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研究生:張博翔
研究生(外文):Po-Hsiang Chang
論文名稱:以幾丁聚醣薄膜作為癌細胞與人類誘導多能幹細胞之新穎三維細胞培養平台
論文名稱(外文):Chitosan Membranes as A Novel 3D Cell Culture Platform for Cancer Cells and Human Induced Pluripotent Stem Cells
指導教授:陳彥榮
指導教授(外文):Edward Chern
口試委員:徐善慧陳佑宗黃兆祺侯詠德黃楓婷
口試委員(外文):Shan-hui HsuYou-Tzung ChenEric HwangYung-Te HouFeng-Ting Huang
口試日期:2020-10-23
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:2020
畢業學年度:109
語文別:英文
論文頁數:174
中文關鍵詞:幾丁聚醣三維細胞培養系統癌症幹性人類誘導多能幹細胞
外文關鍵詞:chitosan3D cell culture systemcancer stemnesshuman induced pluripotent stem cell
DOI:10.6342/NTU202100071
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二維細胞培養常作為細胞生物學與醫學領域的研究模式,但生物體內的各種組織與器官處於複雜的三維網絡中,因此相較於二維細胞培養,三維細胞培養平台能準確地模擬體內真實的狀態。過去研究指出透明質酸與幾丁聚醣複合膜可作為肺癌細胞、胰臟癌細胞與間葉幹細胞的簡易培養平台。本論文則開發以幾丁聚醣為主的三維細胞培養系統,用於培養大腸癌細胞、肝癌細胞與人類誘導多能幹細胞。本論文第一部份,幾丁聚醣薄膜會促進癌細胞的腫瘤進程與幹細胞特性。除此之外,幾丁聚醣可能會活化 CD44 陽性大腸癌中典型的 Wnt/β-catenin-CD44 訊息路徑,也活化 CD44 陰性肝癌中非典型的 Wnt-STAT3 的訊息路徑。第一部分的研究顯示,幾丁聚醣作為培養基材能促進癌細胞的幹細胞特性,以作為未來研究癌症的基礎。基於幾丁聚醣與細胞幹性的交互作用,此薄膜有潛力成為簡便且符合成本效益的誘導多能幹細胞的培養平台。本論文第二部份,人類誘導多能幹細胞於幾丁聚醣薄膜上能長期維持住其增生速率與多能性,甚至相比於作為控制組的玻連蛋白基質,幾丁聚醣能促進類似於原態多能性的表徵。人類誘導多能幹細胞會於幾丁聚醣薄膜上自組裝形成三維球體,這些球體於此薄膜上可直接誘導成具有三維結構的三胚層細胞。第二部分的研究顯示,幾丁聚醣薄膜不僅能促進人類誘導多能幹細胞的類原態多能性特徵,也能作為一個新穎的三維分化模式。總結來說,此簡便以生醫材料為底的系統能作為一個癌細胞與誘導多能幹細胞的簡便三維培養平台,希望能加速再生醫學、疾病模擬與藥物開發的未來發展。
Two-dimensional (2D) adherent cell culture is widely used for research model in cell biology and medicine. However, tissues and organs are constructed through cell-cell and cell-extracellular matrix connections with complex three-dimensional (3D) networks in vertebrates. Emerging evidence indicated that 3D cell culture systems could mimic in vivo conditions and provide the accurate biological properties of cells. Previous studies have demonstrated that chitosan membranes crosslinked with hyaluronic acid could be a simple non-adherent 3D cell culture platform to study lung cancer cells, pancreatic cancer cells, and mesenchymal stem cells. In this dissertation, chitosan-based 3D cell culture system would be developed for the culture of colon cancer cells, hepatocellular carcinoma (HCC) cells, and human induced pluripotent stem cells (hiPSCs). In the first part, chitosan membranes promoted tumor progression and stemness properties. Furthermore, chitosan could activate canonical Wnt/β-catenin-CD44 axis signaling in CD44positive colon cancer cells and noncanonical Wnt-STAT3 signaling in CD44negative HCC cells. Chitosan as a simple culture substrate can regulate cancer stemness for further cancer research and drug screening. On the other hand, based on the relation between chitosan and cell stemness, chitosan probably served as a simplified and cost-effective culture system for hiPSCs. In the second part, chitosan membranes sustained the proliferation and pluripotency of hiPSCs in long-term culture. Moreover, using vitronectin as the comparison group, hiPSCs grown on the membranes displayed naïve-like characteristics. On the chitosan membranes, hiPSCs self-assembled into 3D spheroids which could be directly differentiated into lineage-specific cells from the three germ layers with 3D structures. Chitosan membranes not only promoted the naïve pluripotent features of hiPSCs but also provided a novel 3D differentiation platform. Collectively, this convenient biomaterial-based culture system can provide a convenient platform to study cancer cells and hiPSCs and accelerate the development of regenerative medicine and disease modeling.
口試委員會審定書 I
誌謝 II
中文摘要 III
Abstract IV
List of Abbreviations VI
Chapter 1. Introduction 1
1.1 In vitro cell culture system 1
1.1.1 Three-dimensional cell culture system 1
1.1.2 Polymer-based cell culture system 4
1.1.3 Chitosan 6
1.1.4 Hyaluronic acid 10
1.2 Cancer cell culture 12
1.2.1 Tumor microenvironments 12
1.2.2 Cancer stem cells and cancer stemness 14
1.2.3 Chitosan-based cancer cell culture system 17
1.3 Pluripotent stem cell culture 21
1.3.1 Pluripotent stem cells 21
1.3.2 Feeder-based and feeder-free systems for human pluripotent stem cells 23
1.3.3 3D culture systems for human pluripotent stem cells 26
1.3.4 Chitosan-involved materials for pluripotent stem cells 28
Chapter 2. Motivation and Aim 31
Chapter 3. Materials and Methods 33
3.1 Preparation of chitosan and chitosan-hyaluronic acid membranes 33
3.2 Cell line 34
3.2.1 Culturing cancer cell lines 34
3.2.2 Culturing human induced pluripotent stem cell lines 35
3.2.3 Culturing human mesenchymal stem cells 37
3.2.4 Lentivirus knockdown system 37
3.3 Flow cytometry analysis 38
3.3.1 Extracellular protein marker analysis 38
3.3.2 Intracellular protein marker analysis 39
3.3.3 Aldehyde dehydrogenase activity assay 39
3.3.4 Side population assay 40
3.3.5 Quiescent population assay 40
3.4 Cancer phenotype analysis 41
3.4.1 Transwell migration assay 41
3.4.2 Drug resistance assay 41
3.4.3 Sphere forming assay 42
3.5 Luciferase reporter assay 42
3.6 Immunofluorescence staining 43
3.7 hiPSC phenotype analysis 44
3.7.1 Embryoid body formation assay 44
3.7.2 Teratoma formation assay 44
3.8 Differentiation of hiPSCs 45
3.8.1 Trilineage differentiation 45
3.8.2 Neural stem cell differentiation 45
3.8.3 Cardiomyocyte differentiation 46
3.8.4 Hepatocyte differentiation 47
3.9 Bioinformatics 48
3.9.1 Microarray 48
3.9.2 Bulk RNA sequencing 48
3.10 Western blot 50
3.11 Real-time polymerase chain reaction 50
3.12 Statistical analysis 51
Chapter 4. Chitosan promotes cancer progression and stem cell properties in association with Wnt signaling in colon and hepatocellular carcinoma cells 52
4.1 Experimental design 52
4.2 Results 53
4.2.1 Morphologies of colon cancer and HCC cell lines on the membranes 53
4.2.2 Investigation of gene expression profiling on different substrate-harvested cells 53
4.2.3 Chitosan promoted cell motility and drug resistance 54
4.2.4 Chitosan regulated the cancer stemness properties 55
4.2.5 Chitosan increased the quiescent population 57
4.2.6 Characterization of the Wnt signaling pathways in colon cancer and HCC cells 57
4.2.7 The CD44-dependent effect of the colon cancer cells cultured on the membranes 58
4.3 Discussion 59
Chapter 5. Chitosan membranes serve as a novel feeder-free 3D cell culture system for human induced pluripotent stem cells 67
5.1 Experimental design 67
5.2 Results 68
5.2.1 Characterization of culture substrates and hiPSC behaviors 68
5.2.2 Chitosan-based substrates sustained the pluripotency of hiPSCs 69
5.2.3 Examination of gene expression profiling of hiPSC spheroids 71
5.2.4 Chitosan promoted the naïve-like features of hiPSCs 73
5.2.5 Long-term culture of hiPSCs on chitosan membranes 74
5.2.6 Generation of 3D neural stem cell-like spheroids on chitosan membranes 75
5.2.7 Chitosan membranes served as a 3D differentiation platform for cardiomyocytes 76
5.2.8 Differentiation of hiPSC spheroids into hepatocyte-like spheroids on chitosan membranes 77
5.3 Discussion 78
Chapter 6. Conclusion and Perspective 91
Chapter 7. Figures and Tables 93
Figure 1. Scheme of research into cancer stemness and cell-biomaterial interaction via culturing cancer cells on chitosan-based membranes. 93
Figure 2. Morphology of cancer cell lines cultured on different surfaces 95
Figure 3. Microarray analysis of HT29 grown on different substrates 97
Figure 4. Analysis of cell motility and migration-associated gene expression 100
Figure 5. Analysis of drug resistance and associated gene expression 104
Figure 6. Evaluation of the stemness properties in substrate-harvested cancer cells 107
Figure 7. Analysis of expression levels of specific markers in other cancer cell lines cultured on different substrates and HT29 harvested from a 3D culture system 109
Figure 8. Characterization of quiescent population for HT29 and Huh7 111
Figure 9. Evaluation of canonical and noncanonical Wnt signaling pathways in cancer cells 114
Figure 10. Effect of Wnt inhibition by IWP-4 treatment on morphology and stemnesss marker gene expression 117
Figure 11. Effect of knockdown of CD44 receptor on morphology and expression of stemness marker genes 120
Figure 12. Scheme of developing a feeder-free culture system and a 3D differentiation platform for hiPSCs using chitosan membranes. 121
Figure 13. Characterization of material properties of culture substrates 123
Figure 14. Characterization of hiPSC responses cultured on different substrates 125
Figure 15. Evaluation of hiPSC pluripotency harvested from three biomaterials 129
Figure 16. Transcriptome analysis of substrate-harvested hiPSCs using RNA sequencing 132
Figure 17. Comparison of expression of shared, naïve, and primed pluripotency markers in hiPSCs cultured on three substrates 137
Figure 18. Chitosan promoted the pluripotency and the naïve-like features in long-term hiPSCs 140
Figure 19. Karyotype analysis and expression of different pluripotency markers in hiPSCs cultured on VTN substrates and CS membranes 144
Figure 20. Neural differentiation of hiPSC spheroids harvested from CS membranes 146
Figure 21. Generation of cardiomyocyte spheroids from hiPSC spheroids cultured on CS membranes 148
Figure 22. 3D hepatocyte differentiation of CS-harvested hiPSC spheroids 150
Table 1. Antibody information 151
Table 2. RT-PCR primers and shRNA information 153
References 158
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