Mechanical Stresses in Embryonic Tissues: Patterns, Morphogenetic Role, and Involvement in Regulatory Feedback

Beloussov, L. V.; Saveliev, S. V.; Naumidi, I.I.; Novoselov, Vladimir V.

doi:10.1016/s0074-7696(08)61535-1

Cited by 58 publications

(31 citation statements)

References 25 publications

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“…However, it seems improbable that HR can, by itself, produce a comprehensive series of morphogenetic events such as those postulated by Beloussov et al (1994) for amphibian gastrulation. Genes likely need to occasionally step in to make mid-course corrections or initiate new deformations based on mechanical feedback.…”

Section: Discussionmentioning

confidence: 99%

“…All models presented in this paper are based on Beloussov's Hyper-restoration Hypothesis (Beloussov, 1998;Beloussov et al, 1994;Beloussov and Grabovsky, 2006). The models are relatively simple and phenomenological in nature, but they are based rigorously on the fundamental principles of nonlinear solid mechanics.…”

Section: Primary Ingredients Of the Hyper-restoration Hypothesismentioning

confidence: 99%

“…Beloussov has postulated that mechanical stress plays a key role in regulating morphogenesis. Based on more than three decades of observations and experiments on embryos, he has proposed the following Hyper-restoration (HR) Hypothesis (Beloussov, 1998;Beloussov et al, 1994;Beloussov and Grabovsky, 2006): Whenever a change is produced in the amount of local stress applied to a cell or local region of tissue, the cells or tissue will respond by actively generating forces directed toward the restoration of the initial stress value, but as a rule overshooting it. Whenever such changes in stress are unevenly distributed or are anisotropic, then the responses induced will be directed toward reducing (with an overshoot) whichever deviations were greatest.…”

Section: Introductionmentioning

confidence: 99%

“…For example, Beloussov and colleagues have used tissue dissection to map regions of tension and compression in embryos (Beloussov et al, 1975;Beloussov et al, 1990;Beloussov et al, 2000;Beloussov, 1998;Beloussov et al, 1994). 2 These researchers also have proposed qualitative models that illustrate how a series of HR responses can, in theory, drive a number of basic morphogenetic processes, including gastrulation, neurulation, and convergent extension (Beloussov, 1998;Beloussov et al, 1994). While these models seem plausible, intuition can be misleading in highly nonlinear systems such as the embryo (as will be demonstrated).…”

Section: Introductionmentioning

confidence: 99%

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Theoretical study of Beloussov’s hyper-restoration hypothesis for mechanical regulation of morphogenesis

Taber

2007

Biomech Model Mechanobiol

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Computational models were used to explore the idea that morphogenesis is regulated, in part, by feedback from mechanical stress according to Beloussov's Hyper-restoration (HR) Hypothesis. According to this hypothesis, active tissue responses to stress perturbations restore, but overshoot, the original (target) stress. To capture this behavior, the rate of growth or contraction is assumed to depend on the difference between the current and target stresses. Stress overshoot is obtained by letting the target stress change at a rate proportional to the same stress difference. The feasibility of the HR Hypothesis is illustrated by models for stretching of epithelia, cylindrical bending of plates, invagination of cylindrical and spherical shells, and early amphibian development. In each case, an initial perturbation leads to an active mechanical response that changes the form of the tissue. The results show that some morphogenetic processes can be entirely self-driven by HR responses once they are initiated (possibly by genetic activity). Other processes, however, may require secondary mechanisms or perturbations to proceed to completion.

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Section: Discussionmentioning

confidence: 99%

Section: Primary Ingredients Of the Hyper-restoration Hypothesismentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Theoretical study of Beloussov’s hyper-restoration hypothesis for mechanical regulation of morphogenesis

Taber

2007

Biomech Model Mechanobiol

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“…Recent studies suggest that mechanosensing is involved in several physiological processes, including embryogenesis (Newman and Comper, 1990;Beloussov et al, 1994) and wound healing (Hinz et al, 2001;Tomasek et al, 2002), and in pathological processes such as fibrosis and carcinogenesis (Paszek et al, 2005). Adherent cells seem capable of both responding to applied mechanical forces (Tzima et al, 2005) and applying contractile forces to probe mechanical properties of the environment (Discher et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

Retrograde Fluxes of Focal Adhesion Proteins in Response to Cell Migration and Mechanical Signals

Guo

Wang

2007

MBoC

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Recent studies suggest that mechanical signals mediated by the extracellular matrix play an essential role in various physiological and pathological processes; yet, how cells respond to mechanical stimuli remains elusive. Using live cell fluorescence imaging, we found that actin filaments, in association with a number of focal adhesion proteins, including zyxin and vasodilator-stimulated phosphoprotein, undergo retrograde fluxes at focal adhesions in the lamella region. This flux is inversely related to cell migration, such that it is amplified in fibroblasts immobilized on micropatterned islands. In addition, the flux is regulated by mechanical signals, including stretching forces applied to flexible substrates and substrate stiffness. Conditions favoring the flux share the common feature of causing large retrograde displacements of the interior actin cytoskeleton relative to the substrate anchorage site, which may function as a switch translating mechanical input into chemical signals, such as tyrosine phosphorylation. In turn, the stimulation of actin flux at focal adhesions may function as part of a feedback mechanism, regulating structural assembly and force production in relation to cell migration and mechanical load. The retrograde transport of associated focal adhesion proteins may play additional roles in delivering signals from focal adhesions to the interior of the cell. INTRODUCTIONRecent studies suggest that mechanosensing is involved in several physiological processes, including embryogenesis (Newman and Comper, 1990;Beloussov et al., 1994) and wound healing (Hinz et al., 2001;Tomasek et al., 2002), and in pathological processes such as fibrosis and carcinogenesis (Paszek et al., 2005). Adherent cells seem capable of both responding to applied mechanical forces (Tzima et al., 2005) and applying contractile forces to probe mechanical properties of the environment (Discher et al., 2005). The downstream responses include changes in migration (Pelham and Wang, 1997;Sheetz et al., 1998;Lo et al., 2000), cell-cell interactions (Guo et al., 2006), proliferation (Wang et al., 2000Nelson et al., 2005), differentiation (Engler et al., 2004(Engler et al., , 2006, and apoptosis . For cultured adherent cells, focal adhesions are thought to mediate mechanosensing through integrin-mediated anchorage to the extracellular matrix (Larsen et al., 2006). The molecular repertoire of focal adhesions includes Ͼ100 adaptor and signaling proteins (Bershadsky et al., 2006), in addition to associated actomyosin bundles that provide mechanical forces for probing the environment (Choquet et al., 1997), inside-out signaling (Chrzanowska-Wodnicka and Burridge, 1996;Schwartz and Ginsberg, 2002), and cell migration (Ridley et al., 2003). However, few details are available concerning how these components work in concert to generate the responses to mechanical signals.Several aspects have emerged recently as the key features of integrin-mediated mechanosensing. First is the increase in cortical organization and contractility in resp...

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The role of actin filaments and microtubules in hepatocyte spheroid self-assembly

Tzanakakis

Hansen

2001

Cell Motil. Cytoskeleton

106

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Mechanical Stresses in Embryonic Tissues: Patterns, Morphogenetic Role, and Involvement in Regulatory Feedback

Cited by 58 publications

References 25 publications

Theoretical study of Beloussov’s hyper-restoration hypothesis for mechanical regulation of morphogenesis

Theoretical study of Beloussov’s hyper-restoration hypothesis for mechanical regulation of morphogenesis

Retrograde Fluxes of Focal Adhesion Proteins in Response to Cell Migration and Mechanical Signals

The role of actin filaments and microtubules in hepatocyte spheroid self-assembly

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