Texas Children's Cancer and Hematology Centers and The Faris D. Virani Ewing Sarcoma Center, Baylor College of Medicine, Houston, TX, 77030, USA.
Integrative Molecular and Biomedical Sciences Program, Baylor College of Medicine, Houston, TX, 77030, USA.
Oncogene. 2022 Dec;41(50):5373-5384. doi: 10.1038/s41388-022-02538-w. Epub 2022 Nov 8.
Osteosarcoma, the most common pediatric bone tumor, is an aggressive heterogeneous malignancy defined by complex chromosomal aberrations. Overall survival rates remain at ~70%, but patients with chemoresistant or metastatic disease have extremely poor outcomes of <30%. A subgroup of tumors harbor amplification of chromosome 8q24.2 and increased expression of the oncogenic long noncoding RNA (lncRNA) Plasmacytoma Variant Translocation-1 (PVT-1), which is associated with an extremely poor clinical prognosis. This study demonstrates that PVT-1 is critical for osteosarcoma tumor-initiation potential. Chromatin Hybridization by RNA Purification analysis identified Tripartite-Motif Containing Family 28 (TRIM28) as a novel PVT-1 binding partner. Mechanistically, co-immunoprecipitation studies showed the PVT-1/TRIM28 complex binds and increases SUMOylation of phosphatidylinositol 3-kinase catalytic subunit type 3 (Vps34), which leads to enhanced ubiquitination and degradation of tumor suppressor complex 2 (TSC2), thus contributing to increased self-renewal and stem cell phenotypes. Furthermore, we identified that osteosarcoma cells with increased PVT-1 have enhanced sensitivity to the SUMOylation inhibitor, TAK-981. Altogether, this study elucidated a role for PVT-1 in the enhancement of cancer stem-like behaviors, including migration and invasion, in osteosarcoma, and identified the novel PVT-1/TRIM28 axis signaling cascade as a potential therapeutic target for osteosarcoma treatment.
骨肉瘤是最常见的儿童骨肿瘤,是一种具有复杂染色体异常的侵袭性异质性恶性肿瘤。总体生存率仍保持在约 70%,但对化疗耐药或转移的患者,预后极差,<30%。一小部分肿瘤具有 8q24.2 染色体扩增和致癌长非编码 RNA(lncRNA)浆细胞瘤变异易位 1(PVT-1)表达增加,与极其不良的临床预后相关。本研究表明 PVT-1 对骨肉瘤肿瘤起始潜能至关重要。通过 RNA 纯化分析进行染色质杂交,鉴定出三结构域蛋白家族 28(TRIM28)是 PVT-1 的新型结合伴侣。从机制上讲,共免疫沉淀研究表明 PVT-1/TRIM28 复合物结合并增加了磷脂酰肌醇 3-激酶催化亚单位 3(Vps34)的 SUMO 化,导致肿瘤抑制复合物 2(TSC2)的泛素化和降解增加,从而促进了自我更新和干细胞表型。此外,我们发现 PVT-1 增加的骨肉瘤细胞对 SUMO 化抑制剂 TAK-981 更敏感。总之,本研究阐明了 PVT-1 在增强骨肉瘤中类似癌症干细胞的行为,包括迁移和侵袭中的作用,并确定了新型 PVT-1/TRIM28 轴信号级联作为骨肉瘤治疗的潜在治疗靶点。