食管癌中PLK1的转录调控及作用机制研究
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摘要
丝氨酸／苏氨酸蛋白激酶PLK1 (Polo-like kinase 1)在启动、维持及完成哺乳动物细胞有丝分裂过程中扮演重要角色,并且越来越多的研究表明PLK1在多种恶性肿瘤中表达异常升高。本实验室在前期工作中发现PLK1在食管鳞癌中存在基因扩增和蛋白过表达,敲降PLK1通过线粒体途径诱导食管癌细胞发生凋亡。多因素分析结果显示,PLK1蛋白过表达是一个独立的差预后因子。本研究旨在进一步深入探讨PLK1在食管鳞癌中发挥作用的分子机制。
我们首先利用GST Pull-down结合高效液相色谱-串联质谱技术(LC-MS/MS),高通量筛选了食管癌细胞中PLK1潜在的相互作用蛋白共213个,并利用免疫共沉淀对其中的候选分子IQGAP1、M2-PK和β-catenin与PLK1的相互作用进行了验证。β-catenin蛋白是Wnt信号传导通路中的核心成员,β-catenin/TCF通路的异常激活参与多种恶性肿瘤的发生发展,鉴此本研究对PLK1与β-catenin之间相互作用的分子机制和病理学意义做了进一步探索。研究结果表明,PLK1和β-catenin在食管癌细胞有丝分裂G2／M期存在体内相互作用,RNA干扰PLK1表达或抑制PLK1激酶活性后β-catenin的蛋白水平及转录活性降低,而Ser33磷酸化水平升高。利用蛋白酶体抑制剂MG-132处理后发现,β-catenin的泛素化修饰水平及与其降解相关蛋白GSK-3β/β-TrCP的相互作用随PLK1的下降而增强,提示β-catenin的泛素-蛋白酶体降解途径受PLK1调控。软琼脂集落形成及生长曲线实验显示,敲降PLK1显著抑制食管癌细胞的体外增殖和非锚定依赖生长能力,且该现象可被外源表达的β-catenin所逆转。在食管癌组织中,我们发现PLK1过表达与p-catenin在细胞浆／核中的异常累积具有相关性,并且同时具有PLK1与p-catenin蛋白异常表达的患者术后生存时间显著缩短。这些结果说明：食管癌中PLK1参与调控β-catenin与其降解复合物的相互作用及后续的泛素-蛋白酶体降解过程,PLK1过表达通过活化β-catenin信号通路增强食管癌细胞的恶性能力。
有研究发现β-catenin/TCF信号通路异常活化与细胞抵抗失巢凋亡能力相关,本文也观察到敲降β-catenin表达后食管癌细胞失巢凋亡比例增加,因此本文接下来对PLK1在食管癌细胞抗失巢凋亡中的作用进行了研究。我们首先发现,耐受失巢凋亡的食管癌细胞在诱导悬浮后内源性PLK1 mRNA及蛋白水平明显升高。进一步研究表明,PLK1在食管癌细胞悬浮过程中的表达增加通过激活β-catenin和MEK-ERK通路抑制细胞失巢凋亡。染色质免疫沉淀实验、凝胶电泳迁移率实验和缺失突变体的报告基因检测的结果,共同提示转录因子NF-kappaB p65直接与PLK1基因启动子区结合,并调节在细胞抗失巢凋亡过程中PLK1的转录活性。利用NF-kappaB信号通路抑制剂处理发现,细胞脱离基质后NF-kappaB p65通过上调PLK1的mRNA表达参与食管癌细胞抗失巢凋亡的作用。
本研究揭示了食管癌细胞中PLK1通过泛素-蛋白酶体途径调控β-catenin蛋白水平及转录活性,并进一步通过β-catenin调控细胞抗失巢凋亡能力这一重要现象。我们还发现NF-kappaB信号通路通过调节PLK1的基因转录参与细胞抵抗失巢凋亡这些结果为进一步阐明PLK1在食管癌发生发展中的作用机制提供了新的重要线索。
Serine/threonine kinase Polo-like kinase 1 (PLKl) is pivotal for mammalian cell mitosis regulation and is found frequently overexpressed in various kinds of human tumors. We have previously shown that overexpression of PLK1 is an independent prognostic factor and that depletion of PLK1 activated the intrinsic apoptotic pathway in esophageal squamous cell carcinoma (ESCC).
In the present study, we performed a proteomic analysis to elucidate the substrates and interacting proteins of PLK1. Based on the findings that phospho-dependent ligand recognition by the PBD is necessary for the targeting of PLK1 to specific substrates, GST-PBD was used as a bait to pull-down all the proteins associated with PBD in esophageal cancer cells. After analyzed by LC-MS/MS, a total of 213 proteins were identified potentially interacted with PBD. Co-immunoprecipitation (Co-IP) confirmed that IQGAP1, M2-PK and (3-catenin were all able to form complex with PLKl.
Although PLKl has been recently reported to phosphorylateβ-catenin, the biological consequences of their interaction remain to be elucidated. Here we demonstrated an important role of PLKl in regulating degradation ofβ-catenin protein. GST Pull-Down and Co-IP confirmed that PLKl interacted with (3-catenin in esophageal squamous cell carcinoma (ESCC) cells. SiRNA-mediated knockdown of PLK1 and forced expression of its kinase dead mutant caused a reduction inβ-catenin protein level and its transcription activity. Ubiquitinated form of (3-catenin was increased and interaction between (3-catenin and GSK-3(3/(3-Trcp was enhanced upon PLK1 depletion, suggesting that the destruction process of (3-catenin was accelerated. Overexpression of (3-catenin in PLKl down-regulated cells restored their ability to grow in soft agar. In primary esophageal tumors, (3-catenin accumulation in cytoplasm was correlated with high level of PLK1 expression. Combined survival analysis indicated that PLKl+/β-catenin+was a poor-prognostic factor in ESCC.
It has been reported that activation ofβ-catenin/TCF pathway protected cells from anoikis and we also confirmed this phenomenon in ESCC cells. We then investigated whether PLK1 was also involved in anoikis resistance. We found that detachment of esophageal tumor cells triggered upregulation of both PLK1 mRNA and protein. Enforced overexpression of PLKl delayed ESCC cell anoikis by activating MEK-ERK pathway. EMSA, CHIP and gene reporter assay indicated that NF-kappaB p65 bound directly to PLKl promoter and positively regulated PLK1 mRNA expression during cell suspension. Inhibition of NF-kappaB pathway caused a noticeable downregulation of PLKl and an increase of cell apoptosis after detachment. We conclude that PLKl is an important regulator of the detachment-triggered life signals in ESCC cells.
Taken together, our findings showed that PLKl played an important role in regulating both (3-catenin protein degradation andβ-catenin/TCF signaling pathway. Detachment-induced upregulation of PLK1 was driven by NF-kappaB at the transcription level. These mechanisms were involved in anoikis resistance of esophageal squamous carcinoma cells.
我们首先利用GST Pull-down结合高效液相色谱-串联质谱技术(LC-MS/MS),高通量筛选了食管癌细胞中PLK1潜在的相互作用蛋白共213个,并利用免疫共沉淀对其中的候选分子IQGAP1、M2-PK和β-catenin与PLK1的相互作用进行了验证。β-catenin蛋白是Wnt信号传导通路中的核心成员,β-catenin/TCF通路的异常激活参与多种恶性肿瘤的发生发展,鉴此本研究对PLK1与β-catenin之间相互作用的分子机制和病理学意义做了进一步探索。研究结果表明,PLK1和β-catenin在食管癌细胞有丝分裂G2／M期存在体内相互作用,RNA干扰PLK1表达或抑制PLK1激酶活性后β-catenin的蛋白水平及转录活性降低,而Ser33磷酸化水平升高。利用蛋白酶体抑制剂MG-132处理后发现,β-catenin的泛素化修饰水平及与其降解相关蛋白GSK-3β/β-TrCP的相互作用随PLK1的下降而增强,提示β-catenin的泛素-蛋白酶体降解途径受PLK1调控。软琼脂集落形成及生长曲线实验显示,敲降PLK1显著抑制食管癌细胞的体外增殖和非锚定依赖生长能力,且该现象可被外源表达的β-catenin所逆转。在食管癌组织中,我们发现PLK1过表达与p-catenin在细胞浆／核中的异常累积具有相关性,并且同时具有PLK1与p-catenin蛋白异常表达的患者术后生存时间显著缩短。这些结果说明：食管癌中PLK1参与调控β-catenin与其降解复合物的相互作用及后续的泛素-蛋白酶体降解过程,PLK1过表达通过活化β-catenin信号通路增强食管癌细胞的恶性能力。
有研究发现β-catenin/TCF信号通路异常活化与细胞抵抗失巢凋亡能力相关,本文也观察到敲降β-catenin表达后食管癌细胞失巢凋亡比例增加,因此本文接下来对PLK1在食管癌细胞抗失巢凋亡中的作用进行了研究。我们首先发现,耐受失巢凋亡的食管癌细胞在诱导悬浮后内源性PLK1 mRNA及蛋白水平明显升高。进一步研究表明,PLK1在食管癌细胞悬浮过程中的表达增加通过激活β-catenin和MEK-ERK通路抑制细胞失巢凋亡。染色质免疫沉淀实验、凝胶电泳迁移率实验和缺失突变体的报告基因检测的结果,共同提示转录因子NF-kappaB p65直接与PLK1基因启动子区结合,并调节在细胞抗失巢凋亡过程中PLK1的转录活性。利用NF-kappaB信号通路抑制剂处理发现,细胞脱离基质后NF-kappaB p65通过上调PLK1的mRNA表达参与食管癌细胞抗失巢凋亡的作用。
本研究揭示了食管癌细胞中PLK1通过泛素-蛋白酶体途径调控β-catenin蛋白水平及转录活性,并进一步通过β-catenin调控细胞抗失巢凋亡能力这一重要现象。我们还发现NF-kappaB信号通路通过调节PLK1的基因转录参与细胞抵抗失巢凋亡这些结果为进一步阐明PLK1在食管癌发生发展中的作用机制提供了新的重要线索。
Serine/threonine kinase Polo-like kinase 1 (PLKl) is pivotal for mammalian cell mitosis regulation and is found frequently overexpressed in various kinds of human tumors. We have previously shown that overexpression of PLK1 is an independent prognostic factor and that depletion of PLK1 activated the intrinsic apoptotic pathway in esophageal squamous cell carcinoma (ESCC).
In the present study, we performed a proteomic analysis to elucidate the substrates and interacting proteins of PLK1. Based on the findings that phospho-dependent ligand recognition by the PBD is necessary for the targeting of PLK1 to specific substrates, GST-PBD was used as a bait to pull-down all the proteins associated with PBD in esophageal cancer cells. After analyzed by LC-MS/MS, a total of 213 proteins were identified potentially interacted with PBD. Co-immunoprecipitation (Co-IP) confirmed that IQGAP1, M2-PK and (3-catenin were all able to form complex with PLKl.
Although PLKl has been recently reported to phosphorylateβ-catenin, the biological consequences of their interaction remain to be elucidated. Here we demonstrated an important role of PLKl in regulating degradation ofβ-catenin protein. GST Pull-Down and Co-IP confirmed that PLKl interacted with (3-catenin in esophageal squamous cell carcinoma (ESCC) cells. SiRNA-mediated knockdown of PLK1 and forced expression of its kinase dead mutant caused a reduction inβ-catenin protein level and its transcription activity. Ubiquitinated form of (3-catenin was increased and interaction between (3-catenin and GSK-3(3/(3-Trcp was enhanced upon PLK1 depletion, suggesting that the destruction process of (3-catenin was accelerated. Overexpression of (3-catenin in PLKl down-regulated cells restored their ability to grow in soft agar. In primary esophageal tumors, (3-catenin accumulation in cytoplasm was correlated with high level of PLK1 expression. Combined survival analysis indicated that PLKl+/β-catenin+was a poor-prognostic factor in ESCC.
It has been reported that activation ofβ-catenin/TCF pathway protected cells from anoikis and we also confirmed this phenomenon in ESCC cells. We then investigated whether PLK1 was also involved in anoikis resistance. We found that detachment of esophageal tumor cells triggered upregulation of both PLK1 mRNA and protein. Enforced overexpression of PLKl delayed ESCC cell anoikis by activating MEK-ERK pathway. EMSA, CHIP and gene reporter assay indicated that NF-kappaB p65 bound directly to PLKl promoter and positively regulated PLK1 mRNA expression during cell suspension. Inhibition of NF-kappaB pathway caused a noticeable downregulation of PLKl and an increase of cell apoptosis after detachment. We conclude that PLKl is an important regulator of the detachment-triggered life signals in ESCC cells.
Taken together, our findings showed that PLKl played an important role in regulating both (3-catenin protein degradation andβ-catenin/TCF signaling pathway. Detachment-induced upregulation of PLK1 was driven by NF-kappaB at the transcription level. These mechanisms were involved in anoikis resistance of esophageal squamous carcinoma cells.
引文
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