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研究生:吳恆祥
研究生(外文):Heng-Hsiung
論文名稱:細胞質Apurinic Endonuclease 1經由活化NF-κB路徑促進肺腫瘤之發展與惡化
論文名稱(外文):Cytoplasmi Apurinic Endonuclease 1 Enhances Lung Tumor Progression and Malignancy via NF-κB Activation
指導教授:李 輝
學位類別:博士
校院名稱:中山醫學大學
系所名稱:醫學分子毒理學研究所
學門:醫藥衛生學門
學類:其他醫藥衛生學類
論文種類:學術論文
論文出版年:2010
畢業學年度:98
語文別:中文
論文頁數:159
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Apurinic endonuclease 1 (Ape1) 是一個多功能蛋白,主要參與DNA修補之base excision repair (BER) 路徑和經由氧化還原 (oxidation- reduction, redox) 作用活化 轉錄因子和促進其與DNA之結合能力,但是參與轉錄因子還原活化的Ape1是存在於細胞核 ? 還是細胞質?至今仍不清楚。本研究首先發現肺腫瘤組織與細胞株中Cox-2及細胞質Ape1的表現間有顯著的相關性,因此假設Ape1表現於細胞質時,會參與還原活化NF-κB和Cox-2的表現。為了釐清此一假設,本研究以定點突變 (site-direct mutagenesis) 之技術,將Ape1 之nuclear localization sequence (NLS) 序列刪除或突變,建立不同之Ape1表現載體 (ND7, ND20, ND30, ND41) 以及全序列之Ape1表現載體 (FL),然後將這些戴體轉染至剔除Ape1表現之shApe1#7 H157肺癌穩定細胞株,使其外源性的表現Ape1於細胞質或細胞核中。結果發現轉染ND20和ND30之細胞,具有最高含量之細胞質Ape1表現,同時發現這兩種細胞有較高NF-κB 之活化與Cox-2之表現。但是轉染ND7和ND41之細胞的Cox-2表現與NF-κB之活化與Ape1表現於細胞核的FL細胞一樣,都低於ND20和ND30細胞。若以Ape1還原力抑制劑—Resveratrol處理ND20和ND30細胞,則能有效抑制細胞質Ape1活化NF-κB路徑和Cox-2之表現。在in vitro細胞和in vivo動物之實驗模式中,細胞質Ape1表現較高之ND20和ND30細胞,有較高之致癌潛力 (oncogenic potential) 以及侵襲轉移的能力。在肺癌患者中,細胞質Ape1表現之肺癌患者,較細胞核Ape1表現之患者,有較差之臨床預後 (prognosis)。同時發現細胞質Ape1表現之患者的腫瘤復發或腫瘤遠端轉移的風險是Ape1表現於細胞核之患者的3.722倍。由以上結果推測,細胞質Ape1可經由活化NF-κB路徑而促進腫瘤的發展與惡化。若與resveratrol的合併使用,則會顯著提高細胞質Ape1表現之肺癌患者對cisplatin化療之感受性。
本研究室過去研究顯示,HPV感染與台灣不抽菸女性肺癌之形成有關。本研究進一步分析111個肺腫瘤中HPV16/18 E6致癌蛋白和Ape1表現之相關性,結果發現E6有表現之肺腫瘤組織的細胞質Ape1高表現之頻率,顯著較沒有E6表現之肺腫瘤為高 (P = 0.037)。為了釐清E6是否會促進Ape1之轉錄表現,本研究分別短暫轉染shE6和E6表現載體至TL-1和TL-4細胞中,結果發現TL-4細胞中之Ape1 mRNA和蛋白的表現,會隨者E6的轉染量之增加而增高,而在TL-1細胞則會因E6剔除而下降。同時TL-4細胞中E6的表現會活化NF-κB路徑和增加Cox-2的表現,但是E6剔除之TL-1細胞則會降低NF-κB路徑活化和Cox-2的表現。ChIP分析結果顯示,E6會經由誘發細胞中ROS的增高,增加CREB和AP-1結合至Ape1啟動子的能力,而促進Ape1的轉錄表現。為了瞭解E6是否會促進Ape1蛋白之亞硝化,造成Ape1由細胞核移至細胞質中 (nuclear export),本研究將FL-Ape1和E6表現載體同時短暫轉染至shApe1#7 H157細胞株,並以NO的清除劑carboxyl-PTIO處理,結果發現E6會顯著增加Ape1由細胞核移至細胞質中,而carboxyl-PTIO則會抑制E6所引起的Ape1表現於細胞質。若將不會被亞硝化之突變型Ape1表現載體C93S/C310S-Ape1和E6同時轉染至shApe1#7細胞,則發現E6無法增加突變型Ape1移至細胞質中。這些結果顯示E6會經由Ape1亞硝化,促進Ape1移至細胞質中。更有趣的是,本研究發現E6會經由促進細胞質Ape1的表現,活化Cox-2的表現和腫瘤細胞之侵襲能力。因此本研究結果顯示,細胞質表現之Ape1會經由活化NF-κB路徑和增加Cox-2表現,而促進肺腫瘤之發展與惡化,尤其是在HPV感染所引起之肺癌。


Apurinic endonuclease 1 (Ape1) is not only involved in base excision repair, but also activate some transcriptional factors via its redox activity. However, which subcellular localization of Ape1 involved in the activation of transcriptional factor remains unclear. We first observed that Cox-2 expression was associated with cytoplasmic Ape1 expression in lung tumors and cancer cell lines. We thus hypothesize that NF-κB is activated by cytoplasmic Ape1 to cause Cox-2 expression. Herein, we generated cytoplasmic and nuclear Ape1 in Ape1-knockdown lung cancer cells by exogenous expression of Ape1 containing various deletions and/or mutations of the nuclear localization sequence. It was observed that cytoplasmic Ape1, but not nuclear Ape1, induced Cox-2 expression via NF-κB activation. NF-κB activation by cytoplasmic Ape1 was diminished by the Ape1 redox activity inhibitor resveratrol. Cells expressing cytoplasmic Ape1 exhibited tumor progression and metastasis in vitro and in vivo as xenografts, but cells expressing nuclear Ape1 not. Patients with tumors containing elevated cytoplasmic Ape1 had poor prognosis and 3.722-fold risk of tumor recurrence and/or metastasis. Cytoplasmic Ape1 may therefore enhance lung tumor malignancy via NF-κB activation, suggesting that combination of cisplatin and specific redox inhibitor may improve chemotherapeutic response in patients with tumors containing elevated cytoplasmic Ape1.
Among 111 lung tumors, we further observed that HPV16/18 E6-positive lung tumors had higher cytoplasmic Ape1 expression than in HPV16/18-negative lung tumors (P = 0.037). To verify whether E6 could enhance subcellular localization of Ape1 via increased Ape1 transcription, HPV16 E6-positive TL-1 and –negative TL-4 lung cancer cells were used for knockdown and overexpression of E6 by shE6 and E6 vector, respectively. Our data showed that Ape1 mRNA and protein expression was increased by E6 overexpression in TL-4 cells and decreased by E6-knockdown in TL-1 cells. Meanwhile, increased Cox-2 expression was observed in E6-overexpressed TL-4 cells via activation of NF-κB pathway. By contrast, Cox-2 expression was decreased in E6-knockdown TL-1 cells via blocking NF-κB activation. ChIP analysis further showed that ROS induced by E6 may be linked with Ape1 transcription via increased CREB and AP-1 binding on Ape1 promoter. To further verify whether Ape1 nuclear export promoted by E6 is via increased S-nitrosation of Ape1, FL-Ape1 and E6 vector were co-transfected into shApe1#7 H157 stable clones and then the cells were treated with or without NO scavenger (carboxyl-PTIO). Our data indicated that cytoplasmic Ape1 expression in shApe1#7 stable clones with FL-Ape1 was markedly increased by E6 transfection, but the increase of cytoplasmic Ape1 expression was diminished by the treatment of carboxyl-PTIO. To further verify whether cytoplasmic Ape1 increased by E6 is via S-nitrosation of Ape1, FL-Ape1 was replaced by C93S/C310S mutant Ape1 to be transfected into E6-transfected shApe1#7 stable clones. The increase of cytoplasmic Ape1 was failed in E6-positive stable clones when co-transfected with mutant Ape1. These results strongly suggest that cytoplasmic Ape1 increased by E6 is predominately mediated through S-nitrosation of Ape1. More interestingly, the increase of cytoplamic Ape1 by E6 enhanced significantly cell invasion ability and increased Cox-2 expression. In summary, subcellular localization of Ape1 may be partially responsible for lung tumor progression and malignancy via activation of NF-κB signaling pathway, particularly in HPV E6-positive lung tumors.


1. 中文摘要 1
2. 英文摘要 3
3. 文獻綜論及序言 5
3.1. 肺癌 5
3.1.1. 肺癌之流行病學 5
3.1.2. 慢性發炎反應與肺癌之相關性 6
3.2. Apurinic endonuclease 1/Redox factor 1 (Ape1/Ref-1) 8
3.2.1. Ape1之功能 8
3.2.1.1. DNA鹼基切除修補 9
3.2.1.2. 轉錄因子之還原活化 9
3.2.2. Ape1基因之轉錄調控 10
3.2.3. 細胞中Ape1之轉譯後修飾作用及核、質分布之調控機轉 12
3.2.4. Ape1 表現與腫瘤發展之相關性 15
3.2.5. 以Ape1為標的之癌症治療 16
3.2.5.1. Ape1 DNA修補能力之抑制劑 17
3.2.5.2. Ape1還原能力之抑制劑 17
3.3. NF-κB訊號路徑 18
3.3.1. NF-κB訊號傳遞路逕活化之分子機轉 18
3.3.2. NF-κB與腫瘤發展之相關性 20
3.3.3. NF-κB路徑為目標之腫瘤治療 21
3.3.4. Cox-2表現與肺腫瘤發展之相關性 22
3.4. 人類乳突瘤病毒 (Human papillomavirus; HPV) 22
3.4.1. 人類乳突瘤病毒與不同癌症間之相關性 22
3.4.2. 人類乳突瘤病毒致癌機制 24
3.4.3. E6蛋白與NF-κB訊號路徑之活化 25
3.5 研究動機 26
4. 材料與方法: 29
4.1. 酵素 29
4.2. 商業套組(kit) 29
4.3. 試藥 29
4.4. 質體 29
4.5. 儀器 30
4.6. 細胞培養 31
4.7. 肺癌患者檢體之收集 32
4.8. 肺癌患者肺腫瘤組織RNA之萃取 32
4.9. 萃取肺癌細胞株 RNA 33
4.10. 反轉錄聚合酶連鎖反應 (Reverse transcriptase-RT) 33
4.11. 反轉錄聚合酶連鎖反應-聚合酶連鎖反應 (RT-PCR) 與即時定量聚
合酶連鎖反應 (Real-time PCR) 33
4.11.1. 反轉錄聚合酶連鎖反應-聚合酶連鎖反應 (RT-PCR) 33
4.11.2. 即時定量聚合酶連鎖反應 (Real-time PCR) 34
4.12. 細胞核蛋白與細胞質蛋白的製備 35
4.13. 免疫沈澱法 36
4.14. 西方點墨法 36
4.15. shRNA (small-hairpine RNA) 表現載體之準備 38
4.15.1. 限制酶反應 (Restriction Enzyme digestion) 和質體 (vector)
的處理 38
4.15.2. Insert RNA干擾引子的處理 38
4.15.3. 接合反應 (Ligation) 39
4.16. Ape1表現載體之構築 39
4.16.1. Ape1 insert的構築 39
4.16.2. 限制酶處理(Enzyme Digestion) 40
4.16.3. 從電泳凝膠中純化 DNA 40
4.16.4. 利用CIP(Alkaline Phosphatase,Calf Intestinal)將載體酵素
切位點去磷酸化 41
4.16.5. 接合反應(Ligation) 41
4.17. 利用化學法製備勝任細胞(Preparation of competent cell) 41
4.18. 構築的載體之確認與保存 42
4.18.1. 轉形作用(Transformation) 42
4.18.2. 菌落聚合酵素連鎖反應(Colony Polymerase Chain Reaction) 42
4.18.3. 自動定序反應的製備 (Autosequencing) 43
4.18.4 菌種保存 43
4.19. 萃取質體 DNA 44
4.20. 細胞轉染實驗 44
4.21. 篩選穩定細胞株(Screening of stable clones) 45
4.21.1. 篩選抗G418的shApe1穩定細胞株 (Screening of shApe1
stable clones by G418 selection) 45
4.21.2. 篩選穩定轉染Ape1表現載體之穩定細胞株 (Screening of
Ape1 stable clones) 45
4.22. 細胞免疫染色法 46
4.23. 核染質免疫沈澱聚合酶連鎖反應 46
4.24. Transient transfection和Reporter gene assay 48
4.24.1. 質體DNA的轉染 49
4.24.2. β-galactosidase 活性測定 49
4.24.3. Luciferase 活性測定 49
4.25. 凝膠遲滯分析法(Gel Retardation assay) 50
4.26. p50 reductive degree by F5M fluorescence assay 51
4.27. 細胞計數生長試驗 51
4.28. 群落形成試驗(Colony formation or foci formation) 52
4.29. 細胞侵潤測試 (Invasion) 52
4.30. 軟培養基非附著性生長試驗(Anchorage independent assay) 53
4.31. Mouse models 54
4.32. MTT {3-(4, 5-dimethylthiazol -2-yl) –25-diphenyltetrazolium bromide}
分析法 54
4.33. 免疫組織化學染色 55
4.34. 統計分析 55
4.35. DcFdA ROS 55
5. 結果 57
5.1. 肺腫瘤細胞之Ape1和Cox-2表現之相關性 57
5.2. 細胞質Ape1和細胞核Ape1對於Cox-2表現之影響 58
5.3. 細胞質Ape1活化NF-κB訊號路徑之分子機轉 59
5.3.1. 細胞質Ape1對IκBα/IκBβ之降解與NF-κB轉移至細胞核中
之影響 60
5.3.2. 細胞質Ape1對NF-κB與DNA結合能力之影響 61
5.3.3. Ape1還原能力抑制劑resveratrol 對細胞質Ape1活化 之NF-κB
訊號路徑之影響 61
5.4. 亞硝化 (nitrosation) 對Ape1之nuclear export 和促進Cox-2表現之影
響 62
5.5. 細胞質Ape1對細胞生長、致癌潛力和侵襲能力之影響 64
5.6. 細胞質之Ape1在異種移植腫瘤生長和侵襲轉移能力之影響 65
5.7. 細胞質Ape1細胞之MDR1 (multiple drug resistance 1) 和抗藥性較高 66
5.8. 肺腫瘤組織中Ape1於細胞核、質之分佈與Cox-2表現之相關性 67
5.9. 細胞質Ape1表現和臨床因子與肺癌患者預後之相關性 68
5.10. 細胞質Ape1與肺癌患者之術後腫瘤復發和遠端轉移間的相關性 68
5.11. 肺癌細胞中HPV16 E6蛋白促進Ape1轉錄表現之機制 69
5.12. 肺腫瘤細胞中HPV16 E6表現對Ape1蛋白之亞硝化、nuclear export
和細胞侵襲能力之影響 72
5.13. 剔除Ape1表現或以resveratrol處理會抑制E6蛋白誘發之Cox-2表
現和細胞之侵襲能力 74
5.14. 肺腫瘤中HPV16/18 E6蛋白與Ape1 mRNA、蛋白表現之相關性 75
5.15. 肺腫瘤中HPV16/18 E6蛋白與Ape1蛋白表現於細胞核和細胞質分
佈之相關性 75
5.16. HPV16/18 E6合併細胞質Ape1表現對肺癌患者臨床預後之影響 76
6. 討論 78
6.1. Ape1還原能力對NF-κB訊號路逕活化及Cox-2 表現之重要性 78
6.2. 細胞質Ape1活化NF-κB路徑之探討 78
6.3. 細胞質Ape1誘發之IκBβ降解與慢性發炎反應 80
6.4. 細胞質Ape1促進IκBα/IκBβ降解之可能機制 80
6.5. Cox-2在細胞質Ape1活化NF-κB路徑促進腫瘤發展的過程中之重要
性 82
6.6. 細胞質Ape1對HPV E6誘發NF-κB路徑活化之重要性 83
6.7. 53去活化與Ape1之表現 84
6.8. HPV E6表現造成Ape1亞硝化可能之分子機轉 85
6.9. 細胞質Ape1對抗藥性之影響 86
7. 參考文獻 88
8. 表與圖 115
Table 1. The relative expression of NF-kappaB-dependent genes in cytoplasmic
Ape1 (ND30) to nuclear Ape1 cells (FL). 115
Table 2. Association of Cox-2 expression with Ape1 expression in lung tumors of
cytoplasm, nucleus, and cytoplasm/nucleus subcellular localizations. 116
Table 3. Univariate and multivariate Cox regression analysis of the influence of
cytoplasmic Ape1 on the clinical outcome of lung cancer patients after
surgical therapy. 117
Table 4. Multivariate analysis of the association between cytoplasmic Ape1 levels
on tumor recurrence and/or metastasis of 74 lung cancer patients after surgical therapy. 119
Table 5. Multivariate Cox regression analysis of the influence of cytoplasmic
Ape1/Cox-2 expression on the clinical outcome of lung cancer patients
after surgical therapy. 120
Table 6. Association among HPV16/18 E6, Ape1 mRNA and protein expression
in lung tumors. 121
Table 7. Association between HPV16/18 E6 and subcellular localization of Ape1
in lung tumors 122
Table 8. Cox regression analysis of the potential factors of HPV16/18 E6 and
cytoplasmic Ape1 in lung cancer patients 123
Table 9. Association between nitrotyrosin and subcellular localization of Ape1
in lung tumors. 124
Table 10. Association of MDR1 mRNA expression with Ape1 expression in lung
tumors of cytoplasm, nucleus, and cytoplasm/nucleus subcellular localizations. 125
Figure 1. Correlation of Cox-2 expression in lung cancer cells with Ape1
expression. 126
Figure 2. Correlation of Cox-2 expression in lung cancer cells with the subcellular
localization of Ape1. 129
Figure 3. Cytoplasmic Ape1 increased activation of NF-κB signaling pathway in
Ape1-knockdown H157 cells stable and transiently transfected with the
ND20 and ND30. 132
Figure 4. Cytoplasmic Ape1 increased IκBα and IκBβ degradation, p65 nuclear
localization in Ape1-knockdown H157 cells stable and transiently transfected with the ND20 and ND30. 133
Figure 5. Cytoplasmic Ape1 enhanced NF-κB DNA binding in Ape1-knockdown
H157 cells transiently and stable transfected with the ND20 and
ND30. 135
Figure 6. Increasing Cox-2 and decreasing IκBα and IκBβ expression by
cytoplasmic Ape1 were mediated by the redox activity, but not repair
activity of Ape1. 136
Figure 7. Nitrosation of Ape1 leads to Ape1 nuclear export and Cox-2 induction.
137
Figure 8. Cytoplasmic Ape1 expressed in ND20 and ND30 stable clones
enhances tumor malignancy in vitro compared with FL, shNC and
vector control clones lacking cytoplasmic Ape1. 139
Figure 9. Cytoplasmic Ape1 expressed in ND20 and ND30 stable clones
enhances tumor malignancy in vivo compared with FL, shNC and vector control clones lacking cytoplasmic Ape1. 142
Figure 10. Sensitivity of clones expressed nuclear or cytoplasmic Ape1 to
cisplatin and doxirubicin. 144
Figure 11. Representative immunostainings of Ape1 and Cox-2 in lung tumors. 147
Figure 12. Kaplain-Meier analysis of survival curve between patients with or
without tumor recurrence and/or distant metastatic after surgical
therapy. 148
Figure 13. HPV 16 E6 activates Ape1 transcription via p53 inactivation and ROS
generation. 149
Figure 14. Ape1 nitrosation induced by HPV E6 leads Ape1 nuclear export and
increase of Cox-2 expression and invasion ability. 151
Figure 15. Depletion of Ape expression by shApe1 and treatment of carboxy-PTIO,
resveratrol, and BAY11-7082 abrogates HPV E6-induced Ape1 nuclear
export and increase of Cox-2 expression and invasion ability. 153
Figure 16. Effects of IL1β depletion by shRNA and anti-IL1β neutrolization on
Cox-2, IκBα, IκBβ, and Ape1 expressions in ND30 stable cells. 156
Figure 17. Diagram of GST-pull down assay experimental design. 157
9. 附錄 158
Supplementary Figure S1. Functions of APE1 158
Supplementary Figure S2. Schematic structure, based on functional studies
of APE1 structure with critical residues. 159



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