Subsarcomeric Distribution of Calcium in Demembranated Fibers of Rabbit Psoas Muscle

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 1993 Jan 1

PMID 8431542

Citations 10

Authors

M E Cantino

T S ALLEN

A M Gordon

Affiliations

Soon will be listed here.

Abstract

Direct measurements were made of the Ca distribution within sarcomeres of glycerinated rabbit psoas muscle fibers in rigor using electron probe x-ray microanalysis. Both analogue raster analysis and digital x-ray imaging were used to quantitate the Ca distribution along thick and thin filaments as a function of the concentration of free Ca2+. Even when corrected for the estimated contribution of Ca bound to thick filaments, the Ca measured in the region of overlap between thick and thin filaments significantly exceeded the Ca in the I-band at subsaturating concentrations of free Ca2+. At saturating levels of free Ca2+, the excess Ca in the overlap region was diminished but still statistically significant. The data thus suggest that the formation of rigor linkages exerts multiple effects on the binding of Ca2+ to thin filaments in the overlap region by increasing the affinity of troponin C for Ca2+ and possibly by unmasking additional Ca2+ binding sites. The data also show that the cooperativity invested in the thin filaments is insufficient to permit the effects of rigor cross-bridge formation on Ca2+ binding to propagate far along the thin filaments into the I-band.

Citing Articles

Measurement of calcium dissociation rates from troponin C in rigor skeletal myofibrils.

Little S, Tikunova S, Norman C, Swartz D, Davis J Front Physiol. 2011; 2:70.

PMID: 22013424 PMC: 3190119. DOI: 10.3389/fphys.2011.00070.

Cooperative effects of rigor and cycling cross-bridges on calcium binding to troponin C.

Cantino M, Quintanilla A Biophys J. 2006; 92(2):525-34.

PMID: 17056730 PMC: 1751382. DOI: 10.1529/biophysj.106.093757.

Static and dynamic x-ray diffraction recordings from living mammalian and amphibian skeletal muscles.

Iwamoto H, Wakayama J, Fujisawa T, Yagi N Biophys J. 2003; 85(4):2492-506.

PMID: 14507712 PMC: 1303473. DOI: 10.1016/S0006-3495(03)74672-4.

Isotonic force modulates force redevelopment rate of intact frog muscle fibres: evidence for cross-bridge induced thin filament activation.

Vandenboom R, Hannon J, Sieck G J Physiol. 2002; 543(Pt 2):555-66.

PMID: 12205189 PMC: 2290518. DOI: 10.1113/jphysiol.2002.022673.

Influence of length on force and activation-dependent changes in troponin c structure in skinned cardiac and fast skeletal muscle.

Martyn D, Gordon A Biophys J. 2001; 80(6):2798-808.

PMID: 11371454 PMC: 1301465. DOI: 10.1016/S0006-3495(01)76247-9.

References

Gordon A, Ridgway E, Yates L, Allen T . Muscle cross-bridge attachment: effects on calcium binding and calcium activation. Adv Exp Med Biol. 1988; 226:89-99. View

Phillips R, George P, Rutman R . POTENTIOMETRIC STUDIES OF THE SECONDARY PHOSPHATE IONIZATIONS OF AMP, ADP, AND ATP, AND CALCULATIONS OF THERMODYNAMIC DATA FOR THE HYDROLYSIS REACTIONS. Biochemistry. 1963; 2:501-8. DOI: 10.1021/bi00903a019. View

Somlyo A, Shuman H, Somlyo A . Electron probe X-ray microanalysis of Ca2+, Mg2+, and other ions in rapidly frozen cells. Methods Enzymol. 1989; 172:203-29. DOI: 10.1016/s0076-6879(89)72016-4. View

Phillips R, George P, Rutman R . Thermodynamic studies of the formation and ionization of the magnesium(II) complexes of ADP and ATP over the pH range 5 to 9. J Am Chem Soc. 1966; 88(12):2631-40. DOI: 10.1021/ja00964a002. View

HELLAM D, PODOLSKY R . Force measurements in skinned muscle fibres. J Physiol. 1969; 200(3):807-19. PMC: 1350528. DOI: 10.1113/jphysiol.1969.sp008723. View

Ebashi S, Endo M . Calcium ion and muscle contraction. Prog Biophys Mol Biol. 1968; 18:123-83. DOI: 10.1016/0079-6107(68)90023-0. View

Bremel R, Weber A . Cooperation within actin filament in vertebrate skeletal muscle. Nat New Biol. 1972; 238(82):97-101. DOI: 10.1038/newbio238097a0. View

Gordon A, Godt R, Donaldson S, Harris C . Tension in skinned frog muscle fibers in solutions of varying ionic strength and neutral salt composition. J Gen Physiol. 1973; 62(5):550-74. PMC: 2226133. DOI: 10.1085/jgp.62.5.550. View

Potter J, Gergely J . The calcium and magnesium binding sites on troponin and their role in the regulation of myofibrillar adenosine triphosphatase. J Biol Chem. 1975; 250(12):4628-33. View

10.

Fuchs F . The binding of calcium to glycerinated muscle fibers in rigor. The effect of filament overlap. Biochim Biophys Acta. 1977; 491(2):523-31. DOI: 10.1016/0005-2795(77)90297-5. View

11.

Shuman H, Somlyo A, Somlyo A . Quantitative electron probe microanalysis of biological thin sections: methods and validity. Ultramicroscopy. 1976; 1(4):317-39. DOI: 10.1016/0304-3991(76)90049-8. View

12.

Fuchs F . Cooperative interactions between calcium-binding sites on glycerinated muscle fibers. The influence of cross-bridge attachment. Biochim Biophys Acta. 1977; 462(2):314-22. DOI: 10.1016/0005-2728(77)90130-x. View

13.

Fuchs F . On the relation between filament overlap and the number of calcium-binding sites on glycerinated muscle fibers. Biophys J. 1978; 21(3):273-7. PMC: 1473686. DOI: 10.1016/S0006-3495(78)85524-6. View

14.

OSullivan W, Smithers G . Stability constants for biologically important metal-ligand complexes. Methods Enzymol. 1979; 63:294-336. DOI: 10.1016/0076-6879(79)63014-8. View

15.

Fuchs F, Black B . The effect of magnesium ions on the binding of calcium ions to glycerinated rabbit psoas muscle fibers. Biochim Biophys Acta. 1980; 622(1):52-62. DOI: 10.1016/0005-2795(80)90157-9. View

16.

Trybus K, Taylor E . Kinetic studies of the cooperative binding of subfragment 1 to regulated actin. Proc Natl Acad Sci U S A. 1980; 77(12):7209-13. PMC: 350471. DOI: 10.1073/pnas.77.12.7209. View

17.

Wegner A, Walsh T . Interaction of tropomyosin-troponin with actin filaments. Biochemistry. 1981; 20(19):5633-42. DOI: 10.1021/bi00522a043. View

18.

Hall T, Gupta B . Quantification for the x-ray microanalysis of cryosections. J Microsc. 1982; 126(Pt 3):333-45. DOI: 10.1111/j.1365-2818.1982.tb00389.x. View

19.

Allen D, Kurihara S . The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle. J Physiol. 1982; 327:79-94. PMC: 1225098. DOI: 10.1113/jphysiol.1982.sp014221. View

20.

Wang K . Purification of titin and nebulin. Methods Enzymol. 1982; 85 Pt B:264-74. DOI: 10.1016/0076-6879(82)85025-8. View