Role of Histone Deacetylases in the Pathogenesis of Salivary Gland Tumors and Therapeutic Targeting Options
Abstract
:1. Introduction
2. Molecular Aspects of SGT Pathology
2.1. Genetic Changes in SGTs
Tumor Behavior | Tumor Type | Genetic Aberration | Prevalence | Clinical Course |
---|---|---|---|---|
Malignant | MECs | MECT1/MAML2 fusions | 40–80% | Favorable prognosis [25] |
CRTC3/MAML2 fusions | 6%/younger ages | Favorable prognosis [24] | ||
AdCCs | MYB/NFIB gene fusions | 50% | Unfavorable prognosis [25] | |
AciCCs | HTN3/MSANTD3 fusions | <5% | Indolent course [26] | |
MSANTD3 aberrations | 4–15% | |||
MASCs | ETV6/NTRK3 fusions | Majority | Favorable prognosis [34] | |
(Hyalinizing) CCCs | EWSR1/ATF1 fusions | 93% | Indolent course [35] | |
EWSR1 rearrangement | 82% | |||
Intraductal carcinoma | NCOA4-RET | 35% | Mean OS: 5 years [36] | |
TRIM27-RET | ~10% | Aggressive/apocrine variant [36] | ||
Microsecretory adenocarcinoma | MEF2C-SS18 fusion | Majority | Malignant nature [37] | |
PAC and CASG | PRKD1/2/3 translocations or mutations | PRKD1/2/3 fusions: 13% of PACs; PRKD1 mutations: 56–73% PACs | Indolent course [38] | |
PRKD1/2/3 fusions: 43–80% CASGs; PRKD1 mutations: 20% CASGs | ||||
BCAC | PIK3CA mutations | ~10–30% | Unfavorable prognosis [39,40] | |
CAexPA | PLAG1/HMGA2 fusions | 36% | Indolent course [41] | |
Benign | PAs | PLAG1 translocations | 50% | Indolent course [42] |
HMGA2 translocations | 34–40% | |||
BCA | CTNNB1 mutations | 60% | Indolent course [43] |
2.2. Epigenetic Changes in SGTs
SG Entity | Aberration Form | Related Molecule | References |
---|---|---|---|
AdCCs | ↑ methylation | EN1, RASSF1A, RECK, Stratifin (14-3-3 s), RUNX3 | [63,66,83,84,85] |
↓ methylation | SBSN, AQP1 | [65] | |
↑ Promoter methylation | E-cadherin, RASSF1A, RARb2 | [54,59,67,86] | |
Histone trimethylation | H3K9me3 | [64,87] | |
↑ acetylation | H3K9Ac, H3K18Ac | [71,88] | |
miR-17-92 ↑regulation | miR-17/-20a | [81] | |
MECs | Aberrant expression of ncRNAs | NONHSAT154433.1, has-circ-0012342 | [76,82] |
↑ methylation | RUNX3, H3K9Me3 | [52,85,88] | |
↑ acetylation | H3K9Ac, H3K18Ac | [71,88] | |
SDCs | ↑ methylation | GALR-1/-2 | [56] |
↑ Promoter methylation | RASSF1A, RARb2, | [67] | |
PAs | Dysregulated expression (PLAG1 gene related) | 9110 lncRNAs/7750 mRNAs | [80] |
CAexPA | ↑ Promoter methylation | CDH1 (E-cadherin) | [49,89] |
ACCs | ↑ Promoter methylation | RASSF1A, RARb2 | [67] |
3. Role of Histone Deacetylation in SGTs
3.1. Biochemical and Functional Aspects of Histone Acetylation/Deacetylation
3.2. Role of HDACs in Different SGT Types
4. Targeting Options of HDACis in SGTs
4.1. HDAC Inhibition
4.1.1. HDACis in Mucoepidermoid Carcinoma (MEC)
4.1.2. HDACis in Adenoid Cystic Carcinoma (AdCC)
4.1.3. HDACis in Salivary Gland Ductal Adenocarcinoma (SGDA)
4.2. Phase-I Clinical Studies of HDACis in SGTs
4.2.1. Vorinostat in a Phase I Study
4.2.2. KA2507 Selective HDAC6 Inhibitor
4.3. Phase-II Trials of HDACis in SGTs
4.3.1. SAHA Treatment in AdCC
4.3.2. Combination of Pembrolizumab and Vorinostat in SGTs
5. Conclusions—Outlook
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
References
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Salivary Carcinomas Not Otherwise Specified (NOS) and Emerging Entities | Malignant Epithelial Tumors |
---|---|
Large-cell neuroendocrine carcinoma | Acinic cell carcinoma |
Lymphoepithelial carcinoma | Adenoid cystic carcinoma |
Oncocytic carcinoma | Basal cell adenocarcinoma |
Small-cell neuroendocrine carcinoma | Carcinoma ex pleomorphic adenoma |
Squamous cell carcinoma | Carcinosarcoma |
Undifferentiated carcinoma | Clear cell carcinoma |
Benign Epithelial Tumors | Epithelial–myoepithelial carcinoma |
Basal cell adenoma | Intraductal carcinoma |
Cystadenoma | Microsecretory adenocarcinoma * |
Ductal papillomas | Mucinous adenocarcinoma * |
Intercalated duct adenoma * | Mucoepidermoid carcinoma |
Keratocystoma * | Myoepithelial carcinoma |
Lymphadenoma | Polymorphous adenocarcinoma |
Myoepithelioma | Salivary duct carcinoma |
Oncocytoma | Sclerosing microcystic adenocarcinoma * |
Pleomorphic adenoma | Sebaceous adenocarcinoma |
Sclerosing polycystic adenoma * | Secretory carcinoma |
Sialadenoma papilliferum | Uncertain Malignant Potentiality |
Striated duct adenoma * | Sialoblastoma |
Warthin tumor |
HDAC Class | Subtypes | Cellular Location | Substrate Specificity | Functions and Targets |
---|---|---|---|---|
Class-I | HDAC1, HDAC2, HDAC3, HDAC8 | Nucleus | All four core histones (HDAC1,2); H3, H4 (HDAC8) | Gene repression; Cell-cycle regulation; Apoptosis; DNA repair [93] |
Class-IIa | HDAC4, HDAC5, HDAC7, HDAC9 | Nucleus and Cytoplasm | All four core histones (HDAC4,5) | Cell differentiation; Apoptosis; Angiogenesis; Response to external signals [94] |
Class-IIb | HDAC6, HDAC10 | Cytoplasm (HDAC6); Nucleus (HDAC10) | H3K9, H3K56, α-tubulin (HDAC6); Polyamine catabolism (HDAC10) | Regulation of microtubule stability; Aggresome formation [94] |
Class-III | SIRT1, SIRT2 | Nucleus and Cytoplasm | H4K16, H3K9 (SIRT1); H4K16, H3K56 (SIRT2) | Aging; Metabolism; DNA repair; Stress resistance [93] |
SIRT3, SIRT4, SIRT5 | Mitochondria | H4K16 (SIRT3); Mitochondrial metabolism (SIRT4,5) | Energy homeostasis; Oxidative stress response [93] | |
SIRT6, SIRT7 | Nucleus (SIRT6); Nucleolus (SIRT7) | H3K9, H3K56 (SIRT6); H3K18 (SIRT7) | Genome stability; Ribosome biogenesis [93] | |
Class-IV | HDAC11 | Nucleus and Cytoplasm | H3K9, H3K14 | DNA replication regulation; Immune regulation [93] |
Categorization | Study Type/Method | HDAC Type | Expression Rate | Reference |
---|---|---|---|---|
HN malignancies | Tissue sections (FFPE)/IHC | HDAC2, -9, -10 | ~100% | [107] |
SIRT3, -5, -6, -7 | ~100% | [107] | ||
HDAC1, SIRT1 | ~75% | [107] | ||
SGTs | Tissue sections (FFPE)/IHC | HDAC1 | Benign SGTs: 30% | [110] |
Malignant SGTs: 14% | [110] | |||
Tissue sections (FFPE)/IHC | HDAC2 | Benign SGTs: 86% | [110] | |
Malignant SGTs: 82% | [110] | |||
Tissue sections (FFPE)/IHC | HDAC4 | Benign SGTs: 44% | [110] | |
Malignant SGTs: 36% | [110] | |||
Tissue sections (FFPE)/IHC | HDAC6 | Benign SGTs: 11% | [110] | |
Malignant SGTs: 18% | [110] |
Type of Salivary Gland Malignancy | Substance | Main Outcome | Reference |
---|---|---|---|
MEC (cell line) | Apicidin (HDACi) | ↓ proliferative potential | [143,144] |
MEC (cell line) | Vorinostat (HDACi) | ↓ cancer stem cell population | [145] |
Vorinostat (HDACi) + cisplatin | ↑ sensitivity to cisplatin | ||
AdCC (cell line) Mice transplanted with tumor cells | Vorinostat (HDACi) | ↓ population of cancer cells and stem cells | [146] |
Vorinostat (HDACi) + cisplatin | Further ↓ cancer stem cell population | ||
AdCC (cell line) | Chidamide (HDACi) | ↓ proliferative potential | [113] |
Chidamide (HDACi) + cisplatin | Cell cycle arrest | ||
MEC (cell line) | Vorinostat (HDACi) | ↓ cancer stem cell population | [69] |
Vorinostat (HDACi) + Εmetin (anti-NF-κB) | Achieving combined therapeutic effect | ||
MEC (cell line) | CUDC-101 (EGFRi + HDACi) | ↑ cytotoxicity ↓ cancer stem cell oncogenicity | [147] |
MEC (cell line) Mice transplanted with tumor cells | Sodium butyrate (HDACi) | ↓ proliferative potential no organ toxicities in vivo | [148] |
SGDA (cell line) | HDACi (TSA + Quisinostat) | ↓ proliferation and migration potential ↑ epithelial barrier function | [149] |
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Manou, M.; Kanakoglou, D.S.; Loupis, T.; Vrachnos, D.M.; Theocharis, S.; Papavassiliou, A.G.; Piperi, C. Role of Histone Deacetylases in the Pathogenesis of Salivary Gland Tumors and Therapeutic Targeting Options. Int. J. Mol. Sci. 2023, 24, 10038. https://doi.org/10.3390/ijms241210038
Manou M, Kanakoglou DS, Loupis T, Vrachnos DM, Theocharis S, Papavassiliou AG, Piperi C. Role of Histone Deacetylases in the Pathogenesis of Salivary Gland Tumors and Therapeutic Targeting Options. International Journal of Molecular Sciences. 2023; 24(12):10038. https://doi.org/10.3390/ijms241210038
Chicago/Turabian StyleManou, Maria, Dimitrios S. Kanakoglou, Theodoros Loupis, Dimitrios M. Vrachnos, Stamatios Theocharis, Athanasios G. Papavassiliou, and Christina Piperi. 2023. "Role of Histone Deacetylases in the Pathogenesis of Salivary Gland Tumors and Therapeutic Targeting Options" International Journal of Molecular Sciences 24, no. 12: 10038. https://doi.org/10.3390/ijms241210038