Cell condensation initiates organogenesis: the role of actin dynamics in supracellular self-organizing process
Abstract The emergence of complex tissue architectures from homogeneous stem cell condensates persists as a central enigma in developmental biology. While biochemical signaling gradients have long dominated explanations of organ patterning, the mechanistic interplay between tissue-scale forces and t...
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BMC
2025-07-01
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| Series: | Cell & Bioscience |
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| Online Access: | https://doi.org/10.1186/s13578-025-01429-3 |
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| author | Jun-Xi He Bing-Dong Sui Yan Jin Chen-Xi Zheng Fang Jin |
| author_facet | Jun-Xi He Bing-Dong Sui Yan Jin Chen-Xi Zheng Fang Jin |
| author_sort | Jun-Xi He |
| collection | DOAJ |
| description | Abstract The emergence of complex tissue architectures from homogeneous stem cell condensates persists as a central enigma in developmental biology. While biochemical signaling gradients have long dominated explanations of organ patterning, the mechanistic interplay between tissue-scale forces and thermodynamic constraints in driving symmetry breaking remains unresolved. This review unveils supracellular actin networks as mechanochemical integrators that establish developmental tensegrity structures, wherein Brownian ratchet-driven polymerization generates patterned stress fields to guide condensate stratification. Central to this paradigm is the dynamic remodeling of actin branches, which transduce mechanical loads into adaptive network architectures through force-modulated capping kinetics and angular reorientation. Such plasticity enables fluid-to-solid phase transitions, stabilizing organ primordia through viscoelastic microdomain formation. Crucially, these biophysical processes are functionally coupled with metabolic reprogramming events, where cytoskeletal strain modulates glycolytic flux and nuclear mechanotransduction pathways to inform differentiation decisions, forging a feedback loop between tissue mechanics and cellular fate specification. Building on these insights, we argue that limitations in current organoid self-organization may originate from incomplete reconstitution of actin-mediated mechanical coherence, and modeling of heterogeneous mesenchymal condensation dynamics offers a strategic framework to decode self-organization trajectories, bridging developmental principles with regenerative design. By synthesizing advances from molecular biophysics to tissue mechanics, this work reframes organogenesis not as a hierarchy of molecular commands, but as an emergent continuum where biochemical, mechanical, and thermodynamic constraints coevolve to sculpt living architectures. |
| format | Article |
| id | doaj-art-c2ce3ed1f90a4c21b6ce5dbd7633a879 |
| institution | Kabale University |
| issn | 2045-3701 |
| language | English |
| publishDate | 2025-07-01 |
| publisher | BMC |
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| series | Cell & Bioscience |
| spelling | doaj-art-c2ce3ed1f90a4c21b6ce5dbd7633a8792025-08-20T03:46:21ZengBMCCell & Bioscience2045-37012025-07-0115111110.1186/s13578-025-01429-3Cell condensation initiates organogenesis: the role of actin dynamics in supracellular self-organizing processJun-Xi He0Bing-Dong Sui1Yan Jin2Chen-Xi Zheng3Fang Jin4State Key Laboratory of Oral & Maxillofacial Reconstruction and Regeneration, National Clinical Research Center for Oral Diseases, Shaanxi International Joint Research Center for Oral Diseases, Center for Tissue Engineering, School of Stomatology, The Fourth Military Medical UniversityState Key Laboratory of Oral & Maxillofacial Reconstruction and Regeneration, National Clinical Research Center for Oral Diseases, Shaanxi International Joint Research Center for Oral Diseases, Center for Tissue Engineering, School of Stomatology, The Fourth Military Medical UniversityState Key Laboratory of Oral & Maxillofacial Reconstruction and Regeneration, National Clinical Research Center for Oral Diseases, Shaanxi International Joint Research Center for Oral Diseases, Center for Tissue Engineering, School of Stomatology, The Fourth Military Medical UniversityState Key Laboratory of Oral & Maxillofacial Reconstruction and Regeneration, National Clinical Research Center for Oral Diseases, Shaanxi International Joint Research Center for Oral Diseases, Center for Tissue Engineering, School of Stomatology, The Fourth Military Medical UniversityDepartment of Orthodontics, School of Stomatology, The Fourth Military Medical UniversityAbstract The emergence of complex tissue architectures from homogeneous stem cell condensates persists as a central enigma in developmental biology. While biochemical signaling gradients have long dominated explanations of organ patterning, the mechanistic interplay between tissue-scale forces and thermodynamic constraints in driving symmetry breaking remains unresolved. This review unveils supracellular actin networks as mechanochemical integrators that establish developmental tensegrity structures, wherein Brownian ratchet-driven polymerization generates patterned stress fields to guide condensate stratification. Central to this paradigm is the dynamic remodeling of actin branches, which transduce mechanical loads into adaptive network architectures through force-modulated capping kinetics and angular reorientation. Such plasticity enables fluid-to-solid phase transitions, stabilizing organ primordia through viscoelastic microdomain formation. Crucially, these biophysical processes are functionally coupled with metabolic reprogramming events, where cytoskeletal strain modulates glycolytic flux and nuclear mechanotransduction pathways to inform differentiation decisions, forging a feedback loop between tissue mechanics and cellular fate specification. Building on these insights, we argue that limitations in current organoid self-organization may originate from incomplete reconstitution of actin-mediated mechanical coherence, and modeling of heterogeneous mesenchymal condensation dynamics offers a strategic framework to decode self-organization trajectories, bridging developmental principles with regenerative design. By synthesizing advances from molecular biophysics to tissue mechanics, this work reframes organogenesis not as a hierarchy of molecular commands, but as an emergent continuum where biochemical, mechanical, and thermodynamic constraints coevolve to sculpt living architectures.https://doi.org/10.1186/s13578-025-01429-3Stem cellsOrganogenesisActin cytoskeletonMechanotransductionSelf-organizationRegeneration |
| spellingShingle | Jun-Xi He Bing-Dong Sui Yan Jin Chen-Xi Zheng Fang Jin Cell condensation initiates organogenesis: the role of actin dynamics in supracellular self-organizing process Cell & Bioscience Stem cells Organogenesis Actin cytoskeleton Mechanotransduction Self-organization Regeneration |
| title | Cell condensation initiates organogenesis: the role of actin dynamics in supracellular self-organizing process |
| title_full | Cell condensation initiates organogenesis: the role of actin dynamics in supracellular self-organizing process |
| title_fullStr | Cell condensation initiates organogenesis: the role of actin dynamics in supracellular self-organizing process |
| title_full_unstemmed | Cell condensation initiates organogenesis: the role of actin dynamics in supracellular self-organizing process |
| title_short | Cell condensation initiates organogenesis: the role of actin dynamics in supracellular self-organizing process |
| title_sort | cell condensation initiates organogenesis the role of actin dynamics in supracellular self organizing process |
| topic | Stem cells Organogenesis Actin cytoskeleton Mechanotransduction Self-organization Regeneration |
| url | https://doi.org/10.1186/s13578-025-01429-3 |
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