RUNX2 inhibition disrupts a PAX3::FOXO1-RUNX2 feed-forward loop and dismantles oncogenic gene programs in fusion-positive rhabdomyosarcoma

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RUNX2 inhibition disrupts a PAX3::FOXO1 feed-forward loop, inhibiting fusion-positive rhabdomyosarcoma cell growth, promoting differentiation, inducing apoptosis, and reducing tumor growth in vivo.

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This paper studied fusion-positive rhabdomyosarcoma, focusing on the PAX3::FOXO1 fusion–driven oncogenic program and identifying druggable dependencies using mRNA-seq of RMS patient tumors and experiments in human FP-RMS cell lines (Rh30 and Rh4). RUNX2 was found to be the top druggable dependency, and both genetic (RNAi) and pharmacologic (CADD522) RUNX2 inhibition suppressed cell growth, induced myogenic differentiation and apoptosis, and phenocopied PAX3::FOXO1 suppression; in vivo, RUNX2 blockade (conditional dox-inducible or CADD522) reduced xenograft tumor growth. Mechanistically, the authors report a PAX3::FOXO1 RUNX2 feed-forward loop in which PAX3::FOXO1 binds a RUNX2 enhancer to upregulate genes including MYOD1, while RUNX2 supports PAX3::FOXO1 mRNA and protein expression, though the main limitation explicitly noted is the translational need for pharmacologic tractability beyond the reported preclinical models. Relevance to endometriosis: the paper does not explicitly discuss endometriosis or adenomyosis; it was included in the corpus via a keyword match in the upstream search index.

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Abstract

Fusion-positive rhabdomyosarcoma is an aggressive pediatric cancer of skeletal muscle lineage, with a 5-year overall survival of <30% for high-risk disease, and <8% when metastatic. The PAX3::FOXO1 fusion gene, resulting from t (2:13), is a signature driver of fusion-positive rhabdomyosarcoma, but similar to other transcription-factor based fusion genes in other cancers, not currently pharmacologically tractable. To identify novel druggable proteins in fusion-positive rhabdomyosarcoma tumor tissue and cell lines, we performed mRNA-seq of RMS patient tumors and utilizing the human FP-RMS cell lines Rh30 and Rh4, found that the RUNX2 transcription factor was the top druggable dependency. In vitro loss of function studies using genetic (RNAi) or pharmacologic (small molecule CADD522) inhibition showed that RUNX2 suppression inhibited FP-RMS cell growth, induced myogenic differentiation and apoptosis, and phenocopied PAX3::FOXO1 suppression. In vivo loss of function studies using conditional (dox-inducible) or pharmacologic (small molecule CADD522) blockade of tumor growth in a xenograft model system showed that RUNX2 suppression inhibited tumor growth. Mechanistically, we identify a PAX3::FOXO1 feed-forward loop whereby PAX3::FOXO1 binds a RUNX2 enhancer to upregulate gene expression alongside MYOD1, while RUNX2 expression supports the expression of PAX3::FOXO1 at the mRNA and protein level. Significance RUNX2 inhibition reduces PAX3::FOXO1 expression and signaling, which impairs fusion-positive rhabdomyosarcoma oncogenic phenotypes. In vivo treatment with CADD522 decreased tumor growth and increased survival, indicating that RUNX2 is a promising therapeutic target.
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Abstract Fusion-positive rhabdomyosarcoma is an aggressive pediatric cancer of skeletal muscle lineage, with a 5-year overall survival of <30% for high-risk disease, and <8% when metastatic. The PAX3::FOXO1 fusion gene, resulting from t(2:13), is a signature driver of fusion-positive rhabdomyosarcoma, but similar to other transcription-factor based fusion genes in other cancers, not currently pharmacologically tractable. To identify novel druggable proteins in fusion-positive rhabdomyosarcoma tumor tissue and cell lines, we performed mRNA-seq of RMS patient tumors and utilizing the human FP-RMS cell lines Rh30 and Rh4, found that the RUNX2 transcription factor was the top druggable dependency. In vitro loss of function studies using genetic (RNAi) or pharmacologic (small molecule CADD522) inhibition showed that RUNX2 suppression inhibited FP-RMS cell growth, induced myogenic differentiation and apoptosis, and phenocopied PAX3::FOXO1 suppression. In vivo loss of function studies using conditional (dox-inducible) or pharmacologic (small molecule CADD522) blockade of tumor growth in a xenograft model system showed that RUNX2 suppression inhibited tumor growth. Mechanistically, we identify a PAX3::FOXO1 feed-forward loop whereby PAX3::FOXO1 binds a RUNX2 enhancer to upregulate gene expression alongside MYOD1, while RUNX2 expression supports the expression of PAX3::FOXO1 at the mRNA and protein level. Significance RUNX2 inhibition reduces PAX3::FOXO1 expression and signaling, which impairs fusion-positive rhabdomyosarcoma oncogenic phenotypes. In vivo treatment with CADD522 decreased tumor growth and increased survival, indicating that RUNX2 is a promising therapeutic target. Competing Interest Statement Spouse of CML is founder and owner of Grid Therapeutics, which is developing a monoclonal antibody for adult lung cancer. Lab of CML has received funding from Ryvu. Neither of these are related to the research in this manuscript. DG reports patents EP3897609B1 and WO2023209077A1. Footnotes Target journal: Cancer Research (AACR)

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