具邊際效應標靶肺部遞送藥物載體應用於程式化抗原捕捉傳遞於樹突細胞

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研究生：	黃氏美惠 Huynh, Thi My Hue
論文名稱：	具邊際效應標靶肺部遞送藥物載體應用於程式化抗原捕捉傳遞於樹突細胞 Programmed Antigen Capture-Harnessed Dendritic Cells by Margination-Mimicking Lung Delivery
指導教授：	胡尚秀 Hu, Shang-Hsiu
口試委員:	姜文軒 Chiang, Wen-Hsuan 黃振煌 Huang, Jen-Huang 張佳智 Chang, Chia-Chih 李亦淇 Lee, I-Chi 張建文 Chang, Chien-Wen
學位類別：	博士 Doctor
系所名稱：	原子科學院 - 生醫工程與環境科學系 Department of Biomedical Engineering and Environmental Sciences
論文出版年：	2024
畢業學年度：	112
語文別：	英文
論文頁數：	156
中文關鍵詞：	肺轉移、穿透、細胞膜仿生、銅凋亡、抗原捕獲、紅細胞攜帶、免疫療法
外文關鍵詞：	cell membrane mimetic, hitchhiking
相關次數：	點閱：2 下載：0
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在癌症免疫療法中，像是免疫檢查點阻斷（ICB）和T細胞輸入療法（T-cell-based adoptive cell transfer therapy），已成為腫瘤治療上的突破性方法，徹底改變對抗各種惡性腫瘤的治療方式，特別是對肺癌的治療帶來優勢。免疫抑制腫瘤微環境（TME）是抗腫瘤反應中的核心因子，可以限制免疫檢查點阻斷的免疫治療效果，例如程序性細胞死亡1抗體（PD-1）及其配體（PD-L1）抗體透過抑制細胞毒性T淋巴球（CTL）的抗腫瘤免疫原性。在抗腫瘤免疫反應活化後，細胞毒性T淋巴球的活化、增殖和分化在殺死腫瘤細胞中發揮關鍵作用，為可活化癌症免疫療法的有效策略或替代方法。為了誘導T細胞活化並增強腫瘤免疫治療，有一種新型策略是在目標器官處收集功能性製劑以提高抗原免疫原性。因此，我們開發了基於IONP多功能的細胞膜模擬共聚物（合成細胞）和紅血球（天然細胞），如下：（1）透過級聯響應細胞膜模擬共聚物包裹奈米樹莓進行程序性肺轉移免疫治療-介導的艾司洛莫-銅遞送，以及(2) 透過細胞遷移作用肺部遞送來編程抗原捕獲利用的樹突狀細胞。
在第一部分中，研究了一種包含級聯響應細胞膜模擬共聚物（zwitterionic 2-methacryloyloxyethyl phosphorylcholine-co-3-hydroxypyridin-4-one，PH）和銅凋亡（cuproptosis）分子（elesclomol-Copper，Es-Cu）用於編程T細胞浸潤的腫瘤穿透磁性顆粒（TUP）。特別是使用奈米樹莓樣氧化鐵奈米顆粒（NR）作為高溫熱療平台，這是包括免疫原性細胞死亡（ICD）和逆轉免疫抑制腫瘤微環境在內的雙重免疫療法。在轉移簇中，ES和銅離子在細胞內環境和熱療的觸發下很容易釋放。ES和銅離子同時誘導癌細胞的銅凋亡並刺激免疫反應。兩性離子MPC結構受細胞膜的生物附著作用，而3-hydroxypyridin-4-one結構受螯合劑和抗原儲存庫啟發，將自體腫瘤相關抗原運送至樹突狀細胞，從而誘導持續的免疫活化。
在第二部分中，結合了紅血球遞送（RBC hitchhiking）和免疫調節特徵，通過在紅血球（RBCs）表面加載多粒徑氧化鐵奈米結構（MIO@RBC）進行評估。特別是使用紅細胞作為天然載體劑進行肺腫瘤特異性藥物遞送，通過放置奈米顆粒和多粒徑氧化鐵奈米結構MIOs，可在施加交變磁場（AFM）時作為摩擦熱發生器，以及作為抗原捕獲劑將新抗原和損傷相關分子模式遞送至淋巴結，有助於有效的T細胞招募和免疫療法。MIO@RBC顯示出優異的免疫逃逸和腫瘤特異性靶向能力，顯著提高了體內循環壽命和高腫瘤積聚。

Cancer immunotherapies, including immune checkpoint blockade (ICB) and T-cell-based adoptive cell transfer therapy, has emerged as a groundbreaking approach in the field of oncology, revolutionizing the way we combat various types of malignancies, including lung cancer with its advantages. The immunosuppressive tumor microenvironment (TME), a central factor of the antitumor response, can limit the immunotherapeutic effects of immune checkpoint blockades (ICBs), such as programmed cell death 1 antibodies (PD-1) and its ligand (PD-L1) antibodies by inhibiting the cytotoxic T lymphocytes (CTLs) antitumor immunogenicity. Upon the activation of antitumor immune response, the effective activation, proliferation and differentiation of CTLs, which play a critical role in killing tumor cells, is an effective design strategy and alternative approaches toward activatable cancer immunotherapy. To elicit T cells and achieve the enhanced tumor immunotherapy, a promising strategy is collected functional agents at the targeted organ to improve antigen immunogenicity. Therefore, we developed the IONP multifunction-based cell membrane-mimetic copolymer (synthetic cell), and red blood cells (living cell), as follow: (1) Programmed Lung Metastasis Immunotherapy via Cascade-Responsive Cell Membrane-Mimetic Copolymer-Wrapped Nanoraspberry-Mediated Elesclomol-Copper Delivery, and (2) Programmed antigen capture-harnessed dendritic cells by margination-hitchhiking lung delivery.
In the first part, a tumor penetrating magnetic particles (TUP) containing the cascade-responsive cell membrane-mimetic copolymer (zwitterionic 2-methacryloyloxyethyl phosphorylcholine-co-3-hydroxypyridin-4-one, PH) and cuproptosis molecules (elesclomol-copper, EsCu) for programming T cell infiltration is investigated. In particular, the using of nanorasberry like iron oxide nanoparticles (NR) as platforms for the hyperthermia therapy, which is synergized immunotherapy including immunogenic cell death (ICD) and reversing the immunosuppressive tumor microenvironment. In metastatic clusters, ES and Cu, triggered by intracellular environments and hyperthermia, are readily released. ES and Cu simultaneously induce cuproptosis of cancer cells and stimulate immune responses. The zwitterionic MPC block was inspired by the antifouling structure of cell membranes, and the 3-hydroxypyridin-4-one block was inspired by chelating agent, and antigen reservoirs, transporting autologous tumor-associated antigens to dendritic cells, thereby inducing prolonged immune activation. The therapies facilitate the release of tumor-associated antigens, including neoantigens and damage-associated molecular patterns
In the second part, the combines the features of RBC hitchhiking and immunomodulatory are evaluated by loading a multi-grained iron oxide nanostructures onto the surface of RBC (MIO@RBC). Particularly, the employment of red blood cells (RBCs) as natural carrier agents for lung tumor-specific drug delivery by placing nanoparticles, and a multi-grained iron oxide nanostructure MIOs can be used as a frictional heat generator with applying an alternating magnetic field (AFM), as well as an antigen capture agent to deliver neoantigens and damage-associated molecular patterns to lymph nodes, contributing to efficient T cell recruitment and immunotherapy. MIO@RBC showed the excellent immune escape and tumor-specific targeting capabilities, which significantly improved the in vivo circulation lifetime and high tumor accumulation.

中文摘要    i
Abstract    iii
致谢    v
Acknowledgment    vi
Chapter 1 Introduction    1
Chapter 2 Literature Review and Therapy    4
1. Introduction of Lung Metastasis and Mechanism of Metastatic Lung Cancer    4
2. Current State of Lung Metastasis Treatment    7
2.1. Overview of Immunotherapy in Lung Metastasis Treatment    9
2.2. Introduction of Cupprotosis in Lung Metastasis treatment    15
3. Overviews of Biomimetic Materials    19
3.1. Nanomaterials: A Promising Class of Biomimetic Medical Materials    20
3.2. Cell-based drug delivery systems for immunotherapy    31
3.3. Red blood cells-based drug delivery system    40
Chapter 3 Experiment section    45
1. Materials    45
1.1. Materials used in synthesis for case study 1    45
1.2. Materials used in synthesis for case study 2    45
1.3. Materials used for in vitro study    46
1.4. Materials used for in vivo study    47
2. Apparatus and Instuments    48
3. Synthesis of multi-grained iron oxide nanostructures (MIOs)- Nano-raspberry-like iron oxide nanoparticles (NR)    50
4. Characterization Techniques    50
4.1. Dynamic Light Scattering (DLS)    50
4.2. Scanning Electron Microscopy    51
4.3. Transmission Electron Microscopy    51
4.4. Powder X-ray Diffraction Spectroscopy (XRD)    51
4.5. X-ray Photoelectron Spectroscopy (XPS)    51
4.6. Magnetic Thermal Heating    52
5. In vitro study    52
5.1. Cellular subculture    52
5.2. Cellular uptake, distribution, and cytotoxicity    52
5.3. Flow cytometry for cell uptake    53
5.4. Antigen release    54
5.5. Multicellular spheroids chip fabrication    54
6. In vivo study    55
6.1. In Vivo Imaging System (IVIS)    55
6.2. Immunohistochemistry (IHC) staining    56
6.3. Flow cytometry analysis    56
6.4. Animal Survival Test    57
7. Analytical Analysis    57
Chapter 4    58
Programmed Lung Metastasis Immunotherapy via Cascade-Responsive Cell Membrane-Mimetic Copolymer-Wrapped Nanoraspberry-Mediated Elesclomol-Copper Delivery    58
1. Introduction    58
2. Experiment section    64
2.1. Synthesis of NR, PH and TUP    64
3.2. Characterizations    64
3.3. Membrane disruption property of TUP    65
3.4. Cellular uptake, distribution, and cytotoxicity    66
3.5. Western blot analysis    67
3.6. Multicellular spheroids chip fabrication    68
3.8. In vivo experiment and Immunohistochemistry (IHC) staining    68
3.9. In vivo flow cytometry analyses    69
3.10. Immunofluorescence of lymph node sections    70
3.11. In vivo anticancer efficacy and survival rate with synergistic therapy    70
3.12. Statistical Analysis    71
4. Results and Discussion    71
4.1. Synthesis and Characterization of Copolymer p(MPC-co-HOPO) (PH)    71
4.2. PH Induced Cellular Membrane Leakage    74
4.3. Synthesis and Characterization of EsCu-loaded TUP    75
4.4. Characterization of NR, TUP1 and TUP2    79
4.5.    In vitro cytotoxicity, cell uptake and lysosomal escape of NR and TUP    83
4.6.    Penetrated delivery of TUP in tumor spheroids    89
4.7.    In vivo metastatic tumor penetration study of TUP    92
4.8.    Recruitment of T cells to lung metastases    95
4.9. Antigens capture trigger immune response by TUP    97
5.    Conclusion    100
Chapter 5    102
Programmed antigen capture-harnessed dendritic cells by margination-hitchhiking lung delivery    102
1. Introduction    102
2. Material and method    104
2.1. Synthesis of Multi-Grained Iron Oxide Nanostructures (MIOs)    104
2.2. Blood collection and isolation of RBCs    105
2.3. Binding of MIOs to RBCs    105
2.4. Characterizations    106
2.5. Erythrocyte agglutination by MIO particles    107
2.6. Erythrocyte osmotic fragility:    108
2.7. Cellular uptake, distribution, and cytotoxicity    108
2.8. Immunofluorescence of lymph node sections    109
2.9. Analysis of LN cells by flow cytometry    110
2.10. Biodistribution and survival rate with synergistic therapy in vivo    110
2.11. Identification of Proteins Binding to MIO    111
3. Results and discussion    112
3.1. Binding efficiency of MIOs to RBCs    112
3.2. Cytotoxicity and cell uptake of MIO@RBC    117
3.3. Penetration and margination of MIO@RBC in 3D tumor spheroids    120
3.4. In vivo lung accumulation of MIO@RBC    122
3.5. In vivo mice bearing lung metastasis treated by MIO@RBC    125
3.6. Antigen capture and deliver by MIOs    127
4. Conclusion    130
Chapter 6     Conclusion    132
Chapter 7      Reference    134
Chapter 8     Appendix    152
1. Copyright permission from Elsevier    152
2. Copyright permission from Wiley    152
3. Curriculum Vitae    154

                                

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