Comprehensive Physiology Wiley Online Library
For Librarians For Authors Editors About

Physiology of Insect Flight Muscle

Richard T. Tregear

10.1002/cphy.cp100116

Source: Supplement 27: Handbook of Physiology, Skeletal Muscle

Originally published: 1983

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Design Parameters
1.1 Contraction Timing
1.2 Contraction Extent and Speed
1.3 Energy Storage
1.4 Energy Transduction
1.5 Interactions Between Factors
2 Flight Muscle Preparations
2.1 Intact Muscles
2.2 Demembranated Muscle
3 Oscillatory Response of Asynchronous Muscle
3.1 Full Mechanical Performance
3.2 Specification of the Mechanical Response
3.3 Simulation of the Mechanical Response
4 Myofibrillar Proteins
4.1 Proteins of the Thick Filament
4.2 Proteins of the Thin Filament
4.3 Z‐Line Proteins
4.4 Connecting Proteins
5 Macromolecular Assembly
5.1 Thick‐Filament Connections
5.2 Thick‐Filament Structure
5.3 Cross‐Bridge Interaction
6 Cause of Stretch Activation
6.1 Calcium Binding
6.2 Filament Match
6.3 Filament Strain
6.4 Evolution of Stretch Activation
7 Cross‐Bridge Mechanism
7.1 Mechanical Transients
7.2 Steady‐State Intermediates
7.3 Equilibrium States
8 Conclusions
Figure 1. Figure 1.

Schematic representation of evolutionary distribution of asynchronous flight muscles (shaded areas) within the order Hemiptera. Note that Aphidae and Psyllidae probably separated before asynchrony evolved and that fibrillar muscle also appears in the sound‐producing mechanism of certain Cicadidae.

Adapted from Cullen 33
Figure 2. Figure 2.

Methods of investigating mechanism of asynchronous muscle. A: operation in vivo: muscle pulls rhythmically on the thorax elastic cuticle and the distortion moves the wings up and down 87. B: same muscle detached from the thorax and attached to position sensor (S) that drives the vibrator (P) to resist motion in the muscle. By adjustment of the amplifier (A) characteristics the mechanical system can simulate any desired elasticity, viscosity, and inertia. Motor nerve to muscle is stimulated electrically, and when artificial viscosity is low the system vibrates in “free oscillation” 65. C: same muscle during driven oscillation. Position drive from S to P is adjusted to strongly resist any movement unless a further electrical signal is injected into P, when the fixed point of the system changes. Sinusoidal oscillation applied to amplifier (A) therefore imposes a sinusoidal length change on the muscle independent of the tension within it 66. D: demembranated muscle in an apparatus similar to that shown in C.

Adapted from Tregear 124
Figure 3. Figure 3.

A: relation between power output and ATPase in a bundle of demembranated oscillating Lethocerus flight muscle fibers. Effect of varying frequency of applied vibration is shown. B: linear relation between stiffness and tension during development of activation in isometric demembranated Lethocerus fibers. Activation by calcium (▪) or stretch (□). Relation between stiffness and tension extrapolates close to stiffness of muscle in relaxation (•). Stiffness was measured from tension change occurring during application of rapid change in length. [A, adapted from Steiger and Rüegg 118. B, adapted from White et al. 140.]
Figure 4. Figure 4.

Form of Lethocerus flight muscle mechanical response. A: tension response to abrupt stretch and release by 0.1% of muscle length. Note near‐exponential rise and fall of delayed tension after stretch and release. B: tension response (lower record) to a forced sinusoidal vibration of muscle (upper record). Response is specified by its gain (Go = R/ΔL) and phase (ϕ). At this frequency (5 Hz) muscle tension lagged behind length (L); thus ϕ was negative and work was done by muscle on apparatus.

Adapted from Tregear 124
Figure 5. Figure 5.

Search for linearity in mechanical response. Response of single Lethocerus flight muscle fiber to vibration of amplitude 0.02% (▵), 0.04% (▵), 0.8% (□), or 0.14% (▪). In these experiments the various Fourier components of mechanical response were separated. A: total distortion (d = Σi‐1n); summated gain of all except fundamental component. B: phase angle of fundamental component. C: gain of fundamental component (Go). All data are plotted against frequency of forced vibration. Note low values of A and constancy of B and C with amplitude at lowest values of this parameter, indicating linearity of muscle response.

Adapted from Cuminetti and Rossmanith 35
Figure 6. Figure 6.

Cross‐bridge models of mechanical response. A, actin; M, myosin; AM, actomyocin. A: 2‐state model. Attachment rate constant (f) is assumed to be proportional to muscle extension and detachment rate constant (g) to be independent of extension. Rate constant of delayed tension, r = f + g, and tension cost, c ∝ g. B: 4‐state model. Reactions 1 and 3 are rapid equilibria; reaction 4 is relatively slow and irreversible. [A, adapted from Thorson and White 120. B, adapted from Steiger and Abbott 117.]
Figure 7. Figure 7.

Diagrams illustrating interdigitation of filament lattices of adjacent sarcomeres within Z line. A: interdigitation of I filaments. B: superimposition of complete filament lattices of 2 sarcomeres. Open circles represent filaments from 1 sarcomere, closed circles from the next. Smaller circles represent I filaments, whose formation of hexagonal groups within Z line is indicated. Larger circles represent A filaments, whose relative position in their hypothetical extension into the Z line is thus illustrated.

Adapted from Ashhurst 12
Figure 8. Figure 8.

Diagram illustrating possible filament match in Lethocerus flight muscle. All diagrams are radial projections centered on axis of a single thick filament. A: actin envelope about 1 thick filament. Each thin filament is represented by vertical double line, and solid bars represent regions of thin filaments accessible to cross‐bridge attachment. B: lattice of cross‐bridge origins on thick‐filament surface. Each circle represents a single myosin molecule, bearing 2 potential cross bridges. C, D: extreme mismatch and match positions of arrays shown in A and B. The 2 diagrams differ only in vertical shift of A vs. B.

Adapted from Wray 146
Figure 9. Figure 9.

Pattern of cross‐bridge attachment to thin filaments of Lethocerus flight muscle in rigor (absence of nucleotide). A: thin longitudinal section of overlap zone through a plane connecting thin and thick filaments (cf. Fig. 7). Note angled chevrons crossing interfilament gap at 38‐nm intervals. Many of these chevrons appear double. (Original micrograph supplied by Dr. M. K. Reedy.) B: explanation of double‐chevron formation by restriction of rotation and axial range of the cross bridges. 1, Subunit azimuthal orientation of actin (øA) defined relative to interfilament axis; 2, axial displacement of cross bridge (R) at its contact with actin; 3, cross‐bridge attachment arrays for different degrees of rotational and axial freedom (cases b and f resemble Reedy's observations). C: explanation of double‐chevron formation by attachment of the 2 heads of 1 myosin molecule to adjacent thin filaments. 1, Angles of actin helix at which 2‐filament attachment is expected; 2, resultant longitudinal cross‐bridge array. [B, adapted from Haselgrove and Reedy 47. C, adapted from Offer and Elliott 85.]
Figure 10. Figure 10.

X‐ray diffraction from Lethocerus flight muscle in different steady‐state or equilibrium conditions. Intensities of various lattice‐sampled diffraction reflections are given as percentage of a particular reflection (4, 1 of the equator) in rigor. A: 2 major inner equatorial reflections that depend on movement of cross bridges between filaments. B: 14‐nm meridional reflection that arises from regularity of cross bridges on thick filament. C: 38‐nm layer‐line reflections. Most of the intensity of these reflections arises from regular attachment of cross bridges to thin filaments. The 2, 0 reflection is an exception; it is prohibited from the cross‐bridge attachment lattice by phase cancelation 51.

Adapted from Tregear et al. 126


Figure 1.

Schematic representation of evolutionary distribution of asynchronous flight muscles (shaded areas) within the order Hemiptera. Note that Aphidae and Psyllidae probably separated before asynchrony evolved and that fibrillar muscle also appears in the sound‐producing mechanism of certain Cicadidae.

Adapted from Cullen 33


Figure 2.

Methods of investigating mechanism of asynchronous muscle. A: operation in vivo: muscle pulls rhythmically on the thorax elastic cuticle and the distortion moves the wings up and down 87. B: same muscle detached from the thorax and attached to position sensor (S) that drives the vibrator (P) to resist motion in the muscle. By adjustment of the amplifier (A) characteristics the mechanical system can simulate any desired elasticity, viscosity, and inertia. Motor nerve to muscle is stimulated electrically, and when artificial viscosity is low the system vibrates in “free oscillation” 65. C: same muscle during driven oscillation. Position drive from S to P is adjusted to strongly resist any movement unless a further electrical signal is injected into P, when the fixed point of the system changes. Sinusoidal oscillation applied to amplifier (A) therefore imposes a sinusoidal length change on the muscle independent of the tension within it 66. D: demembranated muscle in an apparatus similar to that shown in C.

Adapted from Tregear 124


Figure 3.

A: relation between power output and ATPase in a bundle of demembranated oscillating Lethocerus flight muscle fibers. Effect of varying frequency of applied vibration is shown. B: linear relation between stiffness and tension during development of activation in isometric demembranated Lethocerus fibers. Activation by calcium (▪) or stretch (□). Relation between stiffness and tension extrapolates close to stiffness of muscle in relaxation (•). Stiffness was measured from tension change occurring during application of rapid change in length. [A, adapted from Steiger and Rüegg 118. B, adapted from White et al. 140.]



Figure 4.

Form of Lethocerus flight muscle mechanical response. A: tension response to abrupt stretch and release by 0.1% of muscle length. Note near‐exponential rise and fall of delayed tension after stretch and release. B: tension response (lower record) to a forced sinusoidal vibration of muscle (upper record). Response is specified by its gain (Go = R/ΔL) and phase (ϕ). At this frequency (5 Hz) muscle tension lagged behind length (L); thus ϕ was negative and work was done by muscle on apparatus.

Adapted from Tregear 124


Figure 5.

Search for linearity in mechanical response. Response of single Lethocerus flight muscle fiber to vibration of amplitude 0.02% (▵), 0.04% (▵), 0.8% (□), or 0.14% (▪). In these experiments the various Fourier components of mechanical response were separated. A: total distortion (d = Σi‐1n); summated gain of all except fundamental component. B: phase angle of fundamental component. C: gain of fundamental component (Go). All data are plotted against frequency of forced vibration. Note low values of A and constancy of B and C with amplitude at lowest values of this parameter, indicating linearity of muscle response.

Adapted from Cuminetti and Rossmanith 35


Figure 6.

Cross‐bridge models of mechanical response. A, actin; M, myosin; AM, actomyocin. A: 2‐state model. Attachment rate constant (f) is assumed to be proportional to muscle extension and detachment rate constant (g) to be independent of extension. Rate constant of delayed tension, r = f + g, and tension cost, c ∝ g. B: 4‐state model. Reactions 1 and 3 are rapid equilibria; reaction 4 is relatively slow and irreversible. [A, adapted from Thorson and White 120. B, adapted from Steiger and Abbott 117.]



Figure 7.

Diagrams illustrating interdigitation of filament lattices of adjacent sarcomeres within Z line. A: interdigitation of I filaments. B: superimposition of complete filament lattices of 2 sarcomeres. Open circles represent filaments from 1 sarcomere, closed circles from the next. Smaller circles represent I filaments, whose formation of hexagonal groups within Z line is indicated. Larger circles represent A filaments, whose relative position in their hypothetical extension into the Z line is thus illustrated.

Adapted from Ashhurst 12


Figure 8.

Diagram illustrating possible filament match in Lethocerus flight muscle. All diagrams are radial projections centered on axis of a single thick filament. A: actin envelope about 1 thick filament. Each thin filament is represented by vertical double line, and solid bars represent regions of thin filaments accessible to cross‐bridge attachment. B: lattice of cross‐bridge origins on thick‐filament surface. Each circle represents a single myosin molecule, bearing 2 potential cross bridges. C, D: extreme mismatch and match positions of arrays shown in A and B. The 2 diagrams differ only in vertical shift of A vs. B.

Adapted from Wray 146


Figure 9.

Pattern of cross‐bridge attachment to thin filaments of Lethocerus flight muscle in rigor (absence of nucleotide). A: thin longitudinal section of overlap zone through a plane connecting thin and thick filaments (cf. Fig. 7). Note angled chevrons crossing interfilament gap at 38‐nm intervals. Many of these chevrons appear double. (Original micrograph supplied by Dr. M. K. Reedy.) B: explanation of double‐chevron formation by restriction of rotation and axial range of the cross bridges. 1, Subunit azimuthal orientation of actin (øA) defined relative to interfilament axis; 2, axial displacement of cross bridge (R) at its contact with actin; 3, cross‐bridge attachment arrays for different degrees of rotational and axial freedom (cases b and f resemble Reedy's observations). C: explanation of double‐chevron formation by attachment of the 2 heads of 1 myosin molecule to adjacent thin filaments. 1, Angles of actin helix at which 2‐filament attachment is expected; 2, resultant longitudinal cross‐bridge array. [B, adapted from Haselgrove and Reedy 47. C, adapted from Offer and Elliott 85.]



Figure 10.

X‐ray diffraction from Lethocerus flight muscle in different steady‐state or equilibrium conditions. Intensities of various lattice‐sampled diffraction reflections are given as percentage of a particular reflection (4, 1 of the equator) in rigor. A: 2 major inner equatorial reflections that depend on movement of cross bridges between filaments. B: 14‐nm meridional reflection that arises from regularity of cross bridges on thick filament. C: 38‐nm layer‐line reflections. Most of the intensity of these reflections arises from regular attachment of cross bridges to thin filaments. The 2, 0 reflection is an exception; it is prohibited from the cross‐bridge attachment lattice by phase cancelation 51.

Adapted from Tregear et al. 126
References
 1. Abbott, R. H. The effects of fibre length and calcium ion concentration on the dynamic response of glycerol‐extracted insect fibrillar muscle. J. Physiol. London 231: 195–208, 1973.
 2. Abbott, R. H., and P. E. Cage. Periodicity in insect flight muscle stretch activation. J. Physiol. London 289: 32P–33P, 1979.
 3. Abbott, R. H., and R. A. Chaplain. Preparation and properties of the contractile element of insect fibrillar muscle. J. Cell Sci. 1: 311–330, 1966.
 4. Abbott, R. H., and H. G. Mannherz. Activation by ADP and the correlation between tension and ATPase activity in insect fibrillar muscle. Pfluegers Arch. 321: 223–232, 1970.
 5. Abbott, R. H., and G. J. Steiger. Temperature and amplitude dependence of tension transients in glycerinated skeletal and insect fibrillar muscle. J. Physiol. London 266: 13–42, 1977.
 6. Aidley, D. J., and D. C. S. White. Mechanical properties of glycerinated fibres from the tymbal muscles of a Brazilian cicada. J. Physiol. London 205: 179–192, 1969.
 7. Armitage, P. M., R. T. Tregear, and A. Miller. Effect of activation by calcium on the X‐ray diffraction pattern from insect flight muscle. J. Mol. Biol. 92: 39–53, 1975.
 8. Ashhurst, D. E. The fibrillar flight muscles of giant waterbugs: an electron‐microscope study. J. Cell Sci. 2: 435–444, 1967.
 9. Ashhurst, D. E. Z‐line of the flight muscle of belostomatid water bugs. J. Mol. Biol. 27: 385–389, 1967.
 10. Ashhurst, D. E. The effect of glycerination on the fibrillar flight muscles of Belostomatid waterbugs. Z. Zellforsch. Mikrosk. Anat. 93: 36–44, 1969.
 11. Ashhurst, D. E. The Z‐line in insect flight muscle. J. Mol. Biol. 55: 283–285, 1971.
 12. Ashhurst, D. E. The Z‐line: its structure and evidence for the presence of connecting filaments. In: Insect Flight Muscle, edited by R. T. Tregear. Amsterdam: North‐Holland, 1977, p. 57–73.
 13. Barrington‐Leigh, J., R. S. Goody, W. Hofmann, K. Holmes, H. G. Mannherz, G. Rosenbaum, and R. T. Tregear. The interpretation of X‐ray diffraction from glycerinated flight muscle fibre bundles: new theoretical and experimental approaches. In: Insect Flight Muscle, edited by R. T. Tregear. Amsterdam: North‐Holland, 1977, p. 137–146.
 14. Barrington‐Leigh, J., K. C. Holmes, H. G. Mannherz, G. Rosenbaum, F. Eckstein, and R. Goody. Effects of ATP analogs on the low‐angle X‐ray diffraction pattern of insect flight muscle. Cold Spring Harbor Symp. Quant. Biol. 37: 443–448, 1973.
 15. Beinbrech, G. Electron micrography of Lethocerus muscle in the presence of nucleotides. In: Insect Flight Muscle, edited by R. T. Tregear. Amsterdam: North‐Holland, 1977, p. 147–160.
 16. Boettiger, E. G. The machinery of insect flight. In: Recent Advances in Invertebrate Physiology, edited by B. T. Scheer. Eugene: Univ. of Oregon Press, 1957, p. 117–142.
 17. Borejdo, J., and A. Oplatka. Heavy meromyosin cross‐links thin filaments in striated muscle myofibrils. Nature London 291: 322–323, 1981.
 18. Buchthal, F., and T. Weis‐Fogh. Contribution of the sarcolemma to the force exerted by resting muscle of insects. Acta Physiol. Scand. 35: 345–364, 1956.
 19. Buchthal, F., T. Weis‐Fogh, and P. Rosenfalck. Twitch contractions of isolated flight muscle of locusts. Acta Physiol. Scand. 39: 246–276, 1957.
 20. Bullard, B., J. L. Bell, R. Craig, and K. Leonard. An actinlike protein from insect muscle. J. Muscle Res. Cell Motil. 1: 194–195, 1980.
 21. Bullard, B., J. L. Bell, and B. M. Luke. Immunological investigation of proteins associated with thick filaments of insect flight muscle. In: Insect Flight Muscle, edited by R. T. Tregear. Amsterdam: North‐Holland, 1977, p. 41–52.
 22. Bullard, B., R. Dabrowska, and L. Winkelman. The contractile and regulatory proteins of insect flight muscle. Biochem. J. 135: 277–286, 1973.
 23. Bullard, B., K. S. Hammond, and B. M. Luke. The site of paramyosin in insect flight muscle and the presence of an unidentified protein between myosin filaments and Z‐line. J. Mol. Biol. 115: 417–440, 1977.
 24. Bullard, B., B. M. Luke, and L. Winkelman. The paramyosin of insect flight muscle. J. Mol. Biol. 75: 359–367, 1973.
 25. Bullard, B., J. W. S. Pringle, and G. M. Sainsbury. Localization of a new protein in the Z‐discs of insect flight and vertebrate striated muscle. J. Physiol. London 317: 25P–26P, 1981.
 26. Bullard, B., and M. K. Reedy. How many myosins per cross‐bridge? II. Flight muscle myosin from the blowfly, Sarcophaga bullata. Cold Spring Harbor Symp. Quant. Biol. 37: 423–428, 1973.
 27. Bullard, B., and G. M. Sainsbury. The proteins in the Z‐line of insect flight muscle. Biochem. J. 161: 399–403, 1977.
 28. Chaplain, R. A. The effect of Ca2+ and fibre elongation on the activation of the contractile mechanism of insect fibrillar flight muscle. Biochim. Biophys. Acta 131: 385–392, 1967.
 29. Chaplain, R. A. Changes of adenosine triphosphatase activity and tension with fibre elongation in glycerinated insect fibrillar flight muscle. Pfluegers Arch. 307: 120–126, 1969.
 30. Clarke, M. L., and R. T. Tregear. Supercooling as a method for storing glycerol‐extracted muscle fibres. J. Physiol. London 308: 104–105, 1980.
 31. Close, R. I. Dynamic properties of mammalian skeletal muscles. Physiol. Rev. 52: 129–197, 1972.
 32. Cloupeau, M., J. F. Devilliers, and D. Devezeaux. Direct measurements of instantaneous lift in desert locust; comparison with Jensen's experiments on detached wings. J. Exp. Biol. 80: 1–15, 1979.
 33. Cullen, M. J. The distribution of asynchronous muscle in insects with particular reference to the Hemiptera: an electron microscope study. J. Entomol. Ser. A 49: 17–41, 1974.
 34. Cullen, M. J. The breeding of giant waterbugs in the laboratory. In: Insect Flight Muscle, edited by R. T. Tregear. Amsterdam: North‐Holland, 1977, p. 357–366.
 35. Cuminetti, R., and A. Rossmanith. Small amplitude non‐linearities in the mechanical response of an asynchronous flight muscle. J. Muscle Res. Cell Motil. 1: 345–356, 1980.
 36. Danzer, A. The flight mechanism of Diptera considered as a resonant system. Z. Vgl. Physiol. 38: 259–283, 1956.
 37. Ford, L. E., A. F. Huxley, and R. M. Simmons. The relation between stiffness and filament overlap in stimulated frog muscle fibres. J. Physiol. London 311: 219–249, 1981.
 38. Freundlich, A., P. K. Luther, and J. M. Squire. High‐voltage electron microscopy of crossbridge interactions in striated muscle. J. Muscle Res. Cell Motil. 1: 321–343, 1980.
 39. Garamvolgyi, N. The arrangement of myofilaments in insect flight muscle. J. Ultrastruct. Res. 13: 409–424, 1965.
 40. Garamvolgyi, N. The structural basis of the elastic properties in the flight muscle of the bee. J. Ultrastruct. Res. 27: 462–471, 1969.
 41. Goll, D. E., M. H. Stromer, R. M. Robson, B. M. Luke, and K. S. Hammond. Extraction, purification, and localization of α‐actinin from asynchronous insect flight muscle. In: Insect Flight Muscle, edited by R. T. Tregear. Amsterdam: North‐Holland, 1977, p. 15–40.
 42. Goody, R. S., J. Barrington‐Leigh, H. G. Mannherz, R. T. Tregear, and G. Rosenbaum. X‐ray titration of binding of β,γ‐imido‐ATP to myosin in insect flight muscle. Nature London 262: 613–615, 1976.
 43. Griffiths, P. J., K. Guth, H. J. Kuhn, and J. C. Rüegg. Cross bridge slippage in skinned frog muscle fibres. Biophys. Struct. Mech. 7: 107–124, 1980.
 44. Griffiths, P. J., H. J. Kuhn, and J. C. Rüegg. Activation of the contractile system of insect fibrillar muscle at very low concentrations of Mg2+ and Ca2+. Pfluegers Arch. 382: 155–163, 1979.
 45. Guth, K., H. J. Kuhn, B. Drexler, W. Berberich, and J. C. Rüegg. Stiffness and tension during and after sudden length changes of glycerinated single insect fibrillar muscle fibres. Biophys. Struct. Mech. 5: 255–276, 1979.
 46. Hammond, K. S., and D. E. Goll. Purification of insect myosin and α‐actinin. Biochem. J. 151: 189–192, 1975.
 47. Haselgrove, J. C., and M. K. Reedy. Modeling rigor cross‐bridge patterns in muscle. I. Initial studies of the rigor lattice of insect flight muscle. Biophys. J. 24: 713–728, 1978.
 48. Heinrich, B. Temperature regulation of the sphinx moth. J. Exp. Biol. 54: 141–152, 1971.
 49. Heinrich, B., and G. A. Bartholomew. An analysis of pre‐flight warm‐up in the sphinx moth. J. Exp. Biol. 55: 223–239, 1971.
 50. Herzig, J. W. A model of stretch activation based on stiffness measurements in glycerol extracted insect fibrillar muscle. In: Insect Flight Muscle, edited by R. T. Tregear. Amsterdam: North‐Holland, 1977, p. 209–219.
 51. Holmes, K. C., R. T. Tregear, and J. Barrington‐Leigh. Interpretation of the low angle X‐ray diffraction from insect flight muscle in rigor. Proc. R. Soc. London Ser. B 207: 13–33, 1980.
 52. Huxley, A. F., and R. M. Simmons. Proposed mechanism of force generation in muscle. Nature London 233: 533–538, 1971.
 53. Huxley, H. E., R. M. Simmons, A. R. Faruqi, M. Kress, J. Bordas, and M. H. J. Koch. Millisecond time‐resolved changes in X‐ray reflections from contracting muscle during rapid mechanical transients, recorded using synchrotron radiation. Proc. Natl. Acad. Sci. USA 78: 2297–2301, 1981.
 54. Jensen, M. The aerodynamics of locust flight. Philos. Trans. R. Soc. London Ser. B 239: 511–552, 1956.
 55. Jensen, M., and T. Weis‐Fogh. The physics of locust cuticle. Philos. Trans. R. Soc. London Ser. B 245: 137–169, 1962.
 56. Jewell, B. R., and J. C. Rüegg. Oscillatory contraction of insect fibrillar muscle after glycerol‐extraction. Proc. R. Soc. London Ser. B 164: 429–459, 1966.
 57. Kuhn, H. J. Transformation of chemical into mechanical energy by glycerol‐extracted fibres of insect flight muscles in the absence of nucleosidetriphosphate‐hydrolysis. Experientia 29: 1086–1088, 1973.
 58. Kuhn, H. J. Reversible transformation of mechanical work into chemical free energy by stretch dependent binding of AMP‐PNP in glycerinated fibrillar muscle fibres. In: Insect Flight Muscle, edited by R. T. Tregear. Amsterdam: North‐Holland, 1977, p. 307–315.
 59. Kuhn, H. J. Cross bridge slippage induced by the ATP analogue AMPPNP and stretch in glycerol‐extracted fibrillar muscle fibres. Biophys. Struct. Mech. 4: 159–168, 1978.
 60. Kuhn, H. J. The mechanochemistry of force production in muscle. J. Muscle Res. Cell Motil. 2: 7–44, 1981.
 61. Kuhn, H. J., K. Guth, B. Drexler, W. Berberich, and J. C. Rüegg. Investigation of the temperature dependence of the cross bridge parameters for attachment, force generation and detachment as deduced from mechano‐chemical studies in glycerinated single fibres from the dorsal longitudinal muscle of Lethocerus maximus. Biophys. Struct. Mech. 6: 1–29, 1979.
 62. Lehman, W., B. Bullard, and K. Hammond. Calcium‐dependent myosin from insect flight muscles. J. Gen. Physiol. 63: 553–563, 1974.
 63. Loxdale, H. D. A method for the continuous assay of picomole quantities of ADP released from glycerol‐extracted skeletal muscle fibres on MgATP activation. J. Physiol. London 260: 4P, 1977.
 64. Loxdale, H. D. Molecular Parameters of Diverse Muscle Systems. Oxford, UK: Univ. of Oxford, 1980. Dissertation.
 65. Machin, K. E. W., and J. W. S. Pringle. Mechanical properties of a beetle flight muscle. Proc. R. Soc. London Ser. B 151: 204–225, 1959.
 66. Machin, K. E. W., and J. W. S. Pringle. The effect of sinusoidal changes of length on a beetle flight muscle. Proc. R. Soc. London Ser. B 152: 311–330, 1960.
 67. Machin, K. E. W., J. W. S. Pringle, and M. Tamasige. The effect of temperature on a beetle muscle. Proc. R. Soc. London Ser. B 155: 493–499, 1962.
 68. Maeda, Y. Arrangement of troponin and cross‐bridges around the thin filaments in crab leg striated muscle. In: Cross‐Bridge Mechanism in Muscle Contraction, edited by H. Sugi and G. H. Pollack. Tokyo: Univ. of Tokyo Press, 1979, p. 457–470.
 69. Maeda, Y., I. Matsubara, and N. Yagi. Structural changes in thin filaments of crab striated muscle. J. Mol. Biol. 127: 191–201, 1979.
 70. Mannherz, H. G. On the reversibility of the biochemical reactions of muscular contraction during the absorption of negative work. FEBS Lett. 10: 233–236, 1970.
 71. Marston, S. B. The nucleotide complexes of myosin in glycerol‐extracted muscle fibres. Biochim. Biophys. Acta 305: 397–412, 1973.
 72. Marston, S. B., C. D. Rodger, and R. T. Tregear. Changes in muscle crossbridges when β,γ‐imido‐ATP binds to myosin. J. Mol. Biol. 104: 263–276, 1976.
 73. Marston, S. B., and R. T. Tregear. Calcium binding and the activation of fibrillar insect flight muscle. Biochim. Biophys. Acta 347: 311–318, 1974.
 74. Marston, S. B., R. T. Tregear, C. D. Rodger, and M. L. Clarke. Coupling between the enzymatic site of myosin and the mechanical output of muscle. J. Mol. Biol. 128: 111–126, 1979.
 75. Maruyama, K., P. E. Cage, and J. L. Bell. The role of connectin in elastic properties of insect flight muscle. Comp. Biochem. Physiol. A 61: 623–627, 1978.
 76. Maruyama, K., S. Matsubara, R. Natori, Y. Nonomura, and S. Kimura. Connectin, an elastic protein of muscle. Characterization and function. J. Biochem. Tokyo 82: 317–337, 1977.
 77. Maruyama, K., F. Murakami, and K. Ohashi. Connectin, an elastic protein of muscle. Comparative biochemistry J. Biochem. Tokyo 82: 339–345, 1977.
 78. Maruyama, K., J. W. S. Pringle, and R. T. Tregear. The calcium sensitivity of ATPase activity of myofibrils and actomyosins from insect flight and leg muscles. Proc. R. Soc. London Ser. B 169: 229–240, 1968.
 79. Meinrenken, W. Calciumionen‐unabhangige Kontraktion und ATPase bei glycerinierten Muskelfasern nach alkalischer Extraktion von Troponin. Pfluegers Arch. 311: 243–255, 1969.
 80. Meisner, D., and G. Beinbrech. Alterations of crossbridge angle induced by β,γ‐imido‐adenosine‐triphosphate. Electron microscope and optical diffraction studies on myofibrillar fragments of abdominal muscles of the crayfish Orconectes limosus. Eur. J. Cell Biol. 19: 189–195, 1979.
 81. Miller, A., and R. T. Tregear. Structure of insect fibrillar flight muscle in the presence and absence of ATP. J. Mol. Biol. 70: 85–104. 1972.
 82. Namba, K., K. Watkabayashi, and T. Mitsui. The structure of thin filament of crab striated muscle in the rigor state. In: Cross‐Bridge Mechanism in Muscle Contraction, edited by H. Sugi and G. H. Pollack. Tokyo: Univ. of Tokyo Press, 1979, p. 445–456.
 83. Neville, A. C. Energy and economy in insect flight. Sci. Prog. London 54: 203–219, 1965.
 84. Neville, A. C., and T. Weis‐Fogh. The effect of temperature on locust flight muscle. J. Exp. Biol. 40: 111–121, 1963.
 85. Offer, G., and A. Elliott. Can a myosin molecule bind to two actin filaments? Nature London 271: 325–329, 1978.
 86. Pringle, J. W. S. Insect Flight. London: Cambridge Univ. Press, 1956.
 87. Pringle, J. W. S. The mechanical characteristics of insect fibrillar muscle. In: Insect Flight Muscle, edited by R. T. Tregear. Amsterdam: North‐Holland, 1977, p. 177–196.
 88. Pringle, J. W. S. The Croonian Lecture, 1977. Stretch activation of muscle: function and mechanism. Proc. R. Soc. London Ser. B 201: 107–130, 1978.
 89. Pringle, J. W. S. The evolution of fibrillar muscle in insects. J. Exp. Biol. 94: 1–14, 1981.
 90. Pringle, J. W. S., and R. T. Tregear. Mechanical properties of insect fibrillar muscle at large amplitudes of oscillation. Proc. R. Soc. London Ser. B 174: 33–50, 1969.
 91. Pybus, J., and R. T. Tregear. The relationship of ATP activity to tension and power output of insect flight muscle. J. Physiol. London 247: 71–89, 1975.
 92. Reedy, M., M. K. Reedy, and R. S. Goody. Crossbridge structure in rigor and AMPPNP states of insect flight muscle. Biophys. J. 33: 22a, 1981.
 93. Reedy, M. K. Ultrastructure of insect flight muscle. I. Screw sense and structural grouping in the rigor cross‐bridge lattice. J. Mol. Biol. 31: 155–176, 1968.
 94. Reedy, M. K., G. F. Bahr, and D. A. Fischman. How many myosins per cross‐bridge? I. Flight muscle myofibrils from the blowfly, Sarcophaga bullata. Cold Spring Harbor Symp. Quant. Biol. 37: 397–422, 1973.
 95. Reedy, M. K., and W. E. Garrett, Jr. Electron microscope studies of Lethocerus flight muscle in rigor. In: Insect Flight Muscle, edited by R. T. Tregear. Amsterdam: North‐Holland, 1977, p. 115–136.
 96. Reedy, M. K., K. C. Holmes, and R. T. Tregear. Induced changes in orientation of the cross‐bridges of glycerinated insect flight muscle. Nature London 207: 1276–1280, 1965.
 97. Reedy, M. K., K. R. Leonard, R. Freeman, and T. Arad. Thick myofilament mass determination by electron scattering measurements with the scanning transmission electron microscope. J. Muscle Res. Cell Motil. 2: 45–64, 1981.
 98. Reger, J. F., and D. P. Cooper. Wing and leg muscles in a lepidopteran. J. Cell Biol. 33: 531–542, 1967.
 99. Roeder, K. C. Movements of the thorax and potential changes in the thoracic muscles of insects during flight. Biol. Bull. Woods Hole, Mass. 100: 95–106, 1951.
 100. Rosenbluth, J. Sarcoplasmic reticulum of an unusually fast‐acting crustacean muscle. J. Cell Biol. 42: 534–547, 1969.
 101. Rüegg, J. C., K. Guth, H. J. Kuhn, J. W. Herzig, P. J. Griffiths, and T. Yamamoto. Muscle stiffness in relation to tension development of skinned striated muscle fibres. In: Cross‐Bridge Mechanism in Muscle Contraction, edited by H. Sugi and G. H. Pollack. Tokyo: Univ. of Tokyo Press, 1979, p. 125–143.
 102. Rüegg, J. C., G. J. Steiger, and M. Schadler. Mechanical activation of the contractile system in skeletal muscle. Pfluegers Arch. 319: 139–145, 1970.
 103. Rüegg, J. C., and R. T. Tregear. Mechanical factors affecting the ATPase activity of glycerol‐extracted insect fibrillar flight muscle. Proc. R. Soc. London Ser. B 165: 497–512, 1966.
 104. Saide, J. D., and W. C. Ullrick. Fine structure of the honeybee Z‐disc. J. Mol. Biol. 79: 329–337, 1973.
 105. Saide, J. D., and W. C. Ullrick. Purification and properties of the isolated honeybee Z‐disc. J. Mol. Biol. 87: 671–683, 1974.
 106. Sainsbury, G., and B. Bullard. New proline‐rich proteins in isolated insect Z‐discs. Biochem. J. 191: 333–339, 1980.
 107. Sainsbury, G. M., and D. Hulmes. Notes on the structure of the Z‐disc of insect flight muscle. In: Insect Flight Muscle, edited by R. T. Tregear. Amsterdam: North‐Holland, 1977, p. 75–78.
 108. Schädler, M. Proportionale Aktivierung von ATPase‐Aktivität und Kontrakionsspannung durch Calciumionen in isolierten contractilen Strukturen verschiedenet Muskelarten. Pfluegers Arch. 296: 70–90, 1967.
 109. Schädler, M., G. J. Steiger, and J. C. Rüegg. Mechanical activation and isometric oscillation in insect fibrillar muscle. Pfluegers Arch. 330: 217–229, 1971.
 110. Smith, D. S. The organization of a flight muscle in a dragonfly. J. Biophys. Biochem. Cytol. 11: 119–145, 1961.
 111. Smith, D. S. The organization and function of the sarcoplasmic reticulum and T‐system of muscle cells. Prog. Biophys. Mol. Biol. 16: 107–142, 1966.
 112. Sotavalta, O. The wingbeat frequency of insects. Acta Entomol. Fenn. 4: 1–117, 1947.
 113. Squire, J. M. General model of myosin filament structure. II. Myosin filaments and cross‐bridge interactions in vertebrate striated and insect flight muscles. J. Mol. Biol. 72: 125–138, 1972.
 114. Squire, J. M. General model of myosin filament structure. III. Molecular packing arrangements in myosin filaments. J. Mol. Biol. 77: 291–323, 1973.
 115. Squire, J. M. Actin target area labelling in rigor striated muscles (Abstract). J. Muscle Res. Cell Motil. 1: 450, 1980.
 116. Steiger, G. J. Stretch activation and tension transients in cardiac, skeletal and insect flight muscle. In: Insect Flight Muscle, edited by R. T. Tregear. Amsterdam: North‐Holland, 1977, p. 221–268.
 117. Steiger, G. J., and R. H. Abbott. Biochemical interpretation of tension transients produced by a four state mechanical model. J. Muscle'Res. Cell Motil. 2: 245–260, 1981.
 118. Steiger, G. J., and J. C. Rüegg. Energetics and efficiency in the isolated contractile machinery of an insect fibrillar muscle. Pfluegers Arch. 307: 1–21, 1969.
 119. Thom, A., and P. Scuart. The forces on an aerofoil at very low speeds. J. R. Aeronaut. Soc. 44: 761–770, 1940.
 120. Thorson, J., and D. C. S. White. Distributed representations for actin‐myosin interaction in the oscillatory contraction of muscle. Biophys. J. 9: 360–390, 1969.
 121. Thorson, J., and D. C. S. White. Dynamic force measurements at the microgram level with application to myofibrils of striated muscle. IEEE Trans. Biomed. Eng. 4: 293–299, 1975.
 122. Tice, L. W., and D. S. Smith. Localization of myofibrillar ATPase activity in the flight muscles of the blowfly. J. Cell Biol. 25: 121–135, 1965.
 123. Tiegs, O. W. The flight muscles of insects. Philos. Trans. R. Soc. London Ser. B 238: 221–348, 1955.
 124. Tregear, R. T. The biophysics of insect flight muscle. In: Insect Muscle, edited by P. N. R. Usherwood. New York: Academic, 1975, p. 357–403.
 125. Tregear, R. T., and S. B. Marston. The crossbridge theory. Ananu. Rev. Physiol. 41: 723–736, 1979.
 126. Tregear, R. T., J. R. Milch, R. S. Goody, K. C. Holmes, and C. D. Rodger. The use of some novel X‐ray diffraction techniques to study the effect of nucleotides on cross‐bridges in insect flight muscle. In: Cross‐Bridge Mechanism in Muscle Contraction, edited by H. Sugi and G. H. Pollack. Tokyo: Univ. of Tokyo Press, 1979, p. 407–423.
 127. Tregear, R. T., and J. M. Squire. Myosin content and filament structure in smooth and striated muscle. J. Mol. Biol. 77: 279–290, 1973.
 128. Trinick, J., and G. Offer. Cross‐linking of actin filaments by heavy meromyosin. J. Mol. Biol. 133: 549–556, 1979.
 129. Trombitas, C., and A. Tigyi‐Sebes. Fine structure and mechanical properties of insect muscle. In: Insect Flight Muscle, edited by R. T. Tregear. Amsterdam: North‐Holland, 1977, p. 79–90.
 130. Ulbrich, M., and J. C. Rüegg. Stretch induced formation of ATP‐32P in glycerinated fibres of insect flight muscle. Experientia 27: 45–46, 1971.
 131. Ullrick, W. C., P. A. Toselli, D. Chase, and K. Dasse. Are there extensions of thick filaments to the Z‐line in vertebrate and invertebrate striated muscle? J. Ultrastruct. Res. 60: 263–271, 1977.
 132. Vom Brocke, H. H. The activating effects of calcium ions on the contractile systems of insect fibrillar flight muscle. Pfluegers Arch. Geasamte Physiol. Menschen Tiere 290: 70–79, 1966.
 133. Vom Brocke, H. H., and J. C. Rüegg. Fractionation of the ATPase of fibrillar insect flight muscle. Helv. Physiol. Pharmacol. Acta 23: c79–c81, 1965.
 134. Weis‐Fogh, T. Flight performance of the desert locust. Philos. Trans. R. Soc. London Ser. B 239: 459–510, 1956.
 135. Weis‐Fogh, T. Tetanic force and shortening in locust flight muscle. J. Exp. Biol. 33: 668–684, 1956.
 136. White, D. C. S. Rigor contraction and the effect of various phosphate compounds on glycerinated insect flight and vertebrate muscle. J. Physiol. London 208: 583–605, 1970.
 137. White, D. C. S., M. M. K. Donaldson, G. E. Pearce, and M. G. A. Wilson. The resting elasticity of insect fibrillar flight muscle and properties of the crossbridge cycle. In: Insect Flight Muscle, edited by R. T. Tregear. Amsterdam: North‐Holland, 1977, p. 197–208.
 138. White, D. C. S., and J. Thorson. Phosphate starvation and the non‐linear dynamics of insect fibrillar flight muscle. J. Gen. Physiol. 60: 307–336, 1972.
 139. White, D. C. S., and J. Thorson. The kinetics of muscle contraction. In: Progress in Biophysics and Molecular Biology, edited by J. A. V. Butler and D. Nobel. Oxford, UK: Pergamon, 1973, vol. 27, p. 173–255.
 140. White, D. C. S., M. G. A. Wilson, and J. Thorson. What does insect flight muscle tell us about the mechanism of active contraction? In: Crossbridge Mechanism in Muscle Contraction, edited by H. Sugi and G. H. Pollack. Tokyo: Univ. of Tokyo Press, 1979, p. 193–210.
 141. Winkelman, L. Comparative studies of paramyosins. Comp. Biochem. Physiol. B 55: 391–397, 1976.
 142. Winkelman, L., and B. Bullard. Phosphorylation of a locust myosin light chain and its effect on calcium regulation. J. Muscle Res. Cell Motil. 1: 221–222, 1980.
 143. Wood, J. An experimental determination of the relationship between lift and aerodynamic power in Calliphora erythrocephala and Phormia regina. J. Exp. Biol. 56: 31–36, 1972.
 144. Wootton, R. J., and D. J. S. Newman. Whitefly have the highest contraction frequencies yet recorded in non‐fibrillar flight muscles. Nature London 280: 402–403, 1979.
 145. Wray, J. S. Filament geometry and the activation of insect flight muscles. Nature London 280: 325–326, 1979.
 146. Wray, J. S. Structure of the backbone in myosin filaments of muscle. Nature London 277: 37–40, 1979.
 147. Wray, J., P. Vibert, and C. Cohen. Actin filaments in muscle: pattern of myosin and tropomyosin/troponin attachments. J. Mol. Biol. 124: 501–521, 1978.
 148. Yount, R. G., D. Ojala, and D. Babcock. Interaction of P‐N‐P and P‐C‐P analogs of adenosine triphosphate with heavy meromyosin, myosin and actomyosin. Biochemistry 10: 2490–2495, 1971.
 149. Zebe, E., W. Meinrenken, and J. C. Rüegg. Supercontraction of glycerol‐extracted insect flight muscles in the presence of ITP. Z. Zellforsch. Mikrosk. Anat. 87: 603–621, 1968.

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Physiology of Insect Flight Muscle
 

How to Cite

Richard T. Tregear. Physiology of Insect Flight Muscle. Compr Physiol 2011, Supplement 27: Handbook of Physiology, Skeletal Muscle: 487-506. First published in print 1983. doi: 10.1002/cphy.cp100116