Skip to main content
SpringerLink
Log in
Book cover

Nature’s Versatile Engine: Insect Flight Muscle Inside and Out pp 44–60Cite as

Stretch Activation

Toward a Molecular Mechanism

  • Chapter

Part of the book series: Molecular Biology Intelligence Unit ((MBIU))

Abstract

Insect flight is often powered by high wing beat frequencies. Surprisingly, the flight muscles of some insects are capable of driving high wing beats without extensive calcium cycling machinery. Rather than precisely timed signals from motor neurons driving each contraction, nervous stimulation is sporadic, which presumably serves to maintain a moderately elevated intracellular calcium concentration. In this calcium activated state the muscle will also produce a delayed increase in tension that is initiated by a stretch (stretch activation), produced when an antagonist muscle shortens. Although stretch activation is enhanced in insect flight and cardiac muscle, it is a general property of all muscles. Historically, the underlying mechanism of stretch activation has been studied using several model systems. Initial studies relied on mechanical and ultrastructural studies of giant water bug (Lethocerus) flight muscle and vertebrate cardiac muscle. More recently, studies of Drosophila flight muscles have allowed powerful genetic methods to be added to the researcher’s arsenal. Using these systems, several mechanisms have been proposed to explain stretch activation: (i) matching of the thick and thin filament lattices, (ii) passive stress in the connecting filaments,1 (iii) myosin regulatory light chain (RLC) phosphorylation,2, 3 and (iv) stretch sensitive calcium sensitivity.1, 4

While popular, models proposing lattice matching have been challenged by more recent analysis of filament lattice geometries form several insect species.5 Insect flight and cardiac muscle exhibit a high passive stiffness and are therefore very sensitive to applied stretch. Recent results obtained with insect flight and cardiac muscle preparations provide new insight into a possible molecular pathway that explains the effects of thick filament stress on crossbridge formation. Evidence suggests that stress is transmitted through connecting filaments that extend from the Z-band to the thick filament. We propose that thick filament stress relieves an inhibitory conformation of myosin, which has been observed by low angle X-ray diffraction of isolated Lethocerus fiber bundles.6 Release of this inhibition by stretch/stress together with RLC phosphorylation increases the recruitment of force generating crossbridges and leads to stretch activation.

Stretch sensitive calcium sensitivity via the thin filament regulatory system is also an attractive hypothesis that has recently gained experimental support.7 Agianian et al7 showed that isometric tension and stretch activated tension are controlled by different isoforms of troponin C (TnC). Although these results can be explained by a stretch sensitive troponin complex,7 the description does not provide a clear explanation for the large body of evidence suggesting thick filament stress and regulatory light chain phosphorylation are important for stretch activation. Any model for stretch activation must incorporate both thick and thin filament influences. Here it is proposed that Ca++ binding to TnC activates isometric force generation at high calcium levels; however, IFM operate at low “permissive” calcium concentrations and that stretch and/or phosphorylation induced effects on myosin position are required for activation.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Pringle JW. The Croonian lecture, 1977. Stretch activation of muscle: Function and mechanism. Proc R Soc Lond B Biol Sci 1978; 201:107–130.

    PubMed  CAS  Google Scholar 

  2. Tohtong R, Yamashita H, Graham M et al. Impairment of muscle function caused by mutations of phosphorylation sites in myosin regulatory light chain. Nature 1995; 374:650–653.

    Article  PubMed  CAS  Google Scholar 

  3. Dickinson MH, Hyatt CJ, Lehmann FO et al. Phosphorylation-dependent power output of transgenic flies: An integrated study. Biophys J 1997; 73:3122–3134.

    PubMed  CAS  Google Scholar 

  4. Qiu F, Lakey A, Agianian B et al. Troponin C in different insect muscle types: Identification of two isoforms in Lethocerus, Drosophila and Anopheles that are specific to asynchronous flight muscle in the adult insect. Biochem J 2003; 371:811–821.

    Article  PubMed  CAS  Google Scholar 

  5. Squire JM. Muscle filament lattices and stretch-activation: The match-mismatch model reassessed. J Muscle Res Cell Motil 1992; 13:183–189.

    Article  PubMed  CAS  Google Scholar 

  6. Al Khayat HA, Hudson L, Reedy MK et al. Myosin head configuration in relaxed insect flight muscle: X-ray modeled resting cross-bridges in a prepowerstroke state are poised for actin binding. Biophys J 2003; 85:1063–1079.

    Google Scholar 

  7. Agianian B, Krzic U, Qiu F et al. A troponin switch that regulates muscle contraction by stretch instead of calcium. EMBO J 2004; 23:772–779.

    Article  PubMed  CAS  Google Scholar 

  8. Baker JE, Brosseau C, Joel PB et al. The biochemical kinetics underlying actin movement generated by one and many skeletal muscle myosin molecules. Biophys J 2002; 82:2134–2147.

    PubMed  CAS  Google Scholar 

  9. Baker JE, Brosseau C, Fagnant P et al. The unique properties of tonic smooth muscle emerge from intrinsic as well as intermolecular behaviors of Myosin molecules. J Biol Chem 2003; 278:28533–28539.

    Article  PubMed  CAS  Google Scholar 

  10. Sotovalta O. The flight tone (wing stroke frequency) of insects. Acta Entomol Fenn 1947; 4:111–117.

    Google Scholar 

  11. Sotovalta O. Recordings of high wing-stroke and thoracic vibration frequency in some midges. Biol Bull Woods Hole 1953; 104:439–444.

    Article  Google Scholar 

  12. Martin JH, Bagby RM. Properties of rattlesnake shaker muscle. J Exp Zool 1973; 185:293–300.

    Article  PubMed  CAS  Google Scholar 

  13. Young D, Josephson RK. 100 Hz is not the upper limit of synchronous muscle contraction. Nature 1984; 309:286–287.

    Article  PubMed  CAS  Google Scholar 

  14. Josephson RK, Malamud JG, Stokes DR. Asynchronous muscle: A primer. J Exp Biol 2000; 203 (Pt 18):2713–2722.

    PubMed  CAS  Google Scholar 

  15. Pringle JW. The excitation and contraction of the flight muscles of insects. J Physiol (Lond) 1949; 108:226–232.

    PubMed  CAS  Google Scholar 

  16. Machin KE, Pringle JW. The physiology of insect fibrillar flight muscle. II. Mechanical properties of a bettle flight muscle. Proc R Soc Lond B Biol Sci 1959; 151:204–225.

    Google Scholar 

  17. Machin KE, Pringle JW. The physiology of insect fibrillar muscle. III. The effect of sinusoidal changes of length on a beetle flight muscle. Proc R Soc Lond B Biol Sci 1960; 152:311–330.

    PubMed  CAS  Google Scholar 

  18. Jewell BR, Ruegg JC. Oscillatory contraction of insect fibrillar flight muscle after glycerol extraction. Proc R Soc Lond B Biol Sci 1964; 164:428–459.

    Google Scholar 

  19. Hyatt CJ, Maughan DW. Fourier analysis of wing beat signals: Assessing the effects of genetic alterations of flight muscle structure in Diptera. Biophys J 1994; 67:1149–1154.

    PubMed  CAS  Google Scholar 

  20. Huxley AF, Simmons RM. Proposed mechanism of force generation in striated muscle. Nature 1971; 233:533–538.

    Article  PubMed  CAS  Google Scholar 

  21. Steiger GJ. Stretch activation and myogenic oscillation of isolated contractile structures of heart muscle. Pflugers Arch 1971; 330:347–361.

    Article  PubMed  CAS  Google Scholar 

  22. Warshaw DM, Fay FS. Tension transients in single isolated smooth muscle cells. Science 1983; 219:1438–1441.

    Article  PubMed  CAS  Google Scholar 

  23. Abbott RH, Steiger GJ. Temperature and amplitude dependence of tension transients in glycerinated skeletal and insect fibrillar muscle. J Physiol 1977; 266:13–42.

    PubMed  CAS  Google Scholar 

  24. Steiger GJ. Tension transients in extracted rabbit heart muscle preparations. J Mol Cell Cardiol 1977; 9:671–685.

    PubMed  CAS  Google Scholar 

  25. Kulke M, Neagoe C, Kolmerer B et al. Kettin, a major source of myofibrillar stiffness in Drosophila indirect flight muscle. J Cell Biol 2001; 154:1045–1057.

    Article  PubMed  CAS  Google Scholar 

  26. Chaplain RA. Changes in adenosine triphosphatase activity and tension with fiber elongation in glycerinated insect flight muscle. Pflugers Arch 1969; 307:120–126.

    Article  PubMed  CAS  Google Scholar 

  27. Guth K, Poole JV, Maughan D et al. The apparent rates of crossbridge attachment and detachment estimated from ATPase activity in insect flight muscle. Biophys J 1987; 52:1039–1045.

    PubMed  Google Scholar 

  28. Lund J, Webb MR, White DC. Changes in the ATPase activity of insect fibrillar flight muscle during calcium and strain activation probed by phosphate-water oxygen exchange. J Biol Chem 1987; 262:8584–8590.

    PubMed  CAS  Google Scholar 

  29. Tregear RT, Edwards RJ, Irving TC et al. X-ray diffraction indicates that active cross-bridges bind to actin target zones in insect flight muscle. Biophys J 1998; 74:1439–1451.

    PubMed  CAS  Google Scholar 

  30. Wray J. Filament geometry and the activation of insect flight muscles. Nature 1979; 280:325–326.

    Article  Google Scholar 

  31. Abbott RH, Cage PE. A possible mechanism of length activation in insect fibrillar flight muscle. J Muscle Res Cell Motil 1984; 5:387–397.

    Article  PubMed  CAS  Google Scholar 

  32. Thorson J, White DCS. Distributed representations for actin-myosin interaction in the oscillatory contraction of muscle. Biophys J 1969; 9:360–390.

    PubMed  CAS  Google Scholar 

  33. Huxley AF. Muscle structure and theories of contraction. Prog Biophys & Biophys Chem 1957; 7:255–317.

    CAS  Google Scholar 

  34. Granzier HL, Wang K. Interplay between passive tension and strong and weak binding cross-bridges in insect indirect flight muscle. A functional dissection by gelsolin-mediated thin filament removal. J Gen Physiol 1993; 101:235–270.

    Article  PubMed  CAS  Google Scholar 

  35. Millman BM. The filament lattice of striated muscle. Physiol Rev 1998; 78:359–391.

    PubMed  CAS  Google Scholar 

  36. Garamvolgyi N. Forces acting between muscle filaments. I. Filament lattice spacing in bee flight muscle. Acta Biochim Biophys Acad Sci Hung 1972; 7:157–164.

    PubMed  CAS  Google Scholar 

  37. Saide JD. Identification of a connecting filament protein in insect fibrillar flight muscle. J Mol Biol 1981; 153:661–679.

    Article  PubMed  CAS  Google Scholar 

  38. Helmes M, Trombitas K, Granzier H. Titin develops restoring force in rat cardiac myocytes. Circ Res 1996; 79:619–626.

    PubMed  CAS  Google Scholar 

  39. Cazorla O, Wu Y, Irving TC et al. Titin-based modulation of calcium sensitivity of active tension in mouse skinned cardiac myocytes. Circ Res 2001; 88:1028–1035.

    PubMed  CAS  Google Scholar 

  40. Pringle JW. The mechanical characteristics of insect fibrillar flight muscle. In: Tregear R, ed. Insect Flight Muscle. Elsevier/North Holland Biomedical Press, 1977:177–208.

    Google Scholar 

  41. Irving TC, Maughan DW. In vivo X-ray diffraction of indirect flight muscle from Drosophila melanogaster. Biophys J 2000; 78:2511–2515.

    PubMed  CAS  Google Scholar 

  42. Konhilas JP, Irving TC, de Tombe PP. Myofilament calcium sensitivity in skinned rat cardiac trabeculae: Role of interfilament spacing. Circ Res 2002; 90:59–65.

    Article  PubMed  CAS  Google Scholar 

  43. Muhle-Goll C, Habeck M, Cazorla O et al. Structural and functional studies of titin’s fn3 modules reveal conserved surface patterns and binding to myosin S1—a possible role in the Frank-Starling mechanism of the heart. J Mol Biol 2001; 313:431–447.

    Article  PubMed  CAS  Google Scholar 

  44. Tskhovrebova L, Trinick J. Role of titin in vertebrate striated muscle. Philos Trans R Soc Lond B Biol Sci 2002; 357:199–206.

    Article  PubMed  CAS  Google Scholar 

  45. Bullard B, Linke WA, Leonard K. Varieties of elastic protein in invertebrate muscles. J Muscle Res Cell Motil 2002; 23:435–447.

    Article  PubMed  Google Scholar 

  46. Ayme-Southgate A, Vigoreaux J, Benian G et al. Drosophila has a twitchin/titin-related gene that appears to encode projectin. Proc Natl Acad Sci USA 1991; 88:7973–7977.

    Article  PubMed  CAS  Google Scholar 

  47. Benian GM, Kiff JE, Neckelmann N et al. Sequence of an unusually large protein implicated in regulation of myosin activity in C. elegans. Nature 1989; 342:45–50.

    Article  PubMed  CAS  Google Scholar 

  48. Royuela M, Fraile B, De Miguel MP et al. Immunohistochemical study and western blotting analysis of titin-like proteins in the striated muscle of Drosophila melanogaster and in the striated and smooth muscle of the oligochaete Eisenia foetida. Microsc Res Tech 1996; 35:349–356.

    Article  PubMed  CAS  Google Scholar 

  49. Saide JD, Chin-Bow S, Hogan-Sheldon J et al. Characterization of components of Z-bands in the fibrillar flight muscle of Drosophila melanogaster. J Cell Biol 1989; 109:2157–2167.

    Article  PubMed  CAS  Google Scholar 

  50. Vigoreaux JO, Saide JD, Pardue ML. Structurally different Drosophila striated muscles utilize distinct vriants of Z-band-associated proteins. J Muscle Res Cell Motil 1991; 12:340–354.

    Article  PubMed  CAS  Google Scholar 

  51. Vigoreaux JO, Saide JD, Valgeirsdottir K et al. Flightin, a novel myofibrillar protein of Drosophila stretch-activated muscles. J Cell Biol 1993; 121:587–598.

    Article  PubMed  CAS  Google Scholar 

  52. Ayer G, Vigoreaux JO. Flightin is a myosin rod binding protein. Cell Biochem Biophys 2003; 38:41–54.

    PubMed  CAS  Google Scholar 

  53. Henkin JA, Maughan DW, Vigoreaux JO. Mutations that affect flightin expression in Drosophila alter the viscoelastic properties of flight muscle fibers. Am J Physiol Cell Physiol 2004; 286:C65–C72.

    Article  PubMed  CAS  Google Scholar 

  54. Vinos J, Domingo A, Marco R et al. Identification and characterization of Drosophila melanogaster paramyosin. J Mol Biol 1991; 220:687–700.

    Article  PubMed  CAS  Google Scholar 

  55. Champagne MB, Edwards KA, Erickson HP et al. Drosophila stretchin-MLCK is a novel member of the Titin/Myosin light chain kinase family. J Mol Biol 2000; 300:759–777.

    Article  PubMed  CAS  Google Scholar 

  56. Patel S, Saide JD. A(225), A novel A-band protein of Drosophila indirect flight muscle. Biophys J 2001; 80:71a.

    Google Scholar 

  57. Tawada K, Kawai M. Covalent cross-linking of single fibers from rabbit psoas increases oscillatory power. Biophys J 1990; 57:643–647.

    PubMed  CAS  Google Scholar 

  58. Trombitas K, Tigyi-Sebes A. The continuity of thick filaments between sarcomeres in honey bee flight muscle. Nature 1979; 281:319–320.

    Article  PubMed  CAS  Google Scholar 

  59. Irving T, Wu Y, Fukuda N et al. Changes in sarcomeric structure as a function of titin-based passive tension in skeletal muscle. Biophys J 2004; 86:188a.

    Google Scholar 

  60. Morano I. Tuning the human heart molecular motors by myosin light chains. J Mol Med 1999; 77:544–555.

    Article  PubMed  CAS  Google Scholar 

  61. Szczesna D, Zhao J, Jones M et al. Phosphorylation of the regulatory light chains of myosin affects Ca2+ sensitivity of skeletal muscle contraction. J Appl Physiol 2002; 92:1661–1670.

    PubMed  CAS  Google Scholar 

  62. Levine RJ, Kensler RW, Yang Z et al. Myosin regulatory light chain phosphorylation and the production of functionally significant changes in myosin head arrangement on striated muscle thick filaments. Biophys J 1995; 68:224S.

    PubMed  CAS  Google Scholar 

  63. Reedy MC, Reedy MK, Leonard KR et al. Gold/Fab immuno electron microscopy localization of troponin H and troponin T in Lethocerus flight muscle. J Mol Biol 1994; 239:52–67.

    Article  PubMed  CAS  Google Scholar 

  64. Steiger GJ. Stretch activation and tension transients in cardiac, skeletal and insect flight muscle. In: Tregear RT, ed. Insect Flight Muscle. North Holland, 1977:221–268.

    Google Scholar 

  65. Schadler M, Steiger GJ, Ruegg JC. Mechanical activation and isometric oscillation in insect fibrillar muscle. Pflugers Arch 1971; 330:217–229.

    Article  PubMed  CAS  Google Scholar 

  66. Smith DA. Quantitative model for Schadler’s isometric oscillations in insect flight and cardiac muscle. J Muscle Res Cell Motil 1991; 12:455–465.

    Article  PubMed  CAS  Google Scholar 

  67. Kreuz AJ, Simcox A, Maughan D. Alterations in flight muscle ultrastructure and function in Drosophila tropomyosin mutants. J Cell Biol 1996; 135:673–687.

    Article  PubMed  CAS  Google Scholar 

  68. Peckham M, Molloy JE, Sparrow JC et al. Physiological properties of the dorsal longitudinal flight muscle and the tergal depressor of the trochanter muscle of Drosophila melanogaster. J Muscle Res Cell Motil 1990; 11:203–215.

    Article  PubMed  CAS  Google Scholar 

  69. van der Velden, Papp Z Zaremba R et al. Increased Ca2+-sensitivity of the contractile apparatus in end-stage human heart failure results from altered phosphorylation of contractile proteins. Cardiovasc Res 2003; 5737–47.

    Article  PubMed  Google Scholar 

  70. Weitkamp B, Jurk K, Beinbrech G. Projectin-thin filament interactions and modulation of the sensitivity of the actomyosin ATPase to calcium by projection kinase. J Biol Chem 1998; 273:19802–19808.

    Article  PubMed  CAS  Google Scholar 

  71. Moore JR, Vigoreaux JO, Maughan DW. The Drosophila projectin mutant, bentD, has reduced stretch activation and altered indirect flight muscle kinetics. J Muscle Res Cell Motil 1999; 20:797–806.

    Article  PubMed  CAS  Google Scholar 

  72. Vigoreaux JO, Moore JR, Maughan DW. Role of the elastic protein projectin in stretch activation and work output of Drosophila flight muscles. Adv Exp Med Biol 2000; 481:237–247.

    PubMed  CAS  Google Scholar 

  73. Marston S, Tregear RT. Calcium binding and the activation of fibrillar insect flight muscle. Biochim Biophys Acta 1974; 347:311–318.

    Article  PubMed  CAS  Google Scholar 

  74. Moore JR, Dickinson MH, Vigoreaux JO et al. The effect of removing the N-terminal extension of the Drosophila myosin regulatory light chain upon flight ability and the contractile dynamics of indirect flight muscle. Biophys J 2000; 78:1431–1440.

    PubMed  CAS  Google Scholar 

  75. Ruiz T, Bullard B, Lepault J. Effects of calcium and nucleotides on the structure of insect flight muscle thin filaments. J Muscle Res Cell Motil 1998; 19:353–364.

    Article  PubMed  CAS  Google Scholar 

  76. Cammarato A, Hatch V, Saide J et al. Drosophila muscle regulation characterized by electron microscopy and three-dimensional reconstruction of thin filament mutants. Biophys J 2004; 86:1618–1624.

    PubMed  CAS  Google Scholar 

  77. Maytum R, Lehrer SS, Geeves MA. Cooperativity and switching within the three-state model of muscle regulation. Biochemistry 1999; 38:1102–1110.

    Article  PubMed  CAS  Google Scholar 

  78. Bernstein SI, O’Donnell PT, Cripps RM. Molecular genetic analysis of muscle development, structure, and function in Drosophila. Int Rev Cytol 1993; 143:63–152.

    Article  PubMed  CAS  Google Scholar 

  79. Rayment I, Holden HM, Sellers JR et al. Structural interpretation of the mutations in the beta-cardiac myosin that have been implicated in familial hypertrophic cardiomyopathy. Proc Natl Acad Sci USA 1995; 92:3864–3868.

    Article  PubMed  CAS  Google Scholar 

  80. Seidman JG, Seidman C. The genetic basis for cardiomyopathy: From mutation identification to mechanistic paradigms. Cell 2001; 104:557–567.

    Article  PubMed  CAS  Google Scholar 

  81. Vemuri R, Lankford EB, Poetter K et al. The stretch-activation response may be critical to the proper functioning of the mammalian heart. Proc Natl Acad Sci USA 1999; 96:1048–1053.

    Article  PubMed  CAS  Google Scholar 

  82. al-Khayat HA, Yagi N, Squire JM. Structural changes in actin-tropomyosin during muscle regulation: Computer modelling of low-angle X-ray diffraction data. J Mol Biol 1995; 252:611–632.

    Article  PubMed  CAS  Google Scholar 

  83. Huxley HE. The structural basis of muscular contraction. Proc R Soc Lond B Biol Sci 1971; 178:131–149.

    PubMed  CAS  Google Scholar 

  84. Parry DA, Squire JM. Structural role of tropomyosin in muscle regulation: Analysis of the x-ray diffraction patterns from relaxed and contracting muscles. J Mol Biol 1973; 75:33–55.

    Article  PubMed  CAS  Google Scholar 

  85. Lehman W, Craig R, Vibert P. Ca(2+)-induced tropomyosin movement in Limulus thin filaments revealed by three-dimensional reconstruction. Nature 1994; 368:65–67.

    Article  PubMed  CAS  Google Scholar 

  86. Xu C, Craig R, Tobacman L et al. Tropomyosin positions in regulated thin filaments revealed by cryoelectron microscopy. Biophys J 1999; 77:985–992.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Molecular Physiology and Biophysics, University of Vermont College of Medicine, Burlington, Vermont, USA

    Jeffrey R. Moore

Authors
  1. Jeffrey R. Moore
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Eurekah.com and Springer Science+Business Media

About this chapter

Cite this chapter

Moore, J.R. (2006). Stretch Activation. In: Nature’s Versatile Engine: Insect Flight Muscle Inside and Out. Molecular Biology Intelligence Unit. Springer, Boston, MA. https://doi.org/10.1007/0-387-31213-7_4

Download citation

Publish with us

Policies and ethics

Search

Navigation