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研究生：	金育誠 Chin, Yu-Cheng
論文名稱：	針對醣蛋白標靶之光動力奈米平台於侵襲性惡性腫瘤之多模態治療與免疫微環境重塑研究 Research on photodynamic nanoplatforms targeting glycoproteins for multimodal therapy and immune microenvironment remodeling in aggressive malignant tumors
指導教授：	黃志嘉 Huang, Chih-Chia
學位類別：	博士 Doctor
系所名稱：	理學院 - 光電科學與工程學系 Department of Photonics
論文出版年：	2026
畢業學年度：	114
語文別：	英文
論文頁數：	294
中文關鍵詞：	膀胱癌、膠質母細胞瘤、胰臟癌、光動力療法 (PDT) 、化學動力療法 (CDT) 、糖蛋白標靶奈米平台、光增強芬頓反應、凝聚半乳糖奈米顆粒 (CG NPs) 、腫瘤微環境重塑、腫瘤相關巨噬細胞 (TAM) 重編程
外文關鍵詞：	Bladder cancer, Glioblastoma, Pancreatic cancer, Photodynamic therapy (PDT), Chemodynamic therapy (CDT), Photo-enhanced Fenton reaction, Glycoprotein-targeted nanoplatform, Condensed galactose nanoparticles (CG NPs), Tumor microenvironment remodeling, Tumor-associated macrophage (TAM) reprogramming.
ORCID：	0000-0002-0302-7925
相關次數：	點閱：11 下載：0
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侵襲性惡性腫瘤如膀胱癌(bladder cancer, BC)、胰臟癌(pancreatic cancer, PC)與膠質母細胞瘤(glioblastoma, GBM)通常具有高度轉移性、快速增殖以及高度復發風險，伴隨腫瘤內缺氧(hypoxia)、高濃度還原性環境(如glutathione, GSH)以及免疫抑制型腫瘤微環境(tumor microenvironment, TME)。上述因素大幅降低傳統手術、化學治療與光治療的治療成效。癌細胞表面過度表現的醣蛋白(glycoprotein)與半乳糖凝集素(galectins)及腫瘤相關巨噬細胞(tumor-associated macrophages, TAMs)多偏向促腫瘤的M2表現型，促進腫瘤免疫逃脫與腫瘤發展。因此，本研究以”醣蛋白標靶奈米平台”為核心概念，發展結合光動力催化、醣基免疫調控與多模態氧化反應之奈米治療策略，以提升侵襲性惡性腫瘤的治療效率並重塑腫瘤免疫微環境。
第一部分研究中，本研究設計並合成 iron oxide@chlorophyll (IO@FeChl) 奈米平台，將氧化鐵(Fe3O4)奈米核心與鐵葉綠素(FeChl)整合為雙功能系統，用於膀胱癌之光動力治療。Fe3O4奈米核心可提供穩定磁性及芬頓反應(Fenton reaction)，而FeChl 則在660 nm紅光雷射照射下產生單態氧(1O2)。特別的是，FeChl中心金屬 Fe2+/Fe3+ 可在腫瘤酸性微環境參與芬頓反應，催化內源性過氧化氫(H2O2)產生高反應性的羥基自由基(·OH)。透過照光強化芬頓(photo-enhanced Fenton)機制形成雙重活性氧 (ROS)放大，有效消耗細胞內 GSH、破壞腫瘤細胞的氧化還原平衡，並誘導粒線體損傷與脂質過氧化，進而引發鐵凋亡(ferroptosis)。此外，過程中亦誘發免疫原性細胞死亡(immunogenic cell death, ICD)，促使腫瘤細胞釋放危險相關分子模式(Damage-associated molecular patterns, DAMPs)，為後續免疫反應的活化奠定基礎，並證明光動力與化學動力協同可顯著提升氧化壓力並克服腫瘤抗氧化屏障。
第二部分研究進一步發展具多價半乳糖結構之Condensed Galactose Nanoparticles(CG NPs)，建立以醣蛋白辨識為核心的主動式腫瘤標靶與免疫調控平台。CG NPs透過水熱縮合形成穩定之多價半乳糖排列，其表面醣官能基與腫瘤細胞表面之醣蛋白(glycoprotein)及半乳糖凝集素(galectins)產生多價交互作用(multivalent interaction)，提升奈米粒子於腫瘤組織的累積與滯留。CG NPs 亦具備免疫調節能力，可與巨噬細胞表面的醣受體作用，活化NF-κB訊號並抑制STAT3活性，促使TAMs由M2表現型轉換為M1表現型，進而改善免疫抑制型腫瘤微環境。本研究進一步將此免疫調控策略應用於高度免疫抑制的胰臟癌與膠質母細胞瘤模型，以評估其於不同侵襲性腫瘤中的治療潛力。
第三部分研究中整合光動力催化與醣基免疫調控策略，建構 IONP@CG@Mn@MB多模態奈米平台。此系統以氧化鐵奈米粒子(IONP)為核心維持類芬頓反應，外層CG提供腫瘤標靶與免疫調控功能，MnO2外殼則可在腫瘤微環境中分解H2O2產生氧氣，改善缺氧狀態並提升光動力治療效率。MnO2分解後釋放之Mn2+可進一步促進類芬頓反應並放大ROS產生，形成時間依賴之雙相催化(biphasic catalysis)。結合光敏劑Methylene blue (MB)後，光照條件下可產生大量ROS，建立氧氣補充、GSH消耗與自由基生成之正回饋循環。此多模態奈米系統不僅顯著抑制腫瘤生長，亦同步降低免疫抑制相關分子表現並延長動物存活時間，展現光動力、化學動力與免疫調控三者協同治療的優勢。
本研究提出一套由光催化氧化壓力誘導、醣蛋白標靶辨識至免疫微環境重塑之階段式多模態奈米治療策略，此模式不僅突破傳統單一治療對氧氣依賴與免疫抑制的限制，也為未來結合光動力治療與免疫調控之奈米醫學在胰臟癌與膠質母細胞瘤等難治性腫瘤中的應用提供重要的設計指引。

Invasive malignant tumors such as bladder cancer (BC), glioblastoma (GBM), and pancreatic cancer (PC) generally exhibit a high degree of invasiveness, rapid proliferation capability, and significant risk of recurrence. Such tumors are typically accompanied by intratumoral hypoxia, high concentrations of reductive molecules (such as Glutathione, GSH), and an immunosuppressive tumor microenvironment (TME), thereby limiting the effectiveness of traditional surgical, chemotherapeutic, and phototherapeutic interventions. Moreover, the overexpression of glycoproteins and galectins on the surface of cancer cells, along with tumor-associated macrophages (TAMs) predominantly exhibiting the pro-tumor M2 phenotype, further enhances the immune evasion mechanisms of cancer cells. Considering the clinical challenges, this study employs a glycoprotein-targeted nanoparticle platform as the central concept, progressively establishing an integrative nanotherapeutic strategy induced by photocatalytic oxidative stress, glycan immune modulation, and multimodal oxidation and hypoxia amelioration, to explore its multi-layered mechanisms and therapeutic potential in invasive malignant tumors.
In the first part, an iron oxide@chlorophyll (IO@FeChl) nanoplatform was designed and synthesized by integrating an Fe3O4 core with Fe-chlorophyll (FeChl) into a dual-functional system. The Fe3O4 nanoparticle core provides stable magnetic properties and participates in Fenton reactions, while FeChl efficiently generates singlet oxygen (1O2) under 660 nm red laser irradiation. More importantly, the Fe2+/Fe3+ redox cycling at the center of FeChl actively participates in Fenton reactions within the acidic TME, catalyzing endogenous hydrogen peroxide (H2O2) into highly reactive hydroxyl radicals (·OH). This photo-enhanced Fenton reaction establishes a dual reactive oxygen species (ROS) amplification loop, effectively depleting intracellular GSH and disrupting redox homeostasis. The elevated oxidative stress induces mitochondrial dysfunction and lipid peroxidation, triggering ferroptosis. Simultaneously, it promotes immunogenic cell death (ICD), leading to the release of tumor-associated antigens and danger-associated molecular patterns (DAMPs), thereby priming subsequent immune activation. This stage demonstrates that the synergistic integration of photodynamic (PDT) and chemodynamic (CDT) therapy significantly enhances oxidative stress and overcomes tumor antioxidant defenses.
In the second part, condensed galactose nanoparticles (CG NPs) with multivalent galactose structures were developed to establish a glycoprotein-recognition-based active targeting and immunomodulatory platform. CG NPs, synthesized via hydrothermal condensation, present densely arranged multivalent galactose motifs on their surface. These glycan functional groups interact with tumor cell surface glycoproteins and galectins through multivalent interactions, significantly enhancing tumor accumulation and retention while improving therapeutic selectivity. Beyond targeting, CG NPs exhibit intrinsic immunomodulatory properties. Within the TME, TAMs predominantly display an M2 phenotype, secreting immunosuppressive cytokines such as IL-10 and TGF-β and promoting angiogenesis and metastasis. This study demonstrates that CG NPs interact with glycan receptors on macrophages, activate the NF-κB signaling pathway, and suppress STAT3 activity, thereby inducing polarization of TAMs from the M2 to the pro-inflammatory M1 phenotype. This shift leads to a substantial reversal of the immunosuppressive microenvironment.
In the third part, the advantages of photo-catalytic ROS amplification and glycan-mediated immune modulation were integrated to construct a multimodal IONP@CG@Mn@MB nanoplatform. The iron oxide nanoparticle (IONP) core sustains Fenton-like catalytic activity, the CG layer provides glycoprotein-targeted recognition and immune regulation, and the MnO2 shell decomposes H2O2 within the TME to generate oxygen, alleviating hypoxia and enhancing PDT efficiency. Upon degradation, MnO2 releases Mn2+ ions, further promoting Fenton-like reactions and amplifying oxidative stress in a time-dependent biphasic catalytic process. Incorporation of the photosensitizer methylene blue (MB) enables robust ROS generation under light irradiation, establishing a positive feedback loop involving oxygen supplementation, GSH depletion, and free radical production. This multimodal integrated system not only markedly suppresses tumor growth but also reduces immunosuppressive markers and prolongs animal survival, demonstrating the synergistic therapeutic advantages of PDT, CDT, and immune microenvironment remodeling.
In summary, this dissertation proposes a staged multimodal nanotherapeutic strategy that progresses from light-triggered catalytic oxidation and glycoprotein-targeted recognition to hypoxia modulation and immune microenvironment remodeling. By overcoming the limitations of oxygen dependence and immune suppression inherent in conventional single-modality treatments, this work presents an innovative therapeutic platform that integrates precise targeting, oxidative stress amplification, and immune activation for the treatment of aggressive malignant tumors.

中文摘要	I
Abstract	III
致謝		VI
Contents	VII
Table Contents	XII
Figure Contents	XIII
Chapter 1. Introduction	1
1	Research Background and Clinical Challenges	1
1.1.	Cancer	1
1.2.	The Challenges in Tumor Therapy	2
1.3.	Bladder cancer (BC)	3
1.4.	Glioblastoma (GBM)	11
1.5.	Pancreatic cancer (PC)	13
1.6.	Photodynamic therapy (PDT)	14
1.7.	Chemodynamic therapy (CDT)	16
2	Mechanistic Background of Nanomedicine and Glycobiology	18
2.1.	Synergistic effect of PDT and CDT	18
2.2.	The utilization of organic and inorganic nanoparticles in the treatment of bladder cancer, GBM and Pancreatic cancer.	21
2.3.	Multivalent interactions between carbohydrates NPs and glycoprotein.					..	22
2.4.	Galectin-Carbohydrate Recognition and Multivalent Binding Mechanisms	24
2.5.	Carbohydrate-Engineered Nanoparticles for Reprogramming Tumor-Associated Macrophages and Enhancing Anti-Tumor Immunity	26
2.6.	Immunogenic Effects of Synergistic PDT and CDT	29
Chapter 2. Motivation	34
1	Iron oxide@chlorophyll nanoparticles effectively target bladder cancer through photodynamic immunotherapy, inducing ferroptosis and enhancing immune response.	34
2	Exploiting the Potential of Sugar-Derived Nanoparticles: A Non-drug Strategy to Augment Immune Checkpoint Inhibition in the Treatment of Glioblastoma and Pancreatic Cancer	36
3	The nanoparticles composed of iron oxide and galactosylation are employed in PDT and immunostimulation for the therapeutic intervention of orthotopic bladder cancer.	39
4	Motivation for Developing Glycoprotein-Targeted Photodynamic Nanoplatforms	42
Chapter 3. Method and materials	45
1.	Materials	45
2.	Equipment	51
3.	Synthesis and experimental method of IO@FeChl	53
3.1.	Synthesis of IO@FeChl	53
3.2.	Synthesis of IO@FeChl-PEG-modified molecules	53
3.3.	Singlet oxygen (1O2) detection	54
3.4.	The catalytic characterization of colorimetric performance	54
3.5.	Photothermal effect under 650 nm and 808 nm laser irradiation	55
3.6.	In vitro cell viability measurement	55
3.7.	Cellular uptake measurement	56
3.8.	In vitro ROS and lipid peroxidation (LPO) analysis	56
3.9.	Western blotting assay	57
3.10.	PD-L1 and IDO-1 detection assay	58
3.11.	In vivo animal experiments	58
3.12.	In vivo synergistic therapy of ferroptosis and PDT	58
3.13.	Histological examination	59
3.14.	Immunohistochemistry (IHC)	59
4.	Synthesis and experimental method of Sugar-Based NPs	60
4.1.	Synthesis of condensed galactose nanoparticles (CG NPs)	60
4.2.	Synthesis of fluorescein isothiocyanate (FITC) and rhodamine B isothiocyanate (RITC)-CG NPs	60
4.3.	CG NPs stability	60
4.4.	The CG NPs conducted the FCS measurements	61
4.5.	qNano system measurement	61
4.6.	The Benedict’s reagent assay	62
4.7.	Using fluorescence imaging for intracellular localization	62
4.8.	Cell culture	63
4.9.	Cell viability (MTT Assay)	63
4.10.	The bone marrow-derived macrophages isolation	64
4.11.	M1/M2 macrophage (CD11b/CD86/CD206) Staining	64
4.12.	Detection of ROS using IF staining.	64
4.13.	Hemolysis measurement	65
4.14.	Enzyme-linked immunosorbent assay (ELISA)	65
4.15.	Blood-Brain Barrier Model	66
4.16.	Multicellular tumor spheroid (MCTS)	66
4.17.	Seahorse Assay	67
4.18.	RNA sequencing	67
4.19.	The proliferation and activation analysis of T-Cell	67
4.20.	The alterations of systemic and local immune after CG NPs treatment	68
4.21.	Establishment of an in situ Pan02-Luc pancreatic tumor model	68
4.22.	Establishment and treatment protocol of an animal model of glioblastoma derived from GL261 cells.	69
4.23.	Western blotting assay	70
4.24.	Cytotoxicity assays of T cells	70
4.25.	Apoptosis analysis of GL621 cells	71
4.26.	Transwell invasion and migration assay	71
4.27.	IVIS imaging system and quantification	72
4.28.	Immunohistochemistry (IHC) staining	72
4.29.	Hematoxylin and eosin (H&E) staining	72
4.30.	MR T2-RARE imaging for tumor tracking	73
4.31.	Biodistribution test of DiR labeled CG NPs and CG-RITC in GBM and PC model	73
4.32.	Biodistribution test of CG NPs by radioactive isotope	73
4.33.	Statistical Analysis	74
5.	Synthesis and experimental method of IONP@CG@Mn@MB	74
5.1.	Synthesis of IONP@CG@Mn NPs	74
5.2.	Synthesis of IONP@CG@Mn@MB NPs	75
5.3.	Measurement of the 1O2 produced by IONP@CG@Mn@MB	75
5.4.	Measurement of the cell viability after PDT	75
5.5.	Lipid peroxidation and ROS detection assay	76
5.6.	In vivo animal experiments	76
5.7.	In vivo orthotopic bladder cancer treatment	76
5.8.	Hematoxylin and Eosin (H&E) staining	77
5.9.	Hemolysis assay	77
5.10.	Apoptosis detection	78
5.11.	Immunohistochemistry (IHC)	79
Chapter 4. Results and discussion	80
1	Iron oxide@chlorophyll nanoparticles effectively target bladder cancer through photodynamic immunotherapy, inducing ferroptosis and enhancing immune response.	80
1.1.	Synthesis and characterization of iron oxide@chlorophyll clustered nanoparticles (IO@FeChl CNPs).	80
1.2.	Characterization of the IO@FeChl CNPs reveals ROS generation and redox imbalance, facilitating GSH oxidation (or degradation) in H2O2.	92
1.3.	CPBA-modified IO@FeChl CNPs nanoparticles exhibit cytotoxic properties and augment the efficacy of PDT in bladder cancer cells.	99
1.4.	ROS-induced lipid peroxidation by IO@FeChl-CPBA CNPs	108
1.5.	Integrating CDT-PDT within an orthotopic murine model of bladder carcinoma.	110
2	Exploiting the Potential of Sugar-Derived Nanoparticles: A Non-drug Strategy to Augment Immune Checkpoint Inhibition in the Treatment of Glioblastoma and Pancreatic Cancer	117
2.1.	Characteristics of Sugar-Based NPs	117
2.2.	Evaluation of the Antitumor Efficacy of CG NPs in Pancreatic Tumor Models	132
2.3.	The Immunoregulatory Potential of Sugar-Based NPs	139
2.4.	SLC16A3 internalized CG NPs may induce M2 macrophage polarization towards M1 macrophages	148
2.5.	The Apoptosis and Mitochondrial Impairment Induced by CG NPs	156
2.6.	CG NPs enhanced the efficacy of Anti-PD-L1 therapy in GBM.	170
3	The nanoparticles composed of iron oxide and galactosylation are employed in PDT and immunostimulation for the therapeutic intervention of orthotopic bladder cancer.	193
3.1.	Preliminary Development of IONP@CG NPs	193
3.2.	Characterization of IONP@CG@Mn	198
3.3.	In vitro catalytic capacity of IONP@CG@Mn	203
3.4.	In vitro photodynamic capacity of IONP@CG@Mn@MB	209
3.5.	The PDT capacity of IONP@CG@Mn@MB at bladder cancer cell.	216
3.6.	The IONP@CG@Mn@MB synergy therapy treated orthotopic bladder tumor	225
Chapter 5. Conclusion	233
References	236
                                    

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