reported) | HepG2 and GAS cells | RNA-Seq analysis | Inhibited HDAC activity Downregulated chromatin profile regulating enzymes. | [254] |
Sulforaphane (SFN) (Purchased) | HepG2 cells | RNA extraction RNA-Seq analysis | Inhibited HDAC activity. Methylation of oncogenic TF binding site motifs affected its activity. | [249] |
Quinones | ||||
Laccaic acid (LA) (Purchased) | HT29 cells | HDAC activity assay | LA + PEITC reduced HDAC1 expression levels (in vivo). | [255] |
Naphthazarin (Naph) (Purchased) | MCF-7 cells | RT-PCR Western blot analysis ChIP method | Activated the p21 promoter by Naph + IR, by inhibiting the binding of multi-domain proteins. | [256] |
Thymoquinone (Purchased) | JK cell line and MDA-MB-468 cells | Gene analysis RT-PCR analysis | Downregulated numerous major epigenetic factors. | [257] |
Carotenoid | ||||
Astaxanthin (Purchased) | LNCaP cells | Cell viability test HDAC activity assay | Inhibited HDAC activity in vitro. | [258] |
Stilbenes | ||||
Resveratrol (RSV) (Purchased) | MDA MB 231 and MCF7 | Bisulfite conversion RT-PCR Western blot analysis | Decreased HDAC1 protein levels. | |
Resveratrol (RSV) (Purchased) | HeLa, SiHa, and Caski cervical cells | Promoter methylation analysis Transient silencing of UHRF1 | Induced PAX1 reactivation via its effect on HDAC, which is mediated through the downregulation of UHRF1, which may affect both histone acetylation and DNA methylation. | [259] |
Resveratrol (RSV) (Not reported) | B16F10 and Tumor-bearing mouse model | Western blot analysis Luciferase reporter assays Bisulfite sequencing PCR ChIP assay | HDAC1 was recruited to the focal adhesion kinase (FAK) promoter region. | [260] |
Resveratrol (RSV) (Purchased) | MDA-MB-231 and MCF-7 cells | MTT assay Clonogenic method HDAC activity | Reduced HDAC activity. | [261] |
Curcumin (Cur) (Purchased) | Hep3B cells | Histone purification Histone acetylation assay Western blot analysis HAT assay HDAC assay RT-PCR | Inhibited histone acetylation in the presence or absence of TSA. Inhibited the activity of HAT both in vitro and in vivo. Induced histone hypoacetylation in vivo. | [262] |
Curcumin (Cur) (Purchased) | Raji cells | Immunocytochemistry analysis Western blot analysis | Reduced HDAC1, HDAC3, and HDAC8 protein expression levels. Increased Ac-histone H4 protein expression. | [263] |
Curcumin (Cur) (Purchased) | Raji cells | MTT assay Western blot analysis RT-PCR | Decreased the amounts of HDAC3, HDAC1, and p300. Reversed the protection degradation of p300 and HDAC1 by MG-132. | [264] |
Curcumin (Cur) (Purchased) | Hela cells | HDAC activity assessment | Inhibited the HDAC activity (IC50 = 115 μM). | [265] |
Curcumin (Cur) (Purchased) | DAOY, D283 Med, and D341 Med (medulloblastoma) | HDAC activity In vivo medulloblastoma xenografts | Reduced the HDAC4 activity and expression. Increased tubulin acetylation. | [266] |
Curcumin (Cur) (Purchased) | LNCaP cells | Western blot analysis DNA extraction and bisulfite genomic sequencing PCR array RNA isolation and RT-PCR ChIP assay Histone H3 methylated lys27 ELISA HDAC activity assay | Altered HDAC expression. Increased the expression of HDAC1, 4, 5, and 8, but decreased the HDAC3. Decreased HDAC activity. Decreased H3K27me3 enrichment at the Neurog1 promoter region and at the global level. | [267] |
Curcumin (Cur) (Purchased) | MCF7 and MDA MB 231 | Bisulfite conversion and MSP RT-PCR Western blot analysis | Decreased protein levels of HDAC1. | |
Curcumin (Cur) (Purchased) | HeLa, SiHa, and Caski cells | MTT assay Quantitative expression of PAX1, UHRF1, and p21 PAX1 promoter methylation analysis Transient silencing of UHRF1 | Induced reactivation of PAX1, due to its effect on HDAC. | [259] |
Calebin-A (Not reported) | MPNST cells | Cell proliferation Western blot analysis Flow cytometry ChIP assay | Reduced the expression of acetyl H3 proteins. | [268] |
Pterostilbene (PTS) (Purchased) | MDA-MB-157, HCC1806, and MCF10A | RT-PCR Western blot analysis SIRT activity assay DNMT activity | RSV + PTS downregulated the SIRT1 (a type III HDAC). | [269] |
Steroids | ||||
Guggulsterone (Purchased) | Breast cancer cells | Bisulfite conversion and MSP RT-PCR Western blot analysis | Decreased protein levels of HDAC1. | |
Withaferin A (WA) (Purchased) | Breast cancer cells | Bisulfite conversion and MSP RT-PCR Western blot analysis | Decreased HDAC1 and MeCP2 protein levels. | |
Withaferin A (WA) (Purchased) | Breast cancer cells | qRT-PCR Western blot analysis HDAC activity | WA + SFN decreased the HDAC activity and expression. | [250] |
Phenolic acids | ||||
Chlorogenic acid (Purchased) | Breast cancer cells | In vitro HDAC inhibition | Inhibited the HDAC activity (IC50 = 375 μM). | [265] |
Caffeic acid (Purchased) | Breast cancer cells | In vitro HDAC inhibition | Moderately inhibited the HDAC activity (IC50 = 2.54 mM). | [265] |
Secoiridoids | ||||
Oleacein (Olea europaea L.) | U266, NCI-H929, RPMI-8226, MM1s, and JJN3 cells | Western blot analysis qRT-PCR HDAC activity | Accumulated α-tubulin and acetylated histones. Downregulated multiple Class I/II HDACs. Inhibited HDACs with downregulation of Sp1. | [270] |
Tannins | ||||
Ellagic acid (EA) (Purchased) | hASCs cells | qPCR Western blot analysis HDAC activity Immunocytochemistry of H3R17me2 and HDAC9 | Inhibited HDAC 9 downregulation. Reduced the histone acetylation levels. | [271] |
Tanshinone | ||||
Tanshinone IIA (Purchased) | HepG2-C8, JB6 P+, JB6-shNrf2 cells | Luciferase reporter activity assay RNA extraction and qRT-PCR Western blot analysis HDAC activity Bisulfite sequencing ChIP method | Inhibited HDAC activity. | [272] |
Others natural compounds | ||||
Arsenic trioxide (AS2O3) (Purchased) | HeLa or HEK293T cells | Luciferase reporter assay RT-PCR ChIP method Flow cytometry | Reduced global histone through direct binding. Increased HDAC4 expression. Inhibited the hMOF activity. | [273] |
Calcium glucarate (CAG) (Purchased) | Female mice cells | RT-PCR Bisulfite sequencing assay Western blot analysis | Downregulated the levels of miR-203 Upregulated DNMT, HDAC, and promoter methylation of miR-203. | [226] |
Proanthocyanidins (GSPs) | Breast cancer cells | Western blot analysis HDAC activity | Reduced HDAC activity. | [261] |
Curcumol (Not reported) | CSLCs cells | qRT-PCR Western blot analysis Global DNA methylation HDAC activity Xenograft tumorigenicity assay Immunohistochemistry | Blocked DNMT/HDAC activity and CSLC self-renewal in vivo and in vitro. Affected CLSCs by HDAC regulation. | [274] |
Selenium (Se) (Not reported) | LNCaP cells | HDAC activity | Reduced HDAC activity. No alteration of mRNA and protein levels of HDACs. Reduced methylated histone H3 on lysine 9 (H3-K9) levels. Increased acetylated H3-K9 levels. | [275] |
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Bouyahya, A.; El Hachlafi, N.; Aanniz, T.; Bourais, I.; Mechchate, H.; Benali, T.; Shariati, M.A.; Burkov, P.; Lorenzo, J.M.; Wilairatana, P.; et al. Natural Bioactive Compounds Targeting Histone Deacetylases in Human Cancers: Recent Updates. Molecules 2022, 27, 2568. https://doi.org/10.3390/molecules27082568
Bouyahya A, El Hachlafi N, Aanniz T, Bourais I, Mechchate H, Benali T, Shariati MA, Burkov P, Lorenzo JM, Wilairatana P, et al. Natural Bioactive Compounds Targeting Histone Deacetylases in Human Cancers: Recent Updates. Molecules. 2022; 27(8):2568. https://doi.org/10.3390/molecules27082568
Chicago/Turabian StyleBouyahya, Abdelhakim, Naoufal El Hachlafi, Tarik Aanniz, Ilhame Bourais, Hamza Mechchate, Taoufiq Benali, Mohammad Ali Shariati, Pavel Burkov, José M. Lorenzo, Polrat Wilairatana, and et al. 2022. "Natural Bioactive Compounds Targeting Histone Deacetylases in Human Cancers: Recent Updates" Molecules 27, no. 8: 2568. https://doi.org/10.3390/molecules27082568