A tug of war between filament treadmilling and myosin induced contractility generates actin rings
In most eukaryotic cells, actin filaments assemble into a shell-like actin cortex under the plasma membrane, controlling cellular morphology, mechanics, and signaling. The actin cortex is highly polymorphic, adopting diverse forms such as the ring-like structures found in podosomes, axonal rings, an...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-10-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/82658 |
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| author | Qin Ni Kaustubh Wagh Aashli Pathni Haoran Ni Vishavdeep Vashisht Arpita Upadhyaya Garegin A Papoian |
| author_facet | Qin Ni Kaustubh Wagh Aashli Pathni Haoran Ni Vishavdeep Vashisht Arpita Upadhyaya Garegin A Papoian |
| author_sort | Qin Ni |
| collection | DOAJ |
| description | In most eukaryotic cells, actin filaments assemble into a shell-like actin cortex under the plasma membrane, controlling cellular morphology, mechanics, and signaling. The actin cortex is highly polymorphic, adopting diverse forms such as the ring-like structures found in podosomes, axonal rings, and immune synapses. The biophysical principles that underlie the formation of actin rings and cortices remain unknown. Using a molecular simulation platform called MEDYAN, we discovered that varying the filament treadmilling rate and myosin concentration induces a finite size phase transition in actomyosin network structures. We found that actomyosin networks condense into clusters at low treadmilling rates or high myosin concentrations but form ring-like or cortex-like structures at high treadmilling rates and low myosin concentrations. This mechanism is supported by our corroborating experiments on live T cells, which exhibit ring-like actin networks upon activation by stimulatory antibody. Upon disruption of filament treadmilling or enhancement of myosin activity, the pre-existing actin rings are disrupted into actin clusters or collapse towards the network center respectively. Our analyses suggest that the ring-like actin structure is a preferred state of low mechanical energy, which is, importantly, only reachable at sufficiently high treadmilling rates. |
| first_indexed | 2024-04-11T14:29:46Z |
| format | Article |
| id | doaj.art-545608be2de84536ba0c939a1640cd5f |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T14:29:46Z |
| publishDate | 2022-10-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-545608be2de84536ba0c939a1640cd5f2022-12-22T04:18:42ZengeLife Sciences Publications LtdeLife2050-084X2022-10-011110.7554/eLife.82658A tug of war between filament treadmilling and myosin induced contractility generates actin ringsQin Ni0https://orcid.org/0000-0002-0738-1817Kaustubh Wagh1https://orcid.org/0000-0001-8514-027XAashli Pathni2https://orcid.org/0000-0003-4196-890XHaoran Ni3Vishavdeep Vashisht4https://orcid.org/0000-0002-9367-0278Arpita Upadhyaya5https://orcid.org/0000-0003-1496-919XGaregin A Papoian6https://orcid.org/0000-0001-8580-3790Department of Chemical and Biomolecular Engineering, University of Maryland, College Park, College Park, United StatesDepartment of Physics, University of Maryland, College Park, College Park, United StatesBiological Sciences Graduate Program, University of Maryland, College Park, College Park, United StatesBiophysics Graduate Program, University of Maryland, College Park, College Park, United StatesBiophysics Graduate Program, University of Maryland, College Park, College Park, United StatesDepartment of Physics, University of Maryland, College Park, College Park, United States; Biophysics Graduate Program, University of Maryland, College Park, College Park, United States; Institute for Physical Science and Technology, University of Maryland, College Park, United StatesBiophysics Graduate Program, University of Maryland, College Park, College Park, United States; Institute for Physical Science and Technology, University of Maryland, College Park, United States; Department of Chemistry and Biochemistry, University of Maryland, College Park, United StatesIn most eukaryotic cells, actin filaments assemble into a shell-like actin cortex under the plasma membrane, controlling cellular morphology, mechanics, and signaling. The actin cortex is highly polymorphic, adopting diverse forms such as the ring-like structures found in podosomes, axonal rings, and immune synapses. The biophysical principles that underlie the formation of actin rings and cortices remain unknown. Using a molecular simulation platform called MEDYAN, we discovered that varying the filament treadmilling rate and myosin concentration induces a finite size phase transition in actomyosin network structures. We found that actomyosin networks condense into clusters at low treadmilling rates or high myosin concentrations but form ring-like or cortex-like structures at high treadmilling rates and low myosin concentrations. This mechanism is supported by our corroborating experiments on live T cells, which exhibit ring-like actin networks upon activation by stimulatory antibody. Upon disruption of filament treadmilling or enhancement of myosin activity, the pre-existing actin rings are disrupted into actin clusters or collapse towards the network center respectively. Our analyses suggest that the ring-like actin structure is a preferred state of low mechanical energy, which is, importantly, only reachable at sufficiently high treadmilling rates.https://elifesciences.org/articles/82658cytoskeletonactomyosin ringmolecular simulationT cells |
| spellingShingle | Qin Ni Kaustubh Wagh Aashli Pathni Haoran Ni Vishavdeep Vashisht Arpita Upadhyaya Garegin A Papoian A tug of war between filament treadmilling and myosin induced contractility generates actin rings eLife cytoskeleton actomyosin ring molecular simulation T cells |
| title | A tug of war between filament treadmilling and myosin induced contractility generates actin rings |
| title_full | A tug of war between filament treadmilling and myosin induced contractility generates actin rings |
| title_fullStr | A tug of war between filament treadmilling and myosin induced contractility generates actin rings |
| title_full_unstemmed | A tug of war between filament treadmilling and myosin induced contractility generates actin rings |
| title_short | A tug of war between filament treadmilling and myosin induced contractility generates actin rings |
| title_sort | tug of war between filament treadmilling and myosin induced contractility generates actin rings |
| topic | cytoskeleton actomyosin ring molecular simulation T cells |
| url | https://elifesciences.org/articles/82658 |
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