Skip to main content
SpringerLink
Log in

Paramyosin content and thick filament structure in insect muscles

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

The myosin filaments of the flight muscles of the locust Locusta migratoria, the cockchafer Melolontha melolontha and the femur muscles of L. migratoria have solid centers. Those of the flight muscles of the housefly Musca domestica and Drosophila melanogaster are tubular. Electron micrographs of myofibrils of the fleshfly Phormia terrae-novae contain both filament types within one sarcomere and suggest the existence of 4 cross-bridges per crown.

Estimates of the ratios of myosin to paramyosin and of myosin to actin on sodium dodecyl sulphate-polyacrylamide gels yielded paramyosin contents of 9% of the thick filament mass for the solid and 2.6% for the tubular filaments (3.8% for P. terrae-novae). Based on the myosinactin ratios up to 6 myosin dimers per crown could be calculated.

The molar ratio of actin to arthrin on SDS gels was found to be 3.37 for native and extracted myofibrils of flight muscles from P. terrae-novae. Arthrin is also present in isolated actin filaments suggesting that it is localized in or on the thin filaments. If we assume that it is constituent part of the helices of the thin filaments the number of myosin dimers per crown can be diminished to 4.5, considerably closer to the values obtained by evaluation of electron micrographs.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Auber J (1965) Sur le mécanisme de la formation des filaments primaires au cours de l'accroissement des myofibrilles chez Calliphora erythrocephala (Mg.) (Insecte, Diptère). C R Acad Sci 260:668–670

    Google Scholar 

  • Auber J, Couteaux R (1963) Ultrastructure de la strie Z dans les muscles de diptères. J Microsc 2:309–324

    Google Scholar 

  • Aust S (1980) Eine Bestimmung des Aktin-, Arthrin-, Myosinund Paramyosin-Gehaltes in den Flugmuskeln der Honigbiene Apis mellifica. Staatsexamensarbeit, Münster

    Google Scholar 

  • Beinbrech G (1968) Elektronenmikroskopische Untersuchungen über die Differenzierung von Insektenmuskeln während der Metamorphose. Z Zellforsch 90:463–494

    Google Scholar 

  • Beinbrech G (1973a) Myofilamentmuster eines Insektenflugmuskels. Naturwiss Rdsch 26 (12):III

    Google Scholar 

  • Beinbrech G (1973b) Die Differenzierung des kontraktilen Systems in Insekten-Flugmuskeln. Arzneim-Forsch (Drug Res) 23:623–624

    Google Scholar 

  • Beinbrech G (1980) Arrowhead periodicities and actin filament structure in arthropod muscles. J Muscle Res Cell Mot 1:194

    Google Scholar 

  • Bullard B, Reedy MK (1973) How many myosins per cross-bridge? II. Flight muscle myosin from the blowfly, Sarcophaga bullata. Cold Spring Harbor Symp Quant Biol 37:423–428

    Google Scholar 

  • Bullard B, Sainsbury GM (1977) The proteins in the Z-line of insect flight muscle. Biochem J 161:399–403

    Google Scholar 

  • Bullard B, Drabowska R, Winkelman L (1973a) The contractile and regulatory proteins of insect flight muscle. Biochem J 135:277–286

    Google Scholar 

  • Bullard B, Luke B, Winkelman L (1973b) The paramyosin of insect flight muscle. J Mol Biol 75:359–367

    Google Scholar 

  • Bullard B, Hammond KS, Luke BM (1977) 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

    Google Scholar 

  • Bullard B, Bell J, Craig R, Leonard K (1980) An actin like protein from insect muscle. J Muscle Res Cell Mot 1:195

    Google Scholar 

  • Goll DE, Stromer MH, Robson RM, Luke BM, Hammond KS (1977) Extraction, purification, and localization of α-actinin from asynchronous insect flight muscle. In: Tregear RT (ed) Insect flight muscle. North Holland Publ Co, Amsterdam New York Oxford, pp 15–40

    Google Scholar 

  • Goode MD (1972) Ultrastructure and contractile properties of isolated myofibrils and myofilaments from Drosophila flight muscle. Trans Am Microsc Soc 91:182–194

    Google Scholar 

  • Hanson J (1967) Axial period of actin filaments. Nature (London) 213:353–356

    Google Scholar 

  • Hodge AJ (1955) Studies on the structure of muscle. III. Phase contrast and electron microscopy of Dipteran flight muscle. J Biophys Biochem Cytol 1:361–380

    Google Scholar 

  • Huxley HE, Brown W (1967) The low-angle X-ray diagram of vertebrate striated muscle. J Mol Biol 30:383–434

    Google Scholar 

  • Ludwig HW (1961) Der Sauerstoffverbrauch fliegender Coleopteren. Verh Dtsch Zool Ges Bonn 1960 Zool Anz Suppl 24:96–99

    Google Scholar 

  • Miller A, Tregear RT (1972) Structure of insect fibrillar flight muscle in the presence and absence of ATP. J Mol Biol 70:85–104

    Google Scholar 

  • Morimoto K, Harrington WF (1973) Isolation and composition of thick filaments from rabbit skeletal muscle. J Mol Biol 77:165–175

    Google Scholar 

  • Pringle JWS (1972) Arthropod muscle. In: Structure and function of muscle. Vol I, Bourne GH (ed). Academic Press, New York London, pp 491–541

    Google Scholar 

  • Reedy MK (1967) Crossbridges and periods in insect fibrillar muscle. Am Zool 7:465–481

    Google Scholar 

  • Reedy MK (1968) Ultrastructure of insect flight muscle. I. Screw sense and structural grouping in the rigor cross-bridge lattice. J Mol Biol 31:155–176

    Google Scholar 

  • Reedy MK, Holmes KC, Tregear RT (1965) Induced changes in orientation of the cross-bridges of glycerinated insect flight muscle. Nature (London) 207:1276–1280

    Google Scholar 

  • Reedy MK, Bahr GF, Fischman DA (1973) How many myosins per cross-bridge? I. Flight muscle myofibrils from the blowfly, Sarcophaga bullata. Cold Spring Harbor Symp Quant Biol 37:397–422

    Google Scholar 

  • Rüegg JC (1971) Smooth muscle tone. Physiol Rev 51:201–248

    Google Scholar 

  • Sainsbury GM, Bullard B (1980) New proline rich proteins in isolated insect Z-discs. Biochem J 191:333–339

    Google Scholar 

  • Sotavalta D (1952) The essential factor regulating the wing-stroke frequency of insects in wing mutilation and loading experiments and in experiments at subatmospheric pressure. Ann Soc Vanamo 2:1–51

    Google Scholar 

  • Squire JM (1971) General model for the structure of all myosincontaining filaments. Nature (London) 233:457–4462

    Google Scholar 

  • Squire JM (1973) General model of myosin filament structure. III. Molecular packing arrangements in myosin filaments. J Mol Biol 77:291–323

    Google Scholar 

  • Stempak JG, Ward RT (1964) An improved staining method for electron microscopy. J Cell Biol 22:697–701

    Google Scholar 

  • Tregear RT, Squire JM (1973) Myosin content and filament structure in smooth and striated muscle. J Mol Biol 77:279–290

    Google Scholar 

  • Trinick J, Offer G (1979) Cross-linking of actin filaments by heavy meromyosin. J Mol Biol 133:549–556

    Google Scholar 

  • Venable JH, Coggeshall R (1965) A simplified lead citrate stain for use in electron microscopy. J Cell Biol 25:407–408

    Article  CAS  PubMed  Google Scholar 

  • Voskresenskaya AK (1947) Functional pecularities of the neuromuscular apparatus of the wings of insects. J Physiol USSR 33:381–392

    Google Scholar 

  • Waterston RH, Fishpool RM, Brenner S (1977) Mutants affecting paramyosin in Caenorhabditis elegans. J Mol Biol 117:679–697

    Google Scholar 

  • Wray J, Vibert P, Cohen C (1978) Actin filaments in muscle: Pattern of myosin and tropomyosin/troponin attachments. J Mol Biol 124:501–521

    Google Scholar 

  • Zebe E (1966) Zur Spaltung von Adenosintriphosphat durch die Z-Scheiben der indirekten Flugmuskeln von Phormia regina (Diptera). Experientia 22:96–97

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Zoologisches Institut der Universität Münster, Münster, Bundesrepublik Deutschland

    Gernot Beinbrech, Ursula Meller & Wolfgang Sasse

Authors
  1. Gernot Beinbrech
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ursula Meller
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wolfgang Sasse
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Dedicated to Prof. Dr. Bernhard Rensch on his 85th birthday

Rights and permissions

Reprints and permissions

About this article

Cite this article

Beinbrech, G., Meller, U. & Sasse, W. Paramyosin content and thick filament structure in insect muscles. Cell Tissue Res. 241, 607–614 (1985). https://doi.org/10.1007/BF00214582

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00214582

Key words

Search

Navigation