APOBEC3G在胰腺癌中分子机制及其关键靶蛋白研究
摘要
目的：
胰腺癌是常见的消化道恶性肿瘤,死亡率居第4位,发病隐匿、进展快、早期出现转移,但治疗手段有限。阐明胰腺癌分子机制是治疗胰腺癌的基础和前提。近年研究提示病毒感染与消化道肿瘤发生发展关系密切,然病毒感染对肿瘤恶性生物学行为影响尚不明了。APOBEC酶作为一种常见的病毒感染反应性蛋白,能使病毒DNA发生超突变,具有广谱抗病毒能力。近来研究提示APOBEC蛋白不仅有抗病毒作用,而且在肿瘤中也有重要功能。本研究目的是通过筛选和鉴定参与肿瘤细胞恶性生物学行为的APOBEC家族成员；检测APOBEC3G(A3G)在胰腺癌中的表达改变；改变A3G表达水平对胰腺癌细胞生物学行为影响的分子机制,以及鉴定其关键作用靶蛋白,从而明确A3G对胰腺癌恶性生物学行为的影响。
方法：
采用全基因cDNA表达谱芯片筛选参与肿瘤细胞恶性生物学行为的病毒相关蛋白。为探讨A3G在胰腺癌表达情况,采用Real-time PCR检测3株胰腺癌细胞系,11例配对胰腺癌及癌旁组织中A3G mRNA水平；采用免疫组化和免疫荧光进一步验证54例配对胰腺癌病理组织切片中A3G蛋白的表达情况。为评价A3G在胰腺癌中的作用,建立了稳定表达A3G的胰腺癌细胞系,并观察过表达A3G对裸鼠皮下移植瘤形成情况的影响。为研究A3G早期促进成瘤的分子机制,采用克隆球形成试验、失巢凋亡(anoikis)实验和流式检测早期凋亡水平,并用western blot检测凋亡相关蛋白表达情况。为进一步研究A3G抑制anoikis的分子机制,我们检测了Akt通路活性,western blot检测了Akt通路中关键抑制蛋白PTEN的表达,并用免疫共沉淀方法检测A3G与PTEN的相互作用。同时采用荧光素酶双报告基因方法检测了Wnt通路活性,用免疫共沉淀筛选作用于Wnt通路的关键蛋白。我们进一步构建各种结构域突变体分析A3G与PTEN、FZD蛋白的结合位点。
结果：
基因芯片筛选发现病毒感染反应性蛋白A3G可能参与肿瘤恶性生物学行为；A3G在胰腺癌细胞和组织中表达升高；高表达A3G早期可促进动物移植瘤的成瘤,晚期又能抑制肿瘤生长；体外研究发现A3G增加了抗凋亡蛋白Bcl-2, Mcl-1和phospho-Bcl-2的表达,显著抑制胰腺癌细胞的anoikis;进一步发现过表达A3G是通过激活Akt激酶活性从而参与anoikis抵抗,A3G激活Akt通路是通过灭活PTEN蛋白活性实现的,A3G与PTEN结合需要A3G的CD2结构域存在,PTEN与A3G结合需要PTEN的C2结构域和PDZ结构域的存在。我们还发现A3G通过与FZD1蛋白结合参与调控Wnt通路,A3G与FZD1结合与A3G磷酸化水平相关,与结构域无明显相关性；FZD1与A3G结合需要两个结构域均存在。
结论：
病毒感染反应性蛋白A3G在胰腺癌中表达升高,可能通过灭活PTEN介导的Akt通路激活导致anoikis抵抗,通过FZD参与调控Wnt通路活性,提示A3G除抗病毒作用外还参与了肿瘤恶性生物学行为的调控。
Purpose:
Pancreatic cancer is a common gastrointestinal malignancy cancers, which is the fourth cause of cancer-related deaths, with occult onset, rapid progression, early metastasis, and limited treatment. To clarify the molecular mechanisms of pancreatic cancer is the basis and premise for the treatment. Recent research suggests that many gastrointestinal cancers are related with virus infection, but the role of virus infection in the biological behaviors of cancer cells remains unclear. As a virus-reactive protein, APOBEC enzyme can cause hypermutation in the viral DNA, presenting extensive anti-virus capability. Recent studies have found that APOBEC protein not only has antiviral activity, but also has an important function in cancers. The purpose of this study is to screen and identify APOBEC family members involved in the malignant behavior of tumor cells; to detect the A3G expression in pancreatic cancer; to observe the molecular mechanisms of APOBEC3G(A3G) in pancreatic cancer, and to identify the target proteins, thereby clarifying the effect of A3G on malignant behavior of pancreatic cancer.
Methods:
The whole genome cDNA expression microarray was used to screen virus-reactive proteins involved in the malignant behavior of cancer cells. The mRNA level of A3G was examined using TaqMan real-time PCR in3kinds of pancreatic cancer cells,11matched human pancreatic cancer and para-cancerous tissues. Immunohistochemistry and immunofluorescence were used to validate the A3G expression in54matched human pancreatic cancer pathological slides. To evaluate the role of A3G in pancreatic cancer in vivo, pancreatic cancer cell line stably expressing A3G was established and injected subcutaneously into nude mice. To investigate the molecular mechanisms of A3G early promoting the tumor formation, the cloning formation assay, anoikis assay and flow cytometry analysis were used. The expression of apoptosis-related proteins were detected by western blot. To clarify the molecular mechanism of A3G-induced anoikis resistance, the Akt kinase activity and PTEN expression were detected. Furthermore, the interaction between A3G and PTEN was examined by immunoprecipitation. The Wnt pathway activity was detected by luciferase dual reporter gene assay, and the target protein in Wnt pathway was revealed by immunoprecipitation. The domain mutants were established to analyze the binding sites of A3G and target proteins.
Results:
Microarray screening found that virus-reactive protein A3G might be involved in the malignant biological behavior of cancer; A3G was significantly up-regulated in pancreatic cancer cells and tissues. Up-regulation of A3G promoted xenograft tumor formation at early stage, and inhibited the tumor sizes at late stage. We further found that A3G could inhibit anoikis in pancreatic cancer cells, with the elevated expression of anti-apoptotic proteins Bcl-2, Mcl-1, and phospho-Bcl-2. Overexpression of A3G participated in anoikis resistance through the activation of Akt kinase activity, Akt pathway was activated by A3G-induced inactivation of PTEN. Furthermore, The combination of A3G and PTEN required the the CD2domain of A3G, the C2tensin-type and PDZ domain of PTEN. We also found that A3G was involved in the regulation of Wnt pathway by binding to FZD1. The combination of A3G and FZD1depended on the phosphorylation level, with no significant correlation with the domain of A3G, but was associated with the conserved and PDZ domain of FZD1.
Conclusions:
The virus-reactive protein A3G is up-regulated in pancreatic cancer cells. Overexpression of A3G activates Akt pathway through inactivation of PTEN, which leads to the anoikis resistance in pancreatic cancer cells, meanwhile A3G combines with FZD to disrupt the activity of Wnt pathway, suggesting that A3G affects the malignant behaviors of pancreatic cancer cells besides antiviral ability.
胰腺癌是常见的消化道恶性肿瘤,死亡率居第4位,发病隐匿、进展快、早期出现转移,但治疗手段有限。阐明胰腺癌分子机制是治疗胰腺癌的基础和前提。近年研究提示病毒感染与消化道肿瘤发生发展关系密切,然病毒感染对肿瘤恶性生物学行为影响尚不明了。APOBEC酶作为一种常见的病毒感染反应性蛋白,能使病毒DNA发生超突变,具有广谱抗病毒能力。近来研究提示APOBEC蛋白不仅有抗病毒作用,而且在肿瘤中也有重要功能。本研究目的是通过筛选和鉴定参与肿瘤细胞恶性生物学行为的APOBEC家族成员；检测APOBEC3G(A3G)在胰腺癌中的表达改变；改变A3G表达水平对胰腺癌细胞生物学行为影响的分子机制,以及鉴定其关键作用靶蛋白,从而明确A3G对胰腺癌恶性生物学行为的影响。
方法：
采用全基因cDNA表达谱芯片筛选参与肿瘤细胞恶性生物学行为的病毒相关蛋白。为探讨A3G在胰腺癌表达情况,采用Real-time PCR检测3株胰腺癌细胞系,11例配对胰腺癌及癌旁组织中A3G mRNA水平；采用免疫组化和免疫荧光进一步验证54例配对胰腺癌病理组织切片中A3G蛋白的表达情况。为评价A3G在胰腺癌中的作用,建立了稳定表达A3G的胰腺癌细胞系,并观察过表达A3G对裸鼠皮下移植瘤形成情况的影响。为研究A3G早期促进成瘤的分子机制,采用克隆球形成试验、失巢凋亡(anoikis)实验和流式检测早期凋亡水平,并用western blot检测凋亡相关蛋白表达情况。为进一步研究A3G抑制anoikis的分子机制,我们检测了Akt通路活性,western blot检测了Akt通路中关键抑制蛋白PTEN的表达,并用免疫共沉淀方法检测A3G与PTEN的相互作用。同时采用荧光素酶双报告基因方法检测了Wnt通路活性,用免疫共沉淀筛选作用于Wnt通路的关键蛋白。我们进一步构建各种结构域突变体分析A3G与PTEN、FZD蛋白的结合位点。
结果：
基因芯片筛选发现病毒感染反应性蛋白A3G可能参与肿瘤恶性生物学行为；A3G在胰腺癌细胞和组织中表达升高；高表达A3G早期可促进动物移植瘤的成瘤,晚期又能抑制肿瘤生长；体外研究发现A3G增加了抗凋亡蛋白Bcl-2, Mcl-1和phospho-Bcl-2的表达,显著抑制胰腺癌细胞的anoikis;进一步发现过表达A3G是通过激活Akt激酶活性从而参与anoikis抵抗,A3G激活Akt通路是通过灭活PTEN蛋白活性实现的,A3G与PTEN结合需要A3G的CD2结构域存在,PTEN与A3G结合需要PTEN的C2结构域和PDZ结构域的存在。我们还发现A3G通过与FZD1蛋白结合参与调控Wnt通路,A3G与FZD1结合与A3G磷酸化水平相关,与结构域无明显相关性；FZD1与A3G结合需要两个结构域均存在。
结论：
病毒感染反应性蛋白A3G在胰腺癌中表达升高,可能通过灭活PTEN介导的Akt通路激活导致anoikis抵抗,通过FZD参与调控Wnt通路活性,提示A3G除抗病毒作用外还参与了肿瘤恶性生物学行为的调控。
Purpose:
Pancreatic cancer is a common gastrointestinal malignancy cancers, which is the fourth cause of cancer-related deaths, with occult onset, rapid progression, early metastasis, and limited treatment. To clarify the molecular mechanisms of pancreatic cancer is the basis and premise for the treatment. Recent research suggests that many gastrointestinal cancers are related with virus infection, but the role of virus infection in the biological behaviors of cancer cells remains unclear. As a virus-reactive protein, APOBEC enzyme can cause hypermutation in the viral DNA, presenting extensive anti-virus capability. Recent studies have found that APOBEC protein not only has antiviral activity, but also has an important function in cancers. The purpose of this study is to screen and identify APOBEC family members involved in the malignant behavior of tumor cells; to detect the A3G expression in pancreatic cancer; to observe the molecular mechanisms of APOBEC3G(A3G) in pancreatic cancer, and to identify the target proteins, thereby clarifying the effect of A3G on malignant behavior of pancreatic cancer.
Methods:
The whole genome cDNA expression microarray was used to screen virus-reactive proteins involved in the malignant behavior of cancer cells. The mRNA level of A3G was examined using TaqMan real-time PCR in3kinds of pancreatic cancer cells,11matched human pancreatic cancer and para-cancerous tissues. Immunohistochemistry and immunofluorescence were used to validate the A3G expression in54matched human pancreatic cancer pathological slides. To evaluate the role of A3G in pancreatic cancer in vivo, pancreatic cancer cell line stably expressing A3G was established and injected subcutaneously into nude mice. To investigate the molecular mechanisms of A3G early promoting the tumor formation, the cloning formation assay, anoikis assay and flow cytometry analysis were used. The expression of apoptosis-related proteins were detected by western blot. To clarify the molecular mechanism of A3G-induced anoikis resistance, the Akt kinase activity and PTEN expression were detected. Furthermore, the interaction between A3G and PTEN was examined by immunoprecipitation. The Wnt pathway activity was detected by luciferase dual reporter gene assay, and the target protein in Wnt pathway was revealed by immunoprecipitation. The domain mutants were established to analyze the binding sites of A3G and target proteins.
Results:
Microarray screening found that virus-reactive protein A3G might be involved in the malignant biological behavior of cancer; A3G was significantly up-regulated in pancreatic cancer cells and tissues. Up-regulation of A3G promoted xenograft tumor formation at early stage, and inhibited the tumor sizes at late stage. We further found that A3G could inhibit anoikis in pancreatic cancer cells, with the elevated expression of anti-apoptotic proteins Bcl-2, Mcl-1, and phospho-Bcl-2. Overexpression of A3G participated in anoikis resistance through the activation of Akt kinase activity, Akt pathway was activated by A3G-induced inactivation of PTEN. Furthermore, The combination of A3G and PTEN required the the CD2domain of A3G, the C2tensin-type and PDZ domain of PTEN. We also found that A3G was involved in the regulation of Wnt pathway by binding to FZD1. The combination of A3G and FZD1depended on the phosphorylation level, with no significant correlation with the domain of A3G, but was associated with the conserved and PDZ domain of FZD1.
Conclusions:
The virus-reactive protein A3G is up-regulated in pancreatic cancer cells. Overexpression of A3G activates Akt pathway through inactivation of PTEN, which leads to the anoikis resistance in pancreatic cancer cells, meanwhile A3G combines with FZD to disrupt the activity of Wnt pathway, suggesting that A3G affects the malignant behaviors of pancreatic cancer cells besides antiviral ability.
引文
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[1]Xu J, Liu H, Chen L, Wang S, Zhou L, Yun X, Sun L, Wen Y, Gu J. Hepatitis B virus X protein confers resistance of hepatoma cells to anoikis by up-regulating and activating p21-activated kinase 1. Gastroenterology 2012; 143(1):199-212.
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[1]Zhong X, Rescorla FJ. Cell surface adhesion molecules and adhesion-initiated signaling:understanding of anoikis resistance mechanisms and therapeutic opportunities. Cell Signal 2012; 24(2):393-401.
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[1]Li X, Ma J, Zhang Q, Zhou J, Yin X, Zhai C, You X, Yu L, Guo F, Zhao L, Li Z, Zeng Y, Cen S. Functional analysis of the two cytidine deaminase domains in APOBEC3G. Virology 2011; 414(2):130-136.
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[1]Herr P, Hausmann G, Basler K. WNT secretion and signalling in human disease. Trends Mol Med 2012; 18(8):483-493.
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