Revisiting tissue tensegrity: Biomaterial-based approaches to measure forces across length scales

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.

Embodied cognitive morphogenesis as a route to intelligent systems

“…Practical examples of bio-developmental-cognitive tensegrity include the structure of fullerene molecules [33], DNA nano-triangles [34] and tensegrity locomotion in robots [35]. Dynamic tension consists of two components: continuous tension and discrete compression [36]. This results in a stable and even robust structure when subjected to extensive forces Clockwise from top left: embodied (nervous system network in anatomical context), enactive (embodied nervous system network interacting with its physical and social environment), extended (cognition stored as symbols in the physical environment), and embedded (intra-agent interactions between nervous system and non-neuronal cellular networks).…”

Functional biomaterials

“…Boghdady and colleagues highlight the role of tensegrity in tissue dynamics across multiple scales of homeostasis, morphogenesis, and pathological dysfunctions. 12 Subsequently, the review by Cui and colleagues summarizes how hydrogel surface patterning-induced topographic features may affect their physicochemical and biological properties, and accordingly, the cellular interactions. 13 Specific applications of mechanotransduction were demonstrated by Marinval and Chew and by Shi and colleagues, respectively, surrounding neuronal tissue 14 and cardiac tissue.…”

Embodied Cognitive Morphogenesis as a Route to Intelligent Systems

“…Practical examples of how tensegrity works include the structure of fullerene molecules [35], DNA nano-triangles [36], and tensegrity locomotion in robots [37]. Dynamic tension consists of two components: continuous tension, and discrete compression [38]. This results in a stable and even robust structure when subjected to extensive forces or dynamic movement.…”

“…According to [38], there are three biological states to which tensegrity contributes. The first is homeostasis, where tensegrity reinforces stable structure.…”

“…Adhesion to a material substrate provides information about forces transduced through cytoplasm via integrins, which keeps the cell structurally stable during changes in shape [53]. This allows for both the local preservation of symmetries and sequential symmetry-breaking events in the developing phenotype [38]. We will return to this aspect of structural phenotypes in our discussion of embodied hypernetworks.…”