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系統識別號 U0026-2811201717293300
論文名稱(中文) 探討 CD44 與 GADD45A 在神經膠質母細胞瘤中扮演的角色
論文名稱(英文) Elucidation of the role of CD44 and GADD45A in glioblastoma multiforme cells
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 106
學期 1
出版年 106
研究生(中文) 王筱涵
研究生(英文) Hsiao-Han Wang
學號 S58001365
學位類別 博士
語文別 英文
論文頁數 165頁
口試委員 指導教授-辛致煒
召集委員-周楠華
口試委員-許桂森
口試委員-莊季瑛
口試委員-陳錦翠
口試委員-侯自銓
中文關鍵字 神經膠質瘤  CD44  透明質酸  癌症幹細胞  GADD45A  帝盟多  抗藥性 
英文關鍵字 glioblastoma  CD44  hyaluronan  cancer stem cell  GADD45A  temozolomide  chemo-resistance 
學科別分類
中文摘要 多形性神經膠母細胞瘤為一種最常見且致死率極高的原發性腦瘤,其對於化學治療及放射線治療具有高度抗性,此特性大幅降低臨床治療的效果,並導致癌症復發。在本實驗室過去研究中針對神經膠質瘤細胞的基因表達譜進行分析,發現CD44、GADD45A、FN1、CD63 及 SPP1的表現與多形性神經膠母細胞瘤有高度相關性。而在本論文中,我們欲進一步釐清在臨床主要化療藥物−帝盟多的投藥過程中多形性神經膠母細胞瘤細胞內分子機制的變化,並期望能從中發現新的治療策略。我們的實驗結果顯示:GADD45A的表現量不論在細胞週期還是細胞凋亡分析中都受到帝盟多的影響而增加。而將GADD45A基因默化後會增強帝盟多抑制細胞生長的效果,並促進細胞凋亡。且在對帝盟多具藥物抗性的T98 及 TR-U373 細胞中也發現同樣的結果。另外,我們也發現在具藥物抗性細胞株 (T98、TR-U373) 中,GADD45A 基因默化降低O6-甲基鳥嘌呤-DNA甲基轉移酶 (MGMT) 的表現。雖然在藥物敏感細胞株 (U87、U373) 中未偵測到MGMT表現,但GADD45A 基因默化可降低由帝盟多誘導的TP53表現量。根據此結果,我們認為GADD45A在藥物敏感及具藥物抗性的細胞株中,可能分別藉由 TP53-dependent 及 MGMT-dependent 途徑達到保護多形性神經膠母細胞瘤的功能。因此 GADD45A 在促進帝盟多對於多形性神經膠母細胞瘤的治療上或許扮演重要的角色。
近年來,癌症幹細胞亦被認為與腫瘤抗藥性及癌症復發息息相關。CD44 在過去被認為是多形性神經膠母細胞瘤幹細胞標誌,本實驗室先前研究也指出:CD44 表現量與神經膠質瘤惡性程度具有高度相關性。然而病患預後分析結果卻顯示:CD44 表現量越高,多形性神經膠母細胞瘤病患的預後反而越好。此研究結果暗示,在多形性神經膠母細胞瘤幹細胞中可能存在 CD44 異質性。因此在本研究中,將進一步探討 CD44 與多形性神經膠母細胞瘤幹細胞的關聯性。我們發現:默化 CD44 基因會降低細胞增殖速率、降低細胞分化指標蛋白 (GFAP)、並增加球體生成能力及多形性神經膠母細胞瘤幹細胞指標蛋白 (CD133 、 Oct4 、 Nanog 、 Nestin) 的表現。另外,添加 CD44 主要受質−透明質酸會降低 CD44 表現,並增加多形性神經膠母細胞瘤幹細胞特性。然而在 CD44 基因默化且原本具有幹細胞特性的細胞中,添加透明質酸反而會促使細胞分化。綜合上述結果顯示:CD44 低表達的多形性神經膠母細胞瘤具有癌症幹細胞特性,因此 CD44 並非適當的神經膠質瘤幹細胞標誌。而動物實驗結果顯示:CD44 主要表現在腫瘤周邊,暗示 CD44 可能在神經膠質瘤細胞侵襲及轉移過程中扮演較為重要的角色。
綜合本論文研究結果,我們發現 CD44 低表達的多形性神經膠母細胞瘤具有腫瘤幹細胞特性,且此一特性受到 CD44 受質−透明質酸的調控。同時,本研究也發現,GADD45A 在神經膠質瘤細胞對帝盟多治療產生藥物抗性的過程中扮演了重要的角色。因此,若能藉由透明質酸改變多形性神經膠母細胞瘤的幹細胞特性,並結合抑制 GADD45A 表現,或許能夠提升臨床藥物帝盟多的療效。
英文摘要 Glioblastoma multiforme (GBM) is the most common malignant and deadly primary brain tumor. The highly chemo-resistance of GBM decreases the efficiency of cancer treatment, results in frequent tumor recurrence. In our previous study, microarray was applied to examine the expression profiles of tumor, and uncovered five potential bio-markers (CD44, GADD45A, fibronectin 1 (FN1), CD63 and secreted phosphoprotein 1 (SPP1)) in association with GBM. In this thesis, we sought to investigate the alternation of cellular mechanisms during temozolomide (TMZ) treatment, the first-line treatment for GBM, in order to identify novel therapeutic targets to improve therapeutic efficiency. Here, we showed that GADD45A is up-regulated by TMZ in both cell cycle and apoptosis arrays. Furthermore, GADD45A knockdown (GADD45Akd) enhanced the growth arrest and cell death induced by TMZ, even in natural (T98) and adapted (TR-U373) TMZ-resistant cells. Interestingly, GADD45Akd decreased the expression of O6-methylguanine-DNA methyltransferase (MGMT) in TMZ-resistant cells (T98 and TR-U373). In MGMT-deficient/ TMZ-sensitive cells (U87 and U373), GADD45Akd decreased TMZ-induced TP53 expression. These results suggested that GADD45A may plays a protective role against TMZ treatment through TP53-dependent and MGMT-dependent pathway in TMZ-sensitive and TMZ-resistant GBM, respectively.
Glioma stem cells (GSC) have been considered an important factor that contributes to chemoresistance, tumor recurrence and poor clinical outcome of GBM. CD44 has been thought to be GSC marker. We demonstrated that level of CD44 expression significantly correlate with histopathological grading of gliomas. However, further study showed that CD44 expression is positively associated with prognosis of GBM patients, implying the heterogeneity of CD44 in GSC. Thus, we attempted to investigate the correlation between CD44 expression and GSC traits. Here, we showed that CD44 knockdown (CD44kd) suppresses the proliferation accompanied by acquisition of GSC traits, including lower level of differentiation marker (glial fibrillary acidic protein, GFAP), higher ability of sphere formation and expression of stem cell markers (CD133, Oct4, Nanog and Nestin). In addition, treatment with hyaluronan (HA+), the major ligand of CD44, inhibited CD44 expression with increased GSC properties. Interestingly, incubation of HA+ with CD44kd cells facilitated glial differentiation. Our data showed that CD44 low-expressing cells exhibit GSC straits, arguing against the pertinence of CD44 as a marker of GSC. The preferential expression of CD44 at the invasive front in rat GBM implies that CD44 may be related to invasion and migration, rather then GSC marker of GBM.
In conclusion, the results of our study indicate that CD44 low-expressing cells exhibit GSC straits, and can be modulated by HA supplement. Additionally, GADD45A may play a protective role against TMZ treatment in GBM. Altogether, our study provides a new therapeutic strategy to enhance TMZ efficiency in GBM through combine action of HA supplement and specific inhibition of GADD45A.
論文目次 Acknowledgement (誌謝) ………………………………………………………I
Chinese Abstract (中文摘要) …………………………………………………...…III
Abstract ………………………………………………………………………….......V
Index ………………………………………………………………………………VII
Table and figure index …………………………………………………………….XII
Abbreviaations ………………………………………………………………….XIV
Chapter 1. Introduction ……………...……………………………………………...1
1. Brain tumor ..........................................................................................................1
2. Glioma ………………………………………………………….………………2
2.1. Glioblastoma multiform (GBM) …………………………………………...4
2.1.1. Etiology of GBM ……………………………………………………...5
2.1.2. Epidemiology of GBM ……………………………………………….6
2.1.3. Diagnosis and treatment of GBM ……………………………………..7
2.1.3.1. Surgical resection …………………………………………..8
2.1.3.2. Radiotherapy ……………………………………………….8
2.1.3.3. Chemotherapy ……………………………………………...9
2.1.3.4. TMZ resistance in GBM ………...………………………10
3. GADD45 family ………………………………………………………………12
3.1. GADD45A …………………………………………………………..……13
3.2. GADD45A in cancer ……………………………………………………..15
3.3. GADD45A and cancer therapy ………………………………..…………16
4. Cancer stem cell ………………………………………………………….……18
4.1. Definition of cancer stem cell …………………………………….........…19
4.2. Tumor heterogeneity and CSC hypothesis …….…………………………19
4.3. Identification of CSC ..……………………………………....................…21
4.4. Glioma stem cell ……………………………….............................………22
4.4.1. Discovery of GSC .…........................………………......……………22
4.4.2. GSC enrichment ………..……………………………....................…23
4.5. Heterogeneity of CSC .……………………………………...................…24
5. CD44 ……………………………………………………………..……………27
5.1. CD44 gene ………………………………………......................................27
5.2. CD44 protein ……………………………………..................................…28
5.3. CD44 in cancer ………………………………...............................………30
5.4. CD44 in CSC .……………………………….................................………33
6. Hyaluronan …………………………………….............................................…35
6.1. HA metabolism ………………………………………...............................37
6.2. HA in cancer ……………………………...................................…………39
6.3. Interaction of HA-CD44 in tumor progression .…….......………………41
6.4. HA-CD44 and CSC .……................……………………….......…………43
7. Statements of issues and research aims ……………………………….………45
Chapter 2. Materials and methods ………………………………................……49
1. Chemicals and medium ……………………………………..........................…49
2. Cell lines and culture ………………………………….............................……49
3. MTT assay ………………………………….............................................……49
4. RNAi transfectants for interference against CD44 ……....……………………50
5. Cell cycle analysis ……………………………………….................................50
6. HA-coated culture dish ………………………………..........................………50
7. RNA isolation and microarray hybridization ………………….....……………50
8. Reverse transcription PCR ………………………………….....................……51
9. Real-time qPCR …………………………………….....................................…52
10. Flow cytometry …………………………………………………..……………52
11. Apoptosis assay …………………………………….…………………………52
12. Western blot analysis …………………………….....…………………………53
13. Immunofluorescence …………………………………………......……………53
14. Immunocytochemistry ………………………………………………...………54
15. Giemsa staining …………………………………………………………….…54
16. Alcian blue stain ………………………………………………………………55
17. Colony-formation assay ……………………………….………………………55
18. Orthotopic glioma model ……………………………...………………………55
19. Patient samples ……………………………………………………..…………55
20. Statistical analysis ……………………………………………..........................56
Chapter 3. Results …………….........................……...............…………………….57
1. The molecular mechanisms affected by TMZ treatment to GBM cells in vitro ………………….....................………………………….......……………57
1.1. The effect of TMZ on cell cycle in U87 GBM cells …...................………57
1.2. The alternation of G2/M phase after TMZ treatment to GBM or non-GBM cell lines ..................................................................................................…57
1.3. Cell cycle and apoptosis-related genes expression in response to TMZ treatment to chemosensitive and chemoresistant GBM cell lines ………….................................………………………………………58
1.4. GADD45A expression in response to TMZ treatment to chemosensitive and chemoresistant GBM cell lines …………………………………...………59
1.5. Knockdown of GADD45A expression by siRNA in GBM cell lines ........59
1.6. Cell growth and morphology of chemosensitive and chemoresistant GBM cell lines in response to TMZ or GADD45Akd .......................................…60
1.7. Apoptosis of chemosensitive and chemoresistant GBM cell lines induced by TMZ or GADD45Akd ……...........................................……….....……61
1.8. Expression of p21 in response to TMZ treatment to chemosensitive and chemoresistant GBM cell lines ...............................................................…62
1.9. Expression of MGMT and TP53 in response to TMZ treatment to chemosensitive and chemoresistant GBM cell lines ...............................…62
2. The correlation of CD44 with GSC characters in GBM cells .......................…63
2.1. Knockdown of CD44 in rat and human GBM cell lines ............…………63
2.2. Effect of CD44kd on cell cycle in rat GBM cells ….....…...........…………63
2.3. Effect of CD44kd on cell morphology and sphere forming ability in rat and human GBM cell lines …................................................................………64
2.4. Effect of CD44kd on expression of GSC markers in rat and human GBM cell lines …..............................................................................................…65
3. The correlation of HA with CD44 and GSC characters in GBM cells ..............66
3.1. Distribution patterns of HA and CD44 in rat and human GBM .............…66
3.2. Effects of HA on cell growth and morphology in rat GBM cell lines ........67
3.3. Effect of HA on expression of GSC markers in rat GBM cell lines ...........68
3.4. Effect of HA on expression of HA metabolism-associated gene in rat GBM cell lines ........................................………………………………......……68
3.5. Effect of TMZ on expression of CD44 and GSC markers in rat and human GBM cell lines.............................................................................................69
Chapter 4. Discussion ................................................................................................70
Chapter 5. Conclusion ..............................................................................................81
Table and Figure ……………………………………………………...……………83
References …………………………………………………………………………132
Publications …………………………………………………….…………………165
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