Qiu Weihua, Zhou Bingsen, Zou Hongzhi, Liu Xiyong, Chu Peiguo G, Lopez Richard, Shih Jennifer, Chung Christopher, Yen Yun
Department of Medical Oncology and Therapeutic Research, City of Hope National Medical Center, 1500 E. Duarte Rd., Duarte, CA 91010-3000, USA.
Am J Pathol. 2004 Nov;165(5):1689-99. doi: 10.1016/s0002-9440(10)63425-6.
Growth arrest DNA damage-inducible gene 45 beta (GADD45beta) has been known to regulate cell growth, apoptotic cell death, and cellular response to DNA damage. Down-regulation of GADD45beta has been verified to be specific in hepatocellular cancer (HCC) and consistent with the p53 mutant, and degree of malignancy of HCC. This observation was further confirmed by eight HCC cell lines and paired human normal and HCC tumor tissues by Northern blot and immunohistochemistry. To better understand the transcription regulation, we cloned and characterized the active promoter region of GADD45beta in luciferase-expressing vector. Using the luciferase assay, three nuclear factor-kappaB binding sites, one E2F-1 binding site, and one putative inhibition region were identified in the proximal promoter of GADD45beta from -865/+6. Of interest, no marked putative binding sites could be identified in the inhibition region between -520/-470, which corresponds to CpG-rich region. The demethylating agent 5-Aza-dC was used and demonstrated restoration of the GADD45beta expression in HepG2 in a dose-dependent manner. The methylation status in the promoter was further examined in one normal liver cell, eight HCC cell lines, eight HCC tissues, and five corresponding nonneoplastic liver tissues. Methylation-specific polymerase chain reaction and sequencing of the sodium bisulfite-treated DNA from HCC cell lines and HCC samples revealed a high percentage of hypermethylation of the CpG islands. Comparatively, the five nonneoplastic correspondent liver tissues demonstrated very low levels of methylation. To further understand the functional role of GADD45beta under-expression in HCC the GADD45beta cDNA constructed plasmid was transfected into HepG2 (p53 WT) and Hep3B (p53 null) cells. The transforming growth factor-beta was assayed by enzyme-linked immunosorbent assay, which revealed a decrease to 40% in transfectant of HepG2, but no significant change in Hep3B transfectant. Whereas, Hep3B co-transfected with p53 and GADD45beta demonstrated significantly reduced transforming growth factor-beta. The colony formation was further examined and revealed a decrease in HepG2-GADD45beta transfectant and Hep3B-p53/GADD45beta co-transfectant. These findings suggested that methylation might play a crucial role in the epigenetic regulation of GADD45beta in hepatocyte transformation that may be directed by p53 status. Thus, our results provided a deeper understanding of the molecular mechanism of GADD45beta down-regulation in HCC.
生长停滞和DNA损伤诱导基因45β(GADD45β)已知可调节细胞生长、凋亡性细胞死亡以及细胞对DNA损伤的反应。GADD45β的下调已在肝细胞癌(HCC)中得到证实,且与p53突变及HCC的恶性程度相关。通过Northern印迹法和免疫组织化学,在8种HCC细胞系以及配对的人正常和HCC肿瘤组织中进一步证实了这一观察结果。为了更好地理解转录调控,我们在表达荧光素酶的载体中克隆并鉴定了GADD45β的活性启动子区域。利用荧光素酶测定法,在GADD45β从-865/+6的近端启动子中鉴定出3个核因子κB结合位点、1个E2F-1结合位点和1个假定的抑制区域。有趣的是,在-520/-470之间的抑制区域(对应富含CpG的区域)未发现明显的假定结合位点。使用去甲基化剂5-氮杂-2'-脱氧胞苷,并证明其能以剂量依赖的方式恢复HepG2中GADD45β的表达。在1种正常肝细胞、8种HCC细胞系、8种HCC组织和5种相应的非肿瘤性肝组织中进一步检测了启动子中的甲基化状态。对HCC细胞系和HCC样本经亚硫酸氢钠处理的DNA进行甲基化特异性聚合酶链反应和测序,结果显示CpG岛的高甲基化比例很高。相比之下,5种非肿瘤性相应肝组织的甲基化水平非常低。为了进一步了解GADD45β在HCC中低表达的功能作用,将构建有GADD45β cDNA的质粒转染到HepG2(p53野生型)和Hep3B(p53缺失型)细胞中。通过酶联免疫吸附测定法检测转化生长因子-β,结果显示HepG2转染细胞中其水平降低至40%,而Hep3B转染细胞中无显著变化。然而,与p53和GADD45β共转染的Hep3B细胞中转化生长因子-β显著降低。进一步检测集落形成,结果显示HepG2-GADD45β转染细胞和Hep3B-p53/GADD45β共转染细胞中的集落形成减少。这些发现表明,甲基化可能在p53状态指导的肝细胞转化中GADD45β的表观遗传调控中起关键作用。因此,我们的结果为深入了解HCC中GADD45β下调的分子机制提供了依据。