(see also "Several Insights into muscle contraction mechanism" part 1 and 2)
For many years, the contractile material in striated muscle was generally supposed to be in the form of continuous filaments which shorten by some kind of folding or coiling.
The continuous-filament view was upset after the discovery of thick and thin filaments (Huxley & Niedergerke, 1954; Huxley & Hanson, 1954) and replaced by the theory of filament discontinuity, which made unimportant even the problem of the existence of a continuous noncontractile material in sarcomere.
Nevertheless, it is almost impossible to account for how the thin filaments can preserve a quasi-rectilineal arrangement in sarcomere, in spite of their great flexibility (Tonomura & Oosawa, 1972), without assuming that their free ends are anchored to the Z line at the opposite end of the sarcomere by some continuous elastic structure.
Furthermore, it is a known fact that a muscle can be stretched so far that the overlap of filaments disappears and a gap occurs between the ends of thick and thin filaments. After cessation of the stretch, muscle fibres are, however, able to regain their initial length together with their contractile properties (Umazume & Fujime, 1975). This means that when the muscle is shortened again, thin filaments do not bend or fold on their coming in contact with the lattice of thick filaments, but penetrate into it, occupying the proper positions, and interdigitate in the same highly ordered manner as before the stretch.
All these facts are difficult to explain using a hypothesis based only on the electrostatic charge of the filaments (Elliott, Rome & Spencer, 1970; Noble & Pollack, 1977). A long range of electrostatic field seems not to be present in a region abundant in ions (Huxley, 1974) and besides this, even if such a field exists, the thin filaments must preserve the same spatial ordered array as previous to the overstretch, before electrostatic interactions begin to act for reinserting them into the thick filament lattice, i.e. each thin filament must reoccupy the same position and be able to be surrounded by the same three thick filaments, which is quite improbable. Any other theory of muscle contraction, including the cross bridge theory, also fails to explain this mechanism satisfactorily.
More probably the thin filaments are guided by “ropes” or “threads” connecting their ends to the Z line at the opposite end of the sarcomere. Some experimental data on tortoise skeletal muscle (Page, 1968) may be accounted for only by supposing that continuous, homogeneous and elastic structures binding the terminals of thin filaments to the opposite Z line do really exist in sarcomere.
The fine structure of tortoise skeletal muscle reveals the presence of two dark lines within the I band on either side of the Z line, known as the N lines, which have also been described in other electron microscope studies of muscle (Bennet & Porter, 1953; Bennet, 1956; Locker & Leet, 1976) presumably corresponding to the N lines (Nebenscheiben) observed in insect muscles by the early light microscopists.
The most striking characteristic of the N line is the manner in which its position within the I band varies with the sarcomere length. As the sarcomere shortens from very stretched lengths the distance between the N and Z lines proportionally diminishes, although not in such a way as the relative position of the N line within either the half of I band or the half of sarcomere be constant (Fig. 1).
When the distance between the N lines becomes equal to the A band width (1,6 µm), it remains constant as if the lattice of the thick filaments hinders the material which forms the N line to move further towards the centre of the sarcomere. It is a known fact that, in passive shortening, the sliding motion of filaments does not go beyond (and may not even reach) the point where thin filaments meet at the centre of the sarcomere (Brown, González-Serratos & Huxley, 1970).
The appearance of regions with greater electron density realizing a so called N line does not permit identification of the nature of the structure which these regions are supposed to be associated to. It is obvious that the N line is not associated to thin filaments because their lengths are known to remain constant during the variation of sarcomere length.
The N line behaves as a homothetic centre for the distance between the free ends of thin filaments and the Z line at the opposite end of the sarcomere, namely the N line, divides this distance into two segments whose ratio is constant (0.30) no matter what the length of sarcomere. But the N line is not a homothetic centre for other distances in sarcomere, e.g. for the distance between Z lines (Z-Z distance) or between the Z line and the ends of thick filaments (Z -thick filament distance) (Table 1).
Values of the ratios of segment lengths into which N line divides, at diferent sarcomere lengths, (a) the distance between Z line and the ends of thin filaments of the opposite half of the sarcomere (ZN/N-thin filament), (b) the distance between Z line and the ends of thick filaments (ZN/N-thick filament), (c) the distance between the two Z lines of the sarcomere (ZN/NZ). Calculation was performed on the assumption that in tortoise skeletal muscle the length of the thin filament is 1,175 µm and the length of the thick filament is l,6 µm (Page, 1968)
The longitudinal structures which might exist in the sarcomere besides the thin and thick filaments, and possibly interconnecting with them in providing continuity of the sarcomere structure, could have the following variants only:
1.Structures spanning from the Z line to the ends of thin filaments in the opposite half of the sarcomere (which seem not to have been mentioned in the literature till now) (Z-thin filament structure).
2. Structures connecting the Z line with the ends of the thick filaments (identified as thick filament extensions in invertebrate flight muscle, but not in vertebrate muscle (Ullrick et al., 1977) (Z-thick filament structure).
3. Structures connecting the two Z lines (identified as superthin T filaments (Hoyle, 1968) (Z-Z structures).
4. Structures connecting the terminals of thin filaments (S-filaments of Huxley & Hanson, 1954), which are unlikely to exist as they would hinder the sliding of filaments in extreme shortening of muscle; the N line cannot associate to them (thin filament-thin filament structures) (Fig. 2).
The constant value of the ratio ZN/ N-thin filament (Table 1) shows that the N line may be associated to Z-thin filament structures and provides evidence for their existence. That N line seems to be associated to Z-thin filament structures is graphically illustrated in Fig. 3.
The existence of Z-thin filament structures in tortoise skeletal muscle is therefore suggested by the presence and the characteristics of N lines which behave as a natural “marker” for them. In other contractile tissues where the N line cannot be observed, the existence of the Z-thin filament structures is only probable but not impossible. It is noteworthy that the UV-absorbing lines observed by Lännergren in frog and snake stretched fibres are seen at about the same position in the I band as that where the N lines occur in tortoise muscle fibres and also that the separation between these UVabsorbing lines increases with increasing sarcomere length (Lănnergren, 1977). At the same time, presence of the N line in tortoise muscle does not suggest, but does not rule out, the existence of some other continuous elastic structures in the sarcomere.
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