Department of Cancer Biology, Dana-Farber Cancer Institute, Boston, Massachusetts 02115, USA.
Nature. 2010 Jan 21;463(7279):374-8. doi: 10.1038/nature08684.
Cyclin D1 belongs to the core cell cycle machinery, and it is frequently overexpressed in human cancers. The full repertoire of cyclin D1 functions in normal development and oncogenesis is unclear at present. Here we developed Flag- and haemagglutinin-tagged cyclin D1 knock-in mouse strains that allowed a high-throughput mass spectrometry approach to search for cyclin D1-binding proteins in different mouse organs. In addition to cell cycle partners, we observed several proteins involved in transcription. Genome-wide location analyses (chromatin immunoprecipitation coupled to DNA microarray; ChIP-chip) showed that during mouse development cyclin D1 occupies promoters of abundantly expressed genes. In particular, we found that in developing mouse retinas-an organ that critically requires cyclin D1 function-cyclin D1 binds the upstream regulatory region of the Notch1 gene, where it serves to recruit CREB binding protein (CBP) histone acetyltransferase. Genetic ablation of cyclin D1 resulted in decreased CBP recruitment, decreased histone acetylation of the Notch1 promoter region, and led to decreased levels of the Notch1 transcript and protein in cyclin D1-null (Ccnd1(-/-)) retinas. Transduction of an activated allele of Notch1 into Ccnd1(-/-) retinas increased proliferation of retinal progenitor cells, indicating that upregulation of Notch1 signalling alleviates the phenotype of cyclin D1-deficiency. These studies show that in addition to its well-established cell cycle roles, cyclin D1 has an in vivo transcriptional function in mouse development. Our approach, which we term 'genetic-proteomic', can be used to study the in vivo function of essentially any protein.
周期蛋白 D1 属于核心细胞周期机制,它在人类癌症中经常过表达。目前尚不清楚周期蛋白 D1 在正常发育和肿瘤发生中的全部功能。在这里,我们开发了 Flag 和血凝素标记的周期蛋白 D1 敲入小鼠品系,允许高通量质谱方法搜索不同小鼠器官中的周期蛋白 D1 结合蛋白。除了细胞周期伙伴外,我们还观察到了几个参与转录的蛋白质。全基因组定位分析(染色质免疫沉淀与 DNA 微阵列相结合;ChIP-chip)表明,在小鼠发育过程中,周期蛋白 D1 占据大量表达基因的启动子。特别是,我们发现,在发育中的小鼠视网膜中——一个对周期蛋白 D1 功能至关重要的器官——周期蛋白 D1 结合 Notch1 基因的上游调控区,在那里它可以募集 CREB 结合蛋白(CBP)组蛋白乙酰转移酶。周期蛋白 D1 的基因缺失导致 CBP 募集减少、Notch1 启动子区域的组蛋白乙酰化减少,从而导致周期蛋白 D1 缺失(Ccnd1(-/-))视网膜中的 Notch1 转录物和蛋白水平降低。将 Notch1 的激活等位基因转导到 Ccnd1(-/-) 视网膜中会增加视网膜祖细胞的增殖,表明 Notch1 信号的上调减轻了周期蛋白 D1 缺乏的表型。这些研究表明,除了其已确立的细胞周期作用外,周期蛋白 D1 在小鼠发育中具有体内转录功能。我们称之为“遗传蛋白质组学”的方法可用于研究体内任何蛋白质的功能。