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©Copyright 2020 Samuel Berry ©Copyright 2020 Samuel Berry Leveraging Open Microfluidics for Platform Development and Cell-Signaling Studies In Vitro Samuel Berry A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy University of Washington 2020 Reading Committee: Ashleigh Theberge, Chair Paul Yager Jesse Zalatan Program Authorized to Offer Degree: Chemistry 2 University of Washington Abstract Leveraging Open Microfluidics for Platform Development and Cell-Signaling Studies In Vitro Samuel Berry Chair of the Supervisory Committee Ashleigh Theberge, Ph.D. Department of Chemistry This dissertation discusses the fundamentals, development, validation, and application of open microfluidic technologies as a research tool in biological studies. Open microfluidics is a rapidly evolving and expanding field, characterized by the study of fluid behavior in channels with dimensions < 1 mm and containing at least one interface that is open to the air (i.e., not enclosed). While still a relatively new field, advances in the mathematical theory describing the fluidics in open channels, the fabrication process and resolution, and the creation of application-driven platforms are supporting the use of open microfluidics in biological and chemical studies. The work presented in this dissertation can be broadly separated into two sections: the first, exploring the fundamental mechanics underlying fluid flow in open systems, such as U-shaped channels and rails, to build up general functionalities and toolboxes that include droplet manipulation and hydrogel patterning; and the second, demonstrating the creation and validation of analytical systems to study cell-cell signaling in vitro with customizable cell-targeting beads and a microscale mycobacterial infection model. Through the elucidation of the theory governing fluid behavior in our systems, we can describe the limitations of our open microfluidic systems and incorporate customizable functionalities for various experimental needs, ultimately improving the transferability of the systems to collaborators and other 3 researchers (Chapters 2 and 3). We couple this fundamental design approach with applications in cell-cell signaling, a vital biological phenomenon that plays important roles in immune response, homeostasis, organ development and function, and tissue repair. However, the microenvironments where these complex intercellular signaling processes occur are difficult to study and prevent researchers from deciphering the role of important cellular communication, illustrating a need for new technologies and approaches to better model and probe these systems (Chapter 4). To partially address this need, we present the development and validation of two novel approaches to study intercellular signaling that can be easily adapted and customized for use in different settings (Chapter 5 and 6). Ultimately, the techniques and technologies described here represent foundational analytical and modeling approaches and warrant further development to increase their potential impact. 4 TABLE OF CONTENTS List of Figures………………………………………………………………………………………..…….7 Acknowledgements………………………………………………………………………………………...8 Chapter 1. Introduction……………………………………………………………………………............12 1.1 Introduction to Microfluidics and Fundamentals…………………………………………………...12 1.2 Open Microfluidics and Development of the Field…………………………………………............13 1.3 Biological Relevance and Importance of Cell-Cell Signaling………………………………...........14 1.4 Microfluidics as Tools for Studying Cell-Signaling Phenomena…………………………….……..15 1.5 References…………………………………………………………………………………………..17 Chapter 2. Droplet Manipulation and Behavior in Open Microfluidic Channels………………………... 19 2.1 Introduction…………………………………………………………………………………............19 2.2 Capillary-driven flow of droplets in open channels………………………………………………...22 2.3 Droplet incubation and transport.…………………………………………………………………...23 2.4 Controlled and adjustable droplet splitting…………………………………….…………………...29 2.5 Conclusion…………………………………………………………………………….…………….31 2.6 Materials and Methods……………………………………………………………………...……... 32 2.7 References…………………………………………………………………………………………..34 Chapter 3. Open-Microfluidic Patterning of Surfaces for Segregated Coculture of Cells………………..36 3.1 Introduction…………………………………………………………………………………............37 3.2 Spontaneous capillary flow along a rail…………………………………………………………….40 3.3 Design optimization of open microfluidic patterning platform…………………………………….43 3.4 Application of hydrogel patterning for cell culture systems………………………………………..45 3.5 Conclusion…………………………………………………………………………………………..51 3.6 Materials and Methods……………………………………………………………………………...52 3.7 References…………………………………………………………………………………………..57 Chapter 4. Mechanisms and Models of Host-Pathogen Communication in Respiratory Microenvironments………………………………………………………………………………………..60 4.1 Introduction…………………………………………………………………………………………61 4.2 Infections and molecular cross-talk…………………………………………………………………63 4.2.1 Soluble factor paracrine signaling……………………………………………………….65 4.2.2 Physical contact juxtacrine signaling…………………………………………………….72 4.2.3 Volatile signaling………………………………………………………...………………77 4.3 Tissue-level communication in the context of pulmonary infection………………………………..80 4.3.1 Signaling in tissue components…………………………………………………………..81 4.3.2 Tissue disruption by underlying disease………………………………...……………….82 4.4 Modeling pulmonary infections and cellular cross-talk………………………………...…………..84 4.4.1 Conventional macroscale platforms……………………………………………...………86 4.4.2 Microfluidic and microfabricated in vitro models…………………………………...…..89 4.5 Conclusion………………………………………………………………………………...………...93 4.6 References……………………………………………………………………………………..……93 5 Chapter 5. Cell-Targeting Beads to Probe the Cellular Signaling Microenvironment…………..………106 5.1 Introduction…………………………………………………………………………………..……106 5.2 Development and validation of in situ sampling bead system………………………………..…...108 5.3 Application of dual-functionalized beads for resuscitation of sequestered signals…………….…110 5.4 Conclusion…………………………………………………………………………….…….……..113 5.5 Materials and Methods…………………………………………………………………….………113 5.6 References……………………………………………………………………………………..…..119 Chapter 6. An Open-Microfluidic Platform for Immune-Microenvironment Signaling During Infection………………………………………………………………………………………………….121 6.1 Introduction……………………………………………………………………………….……….122 6.2 Design and establishment of microscale granuloma model……………………………………… 124 6.3 Validation of model within an open microfluidic platform………………………………….……127 6.4 Modulation of cellular morphology through coculture signaling…………………………………131 6.5 Conclusion…………………………………………………………………………………………134 6.6 Materials and Methods…………………………………………………………………………….135 6.7 References………………………………………………………………………………...……… 140 Chapter 7. Conclusions and Outlook…………………………………………………………………….143 Appendix………………………………………………………………………………………………....146 A………………………………………………………………………………………………………146 B………………………………………………………………………………...…………………….154 C…………………………………………………………………………………...………………….161 D………………………………………………………………………………………………………164 E………………………………………………………………………………………...…………….170 6 List of Figures Figure 1.1: Schematic representation of the contact angle of a droplet on a surface……………...………13 Figure 2.1: Platform design and operation for aqueous droplet translation in an open capillary channel...23 Figure 2.2: Open channel droplet incubation and transport……………………………………………….25 Figure 2.3: Colorimetric droplet assay within open capillary channels……………………….…………..28 Figure 2.4: Controlled and adjustable droplet splitting in open channels with SCF……………...………30 Figure 2.5: Droplet splitting and merging for downstream reagent delivery……………………………...31 Figure 3.1: Monorail device operation utilizing SCF in a rail system…………………………………….42 Figure 3.2: Characterization of SCF along a rail………………………………………………………….43 Figure 3.3: Integrated design features for improving control of hydrogel flows………………………….45 Figure 3.4: Integrity and permeability of patterned hydrogel walls………………………………………47 Figure 3.5: Compatibility of surface-sensitive cells with rail-based hydrogel patterning…………..…….48 Figure 3.6: Multikingdom coculture in a modular rail-based patterning platform……………………..…50 Figure 4.1: Schematic representation of cell signaling microenvironment in the lung…………………...64 Figure 5.1: Schematic workflow of bead-based sampling method………………………………………108 Figure 5.2: Dual-functionalized beads target and bind to CD90+ cells……………………………….….110 Figure 5.3: In situ sampling resuscitates soluble signals in the presence of neutralizing factors……..…112 Figure 6.1: Schematic workflow and illustration of modular mycobacterial infection model……..……127 Figure 6.2: Colocalization of immune cells and mycobacterium in 3D suspended culture wells…...…..128 Figure 6.3: Proinflammatory cytokine secretion profile of microscale infection model……………..….130 Figure 6.4: Coculture of infection model and vasculature model modulates endothelial morphology….133 Additional figures in Appendices A-E. 7 Acknowledgements Nothing exists or occurs in isolation, and completing a PhD is no exception, making this section the most difficult part to write for this thesis. There are many people who have been involved in accomplishing this, and I just want to broadly say thank you to everyone who was been here along the way. First, thank you to all my colleagues and lab mates in the Theberge Lab. Tianzi and Dostie for all the support, baked goods, guidance, and encouragement from the day I joined the
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