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Transcriptional Landscape of CUT-Class Homeobox Genes in Blastic Plasmacytoid Dendritic Cell Neoplasm
Homeobox genes encode developmental transcription factors regulating tissue-specific differentiation processes and drive cancerogenesis when deregulated. Dendritic cells (DCs) are myeloid immune cells occurring as two types, either conventional or plasmacytoid DCs. Recently, we showed that the expre...
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Published in: | International journal of molecular sciences 2024-02, Vol.25 (5), p.2764 |
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description | Homeobox genes encode developmental transcription factors regulating tissue-specific differentiation processes and drive cancerogenesis when deregulated. Dendritic cells (DCs) are myeloid immune cells occurring as two types, either conventional or plasmacytoid DCs. Recently, we showed that the expression of NKL-subclass homeobox gene VENTX is restricted to conventional DCs, regulating developmental genes. Here, we identified and investigated homeobox genes specifically expressed in plasmacytoid DCs (pDCs) and derived blastic plasmacytoid dendritic cell neoplasm (BPDCN). We analyzed gene expression data, performed RQ-PCR, protein analyses by Western blot and immuno-cytology, siRNA-mediated knockdown assays and subsequent RNA-sequencing and live-cell imaging. Screening of public gene expression data revealed restricted activity of the CUT-class homeobox gene CUX2 in pDCs. An extended analysis of this homeobox gene class in myelopoiesis showed that additional CUX2 activity was restricted to myeloid progenitors, while BPDCN patients aberrantly expressed ONECUT2, which remained silent in the complete myeloid compartment. ONECUT2 expressing BPDCN cell line CAL-1 served as a model to investigate its regulation and oncogenic activity. The ONECUT2 locus at 18q21 was duplicated and activated by IRF4, AUTS2 and TNF-signaling and repressed by BMP4-, TGFb- and IL13-signalling. Functional analyses of ONECUT2 revealed the inhibition of pDC differentiation and of CDKN1C and CASP1 expression, while SMAD3 and EPAS1 were activated. EPAS1 in turn enhanced survival under hypoxic conditions which thus may support dendritic tumor cells residing in hypoxic skin lesions. Collectively, we revealed physiological and aberrant activities of CUT-class homeobox genes in myelopoiesis including pDCs and in BPDCN, respectively. Our data may aid in the diagnosis of BPDCN patients and reveal novel therapeutic targets for this fatal malignancy. |
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Dendritic cells (DCs) are myeloid immune cells occurring as two types, either conventional or plasmacytoid DCs. Recently, we showed that the expression of NKL-subclass homeobox gene VENTX is restricted to conventional DCs, regulating developmental genes. Here, we identified and investigated homeobox genes specifically expressed in plasmacytoid DCs (pDCs) and derived blastic plasmacytoid dendritic cell neoplasm (BPDCN). We analyzed gene expression data, performed RQ-PCR, protein analyses by Western blot and immuno-cytology, siRNA-mediated knockdown assays and subsequent RNA-sequencing and live-cell imaging. Screening of public gene expression data revealed restricted activity of the CUT-class homeobox gene CUX2 in pDCs. An extended analysis of this homeobox gene class in myelopoiesis showed that additional CUX2 activity was restricted to myeloid progenitors, while BPDCN patients aberrantly expressed ONECUT2, which remained silent in the complete myeloid compartment. ONECUT2 expressing BPDCN cell line CAL-1 served as a model to investigate its regulation and oncogenic activity. The ONECUT2 locus at 18q21 was duplicated and activated by IRF4, AUTS2 and TNF-signaling and repressed by BMP4-, TGFb- and IL13-signalling. Functional analyses of ONECUT2 revealed the inhibition of pDC differentiation and of CDKN1C and CASP1 expression, while SMAD3 and EPAS1 were activated. EPAS1 in turn enhanced survival under hypoxic conditions which thus may support dendritic tumor cells residing in hypoxic skin lesions. Collectively, we revealed physiological and aberrant activities of CUT-class homeobox genes in myelopoiesis including pDCs and in BPDCN, respectively. Our data may aid in the diagnosis of BPDCN patients and reveal novel therapeutic targets for this fatal malignancy.</description><identifier>ISSN: 1422-0067</identifier><identifier>ISSN: 1661-6596</identifier><identifier>EISSN: 1422-0067</identifier><identifier>DOI: 10.3390/ijms25052764</identifier><identifier>PMID: 38474011</identifier><language>eng</language><publisher>Switzerland: MDPI AG</publisher><subject>ALCL ; AML ; Binding sites ; Biomarkers ; Blood ; Cell Differentiation ; Cell Line ; CUT-code ; Datasets ; Dendritic cells ; Dendritic Cells - metabolism ; DNA binding proteins ; Gene expression ; Genes ; Genes, Homeobox ; Genetic aspects ; Genetic transcription ; Genomes ; Health aspects ; Hematologic Neoplasms - pathology ; homeodomain ; Homeodomain Proteins - genetics ; HOXA9 ; Humans ; Leukemia ; Lymphoma ; Myeloid Cells - metabolism ; NKL-code ; Physiology ; Proteins ; RNA ; Transcription Factors - metabolism ; Tumors</subject><ispartof>International journal of molecular sciences, 2024-02, Vol.25 (5), p.2764</ispartof><rights>COPYRIGHT 2024 MDPI AG</rights><rights>2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2024 by the authors. 2024</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c503t-5c7bf1d732ef2d8344ba3344bcce9dc1054e7a4ff224c25cf236eda8ad1033ab3</cites><orcidid>0000-0002-9448-416X ; 0000-0003-4431-8988 ; 0000-0002-5946-4921</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2955542777/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2955542777?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38474011$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Nagel, Stefan</creatorcontrib><creatorcontrib>Rand, Ulfert</creatorcontrib><creatorcontrib>Pommerenke, Claudia</creatorcontrib><creatorcontrib>Meyer, Corinna</creatorcontrib><title>Transcriptional Landscape of CUT-Class Homeobox Genes in Blastic Plasmacytoid Dendritic Cell Neoplasm</title><title>International journal of molecular sciences</title><addtitle>Int J Mol Sci</addtitle><description>Homeobox genes encode developmental transcription factors regulating tissue-specific differentiation processes and drive cancerogenesis when deregulated. Dendritic cells (DCs) are myeloid immune cells occurring as two types, either conventional or plasmacytoid DCs. Recently, we showed that the expression of NKL-subclass homeobox gene VENTX is restricted to conventional DCs, regulating developmental genes. Here, we identified and investigated homeobox genes specifically expressed in plasmacytoid DCs (pDCs) and derived blastic plasmacytoid dendritic cell neoplasm (BPDCN). We analyzed gene expression data, performed RQ-PCR, protein analyses by Western blot and immuno-cytology, siRNA-mediated knockdown assays and subsequent RNA-sequencing and live-cell imaging. Screening of public gene expression data revealed restricted activity of the CUT-class homeobox gene CUX2 in pDCs. An extended analysis of this homeobox gene class in myelopoiesis showed that additional CUX2 activity was restricted to myeloid progenitors, while BPDCN patients aberrantly expressed ONECUT2, which remained silent in the complete myeloid compartment. ONECUT2 expressing BPDCN cell line CAL-1 served as a model to investigate its regulation and oncogenic activity. The ONECUT2 locus at 18q21 was duplicated and activated by IRF4, AUTS2 and TNF-signaling and repressed by BMP4-, TGFb- and IL13-signalling. Functional analyses of ONECUT2 revealed the inhibition of pDC differentiation and of CDKN1C and CASP1 expression, while SMAD3 and EPAS1 were activated. EPAS1 in turn enhanced survival under hypoxic conditions which thus may support dendritic tumor cells residing in hypoxic skin lesions. Collectively, we revealed physiological and aberrant activities of CUT-class homeobox genes in myelopoiesis including pDCs and in BPDCN, respectively. Our data may aid in the diagnosis of BPDCN patients and reveal novel therapeutic targets for this fatal malignancy.</description><subject>ALCL</subject><subject>AML</subject><subject>Binding sites</subject><subject>Biomarkers</subject><subject>Blood</subject><subject>Cell Differentiation</subject><subject>Cell Line</subject><subject>CUT-code</subject><subject>Datasets</subject><subject>Dendritic cells</subject><subject>Dendritic Cells - metabolism</subject><subject>DNA binding proteins</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genes, Homeobox</subject><subject>Genetic aspects</subject><subject>Genetic transcription</subject><subject>Genomes</subject><subject>Health aspects</subject><subject>Hematologic Neoplasms - pathology</subject><subject>homeodomain</subject><subject>Homeodomain Proteins - genetics</subject><subject>HOXA9</subject><subject>Humans</subject><subject>Leukemia</subject><subject>Lymphoma</subject><subject>Myeloid Cells - metabolism</subject><subject>NKL-code</subject><subject>Physiology</subject><subject>Proteins</subject><subject>RNA</subject><subject>Transcription Factors - metabolism</subject><subject>Tumors</subject><issn>1422-0067</issn><issn>1661-6596</issn><issn>1422-0067</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNptUk1vEzEQXSEQLYUbZ7QSFw6k-HO9e0JtgLZSBBzSszVrj4OjXTvYG0T_PU5TqgQhSx7rzZvn-aqq15Scc96RD349ZiaJZKoRT6pTKhibEdKopwfvk-pFzmtCGGeye16d8FYoQSg9rXCZIGST_GbyMcBQLyDYbGCDdXT1_HY5mw-Qc30dR4x9_F1fYcBc-1BfFnzypv5e7Ajmbore1p8w2OR38ByHof6KcbNzv6yeORgyvnqwZ9Xtl8_L-fVs8e3qZn6xmBlJ-DSTRvWOWsUZOmZbLkQPfHcbg501lEiBCoRzjAnDpHGMN2ihBUsJ59Dzs-pmr2sjrPUm-RHSnY7g9T0Q00pDKtkNqKnsO3Sq57wRgoNogVtjuexcLwWTULQ-7rU2235EazBMCYYj0WNP8D_0Kv7SlHS8JCiLwrsHhRR_bjFPevTZlL5AwLjNmnWyaVpBqSrUt_9Q13GbyjzuWbJkpNQBawWlAh9cLB-bnai-UG0juCoTLqzz_7DKsTh6EwM6X_CjgPf7AJNizgndY5GU6N2O6cMdK_Q3h415JP9dKv4HNEvMNg</recordid><startdate>20240227</startdate><enddate>20240227</enddate><creator>Nagel, Stefan</creator><creator>Rand, Ulfert</creator><creator>Pommerenke, Claudia</creator><creator>Meyer, Corinna</creator><general>MDPI AG</general><general>MDPI</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>MBDVC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-9448-416X</orcidid><orcidid>https://orcid.org/0000-0003-4431-8988</orcidid><orcidid>https://orcid.org/0000-0002-5946-4921</orcidid></search><sort><creationdate>20240227</creationdate><title>Transcriptional Landscape of CUT-Class Homeobox Genes in Blastic Plasmacytoid Dendritic Cell Neoplasm</title><author>Nagel, Stefan ; 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Dendritic cells (DCs) are myeloid immune cells occurring as two types, either conventional or plasmacytoid DCs. Recently, we showed that the expression of NKL-subclass homeobox gene VENTX is restricted to conventional DCs, regulating developmental genes. Here, we identified and investigated homeobox genes specifically expressed in plasmacytoid DCs (pDCs) and derived blastic plasmacytoid dendritic cell neoplasm (BPDCN). We analyzed gene expression data, performed RQ-PCR, protein analyses by Western blot and immuno-cytology, siRNA-mediated knockdown assays and subsequent RNA-sequencing and live-cell imaging. Screening of public gene expression data revealed restricted activity of the CUT-class homeobox gene CUX2 in pDCs. An extended analysis of this homeobox gene class in myelopoiesis showed that additional CUX2 activity was restricted to myeloid progenitors, while BPDCN patients aberrantly expressed ONECUT2, which remained silent in the complete myeloid compartment. ONECUT2 expressing BPDCN cell line CAL-1 served as a model to investigate its regulation and oncogenic activity. The ONECUT2 locus at 18q21 was duplicated and activated by IRF4, AUTS2 and TNF-signaling and repressed by BMP4-, TGFb- and IL13-signalling. Functional analyses of ONECUT2 revealed the inhibition of pDC differentiation and of CDKN1C and CASP1 expression, while SMAD3 and EPAS1 were activated. EPAS1 in turn enhanced survival under hypoxic conditions which thus may support dendritic tumor cells residing in hypoxic skin lesions. Collectively, we revealed physiological and aberrant activities of CUT-class homeobox genes in myelopoiesis including pDCs and in BPDCN, respectively. 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subjects | ALCL AML Binding sites Biomarkers Blood Cell Differentiation Cell Line CUT-code Datasets Dendritic cells Dendritic Cells - metabolism DNA binding proteins Gene expression Genes Genes, Homeobox Genetic aspects Genetic transcription Genomes Health aspects Hematologic Neoplasms - pathology homeodomain Homeodomain Proteins - genetics HOXA9 Humans Leukemia Lymphoma Myeloid Cells - metabolism NKL-code Physiology Proteins RNA Transcription Factors - metabolism Tumors |
title | Transcriptional Landscape of CUT-Class Homeobox Genes in Blastic Plasmacytoid Dendritic Cell Neoplasm |
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