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Interplay between passive tension and strong and weak binding cross- bridges in insect indirect flight muscle. A functional dissection by gelsolin-mediated thin filament removal

The interplay between passive and active mechanical properties of indirect flight muscle of the waterbug (Lethocerus) was investigated. A functional dissection of the relative contribution of cross-bridges, actin filaments, and C filaments to tension and stiffness of passive, activated, and rigor fi...

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Formato: Texto
Lenguaje:English
Publicado: The Rockefeller University Press 1993
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Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2216761/
https://www.ncbi.nlm.nih.gov/pubmed/7681097
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collection PubMed
description The interplay between passive and active mechanical properties of indirect flight muscle of the waterbug (Lethocerus) was investigated. A functional dissection of the relative contribution of cross-bridges, actin filaments, and C filaments to tension and stiffness of passive, activated, and rigor fibers was carried out by comparing mechanical properties at different ionic strengths of sarcomeres with and without thin filaments. Selective thin filament removal was accomplished by treatment with the actin-severving protein gelsolin. Thin filament, removal had no effect on passive tension, indicating that the C filament and the actin filament are mechanically independent and that passive tension is developed by the C filament in response to sarcomere stretch. Passive tension increased steeply with sarcomere length until an elastic limit was reached at only 6-7% sarcomere extension, which corresponds to an extension of 350% of the C filament. The passive tension-length relation of insect flight muscle was analyzed using a segmental extension model of passive tension development (Wang, K, R. McCarter, J. Wright, B. Jennate, and R Ramirez-Mitchell. 1991. Proc. Natl. Acad. Sci. USA. 88:7101-7109). Thin filament removal greatly depressed high frequency passive stiffness (2.2 kHz) and eliminated the ionic strength sensitivity of passive stiffness. It is likely that the passive stiffness component that is removed by gelsolin is derived from weak-binding cross-bridges, while the component that remains is derived from the C filament. Our results indicate that a significant number of weak-binding cross-bridges exist in passive insect muscle at room temperature and at an ionic strength of 195 mM. Analysis of rigor muscle indicated that while rigor tension is entirely actin based, rigor stiffness contains a component that resists gelsolin treatment and is therefore likely to be C filament based. Active tension and active stiffness of unextracted fibers were directly proportional to passive tension before activation. Similarly, passive stiffness due to weak bridges also increased linearly with passive tension, up to a limit. These correlations lead us to propose a stress-activation model for insect flight muscle in which passive tension is a prerequisite for the formation of both weak-binding and strong-binding cross-bridges.
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spelling pubmed-22167612008-04-23 Interplay between passive tension and strong and weak binding cross- bridges in insect indirect flight muscle. A functional dissection by gelsolin-mediated thin filament removal J Gen Physiol Articles The interplay between passive and active mechanical properties of indirect flight muscle of the waterbug (Lethocerus) was investigated. A functional dissection of the relative contribution of cross-bridges, actin filaments, and C filaments to tension and stiffness of passive, activated, and rigor fibers was carried out by comparing mechanical properties at different ionic strengths of sarcomeres with and without thin filaments. Selective thin filament removal was accomplished by treatment with the actin-severving protein gelsolin. Thin filament, removal had no effect on passive tension, indicating that the C filament and the actin filament are mechanically independent and that passive tension is developed by the C filament in response to sarcomere stretch. Passive tension increased steeply with sarcomere length until an elastic limit was reached at only 6-7% sarcomere extension, which corresponds to an extension of 350% of the C filament. The passive tension-length relation of insect flight muscle was analyzed using a segmental extension model of passive tension development (Wang, K, R. McCarter, J. Wright, B. Jennate, and R Ramirez-Mitchell. 1991. Proc. Natl. Acad. Sci. USA. 88:7101-7109). Thin filament removal greatly depressed high frequency passive stiffness (2.2 kHz) and eliminated the ionic strength sensitivity of passive stiffness. It is likely that the passive stiffness component that is removed by gelsolin is derived from weak-binding cross-bridges, while the component that remains is derived from the C filament. Our results indicate that a significant number of weak-binding cross-bridges exist in passive insect muscle at room temperature and at an ionic strength of 195 mM. Analysis of rigor muscle indicated that while rigor tension is entirely actin based, rigor stiffness contains a component that resists gelsolin treatment and is therefore likely to be C filament based. Active tension and active stiffness of unextracted fibers were directly proportional to passive tension before activation. Similarly, passive stiffness due to weak bridges also increased linearly with passive tension, up to a limit. These correlations lead us to propose a stress-activation model for insect flight muscle in which passive tension is a prerequisite for the formation of both weak-binding and strong-binding cross-bridges. The Rockefeller University Press 1993-02-01 /pmc/articles/PMC2216761/ /pubmed/7681097 Text en This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 Unported license, as described at http://creativecommons.org/licenses/by-nc-sa/4.0/).
spellingShingle Articles
Interplay between passive tension and strong and weak binding cross- bridges in insect indirect flight muscle. A functional dissection by gelsolin-mediated thin filament removal
title Interplay between passive tension and strong and weak binding cross- bridges in insect indirect flight muscle. A functional dissection by gelsolin-mediated thin filament removal
title_full Interplay between passive tension and strong and weak binding cross- bridges in insect indirect flight muscle. A functional dissection by gelsolin-mediated thin filament removal
title_fullStr Interplay between passive tension and strong and weak binding cross- bridges in insect indirect flight muscle. A functional dissection by gelsolin-mediated thin filament removal
title_full_unstemmed Interplay between passive tension and strong and weak binding cross- bridges in insect indirect flight muscle. A functional dissection by gelsolin-mediated thin filament removal
title_short Interplay between passive tension and strong and weak binding cross- bridges in insect indirect flight muscle. A functional dissection by gelsolin-mediated thin filament removal
title_sort interplay between passive tension and strong and weak binding cross- bridges in insect indirect flight muscle. a functional dissection by gelsolin-mediated thin filament removal
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2216761/
https://www.ncbi.nlm.nih.gov/pubmed/7681097