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. 2012 Jan 4;102(1):1-9.
doi: 10.1016/j.bpj.2011.11.4004. Epub 2012 Jan 3.

Micro- and macrorheology of jellyfish extracellular matrix

Camille Gambini  1 , Bérengère Abou, Alain Ponton, Annemiek J M Cornelissen
Affiliations

Micro- and macrorheology of jellyfish extracellular matrix

Camille Gambini et al. Biophys J. .

Abstract

Mechanical properties of the extracellular matrix (ECM) play a key role in tissue organization and morphogenesis. Rheological properties of jellyfish ECM (mesoglea) were measured in vivo at the cellular scale by passive microrheology techniques: microbeads were injected in jellyfish ECM and their Brownian motion was recorded to determine the mechanical properties of the surrounding medium. Microrheology results were compared with macrorheological measurements performed with a shear rheometer on slices of jellyfish mesoglea. We found that the ECM behaved as a viscoelastic gel at the macroscopic scale and as a much softer and heterogeneous viscoelastic structure at the microscopic scale. The fibrous architecture of the mesoglea, as observed by differential interference contrast and scanning electron microscopy, was in accord with these scale-dependent mechanical properties. Furthermore, the evolution of the mechanical properties of the ECM during aging was investigated by measuring microrheological properties at different jellyfish sizes. We measured that the ECM in adult jellyfish was locally stiffer than in juvenile ones. We argue that this stiffening is a consequence of local aggregations of fibers occurring gradually during aging of the jellyfish mesoglea and is enhanced by repetitive muscular contractions of the jellyfish.

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Figures

Figure 1
Figure 1
Schematic view of the fibrous network organization of mesoglea of A. aurita. For clarity, the diagram does not show actual sizes of the various structures. (Vertical arrows) Direction of the oral-aboral axis. Characteristic length-scales of jellyfish and mesogleal fibrous architecture network for adult jellyfish (solid) and juvenile jellyfish (shaded). Visualizations by DIC microscopy of the thick vertical and tangential fibers are shown in Fig. 2, A and B, respectively. Visualizations by SEM microscopy of the fine fibers are shown in Fig. 3. Endoderm (en); exumbrella (ex); fine fibers (ff); subumbrellar swimming muscle (mu); thick tangential fibers (tf); thick vertical fibers (vf). Figure adapted from Weber and Schmid (15).
Figure 2
Figure 2
Thick fibers of the ECM. Hand-cut sections of adult jellyfish mesoglea were visualized by DIC microscopy. The thick fibers of the ECM and numerous randomly distributed mesogleal cells can be observed. (A) Thick vertical fibers and mesogleal cells. The slice of mesoglea was cut lateral along the oral-aboral axis, in the middle of the mesoglea, ∼1–2 mm above the endoderm. The thick vertical fibers are parallel and run perpendicularly from the exumbrellar side. (B) Thick tangential fibers and mesogleal cells. The slice of mesoglea was cut perpendicularly to the oral-aboral axis, ∼10 μm under the exumbrella. The thick tangential fibers run tangentially in all directions, near the exumbrellar surface.
Figure 3
Figure 3
Scanning electron micrographs of the mesoglea of juvenile jellyfish in the middle of the mesoglea, ∼100–400 μm above the endoderm. (A) Thick fibers emerging from the three-dimensional network of fine fibrils. The thick fibers are woven together by many fibrils of the three-dimensional network. The fibrils are randomly and heterogeneously distributed and the size of the fibrous mesh is very variable. A similar fibrous organization was observed on pieces of mesoglea cut from adult jellyfish. (B) A mesogleal cell embedded in the fine network of fibrils.
Figure 4
Figure 4
Macrorheological measurements. The frequency dependence of the averaged elastic (circles) and viscous (squares) moduli of mesoglea slices of adult jellyfish were obtained at the macroscopic scale using a shear rheometer. The average was performed over 18 different slices of mesoglea. (Bars) Standard deviation due to the dispersion of the measurements. At macroscopic scale, the mesoglea behaves like a viscoelastic gel.
Figure 5
Figure 5
Microrheological measurements. Time-averaged MSD of 1-μm microbeads embedded in the mesogleal ECM as a function of the lag time. The microprobes were injected and visualized together and each symbol represents the MSD of a different microbead. (Solid line in each panel) Slope of 1. The dispersion of MSD curves shows that the fibrous network of jellyfish ECM is very heterogeneous at the micron scale. (A) MSD of microprobes injected in the mesoglea of a juvenile jellyfish. (B) MSD of microprobes injected in the mesoglea of an adult jellyfish. The dispersion of MSD curves is more important in adult jellyfish than in juvenile ones. Some of the beads enhance a very tiny Brownian motion. They explore stiff microenvironments of the ECM. The other beads move more freely and their MSD are comparable to those observed in the mesoglea of juvenile jellyfish.
Figure 6
Figure 6
Viscoelastic moduli at macroscopic and microscopic scales. Viscoelastic moduli G′ and G″ were obtained from macrorheology and microrheology experiments in adult jellyfish ECM. (Circles) G′; (squares) G″. (Shaded symbols) The moduli G′ and G″ at macroscopic scale, obtained with a shear rheometer. G′ and G″ at microscopic scale were calculated from the MSD curves of two different microbeads: a bead moving very little (slow) and a very mobile bead (fast). (Open symbols) G′ and G″ calculated from the MSD of the probe that moved very little. (Solid symbols) G′ and G″ calculated from the MSD of the very mobile bead. The different behaviors of these two beads correspond to different local viscoelastic moduli. The orders of magnitude of the elastic and viscous moduli measured with a shear rheometer are close to those calculated from the bead moving very little. The more freely moving bead explores a much softer microenvironment (with lower viscoelastic moduli).
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