Authors' Affiliations: Departments of Pathology and Dermatology, New York University School of Medicine; Interdisciplinary Melanoma Cooperative Group, New York University Cancer Institute, New York University Langone Medical Center; Departments of Structural and Chemical Biology and Medicine, Icahn School of Medicine at Mount Sinai, New York, New York; Instituto de Salud Carlos III, Majadahonda, Madrid; and Laboratory of Translational Research in Childhood Cancer, Vall d'Hebrón Institut de Recerca (VHIR), Barcelona, Spain.
Cancer Res. 2013 Oct 15;73(20):6264-76. doi: 10.1158/0008-5472.CAN-13-0122-T. Epub 2013 Aug 15.
Metastatic melanoma remains a mostly incurable disease. Although newly approved targeted therapies are efficacious in a subset of patients, resistance and relapse rapidly ensue. Alternative therapeutic strategies to manipulate epigenetic regulators and disrupt the transcriptional program that maintains tumor cell identity are emerging. Bromodomain and extraterminal domain (BET) proteins are epigenome readers known to exert key roles at the interface between chromatin remodeling and transcriptional regulation. Here, we report that BRD4, a BET family member, is significantly upregulated in primary and metastatic melanoma tissues compared with melanocytes and nevi. Treatment with BET inhibitors impaired melanoma cell proliferation in vitro and tumor growth and metastatic behavior in vivo, effects that were mostly recapitulated by individual silencing of BRD4. RNA sequencing of BET inhibitor-treated cells followed by Gene Ontology analysis showed a striking impact on transcriptional programs controlling cell growth, proliferation, cell-cycle regulation, and differentiation. In particular, we found that, rapidly after BET displacement, key cell-cycle genes (SKP2, ERK1, and c-MYC) were downregulated concomitantly with the accumulation of cyclin-dependent kinase (CDK) inhibitors (p21 and p27), followed by cell-cycle arrest. Importantly, BET inhibitor efficacy was not influenced by BRAF or NRAS mutational status, opening the possibility of using these small-molecule compounds to treat patients for whom no effective targeted therapy exists. Collectively, our study reveals a critical role for BRD4 in melanoma tumor maintenance and renders it a legitimate and novel target for epigenetic therapy directed against the core transcriptional program of melanoma.
转移性黑色素瘤仍然是一种基本无法治愈的疾病。尽管新批准的靶向治疗在一部分患者中有效,但耐药性和复发很快就会出现。操纵表观遗传调节剂和破坏维持肿瘤细胞特征的转录程序的替代治疗策略正在出现。溴结构域和末端结构域(BET)蛋白是已知在染色质重塑和转录调控之间的界面发挥关键作用的表观基因组读取器。在这里,我们报告 BRD4,一种 BET 家族成员,在原发性和转移性黑色素瘤组织中与黑色素细胞和痣相比显著上调。BET 抑制剂的治疗在体外损害了黑色素瘤细胞的增殖,并在体内损害了肿瘤生长和转移行为,这些效应主要通过 BRD4 的单独沉默来重现。用 BET 抑制剂处理的细胞进行 RNA 测序,然后进行基因本体分析,显示出对控制细胞生长、增殖、细胞周期调节和分化的转录程序的惊人影响。特别是,我们发现,在 BET 置换后迅速,关键的细胞周期基因(SKP2、ERK1 和 c-MYC)与细胞周期蛋白依赖性激酶(CDK)抑制剂(p21 和 p27)的积累同时下调,随后发生细胞周期停滞。重要的是,BET 抑制剂的疗效不受 BRAF 或 NRAS 突变状态的影响,为使用这些小分子化合物治疗没有有效靶向治疗的患者开辟了可能性。总的来说,我们的研究揭示了 BRD4 在黑色素瘤肿瘤维持中的关键作用,并使其成为针对黑色素瘤核心转录程序的表观遗传治疗的一个合理的新靶标。