Skip to main content
SpringerLink
Log in

Histochemistry of sarcoplasmic reticulum Ca-ATPase using dysprosium as capturing reagent

  • Papers
  • Published:
The Histochemical Journal Aims and scope Submit manuscript

Summary

This report describes the development of a histochemical method for the demonstration of sarcoplasmic reticulum Ca-ATPase activity in cross-sections of skeletal muscle. The demonstration of sarcoplasmic reticulum Ca-ATPase activity is complicated by the fact that capturing reagents for phosphate inhibit the enzyme. We present a minimal model for heavy-metal-phosphate precipitation reactions which gives a theoretical description of the effect of enzyme inhibition on the rate of phosphate precipitation in the section. The model indicates that the choice of capturing reagent is crucial: whether or not ATPase activity can be demonstrated depends mainly on the inhibition constant and the solubility product of the phosphate salt of the capturing reagent (but also on a fairly large number of other factors). All lanthanides tested can be used to demonstrate sarcoplasmic reticulum Ca-ATPase activity, but dysprosium results in the highest staining intensity. This suggests that dysprosium inhibits sarcoplasmic reticulum Ca-ATPase to a lesser degree than the other lanthanides and/or the solubility product of its phosphate salt is smaller. As an example, the method is used to investigate the effect of thyroid hormone on sarcoplasmic reticulum Ca-ATPase activity in individual fibres of the rat soleus muscle.

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

  • barry,p. h. &diamond,j. m. (1984) Effects of unstirred layers on membrane phenomena.Physiol. Rev. 64, 763–872.

    PubMed  CAS  Google Scholar 

  • herman,m. c.,mcintosh,d. b. &kench,j. e. (1977) Proton inactivation of Ca2+ transport by sarcoplasmic reticulum.J. Biol. Chem. 252, 994–1001.

    Google Scholar 

  • blanco,c. e. &sieck,g. c. (1992) Quantitative determination of calcium-activated myosin adenosine triphosphatase activity in rat skeletal muscle fibres.Histochem. J. 24, 431–44.

    Article  PubMed  CAS  Google Scholar 

  • briggs,n. f.,lee,k. f.,feher,j. j.,Wechsler,a. s.,ohlendieck,k. &campbell,k. (1990) Ca-ATPase isozyme expression in sarcoplasmic reticulum is altered by chronic stimulation of muscle.FEBS Lett. 259, 269–72.

    Article  PubMed  CAS  Google Scholar 

  • buschman, H. P. J., Stienen, G. J. M., Van Der Laarse, W. J. &elzinga, G. (1996) Activationand tension-related heat in single slow- and fasttwitch muscle fibers fromXenopus laevis. (submitted).

  • butcher,r. g. (1983) Enzyme histochemistry of the myocardium. InCardiac Metabolism (edited bydrake-Holland,a. j. &noble,m. i. m.). pp. 445–69. Chichester: John Wiley & Sons Ltd.

    Google Scholar 

  • dejong,a. S. h. (1982) Mechanisms of metal-salt methods in enzyme cytochemistry with special reference to acid phosphatase.Histochem. J. 14, 1–33.

    Article  PubMed  Google Scholar 

  • edman,k. a. p.,reggiani,c.,schiaffino,s. &t.E. Kronnie,g. (1988) Maximum velocity of shortening related to myosin isoform composition in frog skeletal muscles fibres.J. Physiol. 395, 679–94.

    PubMed  CAS  Google Scholar 

  • fujimori,t. &jencks,W. p. (1990) Lanthanum inhibits steady-state turnover of the sarcoplasmic reticulum calcium ATPase by replacing magnesium as the catalytic ion.J. Biol. Chem. 265, 16262–70.

    PubMed  CAS  Google Scholar 

  • guth,l. &samaha,f. j. (1969) Qualitative differences between actomyosin ATPase of slow and fast mammalian muscle.Exp. Neurol. 25, 138–52.

    Article  PubMed  CAS  Google Scholar 

  • hechtenberg,s. &beyersmann,d. (1991) Inhibition of sarcoplasmic reticulum Ca2+-ATPase activity by cadmium, lead and mercury.Enzyme 45, 109–15.

    PubMed  CAS  Google Scholar 

  • hill,a. v. (1965)Trails and Trials in Physiology, pp. 216–7. London: Edward Arnold Ltd.

    Google Scholar 

  • homsher,e. &kean,c. j. (1978) Skeletal muscle energetics and metabolism.Annu. Rev. Physiol. 40, 93–131.

    Article  PubMed  CAS  Google Scholar 

  • jorgenson,a. o.,kalnins,v. &maclennan,d. h. (1979) Localization of sarcoplasmic reticulum protein in rat skeletal muscle by immunofluorescence.J. Cell Biol. 80, 372–84.

    Google Scholar 

  • jorgenson,a. o.,arnold,w.,pepper,d. r.,kahl,s. d.,mandel,f. &campbell,k. p. (1988) A monoclonal antibody to the Ca2+ ATPase of cardiac sarcoplasmic reticulum cross-reacts with slow type I but not with fast type II canine skeletal muscle fibres: an immunocytochemical and immunochemical study.Cell Motil. Cytoskel. 9, 164–74.

    Google Scholar 

  • kahn,m. a. (1976) Histochemical characteristics of vertebrate striated muscle: a review.Prog. Histochem. Cytochem. 8, 1–47.

    Google Scholar 

  • krenács,t.,molnar,e.,dobó,e. &dux,l. (1989) Fibre typing using sarcoplasmic reticulum Ca2+-ATPase and myoglobin immunohistochemistry in rat gastrocnemius muscle.Histochem. J. 21, 145–55.

    Article  PubMed  Google Scholar 

  • lännergren,j. &smith,r. s. (1966) Types of muscle fibres in toad skeletal muscle.Acta Physiol. Scand. 68, 263–74.

    Google Scholar 

  • lytton,j.,Westlin,m. &hanley,m. r. (1991) Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of pumps.J. Biol. Chem. 266, 17067–71.

    PubMed  CAS  Google Scholar 

  • maier,a.,leberer,e. &pette,d. (1986) Distribution of sarcoplasmic reticulum Ca-ATPase and of calsequestrin in rabbit and rat skeletal muscle fibres.Histochemistry 86, 63–69.

    Article  PubMed  CAS  Google Scholar 

  • meijer,a. E. f. h. (1970) Histochemical method for demonstration of myosin adenosine triphosphatase in muscle tissues.Histochemie 22, 51–8.

    Article  PubMed  CAS  Google Scholar 

  • morrison, J. F. &cleland, W. W. (1983) Lanthanideadenosine 5′-triphosphate complexes: determination of their dissociation constants and mechanisms of action as inhibitors of yeast hexokinase.Biochemistry 22, 5507–13.

    Google Scholar 

  • muller,a.,van Derlinden,g. c.,zuidwijk,m. j.,simonides,W. s.,van Derlaarse,W. j. &vanhardeveld,c. (1994) Differential effects of thyroid hormone on the expression of sarcoplasmic reticulum Ca2+-ATPase isoforms in rat skeletal muscle fibres.Biochem. Biophys. Res. Commun. 203, 1035–42.

    Article  PubMed  CAS  Google Scholar 

  • reynolds,e. s. (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy.J. Cell Biol. 17, 208–12.

    Article  PubMed  CAS  Google Scholar 

  • schmalbruch,h. (1985)Handbook of Microscopic Anatomy II/6: Skeletal Muscle, pp. 95–107. Berlin: Springer Verlag.

    Google Scholar 

  • seidler,n. w.,jona,i.,vegh,m. &martonosi,a. (1989) Cyclopiazonic acid is a specific inhibitor of the Ca2+ATPase of sarcoplasmic reticulum.J. Biol. Chem. 264, 17816–23.

    PubMed  CAS  Google Scholar 

  • simonides,W. s. &vanhardeveld,c. (1985) The effect of hypothyroidism on sarcoplasmic reticulum in fasttwitch muscle of the rate.Biochem. Biophys. Acta 844, 129–41.

    PubMed  CAS  Google Scholar 

  • simonides,W. s. &vanhardeveld,c. (1990) An assay for sarcoplasmic reticulum Ca2+-ATPase activity in muscle homogenates.Anal. Biochem. 191, 321–31.

    Article  PubMed  CAS  Google Scholar 

  • simonides,W. s.,van Derlinden,g. c. &vanhardeveld,c. (1990) Thyroid hormone differentially affects mRNA levels of Ca-ATPase isozymes of sarcoplasmic reticulum in fast and slow skeletal muscle.FEBS Lett. 274, 73–6.

    Article  PubMed  CAS  Google Scholar 

  • smith,r. m.,martell,a. e. (1976)Critical Stability Constants, Vol 4:Inorganic Complexes, pp. 57–8. New York: Plenum Press.

    Google Scholar 

  • stahl,W. l. &baskin,d. g. (1990) Histochemistry of ATPases.J. Histochem. Cytochem. 38, 1099–122.

    PubMed  CAS  Google Scholar 

  • tice,l. w. (1969) Lead-adenosine triphosphate complexes in adenosine triphosphate histochemistry.J. Histochem. Cytochem. 17, 85–94.

    PubMed  CAS  Google Scholar 

  • van Derlaarse,W. j.,diegenbach,p. c. &maslam,s. (1984) Quantitative histochemistry of three mouse hind-limb muscles: the relationship between calcium-stimulated myofibrillar ATPase and succinate dehydrogenase activities.Histochem. J. 16, 529–41.

    Article  PubMed  Google Scholar 

  • van Derlaarse,W. j.,diegenbach,p. c. &hemminga,m. a. (1986) Calcium-stimulated myofibrillar ATPase activity correlates with shortening velocity of muscle fibres inXenopus laevis. Histochem. J.18, 487–96.

    Article  PubMed  Google Scholar 

  • van Derlaarse,W. j.,lÄnnergren,j. &diegen-Bach,p. c. (1991) Resistance to fatigue of single muscle fibres fromXenopus related to succinate dehydrogenase and myofibrillar ATPase activities.Exp. Physiol. 76, 589–96.

    PubMed  Google Scholar 

  • van Derlaarse,W. j.,lee-Degroot,m. b. e. &diegenbach,p. c. (1994) The maximum sustainable duty cycle of singleXenopus muscle fibres related to succinate dehydrogenase and myofibrillar ATPase activities.J. Musc. Res. Cell Motil. 15, 180.

    Google Scholar 

  • vanduijn,p. (1991) Model systems. Principles and practice of the use of matrix-immobilized enzymes for the study of the fundamental aspects of cytochemical enzyme methods. InHistochemistry, Theoretical and Applied III (edited bystoward,p. j. &pearse,a. g. e.), pp. 433–72. Edinburgh: Churchill Livingstone.

    Google Scholar 

  • vannoorden,c. j. f. &butcher,r. g. (1991) Quantitative enzyme histochemistry. InHistochemistry, Theoretical and Applied III (edited bystoward,p. j. &pearse,a. g. e.), pp. 355–432. Edinburgh: Churchill Livingstone.

    Google Scholar 

  • yoshizaki,k.,Watari,h. &radda,g. k. (1990) Role of phosphocreatine in energy transport in skeletal muscle of bullfrog studied by31P-NMR.Biochem. Biophys. Acta 1051, 144–50.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory for Physiology, Institute for Cardiovascular Research (ICaR-VU), Vrije Universiteit, Van der Boechorststraat 7, 1081 BT, Amsterdam, The Netherlands

    W. J. Van Der Laarse, P. Van Noort, W. S. Simonides, M. B. E. Lee-De Groot & C. Van Hardeveld

  2. Department of Experimental Zoology, Universiteit van Amsterdam, Kruislaan 320, 1098 SM, Amsterdam, The Netherlands

    P. C. Diegenbach

Authors
  1. W. J. Van Der Laarse
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Van Noort
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. W. S. Simonides
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. C. Diegenbach
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. B. E. Lee-De Groot
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C. Van Hardeveld
    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

Van Der Laarse, W.J., Van Noort, P., Simonides, W.S. et al. Histochemistry of sarcoplasmic reticulum Ca-ATPase using dysprosium as capturing reagent. Histochem J 27, 702–714 (1995). https://doi.org/10.1007/BF02388543

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02388543

Keywords

Search

Navigation