Vrba Lukas, Garbe James C, Stampfer Martha R, Futscher Bernard W
a Arizona Cancer Center; The University of Arizona ; Tucson , AZ USA.
b Life Sciences Division; Lawrence Berkeley National Laboratory ; Berkeley , CA USA.
Epigenetics. 2015;10(11):1074-83. doi: 10.1080/15592294.2015.1106673.
Immortality is an essential characteristic of human carcinoma cells. We recently developed an efficient, reproducible method that immortalizes human mammary epithelial cells (HMEC) in the absence of gross genomic changes by targeting 2 critical senescence barriers. Consistent transcriptomic changes associated with immortality were identified using microarray analysis of isogenic normal finite pre-stasis, abnormal finite post-stasis, and immortal HMECs from 4 individuals. A total of 277 genes consistently changed in cells that transitioned from post-stasis to immortal. Gene ontology analysis of affected genes revealed biological processes significantly altered in the immortalization process. These immortalization-associated changes showed striking similarity to the gene expression changes seen in The Cancer Genome Atlas (TCGA) clinical breast cancer data. The most dramatic change in gene expression seen during the immortalization step was the downregulation of an unnamed, incompletely annotated transcript that we called MORT, for mortality, since its expression was closely associated with the mortal, finite lifespan phenotype. We show here that MORT (ZNF667-AS1) is expressed in all normal finite lifespan human cells examined to date and is lost in immortalized HMEC. MORT gene silencing at the mortal/immortal boundary was due to DNA hypermethylation of its CpG island promoter. This epigenetic silencing is also seen in human breast cancer cell lines and in a majority of human breast tumor tissues. The functional importance of DNA hypermethylation in MORT gene silencing is supported by the ability of 5-aza-2'-deoxycytidine to reactivate MORT expression. Analysis of TCGA data revealed deregulation of MORT expression due to DNA hypermethylation in 15 out of the 17 most common human cancers. The epigenetic silencing of MORT in a large majority of the common human cancers suggests a potential fundamental role in cellular immortalization during human carcinogenesis.
永生是人类癌细胞的一个基本特征。我们最近开发了一种高效、可重复的方法,通过靶向两个关键的衰老障碍,在没有明显基因组变化的情况下使人类乳腺上皮细胞(HMEC)永生。使用来自4个个体的同基因正常有限静止期、异常有限静止后期和永生HMEC的微阵列分析,确定了与永生相关的一致转录组变化。共有277个基因在从静止后期转变为永生的细胞中持续发生变化。对受影响基因的基因本体分析揭示了在永生化过程中显著改变的生物学过程。这些与永生化相关的变化与癌症基因组图谱(TCGA)临床乳腺癌数据中所见的基因表达变化惊人地相似。在永生化步骤中观察到的最显著的基因表达变化是一种未命名、注释不完整的转录本的下调,我们将其称为MORT(mortality,死亡率),因为它的表达与有限寿命的死亡表型密切相关。我们在此表明,MORT(ZNF667-AS1)在迄今为止检测的所有正常有限寿命人类细胞中均有表达,而在永生化的HMEC中丢失。MORT基因在死亡/永生边界处的沉默是由于其CpG岛启动子的DNA高甲基化。这种表观遗传沉默也见于人类乳腺癌细胞系和大多数人类乳腺肿瘤组织中。5-氮杂-2'-脱氧胞苷重新激活MORT表达的能力支持了DNA高甲基化在MORT基因沉默中的功能重要性。对TCGA数据的分析显示,在17种最常见的人类癌症中有15种由于DNA高甲基化导致MORT表达失调。MORT在大多数常见人类癌症中的表观遗传沉默表明其在人类致癌过程中的细胞永生中可能具有潜在的基本作用。