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系統識別號 U0026-2102201109382900
論文名稱(中文) 膠原蛋白接受器Discoidin Domain Receptor 1以及β1 integrin在上皮細胞與間質細胞轉換之機制探討
論文名稱(英文) A Tale of Two Collagen Receptors in Epithelial Cell Differentiation: β1 integrin or Discoidin Domain Receptor 1, that is the question.
校院名稱 成功大學
系所名稱(中) 基礎醫學研究所
系所名稱(英) Institute of Basic Medical Sciences
學年度 99
學期 1
出版年 100
研究生(中文) 葉儀君
研究生(英文) Yi-Chun Yeh
學號 S5894147
學位類別 博士
語文別 英文
論文頁數 208頁
口試委員 指導教授-湯銘哲
召集委員-沈孟儒
口試委員-張玲
口試委員-陳鴻震
口試委員-陳瑞華
中文關鍵字 integrin β1  discoidin domain receptor 1 (DDR1)  上皮細胞與間質細胞之轉換 (EMT) 
英文關鍵字 integrin β1  discoidin domain receptor 1 (DDR1)  Epithelial-to-mesenchymal transition (EMT) 
學科別分類
中文摘要 膠原蛋白為組成身體含量最高的蛋白質之ㄧ。膠原蛋白的主要接受器有兩類,一為integrins,另一為DDRs。 過去數十年的研究證實了,此兩類膠原蛋白接受器於上皮細胞增生、延展、及爬行,所扮演的角色。然而對於他們在上皮細胞的分化過程中所扮演的角色仍不清楚。於是此一論文的目的便是在釐清此兩類膠原蛋白接受器,在上皮細胞分化過程中所扮演的角色。並且也將針對其中的分子機制作進一步的探討。
論文首先,我們證實了integrin β1表現量的上升,會促使上皮細胞的去分化作用,並且在細胞轉型生長因子 (TGF-β1) 所引發的上皮與間質細胞轉換 (epithelial-to-mesenchymal transition, EMT) 過程中扮演重要的角色。過去已知細胞轉型生長因子所促使之EMT在腎臟纖維化的病理進程中扮演重要的影響。實驗中我們發現integrin β1表現量的上升發生於細胞轉型生長因子所促使之多種上皮細胞EMT之過程中,而此調控機制,會受到抑制Smad3基因的表達而受阻。為了近一步證實細胞轉型生長因子對integrin β1基因的調控,我們藉由複製integrin β1的啟動子,並進行啟動子轉錄活性分析,證實了細胞轉型生長因子會藉由調控啟動子之轉錄活性而促使integrin β1之基因表達。而抑制Smad3、或是藉由核甘酸突變之技術,抑制Smad3結合integrin β1之啟動子,皆能抑制細胞轉型生長因子促使之integrin β1啟動子轉錄活性的增加。染色質免疫沉澱法 (Chromatin immunoprecipitation assay) 的結果,更進一步的證實Smad3在細胞轉型生長因子的刺激下會增加與integrin β1啟動子的特定位點的結合能力。在以單側輸尿管结紮手術引發慢性腎臟纖維病變的過程我們發現integrin β1的表現也隨之增加並且表現於上皮細胞與間質細胞都有大量表現。在具有慢性腎衰竭的臨床檢體中,我們也發現integrin β1的表現量與α-smooth muscle actin有伴隨著上升的現象。抑制integrin β1的活性,能夠抑制單側輸尿管结紮手術所引發的慢性腎臟纖維。於是我們認為integrin β1在EMT,以及慢性腎臟纖維化之過程中,扮演重要的角色,而藉由抑制integrin β1之活性可能成為治療腎臟纖維化的方式。
論文的第二部份,我們證實了DDR1的過量表現,會促使細胞間黏附蛋白E-cadherin分布在細胞與細胞連接處。相反的,過量表現缺乏活性、或是抑制DDR1蛋白的表現,則會有抑制E-cadherin分布於細胞與細胞間的情形。DDR1的表現不僅改變了E-cadherin的分布與表現量,同時也促進上皮細胞的分化特性,包括了細胞頂端為絨毛膜 (microvilli) 的表現、及細胞骨架的排列方式。此外,DDR1的表現也抑制了間質細胞特有蛋白的表現。相反的過量表現缺乏活性、或是抑制DDR1的表現皆有相反的結果。這些結果皆顯示了DDR1的活化能夠促使上皮細胞的方化。更進一步的,我們發現DDR1的表現能夠抑制E-cadherin蛋白質的降解速度。利用不同的活細胞影像的分析方式,包括photobleaching與photoconversion,我們進一部證實DDR1能促使了E-cadherin在細胞膜上的穩定度。相反的,缺乏DDR1的表現則有抑制的作用。藉由pull-down assay ,與表現持續活化態、或是持續不活化態的Cdc42,證實了DDR1經由抑制Cdc42的活性,進而影響E-cadherin在細胞表面上的穩定性,並進而影響了上皮細胞的分化。
總結以上的實驗結果,我們陳述了integrin β1 及 DDR1,雖然同為膠原蛋白接受器,對於上皮細胞的分化卻扮演了絕然不同的角色。此研究顯示了integrin β1 及 DDR1在訊息上的平衡,對於維持上皮細胞的分化是相當重要的。
英文摘要 Collagen is the most abundant extracellular matrix in mamalian body. There are two main types of collagen receptors, integrins and discoidin domain receptors (DDRs). Research works conducted in the last decade have lead to remarkable understanding of their functions in cell proliferation, extension, and migration. However, less was known about their functions in cell differentiation, particularly in epithelium. Therefore, the purpose of this thesis was to examine their functions and signal mechanism involved in epithelial cell differentiation.
The first part of this thesis showed that upregulation of integrin β1 promotes epithelial cell dedifferentiation and act as a key mediator in TGF-β1-induced epithelial-to-mesenchymal transition (EMT). TGF-β1-induced EMT contributes to pathophysiological development of kidney fibrosis. In this study, we showed that TGF-β1-induced augmentation of integrin β1 expression was required for EMT in several epithelial cell lines and knockdown of Smad3 inhibited TGF-β1-induced augmentation of integrin β1. TGF-β1 triggered integrin β1 gene promoter activity as assessed by luciferase activity assay. Both knockdown of Smad3 and mutation of Smad-binding element on integrin β1 promoter markedly reduced TGF-β1-induced integrin β1 promoter activity. Chromatin immunoprecipitation assay showed that TGF-β1 enhanced binding of Smad3 to integrin β1 promoter. Furthermore, induction of unilateral ureteral obstruction (UUO) triggered increase of integrin β1 in both renal epithelial and interstitial cells. In human kidney with chronic tubulointerstitial fibrosis, we also found a concomitant increase of integrinβ1 and α-smooth muscle actin (α-SMA) in tubule epithelium. Blocking of integrin β1 signal dampened the UUO-induced progression of tubulointerstitial fibrosis. Taken together, integrin β1 mediates EMT and the following tubulointerstitutial fibrosis and inhibition of integrin β1 can be a possible therapeutic target for prevention of renal fibrosis.
The second part of this thesis showed that DDR1 overexpression augmented, whereas dominant negative mutant (DN-DDR1) or knockdown of DDR1 inhibited E-cadherin localized in cell-cell junctions in epithelial cells. DDR1 changed the localization and abundance of E-cadherin, as well as epithelial plasticity, as manifested by enhancement of microvilli formation and alteration of cytoskeletal organization. DDR1 also reduced protein abundance of mesechymal markers, while DN-DDR1 and sh-DDR1 showed opposite effects. These results suggest that activation is required for DDR1-induced cell differentiation. Expression of DDR1 augmented E-cadherin protein levels by decreasing its degradation rate. Photobleaching and photoconversion of E-cadherin conjugated with Eos fluorescence protein demonstrated that DDR1 increased the stability of E-cadherin on the cell membrane, whereas sh-DDR1 decreased it. Pull-down assay and expression of constitutive active or dominant negative Cdc42 showed that DDR1 stabilized E-cadherin through inactivation of Cdc42. Altogether, our results show that DDR1 promotes cell-cell adhesion and differentiation through stabilization of E-cadherin, which is mediated by Cdc42 inactivation.
In conclusion, we demonstrate that two collagen receptors, integrin β1 and DDR1, act oppositely in regulating epithelial cell differentiation. These studies provide the information that the signaling balance between integrin β1 and DDR1 is important in maintaining epithelial plasticity.
論文目次 CONTENTS
Abstract ------------------------------------------------- 2
Abstract in Chinese -------------------------------------- 4
Acknowledgement ------------------------------------------ 6
Contents ------------------------------------------------- 9
Table contents ------------------------------------------ 13
Figure contents ----------------------------------------- 14
Abbreviations ------------------------------------------- 17

Chapter 1 Introduction --------------------------------- 20
1-1 The biological functions of collagen --------------- 21
1-2 Collagen receptor- Integrins ----------------------- 23
1-2.1 The biological characteristics of integrin β1
1-2.1.1 Genetic background of integrin β1 ------------- 24
1-2.1.2 Structures and ligand binding affinity of integrin β1 ------------- 26
1-2.2 Regulation of integrin β1
1-2.2.1 Activation by post-translational modification ----------------- 29
1-2.2.2 Protein turnover ------------------------------- 30
1-2.2.3 Transcriptional and translational regulation -------- 31
1-2.3 The biological functions of integrin β1
1-2.3.1 Cell growth ------------------------------------ 33
1-2.3.2 Cell migration --------------------------------- 35
1-2.3.3 Tubulogenesis ---------------------------------- 36
1-2.3.4 Mechanical sensing ----------------------------- 37
1-2.4 The physiological functions of integrin β1
1-2.4.1 Cell differentiation in development ------------ 39
1-2.5 The pathological functions of integrin β1
1-2.5.1 Tissue fibrosis -------------------------------- 46
1-2.5.2 Tumorogenesis ---------------------------------- 47
1-3 Collagen receptor- Discoidin domain receptors (DDRs) ------------- 50
1-3.1 The biological characteristics of DDR1
1-3.1.1 Genetic background of DDR1 --------------------- 51
1-3.1.2 Structures and ligand binding affinity of DDR1 --------------- 54
1-3.2 The regulation of DDR1
1-3.2.1 Activation by post-translational modification ---------------- 56
1-3.2.2 Protein turnover ------------------------------- 57
1-3.2.3 Transcriptional and Translational regulation --- 57
1-3.3 The biological functions of DDR1
1-3.3.1 Cell growth ------------------------------------ 59
1-3.3.2 Cell migration --------------------------------- 59
1-3.3.3 Tubulogenesis ---------------------------------- 60
1-3.4 The physiological functions of DDR1
1-3.4.1 Cell differentiation in development ------------ 62
1-3.5 The pathophysiological functions of DDR1
1-3.5.1 Tissue fibrosis -------------------------------- 66
1-3.5.2 Tumorogenesis ---------------------------------- 67
1-3.5.3 Atherosclerosis -------------------------------- 69
1-4 Objectives of study -------------------------------- 71
Chapter 2 Materials and Methods ------------------------ 72
2-1 Cell lines and cell culture --------------------- 73
2-2 Establish DDR1 expression clones, and plasmid construction --------- 73
2-3 Western blot analysis, immunoprecipitation, and pull-down assay ------- 75
2-4 Reverse transcription-polymerase chain reaction (RT-PCR) ------------------ 76
2-5 Transfection and dual luciferase assay ---------- 77
2-6 Chromatin immunoprecipitation (ChIP) ------------ 77
2-7 Immunofluorescence ------------------------------ 78
2-8 Fluorescence loss in photobleaching (FLIP), photoconversion, and image translation ----------------- 78
2-9 Scanning electron microscopy (SEM) -------------- 79
2-10 Animal study- unilateral ureteral obstruction --------------- 80
2-11 HE, and Sirius red staining --------------------- 80
2-12 Clinical tissue samples ------------------------- 81
2-13 Statistics -------------------------------------- 81
Chapter 3 TGF-β1 induces Smad3-dependent β1 integrin gene expression in epithelial-to -mesenchymal transition during chronic tubulointerstitial fibrosis --------------------- 82
3-1 Abstract ---------------------------------------- 83
3-2 Introduction ------------------------------------ 84
3-3 Results ----------------------------------------- 86
3-4 Discussion -------------------------------------- 93
Chapter 4 DDR1 triggers epithelial cell differentiation via promoting cell adhesion through stabilization of E-cadherin ---------------------------------------------- 97
4-1 Abstract --------------------------------------- 98
4-2 Introduction ----------------------------------- 99
4-3 Results --------------------------------------- 102
4-4 Discussion ------------------------------------ 111
Chapter 5 Discussion ---------------------------------- 114
5-1 Integrin β1 may have functions other than EMT during tubulointerstitial fibrosis ---------------------------- 115
5-2 The targeting of injected integrin β1 antibody in the tissue context ---------------------------------------- 115
5-3 The possible downstream signalings in integrin β1-mediated cell de-differentiation ------------------- 116
5-4 The possible role of DDR1 in the pathophysiological condition: renal fibrosis and cancer progression --------116
5-5 The interactions between integrin β1 and DDR1 ----- 120
5-6 Regulations and functions of E-cadherin in epithelial cell differentiation ----------------------------------- 121
5-7 The roles of integrin β1 and DDR1 in E-cadherin-mediated cell-cell contacts ---------------------------- 123
Chapter 6 Summary and prospect ----------------------- 125
References --------------------------------------------- 128
Figures ------------------------------------------------ 158
Curriculum vitae --------------------------------------- 207
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