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Acoustic Manipulation for Cell and Spheroid Cellomics Spheroid and Cell for Manipulation Acoustic Acoustic manipulation for cell and spheroid cellomics Doctoral Thesis in Physics Acoustic manipulation for cell and spheroid cellomics KARL OLOFSSON ISBN TRITASCIFOU : KTH www.kth.se Stockholm, Sweden Acoustic manipulation for cell and spheroid cellomics KARL OLOFSSON Academic Dissertation which, with due permission of the KTH Royal Institute of Technology, is submitted for public defence for the Degree of Doctor of Philosophy on Friday the 11th of June 2021, 10:00 in Air/Fire, Science for Life Laboratory, Tomtebodavägen 23A, Solna Doctoral Thesis in Physics KTH Royal Institute of Technology Stockholm, Sweden 2021 © Karl Olofsson ISBN 978-91-7873-919-6 TRITA-SCI-FOU 2021:24 Printed by: Universitetsservice US-AB, Sweden 2021 Abstract Ultrasonic standing wave (USW) particle manipulation has during the last two decades matured into a valuable tool to combine with microfluidics. Acoustophoresis, migration through sound, is the result of the acoustic radiation force acting on particles suspended in an acoustic field. The acoustic radiation force magnitude is proportional to the acoustic energy density, frequency and particle size. The acoustic radiation force has successfully been implemented in particle washing, size-based separation, mechanical phenotype-based cell separation and trapping applications. The force magnitude and direction also depend on the difference between the mechanical properties of the fluid and particle. In the first part of this thesis, we show that the mechanical properties of dead cells are a function of the surrounding fluid which was used to acoustically separate dead and viable cells in a density modulated medium. The non-invasive and biocompatible acoustic radiation force has also been used in trapping applications tailored towards tissue modelling and engineering. One of the explored models is the multicellular tumor spheroid (MTCS) which is a spherical aggregate of tumor cells. The MCTS models a solid tumor and is increasingly used to replace regular 2D cell culture techniques in cancer research and drug screening pipelines. The majority of this thesis will be dedicated to the formation and culture of scaffold-free MCTSs using the acoustic radiation force in silicon and glass microwells. We have developed two multiwell microplate designs where either a 100 MCTSs in a single compartment or 576 MCTSs divided into 16 compartments can be formed in parallel using USWs. By using a sequential cell seeding method it is possible to control the MCTS structural architecture and create core-shell MCTSs. The glass bottom in the microwells in combination with efficient clearing protocols also enabled whole MCTS imaging which was utilized to characterize the cell cycle and the volumetric parameters of the nuclei within the MCTSs using image analysis. Finally, we used the 16 chamber multiwell microplate to investigate the drug response in MCTSs from 4 different cell lines simultaneously and evaluate the NK cell cytotoxic response towards MCTSs in presence of different treatments. Sammanfattning Ultraljudsbaserad partikelmanipulation har under de senaste två decennierna utvecklats till ett värdefullt verktyg inom mikrofluidik. Akustofores, migration genom ljud, är resultatet av den akustiska strålningskraften som verkar på partiklar suspenderade i ett akustiskt fält. Den akustiska strålningskraftens storlek är proportionell mot den akustiska energitätheten, frekvensen samt partikelstorleken och har framgångsrikt implementerats i partikeltvätt, storleksbaserad separation, mekanisk fenotypbaserad cellseparation och aggregeringsapplikationer. Kraftens magnitud samt riktning beror även på skillnaden mellan vätskans och partikelns mekaniska egenskaper. I den första delen av denna avhandling visar vi att de mekaniska egenskaperna hos döda celler är en funktion av den omgivande vätskan. Konceptet användes för att akustiskt separera döda och levande celler i ett densitetsmodulerat medium. Den icke-invasiva och biokompatibla akustiska strålningskraften har också använts i aggregeringstillämpningar skräddarsydda för vävnadsmodellering. En av de utforskade modellerna är den multicellulära tumörsfäroiden (MCTS) som är ett sfäriskt aggregat av tumörceller. MCTSen modellerar en solid tumör och används i allt högre grad för att ersätta vanliga 2D-cellodlingstekniker i cancerforskning och läkemedelsscreening. Huvuddelen av denna avhandling kommer att ägnas åt bildandet och odlingen av MCTS:er användandes den akustiska strålningskraften i kisel- och glasmikrobrunnar. Vi har utvecklat två mikrobrunnsbaserade mikrochip där antingen 100 MCTS:er i ett enda fack eller 576 MCTS uppdelat i 16 fack kan bildas parallellt med ultraljud. Genom att använda en sekventiell cellsåddningsmetod är det möjligt att kontrollera MCTS-arkitekturen och skapa kärn-skal MCTS:er. Mikrobrunnarnas glasbotten i kombination med effektiva transparensinducerande protokoll möjliggjorde även MCTS-avbildning som användes för att karakterisera cellcykeln och de volymetriska parametrarna för cellkärnor i MCTS:er med hjälp av bildanalys. Slutligen använde vi mikrochippet med 16 kamrar för att undersöka läkemedelsresponsen i MCTS:er från fyra olika cellinjer samt utvärdera NK-cellens cytotoxiska respons mot MCTS:er i närvaro av olika läkemedel. List of papers Paper A K. Olofsson, B. Hammarström and M. Wiklund. “Acoustic separation of living and dead cells using high density medium”, Lab Chip, 20(11), 1981-1990 (2020) Paper B B. Hammarström, N.R. Skov, K. Olofsson, H. Bruus and M. Wiklund. “Acoustic trapping based on surface displacement of resonance modes”, JASA, 149(3), 1445- 1453 (2021) Paper C K. Olofsson, V. Carannante, M. Ohlin, T. Frisk, K. Kushiro, M. Takai, A. Lundquist, B. Önfelt and M. Wiklund. “Acoustic formation of multicellular tumor spheroids enabling on-chip functional and structural imaging”, Lab Chip, 18(12), 2644-2476 (2018) Paper D K. Olofsson, V. Carannante, M. Takai, B. Önfelt and M. Wiklund. “Ultrasound- based scaffold-free core-shell multicellular tumor spheroid formation”, Micromachines, 12(3), 329 (2021) Paper E K. Olofsson, V. Carannante, M. Takai, B. Önfelt and M. Wiklund. “Single cell resolution organization and cell cycle characterization from high-content image analysis of DNA stained multicellular tumor spheroids”, Submitted to Scientific Reports Paper F K. Olofsson, V. Carannante, C. Zambarda, M. Takai, B. Önfelt and M. Wiklund. “Multicellular tumor diskoids: A solid tumor model optimized for imaging”, Manuscript Paper G N. Sandström, V. Carannante, K. Olofsson, P. Sandoz, E. Moussad-Lamodière, B. Seashore-Ludlow, T. Frisk, M. Wiklund, P. Östling and B. Önfelt. “Miniaturized platform for high-content and high-resolution assays of drug toxicology and immune cell cytotoxicity”, Manuscript Ongoing projects The following two projects are ongoing and some preliminary results are presented in this thesis Project A V. Carannante, K. Olofsson, S. Edwards, G. Truyasingura, D. Jans, H. van Ooijen, H. Brismar, A. Lundqvist, M. Wiklund and B. Önfelt. “Characterization of Poliovirus Receptor in 3D cultures of renal carcinoma cells and its role in shaping Natural Killer cell activity in the tumor microenvironment” Project B V. Carannante, S.Y. Neo, K. Olofsson, N. Sandström, M. Wiklund, F. Haglund, A. Lundqvist and B. Önfelt. “Characterization of Natural Killer cell response in sarcoma patients: analysis of tumor infiltrated lymphocyte composition and Natural killer cell in vitro response against sarcoma spheroids” List of additional relevant publications Paper I K. Guldevall, L. Brandt, E. Forslund, K. Olofsson, T. Frisk, P.E. Olofsson, K. Gustafsson, O. Manneberg, B. Vanherberghen. H. Brismar, K. Kärre, M. Uhlin and B. Önfelt. “Microchip screening platform for single cell assessment of NK cell cytotoxicity”, Frontiers in Immunology, 7, 119 (2016) Paper II K. Olofsson, B. Hammarström and M. Wiklund. “Ultrasonic based tissue modelling and engineering”, Micromachines, 9(11), 594 (2018) Paper III M. Ghorbani, K. Olofsson, J-W. Benjamins, K. Loskutova. T. Paulraj. M. Wiklund, D. Grishenkov and A. Svagan. “Unravelling the acoustic and thermal response of perfluorocarbon liquid droplets stabilized with cellulose nanofibers”, Langmuir, 35(40), 13090-13099 (2019) List of abbreviations AUC Area under the curve ECM Extracellular matrix FEM Finite element model MCTD Multicellular tumor spheroid MCTS Multicellular tumor diskoid µPIV Micro-particle image velocimetry NK Natural killer PARF Primary acoustic radiation force PBS Phosphate buffered saline PID Proportional-integrate-derivate PZT Lead zirconate titanate RIMS Refractive index matching solution SARF Secondary acoustic radiation force TME Tumor micro environment USW Ultrasonic standing wave Contents 1 INTRODUCTION....................................................................................... 1 2 ACOUSTOPHORESIS THEORY AND APPLICATION ............................ 3 2.1 ULTRASONIC STANDING WAVES .............................................................. 3 2.1.1 1D ultrasonic standing waves .................................................................. 4 2.1.2 2D ultrasonic standing waves .................................................................. 6 2.2 THE PRIMARY ACOUSTIC RADIATION FORCE ............................................. 7 2.2.1 General formulation ................................................................................ 7 2.2.2 The acoustic radiation force in 1D ........................................................... 8 2.2.3 The acoustic radiation
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