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Spatial mapping of tissue properties in vivo reveals a 3D stiffness gradient in the mouse limb bud.

ABSTRACT: Numerous hypotheses invoke tissue stiffness as a key parameter that regulates morphogenesis and disease progression. However, current methods are insufficient to test hypotheses that concern physical properties deep in living tissues. Here we introduce, validate, and apply a magnetic device that generates a uniform magnetic field gradient within a space that is sufficient to accommodate an organ-stage mouse embryo under live conditions. The method allows rapid, nontoxic measurement of the three-dimensional (3D) spatial distribution of viscoelastic properties within mesenchyme and epithelia. Using the device, we identify an anteriorly biased mesodermal stiffness gradient along which cells move to shape the early limb bud. The stiffness gradient corresponds to a Wnt5a-dependent domain of fibronectin expression, raising the possibility that durotaxis underlies cell movements. Three-dimensional stiffness mapping enables the generation of hypotheses and potentially the rigorous testing of mechanisms of development and disease.

SUBMITTER: Zhu M

PROVIDER: S-EPMC7060671 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Spatial mapping of tissue properties in vivo reveals a 3D stiffness gradient in the mouse limb bud.

Zhu Min M Tao Hirotaka H Samani Mohammad M Luo Mengxi M Wang Xian X Hopyan Sevan S Sun Yu Y

Proceedings of the National Academy of Sciences of the United States of America 20200218 9

Numerous hypotheses invoke tissue stiffness as a key parameter that regulates morphogenesis and disease progression. However, current methods are insufficient to test hypotheses that concern physical properties deep in living tissues. Here we introduce, validate, and apply a magnetic device that generates a uniform magnetic field gradient within a space that is sufficient to accommodate an organ-stage mouse embryo under live conditions. The method allows rapid, nontoxic measurement of the three- ...[more]

PMID: 32071242

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Project description:Structural properties of articular cartilage such as proteoglycan content, collagen content and collagen alignment are known to vary over length scales as small as a few microns (Bullough and Goodfellow, 1968; Bi et al., 2006). Characterizing the resulting variation in mechanical properties is critical for understanding how the inhomogeneous architecture of this tissue gives rise to its function. Previous studies have measured the depth-dependent shear modulus of articular cartilage using methods such as particle image velocimetry (PIV) that rely on cells and cell nuclei as fiducial markers to track tissue deformation (Buckley et al., 2008; Wong et al., 2008a). However, such techniques are limited by the density of trackable markers, which may be too low to take full advantage of optical microscopy. This limitation leads to noise in the acquired data, which is often exacerbated when the data is manipulated. In this study, we report on two techniques for increasing the accuracy of tissue deformation measurements. In the first technique, deformations were tracked in a grid that was photobleached on each tissue sample (Bruehlmann et al., 2004). In the second, a numerical technique was implemented that allowed for accurate differentiation of optical displacement measurements by minimizing the propagated experimental error while ensuring that truncation error associated with local averaging of the data remained small. To test their efficacy, we employed these techniques to compare the depth-dependent shear moduli of neonatal bovine and adult human articular cartilage. Using a photobleached grid and numerical optimization to gather and analyze data led to results consistent with those reported previously (Buckley et al., 2008; Wong et al., 2008a), but with increased spatial resolution and characteristic coefficients of variation that were reduced up to a factor of 3. This increased resolution allowed us to determine that the shear modulus of neonatal bovine and adult human tissue both exhibit a global minimum at a depth z of around 100 microm and plateau at large depths. The consistency of the depth dependence of |G*|(Z) for adult human and neonatal bovine tissue suggests a functional advantage resulting from this behavior.

Dataset Information

Spatial mapping of tissue properties in vivo reveals a 3D stiffness gradient in the mouse limb bud.

Publications

Spatial mapping of tissue properties in vivo reveals a 3D stiffness gradient in the mouse limb bud.

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