Abstract
Cell-generated forces play a foundational role in tissue dynamics and homeostasis and are critically important in several biological processes, including cell migration, wound healing, morphogenesis, and cancer metastasis. Quantifying such forces in vivo is technically challenging and requires novel strategies that capture mechanical information across molecular, cellular, and tissue length scales, while allowing these studies to be performed in physiologically realistic biological models. Advanced biomaterials can be designed to non-destructively measure these stresses in vitro, and here, we review mechanical characterizations and force-sensing biomaterial-based technologies to provide insight into the mechanical nature of tissue processes. We specifically and uniquely focus on the use of these techniques to identify characteristics of cell and tissue “tensegrity:” the hierarchical and modular interplay between tension and compression that provide biological tissues with remarkable mechanical properties and behaviors. Based on these observed patterns, we highlight and discuss the emerging role of tensegrity at multiple length scales in tissue dynamics from homeostasis, to morphogenesis, to pathological dysfunction.
Highlights
The human body is a dynamic and self-stabilizing structure formed through intricate connections between hierarchical building blocks
Cell-generated forces play a foundational role in tissue dynamics and homeostasis and are critically important in several biological processes, including cell migration, wound healing, morphogenesis, and cancer metastasis
Cell-generated forces play critical roles in virtually all biological processes, including cell migration,[5] tissue morphogenesis,[6,7,8,9,10] muscle contraction,[11,12] wound healing,[13] and cancer invasion[14,15] among others. Dysregulation of these forces often correlates with disease onset and progression,[16] and these findings have prompted the development of novel force quantification techniques to better understand the mechanics of morphogenesis and pathogenesis
Summary
The human body is a dynamic and self-stabilizing structure formed through intricate connections between hierarchical building blocks. Scitation.org/journal/apb cell spreading.[30] While microtubules have been found to bear some compressive loads, this is minor compared to extracellular traction forces,[31] and other structures such as the nucleus may play a larger role in resisting tension.[32,33,34,35] Interestingly, the nucleus itself exhibits tensegral features, as it is stabilized by its internal components, nuclear pressure, and the nuclear envelope, further demonstrating the modular and hierarchical arrangement of tensegrity components in a cell.[36] Cellular tensegrity, acts as a stabilizing feature that permits actuation and deformation, giving rise to cellular architecture, stability, and dynamics.[36,37,38] Higher levels of biological organization show tensegral patterns of stabilization in tissues, organs, and the whole body,[39,40] and experimental observations have been interpreted within the framework of tensegrity to illustrate mechanotransductive and morphogenetic processes at the cellular level.[41] quantifying such mechanical forces contributing to tissue structure and dynamics has proven to be a considerable technical challenge due to the spatial scale, time-dependency, and range of forces present in biological systems. We highlight how a tensegral balance between forces plays an important role in stabilizing local architecture and generating morphological and biological responses to microenvironmental stimuli, and theorize that large imbalances in cell-generated forces may lead to disease
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