Structural maturation of myofilaments in engineered 3D cardiac microtissues characterized using small angle x-ray scattering

van Dover, Geoffrey; Javor, Josh; Ewoldt, Jourdan K.; Zhernenkov, Mikhail; Wąsik, Patryk; Freychet, Guillaume; Lee, Josh; Brown, Dana; Chen, Christopher S.; Bishop, David J.

doi:10.1088/1478-3975/ad310e

Title: Structural maturation of myofilaments in engineered 3D cardiac microtissues characterized using small angle x-ray scattering

Journal Article · 19 March 2024 · Physical Biology

DOI: https://doi.org/10.1088/1478-3975/ad310e · OSTI ID:2325503

;

; Bishop, David J.

Abstract Understanding the structural and functional development of human-induced pluripotent stem-cell-derived cardiomyocytes (hiPSC-CMs) is essential to engineering cardiac tissue that enables pharmaceutical testing, modeling diseases, and designing therapies. Here we use a method not commonly applied to biological materials, small angle x-ray scattering, to characterize the structural development of hiPSC-CMs within three-dimensional engineered tissues during their preliminary stages of maturation. An x-ray scattering experimental method enables the reliable characterization of the cardiomyocyte myofilament spacing with maturation time. The myofilament lattice spacing monotonically decreases as the tissue matures from its initial post-seeding state over the span of 10 days. Visualization of the spacing at a grid of positions in the tissue provides an approach to characterizing the maturation and organization of cardiomyocyte myofilaments and has the potential to help elucidate mechanisms of pathophysiology, and disease progression, thereby stimulating new biological hypotheses in stem cell engineering.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0012704

OSTI ID:: 2325503

Alternate ID(s):: OSTI ID: 2320318; OSTI ID: 2336579

Journal Information:: Physical Biology, Journal Name: Physical Biology Journal Issue: 3 Vol. 21; ISSN 1478-3967

Publisher:: IOP PublishingCopyright Statement

Country of Publication:: Country unknown/Code not available

Language:: English

References (31)

Transmission Electron Microscopy of Biological Samples Mielańczyk, Łukasz; Matysiak, Natalia; Klymenko, Olesya The Transmission Electron Microscope - Theory and Applications https://doi.org/10.5772/60680	book	September 2015
Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/β-catenin signaling under fully defined conditions Lian, Xiaojun; Zhang, Jianhua; Azarin, Samira M. Nature Protocols, Vol. 8, Issue 1 https://doi.org/10.1038/nprot.2012.150	journal	December 2012
Mechanical stress-induced sarcomere assembly for cardiac muscle growth in length and width Russell, Brenda; Curtis, Matthew W.; Koshman, Yevgeniya E. Journal of Molecular and Cellular Cardiology, Vol. 48, Issue 5 https://doi.org/10.1016/j.yjmcc.2010.02.016	journal	May 2010
In Vivo Conditioning of Tissue‐engineered Heart Muscle Improves Contractile Performance Birla, Ravi K.; Borschel, Gregory H.; Dennis, Robert G. Artificial Organs, Vol. 29, Issue 11 https://doi.org/10.1111/j.1525-1594.2005.00148.x	journal	October 2005
Atomic model of a myosin filament in the relaxed state Woodhead, John L.; Zhao, Fa-Qing; Craig, Roger Nature, Vol. 436, Issue 7054 https://doi.org/10.1038/nature03920	journal	August 2005
Mechanical Stress Conditioning and Electrical Stimulation Promote Contractility and Force Maturation of Induced Pluripotent Stem Cell-Derived Human Cardiac Tissue Ruan, Jia-Ling; Tulloch, Nathaniel L.; Razumova, Maria V. Circulation, Vol. 134, Issue 20 https://doi.org/10.1161/CIRCULATIONAHA.114.014998	journal	November 2016
Synchrotron-based small-angle X-ray scattering of proteins in solution Skou, Soren; Gillilan, Richard E.; Ando, Nozomi Nature Protocols, Vol. 9, Issue 7 https://doi.org/10.1038/nprot.2014.116	journal	June 2014
Microengineered platforms for characterizing the contractile function of in vitro cardiac models Dou, Wenkun; Malhi, Manpreet; Zhao, Qili Microsystems & Nanoengineering, Vol. 8, Issue 1 https://doi.org/10.1038/s41378-021-00344-0	journal	February 2022
2D and 3D-Organized Cardiac Cells Shows Differences in Cellular Morphology, Adhesion Junctions, Presence of Myofibrils and Protein Expression Soares, Carolina Pontes; Midlej, Victor; Oliveira, Maria Eduarda Weschollek de PLoS ONE, Vol. 7, Issue 5 https://doi.org/10.1371/journal.pone.0038147	journal	May 2012
Imaging of cardiovascular structures using near-infrared femtosecond multiphoton laser scanning microscopy Schenke-Layland, Katja; Riemann, Iris; Stock, Ulrich A. Journal of Biomedical Optics, Vol. 10, Issue 2 https://doi.org/10.1117/1.1896966	journal	January 2005
Cardiac tissue engineering: state-of-the-art methods and outlook Nguyen, Anh H.; Marsh, Paul; Schmiess-Heine, Lauren Journal of Biological Engineering, Vol. 13, Issue 1 https://doi.org/10.1186/s13036-019-0185-0	journal	June 2019
X-Ray Structural Analysis of Single Adult Cardiomyocytes: Tomographic Imaging and Microdiffraction Reichardt, Marius; Neuhaus, Charlotte; Nicolas, Jan-David Biophysical Journal, Vol. 119, Issue 7 https://doi.org/10.1016/j.bpj.2020.08.019	journal	October 2020
Rapid nanomolding of nanotopography on flexible substrates to control muscle cell growth with enhanced maturation Wu, Cong; Chin, Chriss S. M.; Huang, Qingyun Microsystems & Nanoengineering, Vol. 7, Issue 1 https://doi.org/10.1038/s41378-021-00316-4	journal	November 2021
Myocardial Structure and Function Differ in Systolic and Diastolic Heart Failure van Heerebeek, Loek; Borbély, Attila; Niessen, Hans W. M. Circulation, Vol. 113, Issue 16 https://doi.org/10.1161/CIRCULATIONAHA.105.587519	journal	April 2006
Myosin filament-based regulation of the dynamics of contraction in heart muscle Brunello, Elisabetta; Fusi, Luca; Ghisleni, Andrea Proceedings of the National Academy of Sciences, Vol. 117, Issue 14 https://doi.org/10.1073/pnas.1920632117	journal	March 2020
Effects of Geometry on the Mechanics and Alignment of Three-Dimensional Engineered Microtissues Bose, Prasenjit; Eyckmans, Jeroen; Nguyen, Thao D. ACS Biomaterials Science & Engineering, Vol. 5, Issue 8 https://doi.org/10.1021/acsbiomaterials.8b01183	journal	December 2018
Correlating Cardiac Structure to Function Using Nanoscale Resolution Scanning Ion Conductance Microscopy Bhargava, Anamika; Gorelik, Julia Scanning Ion Conductance Microscopy https://doi.org/10.1007/11663_2021_10	book	February 2022
Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010 Lozano, Rafael; Naghavi, Mohsen; Foreman, Kyle The Lancet, Vol. 380, Issue 9859 https://doi.org/10.1016/S0140-6736(12)61728-0	journal	December 2012
High-Resolution Cryo-EM Structure of the Cardiac Actomyosin Complex Risi, Cristina; Schäfer, Luisa U.; Belknap, Betty Structure, Vol. 29, Issue 1 https://doi.org/10.1016/j.str.2020.09.013	journal	January 2021
A Microtissue Platform to Simultaneously Actuate and Detect Mechanical Forces via Non-Contact Magnetic Approach Javor, Josh; Sundaram, Subramanian; Chen, Christopher S. Journal of Microelectromechanical Systems, Vol. 30, Issue 1 https://doi.org/10.1109/JMEMS.2020.3036978	journal	February 2021
Myosin Sequestration Regulates Sarcomere Function, Cardiomyocyte Energetics, and Metabolism, Informing the Pathogenesis of Hypertrophic Cardiomyopathy Toepfer, Christopher N.; Garfinkel, Amanda C.; Venturini, Gabriela Circulation, Vol. 141, Issue 10 https://doi.org/10.1161/CIRCULATIONAHA.119.042339	journal	March 2020
Electrical stimulation directs engineered cardiac tissue to an age-matched native phenotype Lasher, Richard A.; Pahnke, Aric Q.; Johnson, Jeffrey M. Journal of Tissue Engineering, Vol. 3, Issue 1 https://doi.org/10.1177/2041731412455354	journal	January 2012
Single-Cell Determination of Cardiac Microtissue Structure and Function Using Light Sheet Microscopy Turaga, Diwakar; Matthys, Oriane B.; Hookway, Tracy A. Tissue Engineering Part C: Methods, Vol. 26, Issue 4 https://doi.org/10.1089/ten.tec.2020.0020	journal	April 2020
Probing the subcellular nanostructure of engineered human cardiomyocytes in 3D tissue Javor, Josh; Ewoldt, Jourdan K.; Cloonan, Paige E. Microsystems & Nanoengineering, Vol. 7, Issue 1 https://doi.org/10.1038/s41378-020-00234-x	journal	January 2021
X-ray diffraction imaging of cardiac cells and tissue Nicolas, Jan-David; Bernhardt, Marten; Schlick, Susanne F. Progress in Biophysics and Molecular Biology, Vol. 144 https://doi.org/10.1016/j.pbiomolbio.2018.05.012	journal	July 2019
Force-driven evolution of mesoscale structure in engineered 3D microtissues and the modulation of tissue stiffening Zhao, Ruogang; Chen, Christopher S.; Reich, Daniel H. Biomaterials, Vol. 35, Issue 19 https://doi.org/10.1016/j.biomaterials.2014.02.020	journal	June 2014
Calcium and voltage mapping in hiPSC-CM monolayers Herron, Todd J. Cell Calcium, Vol. 59, Issue 2-3 https://doi.org/10.1016/j.ceca.2016.02.004	journal	March 2016
Human perinatal stem cell derived extracellular matrix enables rapid maturation of hiPSC-CM structural and functional phenotypes Block, Travis; Creech, Jeffery; da Rocha, Andre Monteiro Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-76052-y	journal	November 2020
3D culture models of tissues under tension Eyckmans, Jeroen; Chen, Christopher S. Journal of Cell Science, Vol. 130, Issue 1 https://doi.org/10.1242/jcs.198630	journal	December 2016
The fast azimuthal integration Python library: pyFAI Ashiotis, Giannis; Deschildre, Aurore; Nawaz, Zubair Journal of Applied Crystallography, Vol. 48, Issue 2 https://doi.org/10.1107/S1600576715004306	journal	March 2015
Investigation of human iPSC-derived cardiac myocyte functional maturation by single cell traction force microscopy Wheelwright, Matthew; Win, Zaw; Mikkila, Jennifer L. PLOS ONE, Vol. 13, Issue 4 https://doi.org/10.1371/journal.pone.0194909	journal	April 2018

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