Abstract

Both insect flight muscle and cardiac muscle contract rhythmically, but the way in which repetitive contractions are controlled is different in the two types of muscle. We have compared the flight muscle of the water bug, Lethocerus, with cardiac muscle. Both have relatively high resting elasticity and are activated by an increase in sarcomere length or a quick stretch. The larger response of flight muscle is attributed to the highly ordered lattice of thick and thin filaments and to an isoform of troponin C that has no exchangeable Ca2+-binding site. The Ca2+ sensitivity of cardiac muscle and flight muscle can be manipulated so that cardiac muscle responds to Ca2+ like flight muscle, and flight muscle responds like cardiac muscle, showing the malleability of regulation. The interactions of the subunits in flight muscle troponin are described; a model of the complex, using the structure of cardiac troponin as a template, shows an overall similarity of cardiac and flight muscle troponin complexes. The dual regulation by thick and thin filaments in skeletal and cardiac muscle is thought to operate in flight muscle. The structure of inhibited myosin heads folded back on the thick filament in relaxed Lethocerus fibres has not been seen in other species and may be an adaptation to the rapid contractions of flight muscle. A scheme for regulation by thick and thin filaments during oscillatory contraction is described. Cardiac and flight muscle have much in common, but the differing mechanical requirements mean that regulation by both thick and thin filaments is adapted to the particular muscle.

Highlights

  • Robert Hooke (1665) observed the high frequency oscillations of the haltere in Diptera and recognised their importance in keeping insects with high wing beat frequency in balance during flight (Fig. 1)

  • indirect flight muscle (IFM) is restricted by the requirement for nearly constant contraction frequency, which is determined by the resonant properties of the thorax, including the muscles

  • The structure of the IFM is adapted to this requirement: matching periodicities of actin, Tn and target zones on the thin filament, as well as the arrangement of crowns on the thick filament, favour rapid controlled interaction between myosin and actin

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Summary

Introduction

Robert Hooke (1665) observed the high frequency oscillations of the haltere in Diptera and recognised their importance in keeping insects with high wing beat frequency in balance during flight (Fig. 1). Myosin-binding protein C (MyBP-C) affects the activation state of both thick and thin filaments in skeletal and cardiac muscle.

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