Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 1998 Aug;75(2):948–956. doi: 10.1016/S0006-3495(98)77583-6

Distributions of calcium in A and I bands of skinned vertebrate muscle fibers stretched to beyond filament overlap.

M E Cantino 1, J G Eichen 1, S B Daniels 1
PMCID: PMC1299768  PMID: 9675195

Abstract

Measurements were made of the distributions of total calcium along the length of A and I bands in skinned frog semitendinosus muscles using electron probe x-ray microanalysis. Since calcium in the water space was kept below the detection limit of the technique, the signal was assumed to reflect the distribution of calcium bound to myofilament proteins. Data from sarcomeres with overlap between thick and thin filaments showed enhancement of calcium in this region, as previously demonstrated in rabbit psoas muscle fibers in rigor (Cantino, M. E., T. S. Allen, and A. M. Gordon. 1993. Subsarcomeric distribution of calcium in demembranated fibers of rabbit psoas muscle. Biophys. J. 64:211-222). Such enhancement could arise from intrinsic non-uniformities in calcium binding to either thick or thin filaments or from enhancement of calcium binding to either filament by rigor cross-bridge attachment. To test for intrinsic variations in calcium binding, calcium distributions were determined in fibers stretched to beyond filament overlap. Calcium binding was found to be relatively uniform along both thick and thin filaments, and therefore cannot account for the increased calcium observed in the overlap region. From these results it can be concluded that the observed enhancement of calcium is due to an increase in calcium binding to myofilaments as a result of rigor attachment of cross-bridges to actin. The source of the enhancement is most likely an increase in calcium binding to troponin, although enhancement of calcium binding to myosin light chains cannot be ruled out.

Full Text

The Full Text of this article is available as a PDF (246.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allen D. G., Kurihara S. The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle. J Physiol. 1982 Jun;327:79–94. doi: 10.1113/jphysiol.1982.sp014221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Allen T. S., Yates L. D., Gordon A. M. Ca(2+)-dependence of structural changes in troponin-C in demembranated fibers of rabbit psoas muscle. Biophys J. 1992 Feb;61(2):399–409. doi: 10.1016/S0006-3495(92)81846-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bennett A. J., Bagshaw C. R. The kinetics of bivalent metal ion dissociation from myosin subfragments. Biochem J. 1986 Jan 1;233(1):173–177. doi: 10.1042/bj2330173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bremel R. D., Weber A. Cooperation within actin filament in vertebrate skeletal muscle. Nat New Biol. 1972 Jul 26;238(82):97–101. doi: 10.1038/newbio238097a0. [DOI] [PubMed] [Google Scholar]
  5. Cantino M. E., Allen T. S., Gordon A. M. Subsarcomeric distribution of calcium in demembranated fibers of rabbit psoas muscle. Biophys J. 1993 Jan;64(1):211–222. doi: 10.1016/S0006-3495(93)81358-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Carlsen F., Fuchs F., Knappeis G. G. Contractility and ultrastructure in glycerol--extracted muscle fibers. I. The relationship of contractility to sarcomere length. J Cell Biol. 1965 Oct;27(1):25–34. doi: 10.1083/jcb.27.1.25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Carlsen F., Fuchs F., Knappeis G. G. Contractility and ultrastructure in glycerol--extracted muscle fibers. II. Ultrastructure in resting and shortened fibers. J Cell Biol. 1965 Oct;27(1):35–46. doi: 10.1083/jcb.27.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chiu Y. L., Asayama J., Ford L. E. A sensitive photoelectric force transducer with a resonant frequency of 6 kHz. Am J Physiol. 1982 Nov;243(5):C299–C302. doi: 10.1152/ajpcell.1982.243.5.C299. [DOI] [PubMed] [Google Scholar]
  9. Ebashi S., Endo M. Calcium ion and muscle contraction. Prog Biophys Mol Biol. 1968;18:123–183. doi: 10.1016/0079-6107(68)90023-0. [DOI] [PubMed] [Google Scholar]
  10. Fabiato A. Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. Methods Enzymol. 1988;157:378–417. doi: 10.1016/0076-6879(88)57093-3. [DOI] [PubMed] [Google Scholar]
  11. Fink R. H., Stephenson D. G., Williams D. A. Potassium and ionic strength effects on the isometric force of skinned twitch muscle fibres of the rat and toad. J Physiol. 1986 Jan;370:317–337. doi: 10.1113/jphysiol.1986.sp015937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fuchs F. Cooperative interactions between calcium-binding sites on glycerinated muscle fibers. The influence of cross-bridge attachment. Biochim Biophys Acta. 1977 Nov 17;462(2):314–322. doi: 10.1016/0005-2728(77)90130-x. [DOI] [PubMed] [Google Scholar]
  13. Fuchs F. The binding of calcium to glycerinated muscle fibers in rigor. The effect of filament overlap. Biochim Biophys Acta. 1977 Apr 25;491(2):523–531. doi: 10.1016/0005-2795(77)90297-5. [DOI] [PubMed] [Google Scholar]
  14. Gordon A. M., Godt R. E., Donaldson S. K., Harris C. E. Tension in skinned frog muscle fibers in solutions of varying ionic strength and neutral salt composition. J Gen Physiol. 1973 Nov;62(5):550–574. doi: 10.1085/jgp.62.5.550. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gordon A. M., Ridgway E. B., Yates L. D., Allen T. Muscle cross-bridge attachment: effects on calcium binding and calcium activation. Adv Exp Med Biol. 1988;226:89–99. [PubMed] [Google Scholar]
  16. Güth K., Potter J. D. Effect of rigor and cycling cross-bridges on the structure of troponin C and on the Ca2+ affinity of the Ca2+-specific regulatory sites in skinned rabbit psoas fibers. J Biol Chem. 1987 Oct 5;262(28):13627–13635. [PubMed] [Google Scholar]
  17. Hellam D. C., Podolsky R. J. Force measurements in skinned muscle fibres. J Physiol. 1969 Feb;200(3):807–819. doi: 10.1113/jphysiol.1969.sp008723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hofmann P. A., Fuchs F. Effect of length and cross-bridge attachment on Ca2+ binding to cardiac troponin C. Am J Physiol. 1987 Jul;253(1 Pt 1):C90–C96. doi: 10.1152/ajpcell.1987.253.1.C90. [DOI] [PubMed] [Google Scholar]
  19. Holroyde M. J., Potter J. D., Solaro R. J. The calcium binding properties of phosphorylated and unphosphorylated cardiac and skeletal myosins. J Biol Chem. 1979 Jul 25;254(14):6478–6482. [PubMed] [Google Scholar]
  20. Kitazawa T., Shuman H., Somlyo A. P. Calcium and magnesium binding to thin and thick filaments in skinned muscle fibres: electron probe analysis. J Muscle Res Cell Motil. 1982 Dec;3(4):437–454. doi: 10.1007/BF00712093. [DOI] [PubMed] [Google Scholar]
  21. LeFurgey A., Bond M., Ingram P. Frontiers in electron probe microanalysis: application to cell physiology. Ultramicroscopy. 1988;24(2-3):185–219. doi: 10.1016/0304-3991(88)90311-7. [DOI] [PubMed] [Google Scholar]
  22. Moss R. L. Ca2+ regulation of mechanical properties of striated muscle. Mechanistic studies using extraction and replacement of regulatory proteins. Circ Res. 1992 May;70(5):865–884. doi: 10.1161/01.res.70.5.865. [DOI] [PubMed] [Google Scholar]
  23. Pan B. S., Solaro R. J. Calcium-binding properties of troponin C in detergent-skinned heart muscle fibers. J Biol Chem. 1987 Jun 5;262(16):7839–7849. [PubMed] [Google Scholar]
  24. Ridgway E. B., Gordon A. M. Muscle calcium transient. Effect of post-stimulus length changes in single fibers. J Gen Physiol. 1984 Jan;83(1):75–103. doi: 10.1085/jgp.83.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Shuman H., Somlyo A. V., Somlyo A. P. Quantitative electron probe microanalysis of biological thin sections: methods and validity. Ultramicroscopy. 1976 Sep-Oct;1(4):317–339. doi: 10.1016/0304-3991(76)90049-8. [DOI] [PubMed] [Google Scholar]
  26. Somlyo A. V., Shuman H., Somlyo A. P. Electron probe X-ray microanalysis of Ca2+, Mg2+, and other ions in rapidly frozen cells. Methods Enzymol. 1989;172:203–229. doi: 10.1016/s0076-6879(89)72016-4. [DOI] [PubMed] [Google Scholar]
  27. Trybus K. M., Taylor E. W. Kinetic studies of the cooperative binding of subfragment 1 to regulated actin. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7209–7213. doi: 10.1073/pnas.77.12.7209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. WINEGRAD S. AUTORADIOGRAPHIC STUDIES OF INTRACELLULAR CALCIUM IN FROG SKELETAL MUSCLE. J Gen Physiol. 1965 Jan;48:455–479. doi: 10.1085/jgp.48.3.455. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES