Oxygen-supplying platforms to create hyperoxia-inducible hydrogels for In situ tissue regeneration = In situ 조직 재생을 위한 과산소 유도 하이드로젤 생성 산소 공급 플랫폼

국문 초록 (Abstract)

지난 20년간 조직 공학 및 재생 의학 분야 (Tissue engineering and regenerative medicine, TERM)는 조직 손상과 장기 기능 상실에 대한 새롭고 유망한 해결책을 제시하며 크게 발전해 왔다. 이러한 발전은 주로 체외 조직 공학 (Ex vivo tissue engineering) 개발의 기초 프레임워크 역할을 하는 생체 재료의 중추적인 역할에 기인합니다. 하지만, 체외 조직 공학은 기증 조직의 질병 이환율과 세포 배양의 복잡성 등의 한계점에 직면하였다. 이러한 문제들을 바탕으로, 최근 더 유망하고 효율적인 전략으로써, in situ 조직 재생 (In situ tissue regeneration)이 떠오르고 있다. in situ 조직 재생은 생체재료의 다양한 생물•물리•화학적 자극을 통해 신체의 내재된 재생 능력과 조직 환경을 활용하는 전략이다.
조직 재생을 위한 다양한 생체재료 중에서 고분자 하이드로젤은 체내 세포외 환경과의 구조적 유사성, 조절 가능한 특성, 그리고 세포 및 치료제의 간단한 담지 능력 때문에 주목받아 왔다. 최근 조직 공학 및 재생의학의 경향에 맞춰 강성, 지형, 열, pH, 금속 이온 및 산소 등 다양한 생물•물리•화학적 자극을 통해 신체의 내재된 재생 능력을 활용하는 생체 활성 하이드로젤 개발이 최근 전략으로써 제시되고 있다. 다양한 자극들 중, 과산소 환경은 (21% 이상의 산소 분압), 면역세포 유입, 세포 증식, 혈관 생성, 콜라겐 성숙 등 상처 치유에 효과적인 것으로 알려져 많은 주목을 받고 있다. 따라서, 다양한 산소 전달 하이드로젤 (Oxygen-delivering hydrogel, ODG)이 산소 운반 또는 생성 물질들을 사용하여 개발되고 있으며, 유효성과 잠재성을 입증하고 있다. 하지만, 이러한 하이드로젤의 사용은 산소 전달 인자 및 그 부산물과 관련된 세포 독성 문제로 제한된다. 특히 과산화칼슘 (Calcium peroxide, CaO2), 과산화마그네슘 (Magnesium peroxide, MgO2), 과산화수소 (Hydrogen peroxide, H2O2) 등 과산화물 (Peroxide)은 쉽게 구할 수 있고, 우수한 산소 발생 능력을 보이지만, 그 부산물인 과산화수소는 고농도에서 세포 독성을 나타내는 문제가 있다. 따라서, 과산화수소를 물과 산소로 분해하는 카탈레이즈의 사용이 필수적이다. 하지만, 카탈레이즈의 과도한 사용 (>500 U/mL)은 세포 신호 전달 물질의 분해로 세포 신호 전달 기작을 억제할 수 있어, 산소 전달 인자 및 그 부산물의 세포 독성 문제를 극복하는 진보된 산소 전달 하이드로젤의 개발이 요구된다.
현재 조직 재생을 위해 개발된 산소 전달 하이드로젤 전략은 (ⅰ) 조직 손상 후 형성되는 초기 저산소증 완화, (ⅱ) 지속적인 산소 공급을 통한 전반적인 상처 치유 과정 개선, 그리고 (ⅲ) 과산소 산화 스트레스를 통한 체내 재생 능력 유도 세 가지로 분류된다. 모든 전략의 치료 효과는 고압 산소 치료법을 통해 입증되었으며, 대부분의 산소 전달 하이드로젤은 전략 (ⅰ) 및 (ⅱ)를 바탕으로 설계되고 연구된다. 그러나, 현재 산소 전달 하이드로젤을 사용하여 전략 (ⅱ)를 구현하는 것은 상처의 재구성 단계까지 충분한 산소 전달을 할 수 없어 어렵다는 문제가 있다. 따라서, 개발된 산소 전달 하이드로젤을 연구를 위해서는 정확한 전략과 치료 효과의 메커니즘이 요구된다.
따라서, 우리는 in situ 조직 재생을 위한 새로운 유형의 산소 공급 플랫폼을 개발하고, 이를 활용하여 다양한 형태의 산소 방출 하이드로젤을 제작한다. 주요 목표는 가교제, 카탈레이즈 또는 고체 과산화물로부터 생성된 금속 이온 및 과산화수소와 같은 부산물의 함유를 최소화하는 과산소 방출 하이드로젤을 개발하는 것이다. 이 전략을 통해 산소 생성 인자 및 그 부산물에 의한 세포 독성 문제를 해결할 수 있다. 또한, 우리는 과산소 산화 스트레스에 초점을 맞춰 전반적인 상처 치유 과정에 대한 이들의 안전성과 치료 효과를 입증한다. 이를 위해, 우리는 먼저 산소 방출 하이드로젤을 제조하기 위한 기본 재료로 자가 가교 하이드로젤을 처음 개발한다 (2장). 이 하이드로젤은 고분자 간의 티올-엔 반응을 통해 가교제 없이도 형성될 수 있어, 간단한 조성을 가진다. 또한, 이 가교 반응은 조직 표면의 작용기와도 상호 작용할 수 있다. 이 하이드로젤은 간단한 조성을 바탕으로 산소 방출 하이드로젤의 기본 재료로 활용하기 위해 설계되었지만, 우리는 이 하이드로젤을 허혈성 심장 표면에 심근 패치를 고정하기 위한 조직 접착성 생체 실란트로서 연구했다. 바이오 실란트의 기계적 및 조직 접착 특성을 향상하기 위해 강화제로서 과산화칼슘 (Calcium peroxide, CaO2)을 사용하였으며, 이는 과산화수소 생성에 의해 티올화된 젤라틴의 이황화 결합 형성을 유도할 수 있어 상용 피브린 접착제보다 강력한 조직 접착력을 보인다. 이 생체적합성 바이오 실란트를 활용하여 쥐 심근 모델 내에서 심근 패치를 성공적으로 고정하였으며, 섬유화 감소와 함께 심장 기능을 개선했다.
다음으로 우리는 과산화칼슘 매개 도파민 산화 및 카탈라아제 고정화를 통해 산소 공급 주사기 (Oxygen-supplying syringe, Oxyringe (옥시린지))를 개발했다 (3장). 이 옥시린지는 고정된 카탈라아제에 의한 과산화수소 분해를 통해 산소를 생성하여 하이드로젤 용액 내에 고농도 산소를 공급하고, 활성화된 카탈라아제 혼입을 최소화한다. 우리는 이 시스템을 활용하여 주사 가능한 과산소화 유도 하이드로젤을 제작하여 생체 내에서 일시적인 과산소 환경을 제공한다. 흥미롭게도, 이러한 하이드로젤은 생체 내 지혈, 염증, 증식 및 리모델링 단계와 같은 전반적인 상처 치유 과정을 촉진한다.
카탈라아제 고정화 산소 공급 기술의 유효성을 바탕으로, 본 기술의 다양한 산소 전달 시스템 제작에 대한 적용 가능성을 연구한다 (4장). 이 기술을 튜브나 유리병과 같은 상업용 용기에 적용하고, 고정되는 카탈라아제의 농도를 높여 기능성을 향상함으로써 산소 공급 기술의 적용 가능성을 높였다. 이 산소 공급 용기 (Oxygen-supplying container, Oxygener (옥시즈너))는 기존 옥시린지 시스템 대비 3배 이상 향상된 과산화수소 분해 능력과 산소 발생 효율을 보여준다. 옥시즈너를 사용하여 잔존 과산화수소를 최소화하는 산소 담지 미디어를 제작하고, 체외 3차원 세포 배양 환경에서 세포 적합한 고농도 산소 환경을 제공한다. 다음으로, 자가 가교 하이드로젤 디스크를 간단하게 산소 담지 미디어에 담가, 미리 형성된 하이드로젤을 고농도 산소 방출 하이드로젤로 제작하였다. 이러한 산소 담지 미디어와 산소 방출 하이드로젤은 생체 내에서 일시적인 고산소 상태를 제공하여, 생체 내 대식세포 침윤, 세포 증식, 신생 혈관 형성, 섬유아세포 분화 및 콜라겐 성숙 등을 촉진한다. 특히 고농도 산소는 재구성과 관련된 유전자 발현을 상향 조절하는 것으로 나타났다.
결론적으로, 우리는 용존 산소를 공급하는 새로운 유형의 카탈라아제 고정화 산소 공급 시스템을 개발하여, 가교제나 산소 발생 인자 그리고 그 부산물의 혼입을 최소화하는 고산소 산소 방출 하이드로겔을 만들었다. 또한 이러한 하이드로겔은 우수한 생체 적합성과 급성 과산화 스트레스에 의한 전반적인 상처 치유 과정의 촉진을 보였다. 이러한 발견은 현장 조직 재생을 위한 유망한 산소 전달 플랫폼으로서 우리 시스템의 상당한 잠재력을 보여주었다.

다국어 초록 (Multilingual Abstract)

Over the past two decades, tissue engineering and regenerative medicine (TERM) has experienced significant progress, offering promising solutions for treating tissue damage and organ failure. This progress is primarily attributed to the pivotal role of biomaterials in TERM, which serve as a foundational framework for developing ex vivo tissue engineering. However, ex vivo tissue engineering faces significant hurdles, such as donor tissue morbidity and the complexities of cell cultivation. Recognizing these issues, in situ tissue regeneration has recently emerged as a promising and efficient strategy. In situ tissue regeneration leverages innate regenerative capacity and the tissue environment of the body through various biophysicochemical cues of biomaterials.
Polymeric hydrogels have stood out in various biomaterials for tissue regeneration due to their structural resemblance to the native extracellular matrix, easy to control properties, and simple encapsulation of cells and therapeutics. Recent trends in developing advanced hydrogels are to create bioactive hydrogels designed to harness endogenous regenerative capabilities through various biophysicochemical cues (e.g., stiffness, topography, heat, pH, metal ion, and oxygen).
Among various stimuli, hyperoxia, an excessive oxygen tension above 21% pO2, has attracted much attention due to its therapeutic effects on wound healing, such as immune cell recruitment, cell proliferation, angiogenesis, and collagen maturation. Consequently, various oxygen-delivering hydrogels (ODGs) have been developed using oxygen-carrying or oxygen-generating agents, demonstrating their feasibility and potential. However, their applications are limited by some cytotoxic issues related to oxygen-delivering agents and their byproducts. Notably, peroxide materials (e.g., calcium peroxide (CaO2), hydrogen peroxide (H2O2), and magnesium peroxide) exhibit easy availability and high oxygen payload, while their byproducts, such as metal ions and H2O2, have cytotoxic issues at excessive concentrations. Consequently, it is essential to use catalase as an H2O2 scavenger, decomposing H2O2 into oxygen and water. However, excessive use of catalase (>500 U/mL) can suppress cellular signaling pathways by decomposing cellular signaling molecules, such as reactive oxygen and nitrogen species. Thus, it is challenging to develop advanced ODGs to overcome these cytotoxicity issues.
The current strategies of ODGs for tissue regeneration can be categorized into three approaches: (ⅰ) mitigating initial hypoxia after injury, (ⅱ) improving the entire wound healing processes through prolonged oxygen supply, and (ⅲ) stimulating inherent regenerative capacity via hyperoxic oxidative stress. The effectiveness of all strategies has been demonstrated through hyperbaric oxygen therapy, and most ODGs have been designed and discussed using strategies (ⅰ) and (ⅱ). However, implementing strategy (ⅱ) using current ODGs is challenging due to the short oxygen delivery duration, which is insufficient until the wound remodeling phase (approximately 2 weeks or more) in vivo. Consequently, accurate strategy and mechanism of therapeutic outcomes are required to investigate the development of ODGs.
Herein, we develop a new type of oxygen-supplying platform and create various types of oxygen-releasing hydrogels for in situ tissue regeneration. The primary goal is to create hyperoxic oxygen-releasing hydrogels that minimize incorporating additives or byproducts, such as crosslinkers, catalase, H2O2, and metal ions produced from solid peroxide. This approach can address the cytotoxic issues of oxygen-generating agents and their byproducts. Next, we demonstrate their safety and therapeutic effects on the overall wound healing process focused on hyperoxic oxidative stress. To achieve these objectives, we first develop self cross-linkable hydrogels as a base material for fabricating oxygen-releasing hydrogels (Chapter 2). This hydrogel can be formed without a crosslinker through the thiol-ene reaction between polymers, resulting in a simple composition. This crosslinking chemistry can also interact with the functional groups on the tissue surface. Although this hydrogel was designed to be utilized as a base material due to its simple composition for oxygen-releasing hydrogels, we investigated it as a tissue adhesive biosealant to immobilize the cardiac patch onto the infarcted heart surface. To improve the mechanical and tissue adhesive properties of biosealant, we incorporate CaO2 as an enhancer, which can induce disulfide bond formation of thiolated gelatin by H2O2 generation, showing stronger tissue adhesive force than commercial fibrin glue. Using this biosealant, we successfully immobilize the cardiac patch within rat myocardial models, improving cardiac function with reduced fibrosis. Subsequently, we develop the oxygen-supplying syringe (Oxyringe) through CaO2-mediated dopamine oxidation and catalase immobilization (Chapter 3). This Oxyringe generates oxygen through H2O2 decomposition by immobilized catalase, supplying hyperoxic oxygen within hydrogel solution with minimizing activated catalase incorporation. Utilizing this system, we fabricate injectable hyperoxia-inducible hydrogels, providing transient hyperoxic conditions in vivo. Interestingly, these hydrogels facilitate overall wound healing processes, such as hemostasis, inflammation, proliferation, and remodeling phases in vivo. Based on the feasibility of the catalase-immobilized oxygen-supplying technique, we investigated its applicability for fabricating various oxygen-delivering systems (Chapter 4). We adapt this technique to commercial containers, such as tubes and glass vials, with improved functionality by increasing the concentration of immobilized catalase to promote the applicability of the oxygen-supplying technique. This oxygen-supplying container (Oxygener) reveals promoted H2O2-scavenging ability and oxygen-generating efficiency more than threefold compared to the Oxyringe system. Using the Oxygener, we create oxygen-enriched media that minimizes residual H2O2, providing cytocompatible hyperoxic conditions in 3D cell culture conditions in vitro. Next, we fabricate pre-formed hyperoxic oxygen-releasing hydrogels by simply soaking hydrogel discs within the oxygen-enriched media. These oxygen-enriched media and oxygen-releasing hydrogels provide transient hyperoxic conditions in vivo, promoting the resolution of macrophage infiltration, cell proliferation, neovascularization, fibroblast differentiation, and collagen maturation in vivo. Notably, the hyperoxic oxygen upregulated the gene expression-related remodeling phase.
In conclusion, we developed new types of catalase-immobilized oxygen-supplying systems that supply dissolved oxygen to create hyperoxic oxygen-releasing hydrogels that minimize the incorporation of additives or oxygen-generating agents. Furthermore, these hydrogels revealed improved biocompatibility and promoted overall wound healing processes via acute hyperoxic oxidative stress. These findings demonstrated significant potential for our systems as a promising oxygen-delivering platform for in situ tissue regeneration.

목차 (Table of Contents)

• Abstract i
• Table of Contents iv
• List of Tables viii
• List of Figures ix
• List of Abbreviations xi
• Chapter 1. General Introduction
• 1.1 Advanced Polymeric Hydrogels for Tissue Engineering and Regenerative Medicine 1
• 1.1.1 Trends in Tissue Engineering and Regenerative Medicine 1
• 1.1.2 Bioactive Polymeric Hydrogels for In Situ Tissue Regeneration 2
• 1.2 Understanding the Endogenous Wound Healing Process and Foreign Body Reaction 4
• 1.2.1 Innate Wound Healing Process 4
• 1.2.2 Foreign Body Reaction 8
• 1.3 Oxygen in Wound Healing 10
• 1.4 Hyperoxic Oxygen and Its Biological Mechanism 13
• 1.5 Recent Trends in Developing Oxygen-delivering Hydrogels 16
• 1.5.1 Oxygen-releasing Hydrogels 17
• 1.5.1.1 Hb-based Oxygen Carriers and Their Derivates 17
• 1.5.1.2 Perfluorocarbons and Their Derivates 22
• 1.5.2 Oxygen-generating Hydrogels 25
• 1.5.2.1 Solid Peroxides as Powerful Oxygen Generators 25
• 1.5.2.2 Liquid Peroxides and Catalase or Catalase-like Materials 29
• 1.5.2.3 Photosynthetic Microorganisms 33
• 1.5.3 Strategies of Oxygen-delivering Hydrogels for Wound Healing 36
• 1.6 Current Limitations and Requirements for Advances in Developing Oxygen-delivering Hydrogels 44
• 1.6.1 Cytotoxicity and Complexity of Current Techniques 44
• 1.6.2 Strategies of Recent Techniques for Tissue Regeneration 44
• 1.7 Overall Objectives 45
• Chapter 2. Self Cross-linkable Oxygen-generating Biosealant to Immobilize Stem Cell Spheroid-laden 3D Patch for Myocardial Infarction Treatment
• 2.1 Introduction 47
• 2.2 Experimental Section 51
• 2.2.1 Materials 51
• 2.2.2 Synthesis and Characterization of Biosealant Polymers 51
• 2.2.3 Fabrication of Tissue Adhesive Biosealant 53
• 2.2.4 Rheological Analysis of Biosealant 53
• 2.2.5 Tissue Adhesive Test of Biosealants 54
• 2.2.6 Cytocompatibility of Biosealant 54
• 2.2.7 In Vivo Biodegradability and Tissue Compatibility of Biosealant 55
• 2.2.8 Fabrication of S_3DP 56
• 2.2.9 Characterization of Spheroid Morphology 56
• 2.2.10 Quantitative Reverse Transcription-polymerase Chain Reaction 58
• 2.2.11 Protein Analysis using a Western Blot Analysis 58
• 2.2.12 Angiogenesis Analysis 60
• 2.2.13 Acute Rat MI Models and Transplantation of S_3DP In Vivo 60
• 2.2.14 Echocardiographic Evaluation 62
• 2.2.15 Histological Analysis 62
• 2.2.16 Statistical Analysis 63
• 2.3 Results and Discussion 64
• 2.3.1 Fabrication and Characterization of Tissue Adhesive Biosealant 64
• 2.3.2 Controllable Oxygen Generation of Biosealant 68
• 2.3.3 Biocompatible and Biodegradable Biosealant 70
• 2.3.4 Fabrication of S_3DP with Dual Pockets 72
• 2.3.5 Angiogenic Paracrine Effect of S_3DP 75
• 2.3.6 Therapeutic Effects of S_3DP on Cardiac Infarction 77
• 2.3.7 Reduced Cardiac Fibrosis of S_3DP on Cardiac Infarction 79
• 2.4 Conclusion 82
• Chapter 3. Catalase-immobilized Oxygen-supplying Syringe to Fabricate Hyperoxia-inducible Hydrogels for In Situ Tissue Regeneration
• 3.1 Introduction 83
• 3.2 Experimental Section 87
• 3.2.1 Materials 87
• 3.2.2 Oxyringe Fabrication 87
• 3.2.3 Characterization of PDA-modified Syringe 88
• 3.2.4 Catalase Activity of Oxyringe 88
• 3.2.5 Oxygen-generating Kinetics of Oxyringe 92
• 3.2.6 Synthesis and Characterization of GtnSH and GelMA 92
• 3.2.7 Hydrogel Fabrication and Its Phase Transition 93
• 3.2.8 Oxygen-releasing Kinetics of Hydrogels In Vivo 94
• 3.2.9 Rheological Analysis of Hydrogels 96
• 3.2.10 H2O2 Measurements of Oxyringe and Oxygen-releasing Hydrogel 96
• 3.2.11 Cytocompatibility Test of Hyperoxia-inducible Hydrogels 97
• 3.2.12 In Vivo Hemostatic Ability Test 97
• 3.2.13 Subcutaneous Implantation In Vivo 98
• 3.2.14 In Vivo Wound Remodeling Evaluation 98
• 3.2.15 Histological Analysis 99
• 3.2.16 Statistical Analysis 99
• 3.3 Results and Discussion 100
• 3.3.1 PDA-Conjugated Syringe to Immobilize Catalase in an Oxyringe 100
• 3.3.2 Oxyringe Fabrication and Its Controllable Oxygen Generation 103
• 3.3.3 Fabrication and Characterizations of Oxygen-releasing Hydrogels 106
• 3.3.4 Cytocompatible Oxygen-releasing Matrices by H2O2 Scavenging 110
• 3.3.5 Hyperoxia-inducible Hydrogel as a Hemostatic Physical Barrier 114
• 3.3.6 Boosted Inflammation and Proliferation Phases with Hyperoxia-inducible Hydrogels 116
• 3.3.7 Promoted Wound Remodeling Phase via Hyperoxic Condition 120
• 3.4 Conclusion 122
• Chapter 4. Applicability of Oxygen-supplying Technique for Fabricating Various Oxygen-delivering Platforms
• 4.1 Introduction 123
• 4.2 Experimental Section 125
• 4.2.1 Materials 125
• 4.2.2 Oxygener Fabrication 126
• 4.2.3 Characterization of the PDA-coated Container 126
• 4.2.4 H2O2-scavenging Ability of Oxygener 126
• 4.2.5 Synthesis and Characterization of GtnSH and GtnMI 128
• 4.2.6 Oxygen-generating and -supplying Capacity of Oxygener In Vitro 129
• 4.2.7 Fabrication of Cytocompatible Oxygen-enriched Media 129
• 4.2.8 In Vivo Wound Healing Evaluation and Biocompatibility Test 130
• 4.2.9 Total mRNA Sequencing 131
• 4.2.10 Histological Analysis 131
• 4.2.11 Statistical Analysis 132
• 4.3 Results and Discussion 133
• 4.3.1 Fabrication of Oxygener via Improved PDA Coating Efficiency 133
• 4.3.2 Promoted H2O2 Scavenging and Oxygen Generation of Oxygener 136
• 4.3.3 Cytocompatible Oxygen-enriched Media as Hyperoxic Cell Culture Conditions 139
• 4.3.4 Fabrication of Hyperoxic Oxygen-releasing Hydrogels 141
• 4.3.5 Facilitated Wound Healing via Hyperoxic Oxidative Stress 143
• 4.3.6 Rapid Transition of Inflammation Phase into Proliferation Phase 145
• 4.3.7 Expedited Wound Remodeling Phase 148
• 4.4 Conclusion 151
• Chapter 5. Significance and Future Perspective
• 5.1 Novelty of Our Systems 152
• 5.2 Future Direction 153
• References 155
• 국문초록 190

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