Twitchin of mollusc smooth muscles can induce “catch”-like properties in human skeletal muscle: support for the assumption that the “catch” state involves twitchin linkages between myofilaments

Abstract

Molluscan catch muscles can maintain tension with low or even no energy utilization, and therefore, they represent ideal models for studying energy-saving holding states. For many decades it was assumed that catch is due to a simple slowing of the force-generating myosin head cross-bridge cycles. However, recently evidences increased suggesting that catch is rather caused by passive structures linking the myofilaments in a phosphorylation-dependent manner. One possible linkage structure is the titin-like thick filament protein twitchin, which could form bridges to the thin filaments. Twitchin is known to regulate the catch state depending on its phosphorylation state. Here, we found that twitchin induces a catch-like stiffness in skinned human skeletal muscle fibres, when these fibres are exposed to this protein. Subsequent phosphorylation of twitchin reduces the stiffness. These findings support the assumption that catch of molluscan smooth muscle involves twitchin linkages between thick and thin filaments.

Cytoskeletal protein kinases: titin and its relations in mechanosensing

“…Similarly, molluscan twitchin kinase is tightly attached to both actin and myosin filaments and seems to be stretch-activated, thereby possibly contributing to the phosphorylation-mediated maintenance of the catch state in response to stretch [5, 15, 16, 34]. Indeed, the simulated unfolding of C. elegans twitchin kinase and initial force spectroscopy data, showed similar patterns as for TK [38, 39].…”

Hysteresis in the production of force by larval Dipteran muscle

“…Although much is known about a few specialized systems, such as mulluscan catch tension (Andruchov et al, 2006), even these systems leave much to be explored. For example, it is known that both pH and cAMP profoundly modulate tension in mulluscan catch fibers but the precise site of this action and the molecular changes it elicits are not yet clear (Avrova et al, 2009). Recent work in Drosophila indicates that force is modulated by several peptides (Hewes et al, 1998;Clark et al, 2008) as well as the biogenic amines tyramine and octopamine (Wanischeck and Rose, 2006).…”

“…Muscle plasticity is of increasing interest across a broad diversity of organisms [Arthropoda (Zill et al, 1992;; Chordata (Herzog and Leonard, 2002;Harrison et al, 2008); Mullusca (Andruchov et al, 2006;Avrova et al, 2009)] with applications spanning biology and engineering (Dorfmann et al, 2008;Lin et al, 2009). We are excited by the prospect of investigating this form of post-synaptic plasticity using the extraordinary tools available with larval Dipteran preparations.…”

“…Hysteretic force can differ by an order of magnitude from predicted force values, and may be either positive or negative in sign, depending upon the addition or omission of nerve impulses, respectively (Burke et al, 1970;Wilson and Larimer, 1968). Positive hysteresis is evident in a diverse collection of organisms inclusive of both vertebrate and invertebrate clades, suggestive of the phenomenon's generality [Chordata (Burke et al, 1970;Harrison et al, 2008;Avrova et al, 2009); Mullusca (Andruchov et al, 2006); Arthropoda Insecta (Blaschko et al, 1931;Zill and Jepson-Innes, 1988;Zill et al, 1992;Dorfmann et al, 2008); Arthropoda Crustacea (Wilson et al, 1970)]. …”

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

“…Catch could be due to passive linkages interconnecting thick filaments with actin filaments. 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).…”