Park Ji Hyun, Szemes Marianna, Vieira Gabriella Cunha, Melegh Zsombor, Malik Sally, Heesom Kate J, Von Wallwitz-Freitas Laura, Greenhough Alexander, Brown Keith W, Zheng Y George, Catchpoole Daniel, Deery Michael J, Malik Karim
Cancer Epigenetics Laboratory University of Bristol, Bristol BS8 1TD, UK.
Department of Cellular Pathology, Southmead Hospital, Bristol, UK.
Mol Oncol. 2015 Mar;9(3):617-27. doi: 10.1016/j.molonc.2014.10.015. Epub 2014 Nov 15.
Approximately half of poor prognosis neuroblastomas (NBs) are characterized by pathognomonic MYCN gene amplification and MYCN over-expression. Here we present data showing that short-interfering RNA mediated depletion of the protein arginine methyltransferase 5 (PRMT5) in cell-lines representative of NBs with MYCN gene amplification leads to greatly impaired growth and apoptosis. Growth suppression is not apparent in the MYCN-negative SH-SY5Y NB cell-line, or in two immortalized human fibroblast cell-lines. Immunoblotting of NB cell-lines shows that high PRMT5 expression is strongly associated with MYCN-amplification (P < 0.004, Mann-Whitney U-test) and immunohistochemical analysis of primary NBs reveals that whilst PRMT5 protein is ubiquitously expressed in the cytoplasm of most cells, MYCN-amplified tumours exhibit pronounced nuclear PRMT5 staining. PRMT5 knockdown in MYCN-overexpressing cells, including the SHEP-21N cell-line with inducible MYCN expression leads to a dramatic decrease in MYCN protein and MYCN-associated cell-death in SHEP-21N cells. Quantitative gene expression analysis and cycloheximide chase experiments suggest that PRMT5 regulates MYCN at a post-transcriptional level. Reciprocal co-immunoprecipitation experiments demonstrated that endogenous PRMT5 and MYCN interact in both SK-N-BE(2)C and NGP cell lines. By using liquid chromatography - tandem mass spectrometry (LC-MS/MS) analysis of immunoprecipitated MYCN protein, we identified several potential sites of arginine dimethylation on the MYCN protein. Together our studies implicate PRMT5 in a novel mode of MYCN post-translational regulation and suggest PRMT5 plays a major role in NB tumorigenesis. Small-molecule inhibitors of PRMT5 may therefore represent a novel therapeutic strategy for neuroblastoma and other cancers driven by the MYCN oncogene.
大约一半预后不良的神经母细胞瘤(NBs)具有特征性的MYCN基因扩增和MYCN过表达。在此,我们展示的数据表明,在具有MYCN基因扩增的NBs代表性细胞系中,短干扰RNA介导的蛋白质精氨酸甲基转移酶5(PRMT5)缺失会导致生长和凋亡严重受损。在MYCN阴性的SH-SY5Y NB细胞系或两种永生化人成纤维细胞系中,生长抑制并不明显。对NB细胞系进行免疫印迹分析表明,PRMT5高表达与MYCN扩增密切相关(P < 0.004,Mann-Whitney U检验),对原发性NBs进行免疫组化分析显示,虽然PRMT5蛋白在大多数细胞的细胞质中普遍表达,但MYCN扩增的肿瘤显示出明显的细胞核PRMT5染色。在MYCN过表达的细胞中敲低PRMT5,包括具有可诱导MYCN表达的SHEP-21N细胞系,会导致SHEP-21N细胞中MYCN蛋白显著减少以及与MYCN相关的细胞死亡。定量基因表达分析和环己酰亚胺追踪实验表明,PRMT5在转录后水平调节MYCN。相互免疫共沉淀实验证明,内源性PRMT5和MYCN在SK-N-BE(2)C和NGP细胞系中相互作用。通过对免疫沉淀的MYCN蛋白进行液相色谱 - 串联质谱(LC-MS/MS)分析,我们鉴定出MYCN蛋白上几个潜在的精氨酸二甲基化位点。我们的研究共同表明PRMT5参与了MYCN翻译后调控的新模式,并提示PRMT5在NB肿瘤发生中起主要作用。因此,PRMT5的小分子抑制剂可能代表了一种针对神经母细胞瘤和其他由MYCN癌基因驱动的癌症的新型治疗策略。