Skip to main content
SpringerLink
Log in

Digestion of proteins associated with the Z-disc by calpain

  • Papers
  • Published:
Journal of Muscle Research & Cell Motility Aims and scope Submit manuscript

Summary

The Z-disc of striated muscle is degraded by the Ca2+ -activated proteinase, calpain, during autolysis of muscle fibres. The effect of calpain on proteins in preparations of Z-discs isolated fromLethocerus flight muscle has been studied. Calpain releasesα-actinin from the Z-disc and digests two hydrophobic proteins associated with the Z-disc, zeelin 1 (35 kD) and zeelin 2 (23 kD). The Ca2+ sensitivity of zeelin digestion is shifted to lower Ca2+ concentrations (within the physiological range) in the presence of the phospholipids phosphatidyl inositol or phosphatidyl choline and diacylglycerol. The release ofα-actinin is not affected by phospholipid. Preparations of isolated Z-discs have five times as much associated phospholipid (w/w) as myofibrils and the composition of the lipid differs from that of myofibrils. In muscle fibres the action of calpain on zeelins may be controlled by the composition of phospholipid in the fibres as well as by Ca2+.

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

  • Azana, J.-L., Raymond, J., Robin, J.-M., Cottin, P. &Ducastaing, A. (1979) Purification and some physico-chemical and enzymatic properties of a calcium ionactivated neutral proteinase from rabbit skeletal muscle.Biochem. J. 183, 339–47.

    PubMed  Google Scholar 

  • Bangham, A. D. &Horne, R. W. (1964) Negative staining of phospholipids and their structural modifications by surface-active agents as observed in the electron microscope.J. molec. Biol. 8, 660–8.

    Google Scholar 

  • Baron, M. D., Davison, M. D., Jones, P. &Critchley, D. R. (1987) The sequence of chick α-actinin reveals homologies to spectrin and calmodulin.J. Biol. Chem. 262, 17623–9.

    PubMed  Google Scholar 

  • Berridge, M. J. (1988) Inositol lipids and calcium signalling.Proc. Roy. Soc. Ser. B 234, 359–78.

    Google Scholar 

  • Bullard, B., Bell, J., Craig, R. &Leonard, K. (1985) Arthrin: a new actin-like protein in insect flight muscle.J. molec. Biol. 182, 443–54.

    Article  PubMed  Google Scholar 

  • Bullard, B., Dabrowska, R. &Winkelman, L. (1973) The contractile and regulatory proteins of insect flight muscle.Biochem. J. 135, 277–86.

    PubMed  Google Scholar 

  • Bullard, B. &Reedy, M. K. (1973) How many myosins per crossbridge? II Flight muscle myosin from the blowflySarcophaga bullata.Cold Spring Harb. Symp. quant. Biol. 37, 423–8.

    Google Scholar 

  • Busch, W. A., Stromer, M. H., Goll, D. E. &Suzuki, A. (1972) Ca2+ -specific removal of Z-lines from rabbit skeletal muscle.J. Cell Biol. 52, 367–81.

    Article  PubMed  Google Scholar 

  • Cong, J., Goll, D. E., Peterson, A. M. &Kapprell, H. P. (1989) The role of autolysis in activity of the Ca2+ -dependent proteinases (μ-calpain and m-calpain).J. Biol. Chem. 264, 10096–103.

    PubMed  Google Scholar 

  • Coolican, S. A. &Hathaway, D. R. (1984) Effect of L-a-phosphatidylinositol on a vascular smooth muscle Ca2+ -dependent protease. Reduction of the Ca2+ requirement of autolysis.J. Biol. Chem. 259, 11627–30.

    PubMed  Google Scholar 

  • Dayton, W. R., Reville, W. J., Goll, D. E. &Stromer, M. H. (1976) A Ca2+-activated protease possibly involved in myofibrillar protein turnover.Biochemistry 15, 2159–67.

    Article  PubMed  Google Scholar 

  • Dayton, W. R. &Schollmeyer, J. V. (1980) Isolation from porcine cardiac muscle of a Ca2+ -activated protease that partially degrades myofibrils.J. molec. cell. Cardiol. 12, 533–51.

    Article  Google Scholar 

  • Dayton, W. R., Schollmeyer, J. V., Lepley, R. A. &Cortes, L. R. (1981) A calcium-activated protease possibly involved in myofibrillar protein turnover. Isolation of a low-calcium-requiring form of the protease.Biochim. Biophys. Acta 659, 48–61.

    PubMed  Google Scholar 

  • Goll, D. E., Edmunds, T., Kleese, W. C., Sathe, S. K. &Shannon, J. D. (1985) Some properties of the Ca2+ -dependent proteinase.Prog. Clin. Biol. Res. 180, 151–64.

    PubMed  Google Scholar 

  • Goll, D. E., Shannon, J. D., Edmunds, T., Sathe, S. K., Kleese, W. C. &Nagainis, P.A. (1983) Properties and regulation of the Ca2+-dependent proteinase. InCalcium-Binding Proteins (edited byDe Bernard, B., Sottocasa, G. L., Sandri, G., Carafoli, E., Taylor, A. N., Vanaman, T. C. &Williams, R. J. P.), pp. 19–35. Amsterdam: Elsevier Science Publishers.

    Google Scholar 

  • Gopalakrishna, R. &Barsky, S. H. (1986) Hydrophobic association of calpains with subcellular organelles. Compartimentalization of calpains and the endogenous inhibitor calpastatin in tissues.J. Biol. Chem. 261, 13936–42.

    PubMed  Google Scholar 

  • Haeberle, J. R., Coolican, S. A., Evan, A. &Hathaway, D. R. (1985) The effects of a calcium-dependent protease on the ultrastructure and contractile mechanics of skinned uterine smooth muscle.J. Musc. Res. Cell Motil. 6, 347–63.

    Article  Google Scholar 

  • Hathaway, D. R., Werth, D. K. &Haeberle, J. R. (1982) Limited autolysis reduces the Ca2+-requirement of a smooth muscle Ca2+-activated protease.J. Biol. Chem. 257, 9072–7.

    PubMed  Google Scholar 

  • Imajoh, S., Kawasaki, H. &Suzuki, K. (1986) The amino-terminal hydrophobic region of the small subunit of calcium-activated neutral protease (CANP) is essential for its activation by phosphatidylinositol.J. Biochem. 99, 1281–4.

    PubMed  Google Scholar 

  • Kishimoto, A., Kajikawa, N., Shiota, M. &Nishizuka, Y. (1983) Proteolytic activation of calcium-activated, phospholipid-dependent protein kinase by calcium-dependent neutral protease.J. Biol. Chem. 258, 1156–64.

    PubMed  Google Scholar 

  • Kishimoto, A., Takai, Y., Mori, T., Kikkawa, U. &Nishizuka, Y. (1980) Activation of calcium and phopholipid-dependent protein kinase by diacylglycerol, its possible relation to phosphatidylinositol turnover.J. Biol. Chem. 255, 2273–76.

    PubMed  Google Scholar 

  • Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Nature 227, 680–5.

    Article  PubMed  Google Scholar 

  • Martonosi, A. N. &Beeler, T. J. (1983) Mechanism of Ca2+ transport by sarcoplasmic reticulum. InHandbook of Physiology, Skeletal Muscle (edited byPeachey, L. D., Adrian, R. H. &Geiger, S. R.), Vol. 10, pp. 417–85. Bethesda: American Physiol. Soc.

    Google Scholar 

  • McClare, C. W. F. (1971) An accurate and convenient organic phosphorus assay.Anal. Biochem. 39, 527–30.

    Article  PubMed  Google Scholar 

  • Mellgren, R. L. (1980) Canine cardiac calcium-dependent proteases: Resolution of two forms with different requirements for calcium.FEBS Lett. 109, 129–33.

    Article  PubMed  Google Scholar 

  • Mellgren, R. L. (1987) Calcium-dependent proteases: an enzyme system active at cellular membranes?FASEB J. 1, 110–5.

    PubMed  Google Scholar 

  • Miller, N. G. A., Hill, M. W. &Smith, M. W. (1976) Positional and species analysis of membrane phospholipids extracted from goldfish adapted to different environmental temperatures.Biochim. Biophys. Acta 455, 644–54.

    PubMed  Google Scholar 

  • Muguruma, M., Muguruma, Y. &Fukazawa, T. (1980) Contribution of Z-line constituents to the formation of the contraction bands of chicken myofibrils on addition of Mg2+-ATP.J. Biochem. 88, 145–9.

    PubMed  Google Scholar 

  • Murachi, T., Tanaka, K., Hatanaka, M. &Murakami, T. (1981) Intracellular Ca2+-dependent protease (calpain) and its high-molecular-weight endogenous inhibitor (calpastatin).Adv. Enzyme Regul. 19, 407–24.

    Article  Google Scholar 

  • Nishizuka, Y. (1984) The role of protein kinase C in cell surface signal transduction and tumour promotion.Nature 308, 693–8.

    PubMed  Google Scholar 

  • Papahadjopoulos, D. &Miller, N. (1967) Phospholipid model membranes I. Structural characteristics of hydrated liquid crystals.Biochim. Biophys. Acta 135, 624–38.

    PubMed  Google Scholar 

  • Pérrin, D. D. &Sayce, I. G. (1967) Computer calculation of the equilibrium concentrations of metal ions and complexing species.Talanta 14, 833–42.

    Article  Google Scholar 

  • Pontremoli, S., Melloni, E., Sparatore, B., Salamino, F., Michetti, M., Sacco, O. &Horecker, B. L. (1985) Role of phospholipids in the activation of the Ca2+ -dependent neutral proteinase of human erythrocytes.Biochem. Biophys. Res. Commun. 129, 389–95.

    Article  PubMed  Google Scholar 

  • Reddy, M. K., Etlinger, J. D., Rabinowitz, M., Fischman, D. A. &Zak, R. (1975) Removal of Z-lines and alpha-actinin from isolated myofibrils by a calcium-activated neutral protease.J. biol. Chem. 250, 4278–84.

    PubMed  Google Scholar 

  • Reedy, M. K., Leonard, K. R., Freeman, R &Arad, T. (1981) Thick myofilament mass determination by electron scattering measurements with the scanning transmission electron microscope.J. Musc. Res. Cell Motility 2, 45–64.

    Article  Google Scholar 

  • Saide, J. D. &Ullrick, W. C. (1974) Purification and properties of the isolated honeybee Z-disc.J. molec. Biol. 87, 671–83.

    Article  PubMed  Google Scholar 

  • Sainsbury, G. M. &Bullard, B. (1980) New proline-rich proteins in isolated insect Z-discs.Biochem. J. 191, 333–9.

    PubMed  Google Scholar 

  • Sainsbury, G. M. &Hulmes, D. (1977) Notes on the structure of the Z-disc of insect flight muscle. InInsect Flight Muscle (edited byTregear, R. T.), pp. 75–8. Amsterdam: North-Holland.

    Google Scholar 

  • Starkey, P. M. &Barrett, A. J. (1976) Neutral proteinases of human spleen. Purification and criteria for homogeneity of elastase and cathepsin G.Biochem. J. 155, 255–63.

    PubMed  Google Scholar 

  • Sugita, H., Ishiura, S., Suzuki, K. &Imahori, K. (1980) Ca2+ -activated neutral protease and its inhibitors:in vitro effect on intact myofibrils.Muscle Nerve 3, 335–9.

    Article  PubMed  Google Scholar 

  • Suzuki, K. (1987) Calcium-activated neutral protease: domain structure and activity regulation.Trends in biochem. Sci. 12, 103–5.

    Article  Google Scholar 

  • Suzuki, A., Nonami, Y., &Goll, D. E. (1975) Proteins released from myofibrils by CASF (Ca2+-activated sarcoplasmic factor) and trypsin.Agric. Biol. Chem,39, 1461–7.

    Google Scholar 

  • Szpacenko, A., Kay, J., Goll, D. E. &Otsuka, Y. (1981) A different form of the Ca2+ -dependent proteinase activated by micromolar levels of Ca2+. InProteinases and their Inhibitors. Structure, Function and Applied Aspects. (edited byTurk, V. &Vitale, Lj.), pp. 151–61. Ljubljana, Oxford: Mladinska knjiga-Pergamon Press.

    Google Scholar 

  • Turner, P. R., Westwood, T., Regan, C. M. &Steinhardt, R. A. (1988) Increased protein degradation results from elevated free calcium levels found in muscle frommdx mice.Nature 335, 735–8.

    Article  PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Belinda Bullard

    Present address: European Molecular Biology Laboratory, Postfach 10.2209, D-6900, Heidelberg, West Germany

  2. Gillian Sainsbury

    Present address: Department of Pharmacology, South Parks Road, Oxford, UK

Authors and Affiliations

  1. AFRC Institute of Animal Physiology and Genetics Research, CB2 4AT, Babraham, Cambridge, UK

    Belinda Bullard, Gillian Sainsbury & Nigel Miller

Authors
  1. Belinda Bullard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gillian Sainsbury
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nigel Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bullard, B., Sainsbury, G. & Miller, N. Digestion of proteins associated with the Z-disc by calpain. J Muscle Res Cell Motil 11, 271–279 (1990). https://doi.org/10.1007/BF01843580

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01843580

Keywords

Search

Navigation