Molecular basis for elastic energy storage in mineralized tendon

Animals store elastic energy in leg and foot tendons during locomotion. In the turkey, much of the locomotive force generated by the gastrocnemius muscle is stored as elastic energy during tendon deformation. Little energy storage occurs within the muscle. During growth of some avians, including the turkey, leg tendons mineralize in the portions distal to the attached muscle and show increased tensile strength and modulus as a result. The purpose of this study is to test the hypothesis that the degree of elastic energy storage in mineralizing turkey tendon is directly related to the tendon mineral content. To test this hypothesis, the stress-strain behavior of tendons was separated into elastic and viscous components. Both the elastic spring constant and the elastic energy stored, calculated up to a strain of 20%, were found to be proportional to tendon mineral content. It is concluded that mineralization is an efficient means for increasing the amount of elastic energy storage that is required for increased load-bearing ability needed for locomotion of adult birds. Examination of molecular models of the hole region, where mineralization is initiated within the collagen fibril, leads to the hypothesis that elastic energy is stored in the tendon by direct stretching of the flexible regions. Flexible regions within the collagen molecule fall within the positively stained bands of the collagen D period. It is proposed that mineralization increases the stored elastic energy by preventing flexible regions within the positively stained bands from stretching. These observations suggest that mineralization begins in the hole region due to the large number of charged amino acid residues found in the d and e bands.