“Twitchin–actin linkage hypothesis” for the catch mechanism in molluscan muscles: Evidence that twitchin interacts with myosin, myorod, and paramyosin core and affects properties of actomyosin

Shelud’ko, Nikolay S.; Matusovsky, Oleg S.; Permyakova, T. V.; Matusovskaya, Galina G.

doi:10.1016/j.abb.2007.07.014

Cited by 36 publications

(25 citation statements)

References 58 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…These data show that most of the twitchin is bound to the thick filament tightly enough to remain attached during the thick filament isolation procedure [101]. In vitro binding of twitchin has been shown to myosin, paramyosin, and catchin, all of which are components of the thick filaments [102]. Although twitchin binds to both the rod and heavy meromyosin portions of myosin, binding to the latter was stronger.…”

Section: Biochemical Evidence That Twitchin Is the Catch Linkmentioning

confidence: 99%

Mechanism of Catch Force: Tethering of Thick and Thin Filaments by Twitchin

Butler

Siegman

2010

Journal of Biomedicine and Biotechnology

View full text Add to dashboard Cite

Catch is a mechanical state occurring in some invertebrate smooth muscles characterized by high force maintenance and resistance to stretch during extremely slow relaxation. During catch, intracellular calcium is near basal concentration and myosin crossbridge cyctng rate is extremely slow. Catch force is relaxed by a protein kinase A-mediated phosphorylation of sites near the N- and C- temini of the minititin twitchin (~526 kDa). Some catch force maintenance car also occur together with cycling myosin crossbridges at submaximal calcium concentrations, but not when the muscle is maximally activated. Additionally, the link responsible for catch can adjust during shortening of submaximally activated muscles and maintain catch force at the new shorter length. Twitchin binds to both thick and thin filaments, and the thin filament binding shown by both the N- and Cterminal portions of twitchin is decreased by phosphorylation of the sites that regulate catch. The data suggest that the twitchin molecule itself is the catch force beanng tether between thick and thin filaments. We present a model for the regulation of catch in which the twitchin tether can be displaced from thin filaments by both (a) the phosphorylation of twitchin and (b) the attachment of high force myosin crossbridges.

show abstract

Section: Biochemical Evidence That Twitchin Is the Catch Linkmentioning

confidence: 99%

Mechanism of Catch Force: Tethering of Thick and Thin Filaments by Twitchin

Butler

Siegman

2010

Journal of Biomedicine and Biotechnology

View full text Add to dashboard Cite

show abstract

“…Because of its regulatory role and large size, twitchin is a candidate for this interconnection (Shelud'ko et al 2004;Funabara et al 2007;Avrova et al 2009; in a sense, also Yamada et al 2001). Twitchin could either span from the thick filament backbone to the actin filaments (Butler et al 2006;Shelud'ko et al 2007) or it could strongly tie a fraction of myosin heads to the actin filaments (Funabara et al 2007). Alternatively, twitchin binding to the myosin head could mechanically lock the myosin head in one direction (for opposing stretches) while keeping it freely mobile in the opposite direction (for force generation; Galler 2008).…”

Section: Discussionmentioning

confidence: 99%

The highly efficient holding function of the mollusc ‘catch’ muscle is not based on decelerated myosin head cross-bridge cycles

et al. 2009

View full text Add to dashboard Cite

Certain smooth muscles are able to reduce energy consumption greatly when holding without shortening. For instance, this is the case with muscles surrounding blood vessels used for regulating blood flow and pressure. The phenomenon is most conspicuous in 'catch' muscles of molluscs, which have been used as models for investigating this important physiological property of smooth muscle. When the shells of mussels are held closed, the responsible muscles enter the highly energy-efficient state of catch. According to the traditional view, the state of catch is caused by the slowing down of the force-generating cycles of the molecular motors, the myosin heads. Here, we show that catch can still be induced and maintained when the myosin heads are prevented from generating force. This new evidence proves that the long-held explanation of the state of catch being due to the slowing down of force producing myosin head cycles is not valid and that the highly economic holding state is caused by the formation of a rigid network of inter-myofilament connections based on passive molecular structures.

show abstract

“…Recent evidence suggests that twitchin is a force-bearing tether between thick and thin filaments, and as such is responsible for the extended force maintenance and resistance to lengthening exhibited during the catch state (for review see Butler and Siegman 2010). Protein kinase A mediated phosphorylation of twitchin rapidly relaxes catch force most likely by causing detachment of the twitchin mediated tether between thick and thin filaments (Siegman et al 1998; Shelud’ko et al 2007; Funabara et al 2007; Butler et al 2010). …”

Section: Introductionmentioning

confidence: 99%

A force-activated kinase in a catch smooth muscle

Butler

Siegman

2011

J Muscle Res Cell Motil

View full text Add to dashboard Cite

Permeabilized anterior byssus retractor muscles (ABRM) from Mytilus edulis were used as a simple system to test whether there is a stretch dependent activation of a kinase as has been postulated for titin and the mini-titin twitchin. The ABRM is a smooth muscle that shows catch, a condition of high force maintenance and resistance to stretch following stimulation when the intracellular Ca++ concentration has diminished to sub-maximum levels. In the catch state twitchin is unphosphorylated, and the muscle maintains force without myosin crossbridge cycling through what is likely a twitchin mediated tether between thick and thin filaments. In catch, a small change in length results in a large change in force. The phosphorylation state of an added peptide, a good substrate for molluscan twitchin kinase, with the sequence KKRAARATSNVFA was used as a measure of kinase activation. We find that there is about a two-fold increase in phosphorylation of the added peptide with a 10% stretch of the ABRM in catch. The increased phosphorylation is due to activation of a kinase rather than to an inhibition of a phosphatase. The extent of phosphorylation of the peptide is decreased when twitchin is phosphorylated and catch force is not present. However, there is also a large increase in peptide phosphorylation when the muscle is activated in pCa 5, and the catch state does not exist. The force-sensitive kinase activity is decreased by ML-9 and ML-7 which are inhibitors of twitchin kinase, but not by the Rho kinase inhibitor Y-27632. There is no detectable phosphorylation of myosin light chains, but the phosphorylation of twitchin increases by a small, but significant extent with stretch. It is possible that twitchin senses force output resulting in a force-sensitive twitchin kinase activity that results in autophosphorylation of twitchin on site(s) other than those responsible for relaxation of catch.

show abstract

“Twitchin–actin linkage hypothesis” for the catch mechanism in molluscan muscles: Evidence that twitchin interacts with myosin, myorod, and paramyosin core and affects properties of actomyosin

Cited by 36 publications

References 58 publications

Mechanism of Catch Force: Tethering of Thick and Thin Filaments by Twitchin

Mechanism of Catch Force: Tethering of Thick and Thin Filaments by Twitchin

The highly efficient holding function of the mollusc ‘catch’ muscle is not based on decelerated myosin head cross-bridge cycles

A force-activated kinase in a catch smooth muscle

Contact Info

Product

Resources

About