An invertebrate smooth muscle with striated muscle myosin filaments

Abstract

Muscle tissues are classically divided into two major types, depending on the presence or absence of striations. In striated muscles, the actin filaments are anchored at Z-lines and the myosin and actin filaments are in register, whereas in smooth muscles, the actin filaments are attached to dense bodies and the myosin and actin filaments are out of register. The structure of the filaments in smooth muscles is also different from that in striated muscles. Here we have studied the structure of myosin filaments from the smooth muscles of the human parasite Schistosoma mansoni. We find, surprisingly, that they are indistinguishable from those in an arthropod striated muscle. This structural similarity is supported by sequence comparison between the schistosome myosin II heavy chain and known striated muscle myosins. In contrast, the actin filaments of schistosomes are similar to those of smooth muscles, lacking troponin-dependent regulation. We conclude that schistosome muscles are hybrids, containing striated muscle-like myosin filaments and smooth muscle-like actin filaments in a smooth muscle architecture. This surprising finding has broad significance for understanding how muscles are built and how they evolved, and challenges the paradigm that smooth and striated muscles always have distinctly different components.thick filament | muscle structure | muscle contraction | schistosome | Schistosoma mansoni

Conserved Intramolecular Interactions Maintain Myosin Interacting-Heads Motifs Explaining Tarantula Muscle Super-Relaxed State Structural Basis

“…Tables 1 and 2). In the tarantula model, the IHM-interconnecting interactions could only be used to analyze the intermolecular interactions of species exhibiting four helical tracks, like arthropods 5–7, 53 and Platyhelminthes, 12 as these interactions seem to be different in filaments with three 2, 3 or seven 8 helical tracks.

- Interaction “b” : The free head I loop and C loop are close to the blocked head RLC NTE (Fig.

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“…It has been observed by electron microscopy in thick filaments from the striated muscle of arthropods, 5–7 mollusks 8 , the cardiac muscle of vertebrates, 2–4 and the smooth muscle of Platyhelminthes. 12 Electron microscopy has also shown that the motif is present in isolated myosin molecules of intrinsically regulated molecules (like tarantula and Limulus striated muscle and non-muscle myosin IIA) and in unregulated myosins (like skeletal and cardiac muscle). 13 Recently, the motif has been detected on isolated myosin molecules from the smooth muscle of the Cnidarians’ giant sea anemone ( Condylactis gigantea ), 14 but not in isolated myosins from the amoeba Acanthamoeba castellani .…”

Coupling between myosin head conformation and the thick filament backbone structure

“…On the other hand, thick filaments from different muscle types and species are quite variable in structure and composition seemingly having in common only the conformation of their heads in the relaxed state, which is highly conserved in muscle and non-muscle cells (Jung et al, 2008a). Thick filament structures range from short, bipolar types found in non-muscle cells (Scholey et al, 1980), side polar filaments of vertebrate smooth muscle cells (Cooke et al, 1989), bipolar filaments with helically arranged myosin in striated muscle of invertebrates (Pinto et al, 2012; Sulbaran et al, 2015; Woodhead et al, 2013; Woodhead et al, 2005; Zhao et al, 2009) and non-helical, or approximately helical filaments in vertebrates (Zoghbi et al, 2008). …”

“…In the majority of reported thick filament structures (Sulbaran et al, 2015; Woodhead et al, 2013; Woodhead et al, 2005; Zhao et al, 2009; Zoghbi et al, 2008), the IHM folds back onto the rod so that the blocked head contacts its own S2 domain (Fig. 1C).…”

“…1C) (Woodhead et al, 2005). Since then, it has been found in all relaxed thick filament structures investigated (Al-Khayat et al, 2013; Pinto et al, 2012; Sulbaran et al, 2015; Woodhead et al, 2013; Zhao et al, 2009), usually in an orientation in which the IHM is approximately tangential to the surface of the filament backbone with the blocked head contacting the S2 fragment of the myosin rod. More recently and surprisingly, the IHM was found to characterize the relaxed thick filament structure from Lethocerus asynchronous flight muscle (Hu et al, 2016) but in what is so far a unique orientation; it is almost perpendicular to the filament backbone (Fig.…”