{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T13:57:36Z","timestamp":1787061456013,"version":"build-2736575974"},"reference-count":96,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2023,2,7]],"date-time":"2023-02-07T00:00:00Z","timestamp":1675728000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"County of Salzburg, Cancer Cluster Salzburg","award":["20102-P1601064-FPR01-2017"],"award-info":[{"award-number":["20102-P1601064-FPR01-2017"]}]},{"name":"County of Salzburg, Cancer Cluster Salzburg","award":["P33969"],"award-info":[{"award-number":["P33969"]}]},{"name":"County of Salzburg, Cancer Cluster Salzburg","award":["20102-F1901165-KZP"],"award-info":[{"award-number":["20102-F1901165-KZP"]}]},{"name":"County of Salzburg, Cancer Cluster Salzburg","award":["ITAT1054"],"award-info":[{"award-number":["ITAT1054"]}]},{"name":"Austrian Science Fund (FWF)","award":["20102-P1601064-FPR01-2017"],"award-info":[{"award-number":["20102-P1601064-FPR01-2017"]}]},{"name":"Austrian Science Fund (FWF)","award":["P33969"],"award-info":[{"award-number":["P33969"]}]},{"name":"Austrian Science Fund (FWF)","award":["20102-F1901165-KZP"],"award-info":[{"award-number":["20102-F1901165-KZP"]}]},{"name":"Austrian Science Fund (FWF)","award":["ITAT1054"],"award-info":[{"award-number":["ITAT1054"]}]},{"name":"Biomed Center Salzburg","award":["20102-P1601064-FPR01-2017"],"award-info":[{"award-number":["20102-P1601064-FPR01-2017"]}]},{"name":"Biomed Center Salzburg","award":["P33969"],"award-info":[{"award-number":["P33969"]}]},{"name":"Biomed Center Salzburg","award":["20102-F1901165-KZP"],"award-info":[{"award-number":["20102-F1901165-KZP"]}]},{"name":"Biomed Center Salzburg","award":["ITAT1054"],"award-info":[{"award-number":["ITAT1054"]}]},{"name":"European Interreg V-A Italien-\u00d6sterreich project EPIC","award":["20102-P1601064-FPR01-2017"],"award-info":[{"award-number":["20102-P1601064-FPR01-2017"]}]},{"name":"European Interreg V-A Italien-\u00d6sterreich project EPIC","award":["P33969"],"award-info":[{"award-number":["P33969"]}]},{"name":"European Interreg V-A Italien-\u00d6sterreich project EPIC","award":["20102-F1901165-KZP"],"award-info":[{"award-number":["20102-F1901165-KZP"]}]},{"name":"European Interreg V-A Italien-\u00d6sterreich project EPIC","award":["ITAT1054"],"award-info":[{"award-number":["ITAT1054"]}]},{"name":"Priority program ACBN, University of Salzburg","award":["20102-P1601064-FPR01-2017"],"award-info":[{"award-number":["20102-P1601064-FPR01-2017"]}]},{"name":"Priority program ACBN, University of Salzburg","award":["P33969"],"award-info":[{"award-number":["P33969"]}]},{"name":"Priority program ACBN, University of Salzburg","award":["20102-F1901165-KZP"],"award-info":[{"award-number":["20102-F1901165-KZP"]}]},{"name":"Priority program ACBN, University of Salzburg","award":["ITAT1054"],"award-info":[{"award-number":["ITAT1054"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cancers"],"abstract":"<jats:p>Acute myeloid leukemia (AML) is a hematopoietic malignancy characterized by altered myeloid progenitor cell proliferation and differentiation. As in many other cancers, epigenetic transcriptional repressors such as histone deacetylases (HDACs) are dysregulated in AML. Here, we investigated (1) HDAC gene expression in AML patients and in different AML cell lines and (2) the effect of treating AML cells with the specific class IIA HDAC inhibitor TMP269, by applying proteomic and comparative bioinformatic analyses. We also analyzed cell proliferation, apoptosis, and the cell-killing capacities of TMP269 in combination with venetoclax compared to azacitidine plus venetoclax, by flow cytometry. Our results demonstrate significantly overexpressed class I and class II HDAC genes in AML patients, a phenotype which is conserved in AML cell lines. In AML MOLM-13 cells, TMP269 treatment downregulated a set of ribosomal proteins which are overexpressed in AML patients at the transcriptional level. TMP269 showed anti-proliferative effects and induced additive apoptotic effects in combination with venetoclax. We conclude that TMP269 exerts anti-leukemic activity when combined with venetoclax and has potential as a therapeutic drug in AML.<\/jats:p>","DOI":"10.3390\/cancers15041039","type":"journal-article","created":{"date-parts":[[2023,2,7]],"date-time":"2023-02-07T03:24:13Z","timestamp":1675740253000},"page":"1039","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":13,"title":["The Class IIA Histone Deacetylase (HDAC) Inhibitor TMP269 Downregulates Ribosomal Proteins and Has Anti-Proliferative and Pro-Apoptotic Effects on AML Cells"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7636-516X","authenticated-orcid":false,"given":"Laura","family":"Urwanisch","sequence":"first","affiliation":[{"name":"Department of Biosciences and Medical Biology, University of Salzburg, 5020 Salzburg, Austria"},{"name":"Cancer Cluster Salzburg (CCS), 5020 Salzburg, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8677-0983","authenticated-orcid":false,"given":"Michael Stefan","family":"Unger","sequence":"additional","affiliation":[{"name":"Department of Biosciences and Medical Biology, University of Salzburg, 5020 Salzburg, Austria"},{"name":"Cancer Cluster Salzburg (CCS), 5020 Salzburg, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Helene","family":"Sieberer","sequence":"additional","affiliation":[{"name":"Department of Biosciences and Medical Biology, University of Salzburg, 5020 Salzburg, Austria"},{"name":"Cancer Cluster Salzburg (CCS), 5020 Salzburg, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hieu-Hoa","family":"Dang","sequence":"additional","affiliation":[{"name":"Department of Biosciences and Medical Biology, University of Salzburg, 5020 Salzburg, Austria"},{"name":"Cancer Cluster Salzburg (CCS), 5020 Salzburg, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Theresa","family":"Neuper","sequence":"additional","affiliation":[{"name":"Department of Biosciences and Medical Biology, University of Salzburg, 5020 Salzburg, Austria"},{"name":"Cancer Cluster Salzburg (CCS), 5020 Salzburg, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christof","family":"Regl","sequence":"additional","affiliation":[{"name":"Department of Biosciences and Medical Biology, University of Salzburg, 5020 Salzburg, Austria"},{"name":"Cancer Cluster Salzburg (CCS), 5020 Salzburg, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9169-3935","authenticated-orcid":false,"given":"Julia","family":"Vetter","sequence":"additional","affiliation":[{"name":"Bioinformatics Research Group, University of Applied Sciences Upper Austria, Softwarepark 11, 4232 Hagenberg im Muehlkreis, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Susanne","family":"Schaller","sequence":"additional","affiliation":[{"name":"Bioinformatics Research Group, University of Applied Sciences Upper Austria, Softwarepark 11, 4232 Hagenberg im Muehlkreis, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stephan M.","family":"Winkler","sequence":"additional","affiliation":[{"name":"Bioinformatics Research Group, University of Applied Sciences Upper Austria, Softwarepark 11, 4232 Hagenberg im Muehlkreis, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emanuela","family":"Kerschbamer","sequence":"additional","affiliation":[{"name":"Institute for Biomedicine, Eurac Research, Affiliated Institute of the University of L\u00fcbeck, Via A. Volta 21, 39100 Bolzano, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christian X.","family":"Weichenberger","sequence":"additional","affiliation":[{"name":"Institute for Biomedicine, Eurac Research, Affiliated Institute of the University of L\u00fcbeck, Via A. Volta 21, 39100 Bolzano, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter W.","family":"Krenn","sequence":"additional","affiliation":[{"name":"Department of Biosciences and Medical Biology, University of Salzburg, 5020 Salzburg, Austria"},{"name":"Cancer Cluster Salzburg (CCS), 5020 Salzburg, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michela","family":"Luciano","sequence":"additional","affiliation":[{"name":"Department of Biosciences and Medical Biology, University of Salzburg, 5020 Salzburg, Austria"},{"name":"Cancer Cluster Salzburg (CCS), 5020 Salzburg, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lisa","family":"Pleyer","sequence":"additional","affiliation":[{"name":"Cancer Cluster Salzburg (CCS), 5020 Salzburg, Austria"},{"name":"IIIrd Medical Department with Hematology and Medical Oncology, Hemostaseology, Rheumatology and Infectious Diseases, Oncologic Center, Paracelsus Medical University, 5020 Salzburg, Austria"},{"name":"Salzburg Cancer Research Institute with Laboratory of Immunological and Molecular Cancer Research and Center for Clinical Cancer and Immunology Trials, 5020 Salzburg, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4462-3694","authenticated-orcid":false,"given":"Richard","family":"Greil","sequence":"additional","affiliation":[{"name":"Cancer Cluster Salzburg (CCS), 5020 Salzburg, Austria"},{"name":"IIIrd Medical Department with Hematology and Medical Oncology, Hemostaseology, Rheumatology and Infectious Diseases, Oncologic Center, Paracelsus Medical University, 5020 Salzburg, Austria"},{"name":"Salzburg Cancer Research Institute with Laboratory of Immunological and Molecular Cancer Research and Center for Clinical Cancer and Immunology Trials, 5020 Salzburg, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8358-1880","authenticated-orcid":false,"given":"Christian G.","family":"Huber","sequence":"additional","affiliation":[{"name":"Department of Biosciences and Medical Biology, University of Salzburg, 5020 Salzburg, Austria"},{"name":"Cancer Cluster Salzburg (CCS), 5020 Salzburg, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2009-6305","authenticated-orcid":false,"given":"Fritz","family":"Aberger","sequence":"additional","affiliation":[{"name":"Department of Biosciences and Medical Biology, University of Salzburg, 5020 Salzburg, Austria"},{"name":"Cancer Cluster Salzburg (CCS), 5020 Salzburg, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0984-204X","authenticated-orcid":false,"given":"Jutta","family":"Horejs-Hoeck","sequence":"additional","affiliation":[{"name":"Department of Biosciences and Medical Biology, University of Salzburg, 5020 Salzburg, Austria"},{"name":"Cancer Cluster Salzburg (CCS), 5020 Salzburg, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,2,7]]},"reference":[{"key":"ref_1","unstructured":"U.S. National Institutes of Health, National Cancer Institute, Surveillance, Epidemiology, and End Results Program (2022, January 05). Cancer Stat Facts: Acute Myeloid Leukemia (AML), Available online: https:\/\/seer.cancer.gov\/statfacts\/html\/amyl.html."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1136","DOI":"10.1056\/NEJMra1406184","article-title":"Acute Myeloid Leukemia","volume":"373","author":"Dohner","year":"2015","journal-title":"N. Engl. J. Med."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1038\/s41408-020-00376-1","article-title":"New directions for emerging therapies in acute myeloid leukemia: The next chapter","volume":"10","author":"Daver","year":"2020","journal-title":"Blood Cancer J."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1186\/s13045-021-01062-w","article-title":"Emerging agents and regimens for AML","volume":"14","author":"Liu","year":"2021","journal-title":"J. Hematol. Oncol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1016\/S1470-2045(18)30010-X","article-title":"Safety and preliminary efficacy of venetoclax with decitabine or azacitidine in elderly patients with previously untreated acute myeloid leukaemia: A non-randomised, open-label, phase 1b study","volume":"19","author":"Pratz","year":"2018","journal-title":"Lancet Oncol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1277","DOI":"10.1200\/JCO.18.01600","article-title":"Venetoclax Combined With Low-Dose Cytarabine for Previously Untreated Patients With Acute Myeloid Leukemia: Results From a Phase Ib\/II Study","volume":"37","author":"Wei","year":"2019","journal-title":"J. Clin. Oncol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1182\/blood-2018-08-868752","article-title":"Venetoclax combined with decitabine or azacitidine in treatment-naive, elderly patients with acute myeloid leukemia","volume":"133","author":"DiNardo","year":"2019","journal-title":"Blood"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1056\/NEJMoa2012971","article-title":"Azacitidine and Venetoclax in Previously Untreated Acute Myeloid Leukemia","volume":"383","author":"DiNardo","year":"2020","journal-title":"N. Engl. J. Med."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"536","DOI":"10.1158\/2159-8290.CD-19-0710","article-title":"Monocytic Subclones Confer Resistance to Venetoclax-Based Therapy in Patients with Acute Myeloid Leukemia","volume":"10","author":"Pei","year":"2020","journal-title":"Cancer Discov."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1007\/s13238-014-0031-6","article-title":"Driver mutations of cancer epigenomes","volume":"5","author":"Roy","year":"2014","journal-title":"Protein Cell"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"834","DOI":"10.1126\/science.1175371","article-title":"Lysine acetylation targets protein complexes and co-regulates major cellular functions","volume":"325","author":"Choudhary","year":"2009","journal-title":"Science"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1369\/0022155413506582","article-title":"Histone deacetylases: A saga of perturbed acetylation homeostasis in cancer","volume":"62","author":"Parbin","year":"2014","journal-title":"J. Histochem. Cytochem."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"3263","DOI":"10.1007\/s00018-019-03098-1","article-title":"Dysregulation of histone deacetylases in carcinogenesis and tumor progression: A possible link to apoptosis and autophagy","volume":"76","author":"Patra","year":"2019","journal-title":"Cell Mol. Life Sci."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1089\/ars.2014.5863","article-title":"Mechanisms of Histone Deacetylase Inhibitor-Regulated Gene Expression in Cancer Cells","volume":"23","author":"Chueh","year":"2015","journal-title":"Antioxid. Redox Signal."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1332","DOI":"10.1002\/ijc.25151","article-title":"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","volume":"127","author":"Hayashi","year":"2010","journal-title":"Int. J. Cancer"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Ali, A., Ali, A., Khan, S., Ibrahim, M., Alshehri, M.A., and Thirupathi, A. (2021). Inhibition of HDACs Suppresses Cell Proliferation and Cell Migration of Gastric Cancer by Regulating E2F5 Targeting BCL2. Life, 11.","DOI":"10.3390\/life11121425"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"740","DOI":"10.1016\/j.ejca.2008.01.023","article-title":"Effects of FR235222, a novel HDAC inhibitor, in proliferation and apoptosis of human leukaemia cell lines: Role of annexin A1","volume":"44","author":"Petrella","year":"2008","journal-title":"Eur. J. Cancer"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1038\/nm1160","article-title":"Inhibitors of histone deacetylases induce tumor-selective apoptosis through activation of the death receptor pathway","volume":"11","author":"Insinga","year":"2005","journal-title":"Nat. Med."},{"key":"ref_19","first-page":"85","article-title":"Histone deacetylase inhibition: An important mechanism in the treatment of lymphoma","volume":"9","author":"Guo","year":"2012","journal-title":"Cancer Biol. Med."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"San Jose-Eneriz, E., Gimenez-Camino, N., Agirre, X., and Prosper, F. (2019). HDAC Inhibitors in Acute Myeloid Leukemia. Cancers, 11.","DOI":"10.3390\/cancers11111794"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"a026831","DOI":"10.1101\/cshperspect.a026831","article-title":"HDACs and HDAC Inhibitors in Cancer Development and Therapy","volume":"6","author":"Li","year":"2016","journal-title":"Cold Spring Harb. Perspect. Med."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1375","DOI":"10.3324\/haematol.2009.009217","article-title":"A phase 2 study of vorinostat in acute myeloid leukemia","volume":"94","author":"Schaefer","year":"2009","journal-title":"Haematologica"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"51429","DOI":"10.18632\/oncotarget.18009","article-title":"Decitabine-Vorinostat combination treatment in acute myeloid leukemia activates pathways with potential for novel triple therapy","volume":"8","author":"Young","year":"2017","journal-title":"Oncotarget"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"e25","DOI":"10.3324\/haematol.2017.172411","article-title":"Panobinostat monotherapy and combination therapy in patients with acute myeloid leukemia: Results from two clinical trials","volume":"103","author":"Schlenk","year":"2018","journal-title":"Haematologica"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"237","DOI":"10.3346\/jkms.2013.28.2.237","article-title":"Improved therapeutic effect against leukemia by a combination of the histone methyltransferase inhibitor chaetocin and the histone deacetylase inhibitor trichostatin A","volume":"28","author":"Tran","year":"2013","journal-title":"J. Korean Med. Sci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1186\/1868-7083-6-19","article-title":"Epigenetic therapy of acute myeloid leukemia using 5-aza-2\u2019-deoxycytidine (decitabine) in combination with inhibitors of histone methylation and deacetylation","volume":"6","author":"Momparler","year":"2014","journal-title":"Clin. Epigenetics"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1434","DOI":"10.1002\/stem.1398","article-title":"Entinostat prevents leukemia maintenance in a collaborating oncogene-dependent model of cytogenetically normal acute myeloid leukemia","volume":"31","author":"Ramsey","year":"2013","journal-title":"Stem. Cells"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"2781","DOI":"10.1182\/blood-2006-05-021873","article-title":"Phase 1 and pharmacologic study of MS-275, a histone deacetylase inhibitor, in adults with refractory and relapsed acute leukemias","volume":"109","author":"Gojo","year":"2007","journal-title":"Blood"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1007\/s00018-014-1727-8","article-title":"Selective class IIa HDAC inhibitors: Myth or reality","volume":"72","author":"Gagliostro","year":"2015","journal-title":"Cell Mol. Life Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/j.biopha.2018.02.071","article-title":"Inhibition of class IIa histone deacetylase activity by gallic acid, sulforaphane, TMP269, and panobinostat","volume":"101","author":"Choi","year":"2018","journal-title":"Biomed. Pharmacother."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2529","DOI":"10.1200\/JCO.2009.23.4732","article-title":"Clinical utility of microarray-based gene expression profiling in the diagnosis and subclassification of leukemia: Report from the International Microarray Innovations in Leukemia Study Group","volume":"28","author":"Haferlach","year":"2010","journal-title":"J. Clin. Oncol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"802","DOI":"10.1111\/j.1365-2141.2008.07261.x","article-title":"An international standardization programme towards the application of gene expression profiling in routine leukaemia diagnostics: The Microarray Innovations in LEukemia study prephase","volume":"142","author":"Kohlmann","year":"2008","journal-title":"Br. J. Haematol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1367","DOI":"10.1038\/nbt.1511","article-title":"MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification","volume":"26","author":"Cox","year":"2008","journal-title":"Nat. Biotechnol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"D480","DOI":"10.1093\/nar\/gkaa1100","article-title":"UniProt: The universal protein knowledgebase in 2021","volume":"49","author":"UniProt","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1038\/nmeth.3901","article-title":"The Perseus computational platform for comprehensive analysis of (prote)omics data","volume":"13","author":"Tyanova","year":"2016","journal-title":"Nat. Methods"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"2301","DOI":"10.1038\/nprot.2016.136","article-title":"The MaxQuant computational platform for mass spectrometry-based shotgun proteomics","volume":"11","author":"Tyanova","year":"2016","journal-title":"Nat. Protoc."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"732","DOI":"10.1021\/acs.jproteome.8b00523","article-title":"NormalyzerDE: Online Tool for Improved Normalization of Omics Expression Data and High-Sensitivity Differential Expression Analysis","volume":"18","author":"Willforss","year":"2019","journal-title":"J. Proteome Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1111\/j.2517-6161.1995.tb02031.x","article-title":"Controlling the False Discovery Rate\u2014A Practical and Powerful Approach to Multiple Testing","volume":"57","author":"Benjamini","year":"1995","journal-title":"J. R. Stat. Soc. B"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1038\/nprot.2017.147","article-title":"Proteome-wide identification of ubiquitin interactions using UbIA-MS","volume":"13","author":"Zhang","year":"2018","journal-title":"Nat. Protoc."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1089\/omi.2011.0118","article-title":"clusterProfiler: An R package for comparing biological themes among gene clusters","volume":"16","author":"Yu","year":"2012","journal-title":"Omics A J. Integr. Biol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"847958","DOI":"10.3389\/fimmu.2022.847958","article-title":"Helicobacter pylori Infection of Primary Human Monocytes Boosts Subsequent Immune Responses to LPS","volume":"13","author":"Frauenlob","year":"2022","journal-title":"Front. Immunol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/j.bjhh.2014.11.008","article-title":"Acute myeloid leukemia: Survival analysis of patients at a university hospital of Parana","volume":"37","author":"Padilha","year":"2015","journal-title":"Rev. Bras. Hematol. Hemoter."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"470","DOI":"10.12669\/pjms.35.2.614","article-title":"Immunophenotypic characterisation of morphologically diagnosed cases of Acute Myeloid Leukaemia (AML)","volume":"35","author":"Basharat","year":"2019","journal-title":"Pak. J. Med. Sci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"720","DOI":"10.1124\/jpet.103.055541","article-title":"Identification of novel isoform-selective inhibitors within class I histone deacetylases","volume":"307","author":"Hu","year":"2003","journal-title":"J. Pharmacol. Exp. Ther."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"15064","DOI":"10.1073\/pnas.0404603101","article-title":"Crystal structure of a eukaryotic zinc-dependent histone deacetylase, human HDAC8, complexed with a hydroxamic acid inhibitor","volume":"101","author":"Vannini","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"4538","DOI":"10.1158\/1078-0432.CCR-07-0014","article-title":"Synergistic in vivo antitumor effect of the histone deacetylase inhibitor MS-275 in combination with interleukin 2 in a murine model of renal cell carcinoma","volume":"13","author":"Kato","year":"2007","journal-title":"Clin. Cancer Res."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1382","DOI":"10.1016\/j.leukres.2008.02.018","article-title":"MS-275, a novel histone deacetylase inhibitor with selectivity against HDAC1, induces degradation of FLT3 via inhibition of chaperone function of heat shock protein 90 in AML cells","volume":"32","author":"Nishioka","year":"2008","journal-title":"Leuk. Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1388","DOI":"10.1016\/j.biocel.2007.02.009","article-title":"MS-275, a potent orally available inhibitor of histone deacetylases--the development of an anticancer agent","volume":"39","author":"Bracker","year":"2007","journal-title":"Int. J. Biochem. Cell Biol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1038\/nchembio.1223","article-title":"Selective class IIa histone deacetylase inhibition via a nonchelating zinc-binding group","volume":"9","author":"Lobera","year":"2013","journal-title":"Nat. Chem. Biol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1918","DOI":"10.1038\/leu.2015.83","article-title":"Class IIa HDAC inhibition enhances ER stress-mediated cell death in multiple myeloma","volume":"29","author":"Kikuchi","year":"2015","journal-title":"Leukemia"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1186\/s13148-018-0531-y","article-title":"Effects of novel HDAC inhibitors on urothelial carcinoma cells","volume":"10","author":"Kaletsch","year":"2018","journal-title":"Clin. Epigenetics"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"BSR20211577","DOI":"10.1042\/BSR20211577","article-title":"Deregulation of ribosomal proteins in human cancers","volume":"41","author":"Nasr","year":"2021","journal-title":"Biosci. Rep."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"5378","DOI":"10.1093\/nar\/gks189","article-title":"Inhibition of the function of class IIa HDACs by blocking their interaction with MEF2","volume":"40","author":"Jayathilaka","year":"2012","journal-title":"Nucleic Acids Res."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/j.ejphar.2006.08.010","article-title":"The novel histone deacetylase inhibitor BML-210 exerts growth inhibitory, proapoptotic and differentiation stimulating effects on the human leukemia cell lines","volume":"549","author":"Savickiene","year":"2006","journal-title":"Eur. J. Pharmacol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1038\/nbt.1759","article-title":"Chemoproteomics profiling of HDAC inhibitors reveals selective targeting of HDAC complexes","volume":"29","author":"Bantscheff","year":"2011","journal-title":"Nat. Biotechnol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"501","DOI":"10.2478\/s11658-012-0024-5","article-title":"Antileukemic activity of combined epigenetic agents, DNMT inhibitors zebularine and RG108 with HDAC inhibitors, against promyelocytic leukemia HL-60 cells","volume":"17","author":"Savickiene","year":"2012","journal-title":"Cell Mol. Biol. Lett."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Vire, B., de Walque, S., Restouin, A., Olive, D., Van Lint, C., and Collette, Y. (2009). Anti-leukemia activity of MS-275 histone deacetylase inhibitor implicates 4-1BBL\/4-1BB immunomodulatory functions. PLoS ONE, 4.","DOI":"10.1371\/journal.pone.0007085"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"2590","DOI":"10.1158\/0008-5472.CAN-03-2631","article-title":"The histone deacetylase inhibitor MS-275 interacts synergistically with fludarabine to induce apoptosis in human leukemia cells","volume":"64","author":"Maggio","year":"2004","journal-title":"Cancer Res."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"4592","DOI":"10.1073\/pnas.96.8.4592","article-title":"A synthetic inhibitor of histone deacetylase, MS-27-275, with marked in vivo antitumor activity against human tumors","volume":"96","author":"Saito","year":"1999","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"18252","DOI":"10.3390\/ijms160818252","article-title":"The Histone Deacetylase Inhibitor BML-210 Influences Gene and Protein Expression in Human Promyelocytic Leukemia NB4 Cells via Epigenetic Reprogramming","volume":"16","author":"Borutinskaite","year":"2015","journal-title":"Int. J. Mol. Sci."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"994","DOI":"10.1158\/1541-7786.MCR-16-0109","article-title":"HDAC6 Deacetylates HMGN2 to Regulate Stat5a Activity and Breast Cancer Growth","volume":"14","author":"Medler","year":"2016","journal-title":"Mol. Cancer Res."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"5565","DOI":"10.1182\/bloodadvances.2021005538","article-title":"Venetoclax and azacitidine compared with induction chemotherapy for newly diagnosed patients with acute myeloid leukemia","volume":"5","author":"Cherry","year":"2021","journal-title":"Blood Adv."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"2040620719860645","DOI":"10.1177\/2040620719860645","article-title":"Novel therapy in Acute myeloid leukemia (AML): Moving toward targeted approaches","volume":"10","author":"Winer","year":"2019","journal-title":"Ther. Adv. Hematol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1894","DOI":"10.1016\/S0140-6736(06)69780-8","article-title":"Acute myeloid leukaemia","volume":"368","author":"Estey","year":"2006","journal-title":"Lancet"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"133","DOI":"10.3389\/fgene.2019.00133","article-title":"Epigenetic Modifications in Acute Myeloid Leukemia: Prognosis, Treatment, and Heterogeneity","volume":"10","author":"Goldman","year":"2019","journal-title":"Front. Genet"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"e441","DOI":"10.1038\/bcj.2016.50","article-title":"Acute myeloid leukemia: A comprehensive review and 2016 update","volume":"6","year":"2016","journal-title":"Blood Cancer J"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1268","DOI":"10.1200\/JCO.1989.7.9.1268","article-title":"On the value of intensive remission-induction chemotherapy in elderly patients of 65+ years with acute myeloid leukemia: A randomized phase III study of the European Organization for Research and Treatment of Cancer Leukemia Group","volume":"7","author":"Lowenberg","year":"1989","journal-title":"J. Clin. Oncol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"2544","DOI":"10.3324\/haematol.2020.269134","article-title":"Dose intensity for induction in acute myeloid leukemia: What, when, and for whom?","volume":"106","author":"McCurdy","year":"2021","journal-title":"Haematologica"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"584974","DOI":"10.3389\/fonc.2020.584974","article-title":"Targeting Bcl-2 Proteins in Acute Myeloid Leukemia","volume":"10","author":"Wei","year":"2020","journal-title":"Front. Oncol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1111\/bjh.12425","article-title":"Survival and cure of acute myeloid leukaemia in England, 1971-2006: A population-based study","volume":"162","author":"Shah","year":"2013","journal-title":"Br. J. Haematol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1186\/s12943-019-1127-7","article-title":"Role of HDACs in normal and malignant hematopoiesis","volume":"19","author":"Wang","year":"2020","journal-title":"Mol. Cancer"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1016\/j.cell.2012.06.013","article-title":"Cancer epigenetics: From mechanism to therapy","volume":"150","author":"Dawson","year":"2012","journal-title":"Cell"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1016\/j.critrevonc.2017.05.010","article-title":"Azacitidine in adult patients with acute myeloid leukemia","volume":"116","author":"Schuh","year":"2017","journal-title":"Crit. Rev. Oncol. Hematol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"3898","DOI":"10.3390\/molecules20033898","article-title":"Histone deacetylase inhibitors in clinical studies as templates for new anticancer agents","volume":"20","author":"Mottamal","year":"2015","journal-title":"Molecules"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"3426","DOI":"10.3109\/10428194.2015.1034705","article-title":"Analysis of class I and II histone deacetylase gene expression in human leukemia","volume":"56","author":"Yang","year":"2015","journal-title":"Leuk. Lymphoma"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1833","DOI":"10.1111\/j.1582-4934.2011.01321.x","article-title":"Class IIa HDACs: From important roles in differentiation to possible implications in tumourigenesis","volume":"15","author":"Clocchiatti","year":"2011","journal-title":"J. Cell Mol. Med."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"3371","DOI":"10.1158\/1078-0432.CCR-19-1900","article-title":"5-Azacitidine Induces NOXA to Prime AML Cells for Venetoclax-Mediated Apoptosis","volume":"26","author":"Jin","year":"2020","journal-title":"Clin. Cancer Res."},{"key":"ref_78","doi-asserted-by":"crossref","unstructured":"Verza, F.A., Das, U., Fachin, A.L., Dimmock, J.R., and Marins, M. (2020). Roles of Histone Deacetylases and Inhibitors in Anticancer Therapy. Cancers, 12.","DOI":"10.3390\/cancers12061664"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1038\/s41392-021-00728-8","article-title":"Ribosomal proteins and human diseases: Molecular mechanisms and targeted therapy","volume":"6","author":"Kang","year":"2021","journal-title":"Signal Transduct. Target. Ther."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1007\/s11010-014-2128-x","article-title":"Lyar, a cell growth-regulating zinc finger protein, was identified to be associated with cytoplasmic ribosomes in male germ and cancer cells","volume":"395","author":"Yonezawa","year":"2014","journal-title":"Mol. Cell Biochem."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"9979707","DOI":"10.1155\/2021\/9979707","article-title":"LYAR Promotes Colorectal Cancer Progression by Upregulating FSCN1 Expression and Fatty Acid Metabolism","volume":"2021","author":"Wu","year":"2021","journal-title":"Oxid. Med. Cell Longev."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"10357","DOI":"10.1093\/nar\/gkz747","article-title":"LYAR potentiates rRNA synthesis by recruiting BRD2\/4 and the MYST-type acetyltransferase KAT7 to rDNA","volume":"47","author":"Izumikawa","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1111\/gtc.12129","article-title":"Human cell growth regulator Ly-1 antibody reactive homologue accelerates processing of preribosomal RNA","volume":"19","author":"Miyazawa","year":"2014","journal-title":"Genes Cells"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"1645","DOI":"10.1038\/cdd.2017.98","article-title":"Upregulation of LYAR induces neuroblastoma cell proliferation and survival","volume":"24","author":"Sun","year":"2017","journal-title":"Cell Death Differ."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"282","DOI":"10.5603\/FHC.a2021.0030","article-title":"LYAR promotes the proliferation of non-small cell lung cancer and is associated with poor prognosis","volume":"59","author":"Lu","year":"2021","journal-title":"Folia Histochem. Cytobiol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"3542","DOI":"10.1038\/s41467-020-17237-x","article-title":"Structural snapshots of human pre-60S ribosomal particles before and after nuclear export","volume":"11","author":"Liang","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"1799","DOI":"10.1093\/nar\/gkt971","article-title":"Regulation of the HDM2-p53 pathway by ribosomal protein L6 in response to ribosomal stress","volume":"42","author":"Bai","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref_88","doi-asserted-by":"crossref","unstructured":"Wu, Q., Gou, Y., Wang, Q., Jin, H., Cui, L., Zhang, Y., He, L., Wang, J., Nie, Y., and Shi, Y. (2011). Downregulation of RPL6 by siRNA inhibits proliferation and cell cycle progression of human gastric cancer cell lines. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0026401"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"507","DOI":"10.21037\/jtd-22-116","article-title":"Downregulated RPL6 inhibits lung cancer cell proliferation and migration and promotes cell apoptosis by regulating the AKT signaling pathway","volume":"14","author":"Zhang","year":"2022","journal-title":"J. Thorac. Dis."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"5264","DOI":"10.1093\/nar\/gkr114","article-title":"Structural basis for the binding of IRES RNAs to the head of the ribosomal 40S subunit","volume":"39","author":"Muhs","year":"2011","journal-title":"Nucleic Acids Res."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1016\/0014-5793(92)80041-E","article-title":"Regulation of ribosomal protein S25 in HL60 cells isolated for resistance to adriamycin","volume":"298","author":"Li","year":"1992","journal-title":"FEBS Lett."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"4147","DOI":"10.1074\/jbc.M109785200","article-title":"Ribosomal protein S25 mRNA partners with MTF-1 and La to provide a p53-mediated mechanism for survival or death","volume":"277","author":"Adilakshmi","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"1343","DOI":"10.1093\/carcin\/bgm302","article-title":"Loss-of-function genetic screening identifies a cluster of ribosomal proteins regulating p53 function","volume":"29","author":"Castro","year":"2008","journal-title":"Carcinogenesis"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1186\/s12935-021-02199-x","article-title":"RPL35A is a key promotor involved in the development and progression of gastric cancer","volume":"21","author":"Wu","year":"2021","journal-title":"Cancer Cell Int."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/S0304-3835(02)00024-1","article-title":"Inhibition of cell death by ribosomal protein L35a","volume":"180","author":"Lopez","year":"2002","journal-title":"Cancer Lett."},{"key":"ref_96","first-page":"125","article-title":"Resistance to venetoclax and hypomethylating agents in acute myeloid leukemia","volume":"4","author":"Saliba","year":"2021","journal-title":"Cancer Drug. Resist."}],"container-title":["Cancers"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6694\/15\/4\/1039\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:26:24Z","timestamp":1760120784000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6694\/15\/4\/1039"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,2,7]]},"references-count":96,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2023,2]]}},"alternative-id":["cancers15041039"],"URL":"https:\/\/doi.org\/10.3390\/cancers15041039","relation":{},"ISSN":["2072-6694"],"issn-type":[{"value":"2072-6694","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,2,7]]}}}