The structural principles of multidomain organization of the giant polypeptide chain of the muscle titin protein: SAXS/WAXS studies during the stretching of oriented titin fibres

Elasticity of titin is a key parameter that determines the mechanical properties of muscle. These include reversibility, i.e., the muscle’s capacity to change its length many-fold and return to its original state, and the transduction of passive tension generated by the stretched muscle. The morphology and elastic properties of oriented fibres of titin molecules were studied using SAXS and WAXS (small- and wide-angle X-ray scattering, respectively) and mechanical techniques. We succeeded in obtaining oriented filaments of purified titin suitable for diffraction measurements. Our X-ray data suggest a model of titin as a nanoscale, morphological, and aperiodical array of rigid Ig- and Fn3-type domains covalently connected by conformationally variable short loops. The line group symmetry of the model can be defined as SM with axial translation τ∞. Both tension transduction and high elasticity of titin can be explained in terms of crystalline polymer physics. Titin stretching experiments show that each individual titin macromolecule can adopt a novel two-phase state within the fibre. Conversion between high elasticity and strength can be explained as a phase transition under external tension. In the terms of the concept of orientational melting the origin of the functional heterogeneity along the titin strand becomes interpretable.