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研究生:蔡宜珍
研究生(外文):Yi-Jane Tsai
論文名稱:組蛋白乙醯化修飾於光動力治療所引發促存活分子表達之機制探討及臨床應用
論文名稱(外文):Histone acetylation involves in the increased expression of prosurvival molecules induced by photodynamic therapy: mechanistic investigation and clinical implication
指導教授:陳進庭
口試委員:楊維中李銘仁張麗冠林晉玄
口試日期:2015-07-23
學位類別:博士
校院名稱:國立臺灣大學
系所名稱:生化科技學系
學門:生命科學學門
學類:生物科技學類
論文種類:學術論文
論文出版年:2015
畢業學年度:103
語文別:中文
論文頁數:168
中文關鍵詞:光動力治療組蛋白乙醯化組蛋白乙醯化轉酶COX-2survivin
外文關鍵詞:Photodynamic therapyHistone acetylationHistone acetyltransferaseCOX-2survivin
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光動力治療(Photodynamic therapy, PDT)能藉由產生氧化壓力引發腫瘤毒殺效應,為極有潛力之癌症治療方式。但是近年研究發現,經過光動力治療後之腫瘤細胞可能會經由誘發促存活分子cyclooxygenase-2 (COX-2)的表達,導致腫瘤復發。然而目前對於COX-2是如何在光動力治療後表現的相關機轉尚未明瞭,因此於本研究中,我們將深入探討光動力治療引發促存活分子COX-2轉錄的分子機轉,並藉此發展增進光動力治療之治療模式。本研究首先發現處以光感物質五氨基酮戊酸(ALA)或chlorin e6 (Ce6)之光動力治療皆能活化p38MAPK,並顯著提升人類黑色素瘤A375和老鼠大腸癌C26細胞中組蛋白乙醯化轉酶(histone acetyltransferase) p300HAT的表現及活性,且能觀察到光動力治療後組蛋白乙醯化(Histone acetylation)顯著上升。以組蛋白乙醯化轉酶抑制劑anacardic acid (AA)或p300HAT之shRNA阻止p300HAT於光動力治療後上升,會大幅減低細胞核內組蛋白乙醯化程度,並抑制COX-2表現。使用染色質免疫沉澱(chromatin immunoprecipitation)分析,顯示光動力治療後會吸引更多p300HAT結合至COX-2的啟動子區域,加強組蛋白及轉錄因子NF-κB之乙醯化修飾,提升COX-2的轉錄,而類似的結果能經由處理過PEGylated Liposome Ce6 (PL-Ce6)-PDT之A375或C26小鼠腫瘤模式獲得證實。接著使用組蛋白乙醯化轉酶抑制劑anacardic acid (AA)處理A375和C26細胞,發現能有效提升光動力治療之細胞毒殺效果。進一步於植有C26腫瘤之BALB/c小鼠進行實驗,發現相較於只接受光動力治療,或光動力治療結合COX-2抑制劑組別,組蛋白乙醯化轉酶抑制劑AA結合光動力治療能最為顯著抑制腫瘤生長。實驗更發現除了COX-2外,促存活分子survivin在光動力治療後,同樣也會受到活化的組蛋白乙醯化轉酶調控而加強其表現。最後證實結合組蛋白乙醯化轉酶抑制劑AA與光動力治療之結合型治療能藉由抑制survivin表現,提升caspase-3活性,造成Becline-1裂解而阻礙光動力治療後之細胞自噬,同時加強細胞凋亡發生。綜合以上,顯示光動力治療能藉由p38MAPK路徑活化組蛋白乙醯化轉酶,而促使促存活分子表現,我們藉此發展組蛋白乙醯化轉酶抑制劑結合光動力治療之結合型治療模式,並證實在細胞和動物實驗中都能有效提升光動力之治療效益,希望對於將來臨床應用能提供新的治療方向。

Oxidative stress induced by photodynamic therapy (PDT) mediates the tumoricidal effect, but has also been shown to induce the expression of pro-survival molecules, such as cyclooxygenase-2 (COX-2), which are involved in tumor recurrences after PDT. However, the molecular mechanism is still not fully understood. In this study, we found that PDT-induced p38MAPK activation could significantly up-regulate the activity and expression of histone acetyltransferase p300 (p300HAT) in A375 and C26 cells under ALA or chlorin e6 (Ce6) mediated photodynamic treatment. Colony-formation assay showed PDT-induced cytotoxicity was dramatically elevated in the presence of p300HAT inhibitor, anacardic acid (AA). Further studies showed that the increased p300HAT can transfer the acetyl group to histone H3 and NF-κB p65 subunit to up-regulate the COX-2 expression. The effect was reduced by the shRNA of AA or p300HAT. Using chromatin immunoprecipitation analysis, we found that the acetylation of histone H3 and NF-κB increases their binding to the COX-2 promoter region. These findings were further verified in the in vivo xenograft mouse model bearing murine C26 and human A375 tumors treated with PEGylated Liposome Ce6 (PL-Ce6) mediated PDT. Meanwhile, the combination of PDT and AA resulted in a greater tumor regression in BALB/c mice bearing C26 tumors, compared to those treated with PDT only or combined with COX-2 inhibitor. Finally, we demonstrated that suppression of the PDT-induced p300HAT activity also resulted in the decreased expression of survivin, restoring caspase-3 activity and sensitizing PDT-treated cells from autophagy to apoptosis due to the Becline-1 cleavage. This study demonstrates that the molecular mechanisms involved in histone modification induced by PDT-mediated oxidative stress, suggesting that HAT inhibitors may provide a novel therapeutic approach for improving PDT response.

摘要 6
Abstract 8
第一章 緒論 10
1.1 光動力治療 10
1.1.1光化學作用機制 11
1.1.2光動力發展與應用 12
1.1.3 五胺基酮戊酸(5-Aminolevulinic Acid, ALA)光動力療法 13
1.1.4 Chlorin e6(Ce6)及微脂體包埋光Ce6之光動力療法 14
1.2 光動力致氧化效應 15
1.2.1 活性氧分子(Reactive oxygen species, ROS) 15
1.2.2活性氧分子對訊息分子之調控 16
1.2.3 MAPK (Mitogen-activated protein kinases) 17
1.2.4 NF-κB (nuclear factor-κB) 21
1.3氧化壓力造成的細胞死亡 23
1.3.1 細胞凋亡(Apoptosis) 23
1.3.2 細胞壞死(Necrosis) 26
1.3.3 細胞自噬(Autophagy) 27
1.3.4 細胞死亡間的交互作用 29
1.4 抗細胞凋亡家族 30
1.4.1 生存素Survivin 30
1.5 環氧化酵素-2 (Cyclooxygenase-2, COX-2) 32
1.6 組蛋白乙醯化(Histone acetylation) 34
1.7 研究動機與目的 38
第二章 材料與方法 41
2.1 細胞株與細胞培養 41
2.2 in vitro光動力治療 41
2.3 細胞存活率試驗 42
2.3.1 MTT assay 42
2.3.2 Colony-formation assay 42
2.4 基因表達分析 43
2.4.1萃取RNA (RNA extraction) 43
2.4.2反轉錄作用 (Reverse Transcription, RT) 44
2.4.3聚合酶連鎖反應 (Polymerase Chain Reaction, PCR) 44
2.5 蛋白質表達分析 45
2.5.1 Total蛋白質萃取 45
2.5.2 細胞質/細胞核蛋白質萃取 46
2.5.3 蛋白質定量 46
2.5.4西方點墨法 (Western Blot) 47
2.6 細胞凋亡(apoptosis)檢測 49
2.6.1 Hoechst染色 49
2.6.2 Annexin V/PI染色 49
2.6.3 Caspase-3活性檢測 50
2.7 細胞自噬(autophagy)檢測 51
2.7.1 Monodansylcadaverine (MDC)染色 51
2.7.2 GFP-LC3螢光檢測 51
2.8 HAT活性偵測 52
2.9 HDAC活性偵測 52
2.10 干擾性核醣核酸(RNA interference, RNAi) 53
2.11 轉染(Transfection) 53
2.12 免疫沉澱技術 (Immunoprecipitation assay, IP assay) 54
2.13 染色質免疫沉澱技術 (Chromatin Immunoprecipitation assay, ChIP assay) 54
2.14 活體動物實驗 57
2.14.1 動物與腫瘤模式 57
2.14.2 In vivo光動力治療 57
2.14.3 In vivo光動力與HAT抑制劑之結合型治療 57
2.15 統計分析 58
第三章 結果 59
3.1 光動力氧化效應透過p300HAT表現及活性增加,增加組蛋白乙醯化修飾 59
3.2 光動力氧化效應藉由p300HAT所引發之組蛋白乙醯化修飾,增加COX-2基因轉錄 60
3.3 光動力氧化效應透過p38MAPK訊息調控p300HAT表現、活性及組蛋白乙醯化修飾,加強COX-2基因轉錄 62
3.4 光動力氧化效應會藉由p300HAT增加COX-2轉錄因子NF-κB之乙醯化修飾,促進其對COX-2之轉錄活性 63
3.5 Ce6-PDT藉由p38-p300HAT-acetylation增加COX-2轉錄表現 64
3.6 In vivo光動力氧化效應會藉由p300HAT增加COX-2 promoter位置乙醯化修飾,促進對COX-2之轉錄 65
3.7 HAT抑制劑AA顯著提升光動力治療對腫瘤細胞之細胞毒殺效果 65
3.8 HAT抑制劑AA增加光動力治療於小鼠C26腫瘤之治療效應 66
3.9 光動力治療結合HAT抑制劑AA會抑制pro-survival蛋白質 survivin表現,加強細胞死亡 67
3.10 結合光動力治療和HAT抑制劑AA會誘發腫瘤細胞進行apoptosis導致細胞死亡 68
3.11 HAT抑制劑AA結合光動力治療會藉由提升caspase活性而抑制autophagy發生 69
第四章 討論 71
4.1光動力治療會引發p38MAPK-p300HAT-hyperacetylation 71
4.2光動力治療與乙醯化修飾 72
4.3氧化壓力與乙醯化修飾 73
4.4 HATs與HDACs活性改變之調控 74
4.5光動力治療與p38MAPK活化 77
4.6光動力氧化效應下COX-2轉錄機轉之探討 78
4.7光動力作用與COX-2抑制劑之結合型治療 80
4.8光動力氧化效應與survivin活化 81
4.9 ALA-PDT與ALA-PDT結合AA引發之細胞死亡路徑探討 82
4.10 光動力治療結合HAT抑制劑於腫瘤治療之應用 85
第五章 結論 87
Figure 1光動力致壓效應會導致組蛋白乙醯化程度上升。 88
Figure 2 光動力處理會導致HAT的活性上升。 89
Figure 3 光動力處理會導致HDAC的活性下降。 90
Figure 4 光動力處理會促使p300HAT mRNA的上升。 91
Figure 5 光動力處理不影響HDACs mRNA的表現量。 92
Figure 6 Pro-survival蛋白質COX-2於光動力治療後顯著上升。 93
Figure 7使用HAT抑制劑AA能有效阻止COX-2於光動力治療後上升。 94
Figure 8 使用shp300能抑制光動力治療後上升之p300HAT 及COX-2 mRNA的表現。 96
Figure 9 使用shp300能抑制光動力治療後上升之組蛋白乙醯化及COX-2蛋白質的表現。 97
Figure 10 光動力治療促使大量p300HAT蛋白質結合至COX-2 promoter上,導致COX-2 promoter組蛋白乙醯化程度上升。 98
Figure 11 光動力治療會引發p38MAPK活化。 99
Figure 12使用p38MAPK抑制劑能抑制光動力治療後p38MAPK磷酸化及COX-2的表現。 101
Figure 13 使用p38MAPK抑制劑能抑制光動力治療後上升之p300HAT mRNA表現、HAT活性及組蛋白乙醯化程度。 103
Figure 14光動力治療會造成NF-κB lysine310 (K310)乙醯化程度上升。 104
Figure 15 ALA-PDT經由p38MAPK活化引發p300表現及HAT活性提升,導致NF-κB乙醯化程度上升。 105
Figure 16 ALA-PDT後乙醯化NF-κB結合於COX-2 promoter上之分析。 106
Figure 17 Ce6-PDT能藉由活化p38MAPK提升HAT活性,增加COX-2 promoter上NF-κB p65與組蛋白乙醯化程度。 108
Figure 18 ALA-PDT藉由提升HAT活性,促使C26細胞內COX-2 promoter上組蛋白乙醯化程度提升,造成COX-2表現增加。 110
Figure 19 PL-Ce6-PDT會提升NU/NU小鼠身上A375腫瘤之HAT活性,增加腫瘤內COX-2 promoter上組蛋白乙醯化程度,促進COX-2轉錄。 112
Figure 20 PL-Ce6-PDT會提升BALB/c小鼠身上C26腫瘤之HAT活性,增加腫瘤內COX-2 promoter上組蛋白乙醯化程度,促進COX-2轉錄。 114
Figure 21 HAT抑制劑Anacardic acid (AA) 能提升ALA-PDT細胞毒殺效應。 115
Figure 22 ALA-PDT結合HAT抑制劑能抑制A375細胞形成colonies。 116
Figure 23 ALA-PDT結合HAT抑制劑能抑制C26細胞形成colonies。 117
Figure 24 單獨使用AA或NS-398不能抑制C26腫瘤生長。 118
Figure 25 PL-Ce6-PDT結合AA能有效抑制C26腫瘤生長。 121
Figure 26 長期給予HAT抑制劑AA結合PL-Ce6-PDT能抑制C26腫瘤生長。 123
Figure 27 COX-2抑制劑NS-398無法提升ALA-PDT後之細胞毒殺效應。 124
Figure 28使用HAT抑制劑AA能有效阻止survivin於光動力治療後上升。 125
Figure 29使用HAT抑制劑AA能有效阻止survivin於光動力治療後上升,且活化caspase 3及PARP。 126
Figure 30使用HAT抑制劑AA結合ALA-PDT能顯著提升caspase 3活性。 127
Figure 31使用shsurvivin阻止Survivin於光動力治療後上升,能大幅提升活化態之caspase 3及PARP表現。 128
Figure 32 ALA-PDT結合HAT抑制劑AA會引發細胞核內染色質聚集。 129
Figure 33 ALA-PDT結合HAT抑制劑AA會強烈引發Phosphatidylserine (PS)外翻之apoptosis現象。 131
Figure 34 使用caspases抑制劑Z-VAD-FMK能阻止ALA-PDT結合AA所引發之細胞死亡。 133
Figure 35 ALA-PDT結合HAT抑制劑AA會抑制光動力效應引發之autophagosomes形成。 134
Figure 36 ALA-PDT結合HAT抑制劑AA會抑制光動力效應引發之autophagy。 135
Figure 37 ALA-PDT結合HAT抑制劑AA會抑制光動力效應引發之autophagosomes形成,而加入caspases抑制劑Z-VAD-FMK則阻止此現象發生。 136
Figure 38 ALA-PDT結合HAT抑制劑AA會抑制光動力效應引發之autophagy,而加入caspases抑制劑Z-VAD-FMK則阻止此現象發生。 137
Figure 39 ALA-PDT結合HAT抑制劑AA活化之caspases會造成autophagy重要因子Beclin-1分解,而加入caspases抑制劑Z-VAD-FMK則阻止此現象發生。 138
Figure 40光動力治療後一系列訊息傳遞之過程。 139
Figure 41結論示意圖。 140
附圖一、光動力作用模式。 141
附圖二、血紅素生合成路徑(Adapted from [298])。 142
附圖三、p38MAPK參與調控的細胞反應(Adapted from[96])。 143
參考文獻 144


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