Peng Min, Yang Zheqiong, Zhang Hao, Jaafar Lahcen, Wang Guanghu, Liu Min, Flores-Rozas Hernan, Xu Jianming, Mivechi Nahid F, Ko Lan
Cancer Center, Institute of Molecular Medicine and Genetics, Medical College of Georgia, Georgia Regents University, Augusta, GA, USA.
Genes Cancer. 2013 Jan;4(1-2):26-38. doi: 10.1177/1947601913486345.
Alternative pre-mRNA splicing yields functionally distinct splice variants in regulating normal cell differentiation as well as cancer development. The putative tumor suppressor gene GT198 (PSMC3IP), encoding a protein also known as TBPIP and Hop2, has been shown to regulate steroid hormone receptor-mediated transcription and to stimulate homologous recombination in DNA repair. Here, we have identified 6 distinct GT198 splice variant transcripts generated by alternative promoter usage or alternative splicing. Various splice variant transcripts preserve a common open reading frame, which encodes the DNA binding domain of GT198. The splice variants act as dominant negatives to counteract wild-type GT198 activity in transcription and to abolish Rad51 foci formation during radiation-induced DNA damage. In fallopian tube cancer, we have identified 44 point mutations in GT198 clustered in 2 mutation hotspot sequences. The mutation hotspots coincide with the regulatory sequences responsible for alternative splicing, strongly supporting that imbalanced alternative splicing is a selected consequence in cancer. In addition, splice variant-associated cytoplasmic expression is found in tumors carrying germline or somatic GT198 mutations. An altered alternative splicing pattern with increased variants is also present in lymphoblastoid cells derived from familial breast cancer patients carrying GT198 germline mutations. Furthermore, GT198 and its variant are reciprocally expressed during mouse stem cell differentiation. The constitutive expression of the GT198 variant but not the wild type induces tumor growth in nude mice. Our results collectively suggest that mutations in the GT198 gene deregulate alternative splicing. Defective alternative splicing promotes antagonizing variants and in turn induces a loss of the wild type in tumorigenesis. The study highlights the role of alternative splicing in tumor suppressor gene inactivation.
可变前体mRNA剪接在调节正常细胞分化以及癌症发展过程中产生功能不同的剪接变体。假定的肿瘤抑制基因GT198(PSMC3IP)编码一种也被称为TBPIP和Hop2的蛋白质,已被证明可调节类固醇激素受体介导的转录,并在DNA修复中刺激同源重组。在此,我们鉴定出了6种由可变启动子使用或可变剪接产生的不同GT198剪接变体转录本。各种剪接变体转录本保留了一个共同的开放阅读框,该开放阅读框编码GT198的DNA结合结构域。这些剪接变体作为显性负性因子,在转录过程中抵消野生型GT198的活性,并在辐射诱导的DNA损伤期间消除Rad51灶的形成。在输卵管癌中,我们在GT198中鉴定出44个点突变,这些突变聚集在2个突变热点序列中。突变热点与负责可变剪接的调控序列重合,有力地支持了不平衡的可变剪接是癌症中的一个选择结果。此外,在携带种系或体细胞GT198突变的肿瘤中发现了与剪接变体相关的细胞质表达。在携带GT198种系突变的家族性乳腺癌患者来源的淋巴母细胞中也存在可变剪接模式改变且变体增加的情况。此外,GT198及其变体在小鼠干细胞分化过程中相互表达。GT198变体而非野生型的组成性表达在裸鼠中诱导肿瘤生长。我们的结果共同表明,GT198基因中的突变会使可变剪接失调。有缺陷的可变剪接促进拮抗变体的产生,进而在肿瘤发生过程中导致野生型的丧失。这项研究突出了可变剪接在肿瘤抑制基因失活中的作用。