Limits...
Monolayer stress microscopy: limitations, artifacts, and accuracy of recovered intercellular stresses.

Tambe DT, Croutelle U, Trepat X, Park CY, Kim JH, Millet E, Butler JP, Fredberg JJ - PLoS ONE (2013)

Bottom Line: To assess the validity of these assumptions and to quantify associated errors, here we report new analytical, numerical, and experimental investigations.For several commonly used experimental monolayer systems, the simplifying assumptions used previously lead to errors that are shown to be quite small.Out-of-plane components of displacement and traction fields can be safely neglected, and characteristic features of intercellular stresses that underlie plithotaxis remain largely unaffected.

View Article: PubMed Central - PubMed

Affiliation: Department of Environmental Health, Harvard School of Public Health, Boston, Massachusetts, USA. dhananjay@alumni.brown.edu

ABSTRACT
In wound healing, tissue growth, and certain cancers, the epithelial or the endothelial monolayer sheet expands. Within the expanding monolayer sheet, migration of the individual cell is strongly guided by physical forces imposed by adjacent cells. This process is called plithotaxis and was discovered using Monolayer Stress Microscopy (MSM). MSM rests upon certain simplifying assumptions, however, concerning boundary conditions, cell material properties and system dimensionality. To assess the validity of these assumptions and to quantify associated errors, here we report new analytical, numerical, and experimental investigations. For several commonly used experimental monolayer systems, the simplifying assumptions used previously lead to errors that are shown to be quite small. Out-of-plane components of displacement and traction fields can be safely neglected, and characteristic features of intercellular stresses that underlie plithotaxis remain largely unaffected. Taken together, these findings validate Monolayer Stress Microscopy within broad but well-defined limits of applicability.

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Sensitivity of the recovered monolayer stresses to change in the assumed elastic properties of the monolayer.(a) Map of maximum principal orientation (for enlarged version of this image, see Supporting Information S8; Figs. S11–13; in File S1), (b) map of average normal stress, and (c) map of maximum shear stress obtained by assuming monolayer elastic properties to be homogeneous with . (d–f) The stress maps with  instead. (g–i) The stress maps when  is heterogeneous with , here  was assumed to be proportional to the map of the average normal stress (b). (j) Scatter plots for maximum principal orientation where, red points quantify effect of  on the maps (a) and (d), and blue points quantify effect of heterogeneity of  on the (a) and (g). (k) Scatter plots for average normal stress, (l) scatter plots for maximum shear stress. Regression parameters for a straight line fit,  in (j–l): blue points, (j) , (k) , and (l) ; red points, (j) , (k) , and (l) .
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pone-0055172-g004: Sensitivity of the recovered monolayer stresses to change in the assumed elastic properties of the monolayer.(a) Map of maximum principal orientation (for enlarged version of this image, see Supporting Information S8; Figs. S11–13; in File S1), (b) map of average normal stress, and (c) map of maximum shear stress obtained by assuming monolayer elastic properties to be homogeneous with . (d–f) The stress maps with instead. (g–i) The stress maps when is heterogeneous with , here was assumed to be proportional to the map of the average normal stress (b). (j) Scatter plots for maximum principal orientation where, red points quantify effect of on the maps (a) and (d), and blue points quantify effect of heterogeneity of on the (a) and (g). (k) Scatter plots for average normal stress, (l) scatter plots for maximum shear stress. Regression parameters for a straight line fit, in (j–l): blue points, (j) , (k) , and (l) ; red points, (j) , (k) , and (l) .

Mentions: In an island of rat pulmonary microvascular endothelial (RPME) cells, tractions demonstrated extreme spatial fluctuations (, Fig. 3b; and , Fig. 3c). These fluctuations are comparable to those previously reported [22], [27]. Using these traction fields together with Eqs. 1 and 2, and assuming the monolayer elastic properties to be homogeneous and incompressible (), the resulting intercellular stress landscape demonstrated the same characteristic ruggedness as observed previously by Tambe et al. [22] (Fig. 4a–c).


Monolayer stress microscopy: limitations, artifacts, and accuracy of recovered intercellular stresses.

Tambe DT, Croutelle U, Trepat X, Park CY, Kim JH, Millet E, Butler JP, Fredberg JJ - PLoS ONE (2013)

Sensitivity of the recovered monolayer stresses to change in the assumed elastic properties of the monolayer.(a) Map of maximum principal orientation (for enlarged version of this image, see Supporting Information S8; Figs. S11–13; in File S1), (b) map of average normal stress, and (c) map of maximum shear stress obtained by assuming monolayer elastic properties to be homogeneous with . (d–f) The stress maps with  instead. (g–i) The stress maps when  is heterogeneous with , here  was assumed to be proportional to the map of the average normal stress (b). (j) Scatter plots for maximum principal orientation where, red points quantify effect of  on the maps (a) and (d), and blue points quantify effect of heterogeneity of  on the (a) and (g). (k) Scatter plots for average normal stress, (l) scatter plots for maximum shear stress. Regression parameters for a straight line fit,  in (j–l): blue points, (j) , (k) , and (l) ; red points, (j) , (k) , and (l) .
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3585344&req=5

pone-0055172-g004: Sensitivity of the recovered monolayer stresses to change in the assumed elastic properties of the monolayer.(a) Map of maximum principal orientation (for enlarged version of this image, see Supporting Information S8; Figs. S11–13; in File S1), (b) map of average normal stress, and (c) map of maximum shear stress obtained by assuming monolayer elastic properties to be homogeneous with . (d–f) The stress maps with instead. (g–i) The stress maps when is heterogeneous with , here was assumed to be proportional to the map of the average normal stress (b). (j) Scatter plots for maximum principal orientation where, red points quantify effect of on the maps (a) and (d), and blue points quantify effect of heterogeneity of on the (a) and (g). (k) Scatter plots for average normal stress, (l) scatter plots for maximum shear stress. Regression parameters for a straight line fit, in (j–l): blue points, (j) , (k) , and (l) ; red points, (j) , (k) , and (l) .
Mentions: In an island of rat pulmonary microvascular endothelial (RPME) cells, tractions demonstrated extreme spatial fluctuations (, Fig. 3b; and , Fig. 3c). These fluctuations are comparable to those previously reported [22], [27]. Using these traction fields together with Eqs. 1 and 2, and assuming the monolayer elastic properties to be homogeneous and incompressible (), the resulting intercellular stress landscape demonstrated the same characteristic ruggedness as observed previously by Tambe et al. [22] (Fig. 4a–c).

Bottom Line: To assess the validity of these assumptions and to quantify associated errors, here we report new analytical, numerical, and experimental investigations.For several commonly used experimental monolayer systems, the simplifying assumptions used previously lead to errors that are shown to be quite small.Out-of-plane components of displacement and traction fields can be safely neglected, and characteristic features of intercellular stresses that underlie plithotaxis remain largely unaffected.

View Article: PubMed Central - PubMed

Affiliation: Department of Environmental Health, Harvard School of Public Health, Boston, Massachusetts, USA. dhananjay@alumni.brown.edu

ABSTRACT
In wound healing, tissue growth, and certain cancers, the epithelial or the endothelial monolayer sheet expands. Within the expanding monolayer sheet, migration of the individual cell is strongly guided by physical forces imposed by adjacent cells. This process is called plithotaxis and was discovered using Monolayer Stress Microscopy (MSM). MSM rests upon certain simplifying assumptions, however, concerning boundary conditions, cell material properties and system dimensionality. To assess the validity of these assumptions and to quantify associated errors, here we report new analytical, numerical, and experimental investigations. For several commonly used experimental monolayer systems, the simplifying assumptions used previously lead to errors that are shown to be quite small. Out-of-plane components of displacement and traction fields can be safely neglected, and characteristic features of intercellular stresses that underlie plithotaxis remain largely unaffected. Taken together, these findings validate Monolayer Stress Microscopy within broad but well-defined limits of applicability.

Show MeSH
Related in: MedlinePlus