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Barr, F. G.

Publications and source records attributed to Barr, F. G..

5 recordsLinked to original sources

Role of Myc family proteins in transcriptional regulation of growth and oncogenic transformation in fusion-positive rhabdomyosarcoma

Fusion-positive rhabdomyosarcoma (FP-RMS) is driven by a PAX3::FOXO1 (P3F) or PAX7::FOXO1 fusion gene. After finding that MYCN is required for P3F-induced oncogenic transformation in a human myoblast model of FP-RMS, we further investigated the role of Myc family proteins in FP-RMS. Expression studies revealed that myoblast models and a subset of FP-RMS lines have predominant MYCN or MYC expression whereas other FP-RMS lines have both high MYCN and MYC expression. In myoblast models, MYCN was required for optimal P3F binding to and high-level activation of FGF8, a P3F target that is necessary and sufficient for oncogenic transformation. MYCN or MYC knockdown suppressed transformation in myoblast and FP-RMS lines with dominant MYCN or MYC expression, respectively. In FP-RMS lines with high MYCN and MYC expression, there was partial loss of transformation when one gene was targeted and complete loss when both genes were targeted. Despite the loss of oncogenic activity in lines with knockdown of a dominant Myc family member, FGF8 expression was not decreased. Transcriptomic analyses revealed that P3F target genes were not affected by MYCN or MYC knockdown, and instead a group of Myc-specific targets was down-regulated. Collectively, these results indicate that MYCN or MYC is functionally dominant in myoblast models and FP-RMS lines with dominant expression of one Myc family protein whereas MYCN and MYC are functionally redundant in FP-RMS cell lines with high expression of both. These Myc family proteins contribute to oncogenic properties by facilitating P3F activation of FGF8 and increasing expression of Myc-specific targets.

cancer biology↗

MIR17HG Expression Is Transcriptionally Regulated by PAX3::FOXO1 and MYCN 1 and is Necessary for Oncogenic Activity in Fusion-Positive Rhabdomyosarcoma

Alveolar rhabdomyosarcoma (RMS), an aggressive pediatric soft tissue cancer, is driven by the oncogenic fusion transcription factor PAX3::FOXO1 (P3F) or PAX7::FOXO1. In a subset of fusion-positive (FP)-RMS cases, amplification of the MIR17HG locus leads to overexpression of the miR-17-92 cluster of microRNAs (miRNAs). However, miR-17-92 is also highly expressed in FP-RMS tumors lacking this amplification, suggesting alternative regulatory mechanisms. Here, we show that P3F and MYCN cooperatively drive miR-17-92 expression in FP-RMS. CRISPR/Cas9-mediated knockout of P3F or MYCN in FP-RMS cell lines substantially reduced miR-17-92 expression. Using a human myoblast line or low P3F FP-RMS variant with inducible P3F or MYCN expression, P3F or MYCN alone induces minimal to low miR-17-92 expression whereas introduction of both MYCN and P3F leads to robust activation of the miR-17-92 cluster and acquisition of oncogenic phenotypes. Chromatin immunoprecipitation sequencing (ChIP-seq) revealed a P3F binding motif located 1.84 Mb upstream of the MIR17HG promoter. CRISPR-mediated deletion of this region in the myoblast system resulted in marked reduction of miR-17-92 expression and impaired oncogenic transformation. Functional inhibition of mature miRNAs of this cluster in FP-RMS cells using miRNA-sponge constructs suppressed proliferation and transformation. In the myoblast model system, transduction studies with exogenous miR-17-92 or miRNA-sponge expression constructs indicated that miR-17-92 is necessary but not sufficient for oncogenic transformation. Together, these findings establish a cooperative transcriptional axis in FP-RMS involving P3F and MYCN that activates MIR17HG through a distal regulatory element, thereby contributing to oncogenic behavior and uncovering a novel mechanistic vulnerability.

cancer biology↗

NAPRT expression and epigenetic regulation in pediatric rhabdomyosarcoma as a potential biomarker for NAMPT inhibition

PurposeNew treatments are needed to improve survival in children with rhabdomyosarcoma (RMS). NAD biosynthesis, regulated by the enzymes NAPRT and NAMPT, represents a metabolic vulnerability due to high NAD turnover in cancers. Although NAMPT inhibitors (NAMPTi) show preclinical promise, clinical translation has been limited by toxicity and the lack of predictive biomarkers. Here, we evaluated NAPRT expression in RMS and its potential as an actionable biomarker to guide NAMPTi therapy. Experimental DesignNAPRT promoter methylation, transcript levels, and protein expression were assessed in RMS cells, PDXs, and primary tumors (n=109) from the Childrens Oncology Group. In vitro sensitivity to NAMPTi was tested in molecularly diverse and isogenic RMS cell lines, examining the role of NAPRT expression in mediating cytotoxicity and the ability of nicotinic acid (NA) to rescue viability. In vivo efficacy was assessed using NAPRT-isogenic orthotopic xenograft models. ResultsNAPRT promoter hypermethylation was found in a subset of RMS models and patient samples. Immunohistochemistry showed loss of NAPRT protein in 30-40% of tumors, defined as <1% tumor cell staining. Methylation modestly correlated with protein expression. NAPRT-silenced cells were highly sensitive to NAMPTi, driven by NAD depletion and not reversible with NA. In vivo, NAMPTi induced significant tumor regression, which was not abrogated with NA administration in NAPRT-silenced models. ConclusionsNAPRT loss occurs in a subset of RMS, offering a potential strategy to expand the therapeutic window of NAMPTi. Further research is needed to understand NAPRT regulation and optimize biomarker assay strategies for use in future clinical trials.

cancer biology↗

Fusion transcription factor dosage controls cell state in rhabdomyosarcoma

In the fusion-positive subset of rhabdomyosarcoma, the PAX3::FOXO1 oncoprotein is the most common fusion driver. We previously established a human myoblast system for inducible expression of PAX3::FOXO1. In the current study, we modulate PAX3::FOXO1 protein expression to understand the epigenetic and phenotypic functions at different PAX3::FOXO1 levels. Proliferative and oncogenic outcomes depend on PAX3::FOXO1 dosage in this system with transformation dominant at intermediate levels and growth suppression dominant at high levels. After prolonged PAX3::FOXO1 expression, there is dosage-dependent heterogeneity in single cell gene expression profiles. We observe a dosage-specific effect for PAX3::FOXO1 chromatin recognition and identify factors that modulate PAX3::FOXO1 chromatin binding. PAX3::FOXO1 dosage affects expression signatures related to cell cycle, epithelial-mesenchymal transition, and myogenesis. Whereas intermediate PAX3::FOXO1 expression maximizes chromatin binding to modulate gene expression, high PAX3::FOXO1 expression alters S phase progression and increases accessibility behind the replication fork. We conclude that PAX3::FOXO1 exerts dosage-dependent functions to influence epigenetic heterogeneity in fusion-positive rhabdomyosarcoma.

genomics↗

Pioneer activity of an oncogenic fusion transcription factor at inaccessible chromatin

Recent characterizations of pioneer transcription factors have led to new insights into their structures and patterns of chromatin recognition that are instructive for understanding their role in cell fate commitment and transformation. Intersecting with these basic science concepts, the identification of pioneer factors (PFs) fused together as driver translocations in childhood cancers raises questions of whether these fusions retain the fundamental ability to invade repressed chromatin, consistent with their monomeric PF constituents. In this study, we define the cellular and chromatin localization of the translocation, PAX3-FOXO1, an oncogenic driver of childhood rhabdomyosarcoma (RMS), derived from a genetic fusion of PFs. To quantitatively define its chromatin-targeting functions and capacity to drive epigenetic reprogramming, we developed a new method for ChIP-seq with per-cell normalization (pc-ChIP-seq). Our quantitative localization studies address structural variation in RMS genomes and reveal novel insights into heterochromatin localization of PAX3-FOXO1. From these studies, we report novel pioneer function for the major driver oncogene in RMS, with repressed chromatin binding and nucleosome-motif targeting in human cells.

genomics↗