高生產力的珊瑚礁生態系建立於腔腸動物與Symbiodinium屬渦鞭毛藻胞內共生現象的基礎上。然而，宿主和共生藻之間複雜的生物過程與未知的交互作用仍尚未被澄清。在這裡，我以美麗海葵Aiptasia pulchella為模式生物，先對Aprab11、Aprab3與Aprab4的角色做探討，描述共生小體與宿主細胞囊泡系統之間的互動，再提出兩種方法深究胞內共生的分子調控機制。一是對宿主cathepsin（CTS）家族蛋白酶的角色探討，另一個是利用扣減雜交技術（SSH）識別出共生／游離態具有差異表達的Symbiodinium基因。結果指出共生小體上沒有Aprab11的分布，可能代表慢速再循環途徑無法與共生小體互動。Aprab3與Aprab4的持續出現，則顯示共生小體與快速再循環途徑及TGN有交互作用。宿主細胞胞噬小體及共生小體的lysotracker red染色及bafilomycin A1處理結果，表明胞噬小體的酸化受到ApV-ATPase所調控且共生小體內腔的酸性較弱。這與免疫染色發現共生小體內，只缺乏ApCTSH與ApV-ATPase外，尚包含其他的ApCTSs的結果有一致性。細胞內ApCTSH蛋白酶也被發現累積在早期的胞噬小體及部分Aprab5-positive早期胞飲小體內，且其活性可於pH 6.8下活化。但以DCMU處理健康的共生小體時，同時誘使酸化產生及ApCTSH與ApV-ATPase回到共生小體上。這些結果顯示共生藻主動排除ApCTSH與ApV-ATPase於共生小體上，維持共生小體內腔的pH，避免受到ApCTS蛋白酶的損害。另一方面，SSH技術的應用發現216個共生與175個非共生的共生藻差異表現基因。獲得的差異表現基因依照不同的生理功能共分成細胞分裂、細胞訊息傳導／溝通、細胞結構／移動、細胞／生物防禦、RNA合成、蛋白質合成、新陳代謝及未分類等組別。不幸地，無論是共生還是非共生態，都約有30 %的差異表達基因屬於未知基因，代表我們對共生藻的了解甚為不足。定量PCR分析描繪出共生態共生藻在囊泡運輸、細胞骨架、蛋白酶抑制子、逆境反應及光合作用等相關基因的表現較為活躍。反之，游離態共生藻的高表達差異基因則出現在鞭毛形成與運動、細胞分裂、氮源輸送、細胞壁等相關功能中。總而言之，宿主CTS蛋白酶家族與共生差異表現基因的研究提供了更多有關胞內共生調控機制的知識與線索。

The highly productive coral reef ecosystem is based on the cnidarian-dinoflagellate endosymbiosis. However, the complex biological processes and interactions between the host and symbionts were still unclarified. Here, I firstly investigated the roles of Aprab11, Aprab3 and Aprab4 to describe the interaction between the symbiosomes and vesicles in host cell, which based on a sea anemone model organism, Aiptasia pulchella. Additionally, I also presented two approaches to dissect the molecular regulatory mechanism of the endosymbiosis. One was the characterization of host cathepsin family proteases, and the other was the identification of differentially expressed Symbiodinium genes during the symbiosis/free-living stages by surppressive subtractive hybridization (SSH). The results showed most of zooxanthellae-harbored symbiosomes were absent of Aprab11 but were abundant of Aprab3 and Aprab4 that indicated the TGN-derived vesicles and fast recycling routes were interacted with symbiosomes, but slow recycling routes were not. Lysotracker red staining and bafilomycin A1 treatment with phagosomes/symbisosomes in host cells indicated that the acidification of phagosomes was mainly mediated by ApV-ATPase and the symbiosomal lumen was mildly acidic. That’s consistent with the findings of immunostaining which the symbiosome were filled with many Apcathepsins except Apcathepsin H and ApV-ATPase. Additionally, the intracellular Apcathepsin H protease also accumulated in the early phagosmes and part of Aprab5-positive early endosomes and its proteolytic acivity could be activated at pH 6.8. But DCMU treatment of healthy symbiosomes could simultaneously induce the acidification and re-contribution of Apcathepsin H and ApV-ATPase to symbiosomes. Consequently, these results revealed that the Apcathepsin H and ApV-ATPase were actively excluded from symbiosome by the zooxanthellae to maintain the pH of symbiosomal lumen which were able to prevent damages from Apcathepsin proteases. On the other hand, the application of SSH technique produced 216 symbiosis and 175 nonsymbiosis differentially expressed zooxanthellae genes. These differentially-expressed genes were classified with different biological processes into cell division, cell signaling/communication, cell structure/motility, cell/organism defense, RNA synthesis, proten synthesis, metabolism and unclassified. Unfortunately, ~ 30 % differentially-expressed genes were belonged to unknown genes whether symbiosis or nonsymbiosis that implicated the understanding to zooxanthellae was still less than clear. Quantitative PCR assay revealed that the zooxanthellal genes related with vesicle trafficking, cytoskeleton, protease inhibitor, stress response and photosynthesis were more active during symbiotic phase. Conversely, the zooxanthellal genes highly expressed at the nonsymbiotic phase were involved with flagellate formation and motility, nitrogen transporter, cell division, cell wall-associated process… and so on. Together, the current investigation of host cathepsin family and symbiosis differentially-expressed zooxanthellal genes provided new knowledge and insights of endosymbiosis regulatory mechanism.

目錄
論文審定書．．．．．．．．．．．．．．．．．．．．．．．．．．．．．．i
誌謝．．．．．．．．．．．．．．．．．．．．．．．．．．．．．．．．．ii
中文摘要．．．．．．．．．．．．．．．．．．．．．．．．．．．．． iii
英文摘要．．．．．．．．．．．．．．．．．．．．．．．．．．．．． v
目錄．．．．．．．．．．．．．．．．．．．．．．．．．．．．．．．vii
圖表目錄．．．．．．．．．．．．．．．．．．．．．．．．．．．．．．xii
縮寫字對照表．．．．．．．．．．．．．．．．．．．．．．．．．．．．xv
第一章 總論．．．．．．．．．．．．．．．．．．．．．．．．．．．．．1
壹、 研究背景．．．．．．．．．．．．．．．．．．．．．．．．．2
一、 胞內共生對珊瑚礁的意義．．．．．．．．．．．．．．．．2
二、 共生藻的分類與形態特徵．．．．．．．．．．．．．．．．3
三、 共生小體是經由共生藻修飾過的胞噬小體而演變來的．．．．4
貳、本論文研究方向與實驗架構．．．．．．．．．．．．．．．．．6
参、參考文獻．．．．．．．．．．．．．．．．．．．．．．．．．7
第二章　rab蛋白於共生小體形成時所扮演的角色之探討．．．．．．．．．．10
壹、中文摘要．．．．．．．．．．．．．．．．．．．．．．．．11
貳、英文摘要．．．．．．．．．．．．．．．．．．．．．．．．12
参、著作發表．．．．．．．．．．．．．．．．．．．．．．．．13
第三章　V-ATPase與共生小體內腔pH值調控機制之相關性探討．．．．．．14
壹、中文摘要．．．．．．．．．．．．．．．．．．．．．．．．15
貳、英文摘要．．．．．．．．．．．．．．．．．．．．．．．．16
参、文獻回顧．．．．．．．．．．．．．．．．．．．．．．．．17
一、 胞噬小體的形成與成熟．．．．．．．．．．．．．．．．17
二、 胞噬小體的酸化主要由V-ATPase促成．．．．．．．．．．17
三、 藉由V-ATPase探討共生小體無法酸化之機制．．．．．．．19
肆、材料與方法．．．．．．．．．．．．．．．．．．．．．．．20
一、 實驗生物的取得與飼養．．．．．．．．．．．．．．．．20
二、 實驗生物的RNA抽取與cDNA基因庫製作．．．．．．．．21
三、 ApCTSs與ApVHD的基因選殖序列分析．．．．．．．．．22
四、 ApCTSs與ApVHD重組蛋白的建構、表現與純化．．．．．23
五、 哺乳動物細胞之EGFP reporter分析．．．．．．．．．．．25
六、 抗體．．．．．．．．．．．．．．．．．．．．．．．．26
七、 西方墨點法．．．．．．．．．．．．．．．．．．．．．26
八、 免疫螢光染色技術．．．．．．．．．．．．．．．．．．27
九、 胞噬作用分析．．．．．．．．．．．．．．．．．．．．28
十、 細胞內酸性囊泡的測定．．．．．．．．．．．．．．．．28
十一、 DCMU光合作用抑制劑與bafilomycin A1抑制劑處理．29
伍、結果．．．．．．．．．．．．．．．．．．．．．．．．．．31
一、 ApVHD基因序列及推演的氨基酸序列．．．．．．．．．．31
二、 ApVHD無法在哺乳動物細胞株系統有正常的細胞內分布．．32
三、 辨認ApVHD的抗體具有相當程度的專一性．．．．．．．．33
四、 絕大部分的共生小體上缺乏ApVHD蛋白的存在．．．．．．33
五、 ApVHD會隨著胞噬小體的成熟而逐漸累積其上．．．．．．33
六、 海葵宿主細胞內的胞噬小體酸化與ApVHD的累積呈正相關關係並且可以被bafilomycin A1所抑制．．．．．．．．．．．34
七、 DCMU處理後，ApVHD會再分布於共生小體上．．．．．．34
八、 酸性共生小體的族群個數隨著DCMU的處理而增加，但可以被bafilomycin A1有效地抑制．．．．．．．．．．．．．．．35
陸、結論．．．．．．．．．．．．．．．．．．．．．．．．．．37
柒、參考文獻．．．．．．．．．．．．．．．．．．．．．．．．38
第四章　共生藻避開宿主cathepsin蛋白酶的機制之探討．．．．．．．．．．43
壹、中文摘要．．．．．．．．．．．．．．．．．．．．．．．．44
貳、英文摘要．．．．．．．．．．．．．．．．．．．．．．．．45
参、文獻回顧．．．．．．．．．．．．．．．．．．．．．．．．46
一、 在胞噬小體成熟過程中會活化cathepsin蛋白酶的活性．．．46
二、 共生藻存活於胞噬小體內的策略．．．．．．．．．．．．47
三、 藉由cathepsin蛋白酶來探討 Aiptasia pulchella-Symbiodinium胞內共生．．．．．．．．．．．．．．．．．．．．．．．50
肆、材料與方法．．．．．．．．．．．．．．．．．．．．．．．52
一、 實驗生物的取得與飼養．．．．．．．．．．．．．．．．52
二、 實驗生物的RNA抽取與cDNA基因庫製作．．．．．．．52
三、 ApCTSs與ApVHD的基因選殖序列分析．．．．．．．．．52
四、 ApCTSs與ApVHD重組蛋白的建構、表現與純化．．．．．53
五、 哺乳動物細胞之EGFP reporter分析．．．．．．．．．．．55
六、 抗體．．．．．．．．．．．．．．．．．．．．．．．．56
七、 西方墨點法．．．．．．．．．．．．．．．．．．．．．57
八、 免疫螢光染色技術．．．．．．．．．．．．．．．．．．57
九、 胞噬作用分析．．．．．．．．．．．．．．．．．．．．57
十、 DCMU光合作用抑制劑處理．．．．．．．．．．．．．．57
十一、 次細胞分層技術．．．．．．．．．．．．．．．．．57
十二、 蛋白酶酵素活性分析．．．．．．．．．．．．．．．59
伍、結果．．．．．．．．．．．．．．．．．．．．．．．．．．60
一、 ApCTS基因序列以及推演的氨基酸序列．．．．．．．．．60
二、 ApCTSL無法在哺乳動物細胞株系統有正常的細胞內分布．．62
三、 用來辨認ApCTSs與Aprab5的抗體具有相當程度的專一性．63
四、 絕大部分的共生小體上缺乏ApCTSH蛋白的存在．．．．．64
五、 ApCTSs隨著胞噬小體的成熟中會有不同的分布趨勢．．．．65
六、 DCMU處理後ApCTSH會再分布於共生小體上．．．．．．66
七、 ApCTSH與ApCTSL的最大活性分別坐落在不同的胞飲小體上．．．．．．．．．．．．．．．．．．．．．．．．．66
八、 ApCTSS與ApCTSD各自都與細胞內Aprab7分布位置重疊．67
陸、結論．．．．．．．．．．．．．．．．．．．．．．．．．．69
柒、參考文獻．．．．．．．．．．．．．．．．．．．．．．．．70
第五章　共生／非共生態共生藻差異性表現基因之探討．．．．．．．．．．78
壹、中文摘要．．．．．．．．．．．．．．．．．．．．．．．．79
貳、英文摘要．．．．．．．．．．．．．．．．．．．．．．．．80
参、文獻回顧．．．．．．．．．．．．．．．．．．．．．．．．81
一、 共生與非共生態共生藻會面臨到的生理狀況與挑戰．．．．81
二、 調控腔腸動物與共生藻胞內共生的關鍵因子．．．．．．．83
三、 藉由扣減雜交技術搜尋Aiptasia-Symbiodinium胞內共生的差異性表現基因及關鍵因子．．．．．．．．．．．．．．．．84
肆、材料與方法．．．．．．．．．．．．．．．．．．．．．．．86
一、 實驗生物的取得與飼養．．．．．．．．．．．．．．．．86
二、 實驗生物的RNA抽取與cDNA基因庫製作．．．．．．．86
三、 扣減雜交技術．．．．．．．．．．．．．．．．．．．．86
四、 次世代定序技術．．．．．．．．．．．．．．．．．．．87
五、 差異性表現基因片段的延長與序列分析．．．．．．．．．88
六、 即時聚合酶連鎖反應．．．．．．．．．．．．．．．．．88
七、 穿透式電子顯微鏡分析．．．．．．．．．．．．．．．．89
伍、結果．．．．．．．．．．．．．．．．．．．．．．．．．．91
一、 美麗海葵與共生藻基因資料庫的建立．．．．．．．．．．91
二、 共生/非共生態共生藻的RNA品質接近一致，並且都已降低外在因子與海葵宿主RNA污染的干擾．．．．．．．．．．．．91
三、 差異性表現基因片段的延長與序列比對．．．．．．．．．92
四、 差異性表現基因的分類及功能區分．．．．．．．．．．．93
五、 共生藻house-keeping基因的確定．．．．．．．．．．．．95
六、 差異性表現基因的定量分析．．．．．．．．．．．．．．95
陸、結論．．．．．．．．．．．．．．．．．．．．．．．．．．100
柒、參考文獻．．．．．．．．．．．．．．．．．．．．．．．．101
第六章　綜合討論與未來研究方向．．．．．．．．．．．．．．．．．．．106
壹、綜合討論與未來研究方向．．．．．．．．．．．．．．．．．107
一、共生藻建立共生小體的分子機制．．．．．．．．．．．．107
二、共生／非共生態共生藻差異性表現基因之調控．．．．．．110
貳、參考文獻．．．．．．．．．．．．．．．．．．．．．．．．115
圖表．．．．．．．．．．．．．．．．．．．．．．．．．．．．．．．．120
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