Abstract
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.
Highlights
The hallmark of the contractile process in smooth muscle is its ability to maintain force with a very high economy, that is, a low expenditure of energy, through the slow cycling of force-bearing crossbridges
This force, familiar to those who have attempted to open the shells of oysters, scallops, clams, and mussels, as well as the contraction of the anterior byssus retractor muscle (ABRM) of the edible mussel Mytilus edulis, reflects an unusual contractile state called “catch.” Functionally, the catch state is an adaptation that allows the muscle to resist stretch; this is important in the scallop, for example, in controlling gape and for the mussel in holding its byssus threads, which anchor it to rocks and other substrates, tautly
Castellani and Cohen showed that phosphatase inhibition with NaF, or the use of a nonhydrolysable substrate such as ATP-γ-S prevents catch, but not the initial force development [46]. This suggests that calcium and phosphorylation of specific proteins have separate roles in the regulation of contraction and catch, but these have not yet been defined. They showed that prolonged treatment of the muscle with detergent during permeabilization leads to the loss of catch force maintenance which can be restored by the addition of calcineurin, a calcium-calmodulin-regulated type 2B phosphatase [56]
Summary
The hallmark of the contractile process in smooth muscle is its ability to maintain force with a very high economy, that is, a low expenditure of energy, through the slow cycling of force-bearing crossbridges. In certain invertebrate smooth muscles, such as adductors, force can be maintained for many hours This force, familiar to those who have attempted to open the shells of oysters, scallops, clams, and mussels, as well as the contraction of the anterior byssus retractor muscle (ABRM) of the edible mussel Mytilus edulis, reflects an unusual contractile state called “catch.” Functionally, the catch state is an adaptation that allows the muscle to resist stretch; this is important in the scallop, for example, in controlling gape (openness of its shell) and for the mussel in holding its byssus threads, which anchor it to rocks and other substrates, tautly. Upon cholinergic nerve stimulation of the intact ABRM, intracellular calcium rises rapidly and decays to near-resting concentrations [3] (Figure 1(b)). It is at these low calcium concentrations that the catch state ensues, and (in the absence of stimulation) force declines very slowly, over a period of minutes, or even hours. Leads to abrupt relaxation was of interest to us because it might provide a handle on how highly economical force (latch, catch) was maintained and eventually released during relaxation in mammalian as well as invertebrate smooth muscles
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