A Drosophila cardiac myosin increases jump muscle stretch activation and shortening deactivation.

Abstract

Stretch activation (SA), a delayed increase in force production after rapid muscle lengthening, is critical to the function of vertebrate cardiac muscle and insect asynchronous indirect flight muscle. SA enables or increases power generation in muscle types used in a cyclical manner. Recently, myosin isoform expression has been implicated as a mechanism for varying the amplitude of SA in some muscle types. For instance, we found that expressing a larval Drosophila myosin isoform in a muscle type with minimal SA, the Drosophila jump muscle, substantially increased SA amplitude and enabled positive cyclical power generation. To test whether other myosin isoforms could increase SA amplitude and whether the Drosophila heart benefits from SA, we identified two Drosophila cardiac myosin isoforms, CardM1 and CardM2, and expressed them in Drosophila jump muscle. CardM1, CardM2, and control jump muscle fibers all displayed the characteristic phase 3 of SA, with CardM2 SA amplitude ∼60% greater than that of CardM1 and control fibers. Increasing [P_i] from 0 to 16 mM increased CardM2 SA tension amplitude by 74%, yet had minimal or no effect on CardM1 or control muscle SA amplitude. CardM2 displayed the most prominent phase 3 dip when we induced shortening deactivation, a delayed decrease in force after muscle shortening. The magnitude of CardM2 shortening deactivation tension was ∼50% greater than control or CardM1 fibers. This, along with its greater stretch-activated tension, caused CardM2 to be the only isoform to produce positive power when its fiber length was sinusoidally oscillated. The results support our hypotheses that some myosin isoforms enable greater SA tension levels and suggest that the Drosophila heart is benefiting from SA and shortening deactivation in a manner similar to vertebrate hearts.