Computational analysis of viscoelastic properties of crosslinked actin networks
Mechanical force plays an important role in the physiology of eukaryotic cells whose dominant structural constituent is the actin cytoskeleton composed mainly of actin and actin crosslinking proteins (ACPs). Thus, knowledge of rheological properties of actin networks is crucial for understanding the...
| Main Authors: | , , , |
|---|---|
| Other Authors: | |
| Format: | Article |
| Language: | en_US |
| Published: |
Public Library of Science
2010
|
| Online Access: | http://hdl.handle.net/1721.1/52473 https://orcid.org/0000-0002-7232-304X |
| _version_ | 1826192945788747776 |
|---|---|
| author | Hwang, Wonmuk Lee, Hyungsuk Kim, Taeyoon Kamm, Roger Dale |
| author2 | Massachusetts Institute of Technology. Department of Mechanical Engineering |
| author_facet | Massachusetts Institute of Technology. Department of Mechanical Engineering Hwang, Wonmuk Lee, Hyungsuk Kim, Taeyoon Kamm, Roger Dale |
| author_sort | Hwang, Wonmuk |
| collection | MIT |
| description | Mechanical force plays an important role in the physiology of eukaryotic cells whose dominant structural constituent is the actin cytoskeleton composed mainly of actin and actin crosslinking proteins (ACPs). Thus, knowledge of rheological properties of actin networks is crucial for understanding the mechanics and processes of cells. We used Brownian dynamics simulations to study the viscoelasticity of crosslinked actin networks. Two methods were employed, bulk rheology and segment-tracking rheology, where the former measures the stress in response to an applied shear strain, and the latter analyzes thermal fluctuations of individual actin segments of the network. It was demonstrated that the storage shear modulus (G′) increases more by the addition of ACPs that form orthogonal crosslinks than by those that form parallel bundles. In networks with orthogonal crosslinks, as crosslink density increases, the power law exponent of G′ as a function of the oscillation frequency decreases from 0.75, which reflects the transverse thermal motion of actin filaments, to near zero at low frequency. Under increasing prestrain, the network becomes more elastic, and three regimes of behavior are observed, each dominated by different mechanisms: bending of actin filaments, bending of ACPs, and at the highest prestrain tested (55%), stretching of actin filaments and ACPs. In the last case, only a small portion of actin filaments connected via highly stressed ACPs support the strain. We thus introduce the concept of a ‘supportive framework,’ as a subset of the full network, which is responsible for high elasticity. Notably, entropic effects due to thermal fluctuations appear to be important only at relatively low prestrains and when the average crosslinking distance is comparable to or greater than the persistence length of the filament. Taken together, our results suggest that viscoelasticity of the actin network is attributable to different mechanisms depending on the amount of prestrain. |
| first_indexed | 2024-09-23T09:31:35Z |
| format | Article |
| id | mit-1721.1/52473 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T09:31:35Z |
| publishDate | 2010 |
| publisher | Public Library of Science |
| record_format | dspace |
| spelling | mit-1721.1/524732022-09-26T12:01:49Z Computational analysis of viscoelastic properties of crosslinked actin networks Hwang, Wonmuk Lee, Hyungsuk Kim, Taeyoon Kamm, Roger Dale Massachusetts Institute of Technology. Department of Mechanical Engineering Kamm, Roger Dale Lee, Hyungsuk Kim, Taeyoon Kamm, Roger Dale Mechanical force plays an important role in the physiology of eukaryotic cells whose dominant structural constituent is the actin cytoskeleton composed mainly of actin and actin crosslinking proteins (ACPs). Thus, knowledge of rheological properties of actin networks is crucial for understanding the mechanics and processes of cells. We used Brownian dynamics simulations to study the viscoelasticity of crosslinked actin networks. Two methods were employed, bulk rheology and segment-tracking rheology, where the former measures the stress in response to an applied shear strain, and the latter analyzes thermal fluctuations of individual actin segments of the network. It was demonstrated that the storage shear modulus (G′) increases more by the addition of ACPs that form orthogonal crosslinks than by those that form parallel bundles. In networks with orthogonal crosslinks, as crosslink density increases, the power law exponent of G′ as a function of the oscillation frequency decreases from 0.75, which reflects the transverse thermal motion of actin filaments, to near zero at low frequency. Under increasing prestrain, the network becomes more elastic, and three regimes of behavior are observed, each dominated by different mechanisms: bending of actin filaments, bending of ACPs, and at the highest prestrain tested (55%), stretching of actin filaments and ACPs. In the last case, only a small portion of actin filaments connected via highly stressed ACPs support the strain. We thus introduce the concept of a ‘supportive framework,’ as a subset of the full network, which is responsible for high elasticity. Notably, entropic effects due to thermal fluctuations appear to be important only at relatively low prestrains and when the average crosslinking distance is comparable to or greater than the persistence length of the filament. Taken together, our results suggest that viscoelasticity of the actin network is attributable to different mechanisms depending on the amount of prestrain. National Institutes of Health (GM076689) 2010-03-10T19:11:49Z 2010-03-10T19:11:49Z 2009-07 2009-01 Article http://purl.org/eprint/type/JournalArticle 1553-734X 1553-7358 http://hdl.handle.net/1721.1/52473 Kim, Taeyoon et al. “Computational Analysis of Viscoelastic Properties of Crosslinked Actin Networks.” PLoS Comput Biol 5.7 (2009): e1000439. https://orcid.org/0000-0002-7232-304X en_US http://dx.doi.org/10.1371/journal.pcbi.1000439 PLoS Computational Biology Creative Commons Attribution http://creativecommons.org/licenses/by/2.5/ application/pdf Public Library of Science PLoS |
| spellingShingle | Hwang, Wonmuk Lee, Hyungsuk Kim, Taeyoon Kamm, Roger Dale Computational analysis of viscoelastic properties of crosslinked actin networks |
| title | Computational analysis of viscoelastic properties of crosslinked actin networks |
| title_full | Computational analysis of viscoelastic properties of crosslinked actin networks |
| title_fullStr | Computational analysis of viscoelastic properties of crosslinked actin networks |
| title_full_unstemmed | Computational analysis of viscoelastic properties of crosslinked actin networks |
| title_short | Computational analysis of viscoelastic properties of crosslinked actin networks |
| title_sort | computational analysis of viscoelastic properties of crosslinked actin networks |
| url | http://hdl.handle.net/1721.1/52473 https://orcid.org/0000-0002-7232-304X |
| work_keys_str_mv | AT hwangwonmuk computationalanalysisofviscoelasticpropertiesofcrosslinkedactinnetworks AT leehyungsuk computationalanalysisofviscoelasticpropertiesofcrosslinkedactinnetworks AT kimtaeyoon computationalanalysisofviscoelasticpropertiesofcrosslinkedactinnetworks AT kammrogerdale computationalanalysisofviscoelasticpropertiesofcrosslinkedactinnetworks |