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Heart-Specific Stiffening in Early Embryos Parallels Matrix and Myosin Expression to Optimize Beating
Open accessAbstract
In development and differentiation, morphological changes often accompany mechanical changes [1], but it is unclear whether or when cells in embryos sense tissue elasticity. The earliest embryo is uniformly pliable, while adult tissues vary widely in mechanics from soft brain and stiff heart to rigid bone [2]. However, cell sensitivity to microenvironment elasticity is debated based in part on results from complex three-dimensional culture models [3]. Regenerative cardiology provides strong motivation to clarify any cell-level sensitivities to tissue elasticity because rigid postinfarct regions limit pumping by the adult heart [4]. Here, we focus on the spontaneously beating embryonic heart and sparsely cultured cardiomyocytes, including cells derived from pluripotent stem cells. Tissue elasticity, Et, increases daily for heart to 1-2 kPa by embryonic day 4 (E4), and although this is ~10-fold softer than adult heart, the beating contractions of E4 cardiomyocytes prove optimal at ~Et,E4 both in vivo and in vitro. Proteomics reveals daily increases in a small subset of proteins, namely collagen plus cardiac-specific excitation-contraction proteins. Rapid softening of the heart's matrix with collagenase or stiffening it with enzymatic crosslinking suppresses beating. Sparsely cultured E4 cardiomyocytes on collagen-coated gels likewise show maximal contraction on matrices with native E4 stiffness, highlighting cell-intrinsic mechanosensitivity. While an optimal elasticity for striation proves consistent with the mathematics of force-driven sarcomere registration, contraction wave speed is linear in Et as theorized for excitation-contraction coupled to matrix elasticity. Pluripotent stem cell-derived cardiomyocytes also prove to be mechanosensitive to matrix and thus generalize the main observation that myosin II organization and contractile function are optimally matched to the load contributed by matrix elasticity.
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“suggesting the elastic nature of the gels with a stiffness similar to that of the late embryonic heart31.”
From In situ expansion, differentiation, and electromechanical coupling of human cardiac muscle in a 3D bioprinted, chambered organoid (2020) · cites this paper as [31]
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Metadata
- Authors
- Majkut, S., Idema, T., Swift, J., Krieger, C., Liu, A., & Discher, D. E.
- Affiliations
- University of Pennsylvania (US)
- Corresponding author
- Discher, Dennis E.
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2013-12
- Volume
- 23
- Issue
- 23
- Pages
- 2434-2439
- ISSN
- 0960-9822 (ISSN-L)
- PMC
- PMC4116639
- OpenAlex
- W2037426481
- Cited by
- 198
- References
- 37
- Citations by year
- 2026: 10 · 2025: 12 · 2024: 9 · 2023: 17 · 2022: 13 · 2021: 16 · 2020: 20 · 2019: 21 · 2018: 17 · 2017: 15 · 2016: 19 · 2015: 14 · 2014: 13 · 2013: 2
- FWCI
- 9.28
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Science Foundation
- National Institutes of Health (UL1TR000003)
- National Heart, Lung, and Blood Institute (R01HL062352)
- National Institute of Allergy and Infectious Diseases (R21AI087516)
- National Institute of Diabetes and Digestive and Kidney Diseases (P01DK032094)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R21AR056128)
- National Institute of Biomedical Imaging and Bioengineering (R21EB003164, R01EB007049, R21EB004489, R21EB004000)
- National Center for Research Resources (S10RR022575)
- National Center for Advancing Translational Sciences
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Keywords
- embryonic heart development, tissue stiffness, mechanosensitivity, cardiomyocyte beating, extracellular matrix, collagen, myosin II, sarcomere organization, excitation-contraction coupling, pluripotent stem cell-derived cardiomyocytes, cardiomyocyte differentiation
- MeSH terms
- Cell Differentiation, Cells, Cultured, Collagen, Elasticity, Heart, Heart Rate, Heterocyclic Compounds, 4 or More Rings, Humans, Myocardial Contraction, Myofibrils, Myosins, Sarcomeres, Extracellular Matrix Proteins, Collagenases, Cardiac Myosins, Myocytes, Cardiac, Embryonic Stem Cells, Induced Pluripotent Stem Cells
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