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Strain-induced alignment in collagen gels.

Vader D, Kabla A, Weitz D, Mahadevan L - PLoS ONE (2009)

Bottom Line: This alignment is found to be irreversibly imprinted in uncrosslinked collagen networks, suggesting a simple mechanism for tissue organization at the microscale.Plasticity is therefore not required to align fibers.On the contrary, our data show that this effect is part of the fundamental non-linear properties of fibrous biological networks.

View Article: PubMed Central - PubMed

Affiliation: School of Engineering and Applied Sciences, Harvard University, Cambridge, Massachusetts, United States of America.

ABSTRACT
Collagen is the most abundant extracellular-network-forming protein in animal biology and is important in both natural and artificial tissues, where it serves as a material of great mechanical versatility. This versatility arises from its almost unique ability to remodel under applied loads into anisotropic and inhomogeneous structures. To explore the origins of this property, we develop a set of analysis tools and a novel experimental setup that probes the mechanical response of fibrous networks in a geometry that mimics a typical deformation profile imposed by cells in vivo. We observe strong fiber alignment and densification as a function of applied strain for both uncrosslinked and crosslinked collagenous networks. This alignment is found to be irreversibly imprinted in uncrosslinked collagen networks, suggesting a simple mechanism for tissue organization at the microscale. However, crosslinked networks display similar fiber alignment and the same geometrical properties as uncrosslinked gels, but with full reversibility. Plasticity is therefore not required to align fibers. On the contrary, our data show that this effect is part of the fundamental non-linear properties of fibrous biological networks.

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Characterization of the reversibility of alignment and densification in crosslinked and uncrosslinked collagen samples.Response to cycles of deformation for untreated collagen gels (A–E) and gels treated with glutaraldehyde (F–K). (A) Histograms of the fiber orientation as a function of the imposed strain for untreated sample; color at each point corresponds to the relative count of fibers oriented along a specific direction at a given strain . (B) Resulting order parameter for untreated sample. (C–E) Confocal reflectance images of a 1 mg/mL collagen sample cycled 4 times up to 15% stretch and back to 0%, showing the extent of the reversibility at the microstructural level: (C) beginning of 1st stretch cycle; (D) middle of 1st stretch cycle; (E) end of 1st stretch cycle; bars = 50 µm. (F) Histograms of the fiber orientation as a function of imposed strain for glutaraldehyde-treated sample; color-coding as in (A). (G) Resulting order parameter and density for glutaraldehyde-treated sample. (H–J) Confocal images of a 1 mg/mL collagen samples with glutaraldehyde, cycled 4 times up to 15% stretch and back to 0%: (H) beginning of 3rd stretch cycle; (I) middle of 3rd stretch cycle; (J) end of 3rd stretch cycle; bars = 25 µm. (K) Mesoscopic response to 15% strain cycles for various strain rates at a constant imposed strain amplitude. The bold line corresponds to the strain rate used for all other experiments.
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pone-0005902-g007: Characterization of the reversibility of alignment and densification in crosslinked and uncrosslinked collagen samples.Response to cycles of deformation for untreated collagen gels (A–E) and gels treated with glutaraldehyde (F–K). (A) Histograms of the fiber orientation as a function of the imposed strain for untreated sample; color at each point corresponds to the relative count of fibers oriented along a specific direction at a given strain . (B) Resulting order parameter for untreated sample. (C–E) Confocal reflectance images of a 1 mg/mL collagen sample cycled 4 times up to 15% stretch and back to 0%, showing the extent of the reversibility at the microstructural level: (C) beginning of 1st stretch cycle; (D) middle of 1st stretch cycle; (E) end of 1st stretch cycle; bars = 50 µm. (F) Histograms of the fiber orientation as a function of imposed strain for glutaraldehyde-treated sample; color-coding as in (A). (G) Resulting order parameter and density for glutaraldehyde-treated sample. (H–J) Confocal images of a 1 mg/mL collagen samples with glutaraldehyde, cycled 4 times up to 15% stretch and back to 0%: (H) beginning of 3rd stretch cycle; (I) middle of 3rd stretch cycle; (J) end of 3rd stretch cycle; bars = 25 µm. (K) Mesoscopic response to 15% strain cycles for various strain rates at a constant imposed strain amplitude. The bold line corresponds to the strain rate used for all other experiments.

Mentions: Strain-induced alignment arises a priori from a combination of reversible elastic effects and irreversible inelastic effects. To disentangle these two contributions, we apply repeated strain cycles to the sample. All pure type-I collagen samples display very little reversibility regardless of their concentration once the imposed strains exceed about 10%; the gel never recovers its initial configuration once the capillary tips return to their initial location. In figures 7A,B we show the evolution of the fiber orientation histograms as the material is cyclically stretched up to strains of 15%: fiber aligment is permanently imprinted (7C–E).


Strain-induced alignment in collagen gels.

Vader D, Kabla A, Weitz D, Mahadevan L - PLoS ONE (2009)

Characterization of the reversibility of alignment and densification in crosslinked and uncrosslinked collagen samples.Response to cycles of deformation for untreated collagen gels (A–E) and gels treated with glutaraldehyde (F–K). (A) Histograms of the fiber orientation as a function of the imposed strain for untreated sample; color at each point corresponds to the relative count of fibers oriented along a specific direction at a given strain . (B) Resulting order parameter for untreated sample. (C–E) Confocal reflectance images of a 1 mg/mL collagen sample cycled 4 times up to 15% stretch and back to 0%, showing the extent of the reversibility at the microstructural level: (C) beginning of 1st stretch cycle; (D) middle of 1st stretch cycle; (E) end of 1st stretch cycle; bars = 50 µm. (F) Histograms of the fiber orientation as a function of imposed strain for glutaraldehyde-treated sample; color-coding as in (A). (G) Resulting order parameter and density for glutaraldehyde-treated sample. (H–J) Confocal images of a 1 mg/mL collagen samples with glutaraldehyde, cycled 4 times up to 15% stretch and back to 0%: (H) beginning of 3rd stretch cycle; (I) middle of 3rd stretch cycle; (J) end of 3rd stretch cycle; bars = 25 µm. (K) Mesoscopic response to 15% strain cycles for various strain rates at a constant imposed strain amplitude. The bold line corresponds to the strain rate used for all other experiments.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2691583&req=5

pone-0005902-g007: Characterization of the reversibility of alignment and densification in crosslinked and uncrosslinked collagen samples.Response to cycles of deformation for untreated collagen gels (A–E) and gels treated with glutaraldehyde (F–K). (A) Histograms of the fiber orientation as a function of the imposed strain for untreated sample; color at each point corresponds to the relative count of fibers oriented along a specific direction at a given strain . (B) Resulting order parameter for untreated sample. (C–E) Confocal reflectance images of a 1 mg/mL collagen sample cycled 4 times up to 15% stretch and back to 0%, showing the extent of the reversibility at the microstructural level: (C) beginning of 1st stretch cycle; (D) middle of 1st stretch cycle; (E) end of 1st stretch cycle; bars = 50 µm. (F) Histograms of the fiber orientation as a function of imposed strain for glutaraldehyde-treated sample; color-coding as in (A). (G) Resulting order parameter and density for glutaraldehyde-treated sample. (H–J) Confocal images of a 1 mg/mL collagen samples with glutaraldehyde, cycled 4 times up to 15% stretch and back to 0%: (H) beginning of 3rd stretch cycle; (I) middle of 3rd stretch cycle; (J) end of 3rd stretch cycle; bars = 25 µm. (K) Mesoscopic response to 15% strain cycles for various strain rates at a constant imposed strain amplitude. The bold line corresponds to the strain rate used for all other experiments.
Mentions: Strain-induced alignment arises a priori from a combination of reversible elastic effects and irreversible inelastic effects. To disentangle these two contributions, we apply repeated strain cycles to the sample. All pure type-I collagen samples display very little reversibility regardless of their concentration once the imposed strains exceed about 10%; the gel never recovers its initial configuration once the capillary tips return to their initial location. In figures 7A,B we show the evolution of the fiber orientation histograms as the material is cyclically stretched up to strains of 15%: fiber aligment is permanently imprinted (7C–E).

Bottom Line: This alignment is found to be irreversibly imprinted in uncrosslinked collagen networks, suggesting a simple mechanism for tissue organization at the microscale.Plasticity is therefore not required to align fibers.On the contrary, our data show that this effect is part of the fundamental non-linear properties of fibrous biological networks.

View Article: PubMed Central - PubMed

Affiliation: School of Engineering and Applied Sciences, Harvard University, Cambridge, Massachusetts, United States of America.

ABSTRACT
Collagen is the most abundant extracellular-network-forming protein in animal biology and is important in both natural and artificial tissues, where it serves as a material of great mechanical versatility. This versatility arises from its almost unique ability to remodel under applied loads into anisotropic and inhomogeneous structures. To explore the origins of this property, we develop a set of analysis tools and a novel experimental setup that probes the mechanical response of fibrous networks in a geometry that mimics a typical deformation profile imposed by cells in vivo. We observe strong fiber alignment and densification as a function of applied strain for both uncrosslinked and crosslinked collagenous networks. This alignment is found to be irreversibly imprinted in uncrosslinked collagen networks, suggesting a simple mechanism for tissue organization at the microscale. However, crosslinked networks display similar fiber alignment and the same geometrical properties as uncrosslinked gels, but with full reversibility. Plasticity is therefore not required to align fibers. On the contrary, our data show that this effect is part of the fundamental non-linear properties of fibrous biological networks.

Show MeSH
Related in: MedlinePlus