Phosphorylation of Myosin Regulatory Light Chain Eliminates Force-dependent Changes in Relaxation Rates in Skeletal Muscle

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 1998 Feb 4

PMID 9449336

Citations 23

Authors

J R Patel

G M Diffee

X P Huang

R L Moss

Affiliations

Soon will be listed here.

Abstract

The rate of relaxation from steady-state force in rabbit psoas fiber bundles was examined before and after phosphorylation of myosin regulatory light chain (RLC). Relaxation was initiated using diazo-2, a photolabile Ca2+ chelator that has low Ca2+ binding affinity (K(Ca) = 4.5 x 10(5) M(-1)) before photolysis and high affinity (K(Ca) = 1.3 x 10(7) M(-1)) after photolysis. Before phosphorylating RLC, the half-times for relaxation initiated from 0.27 +/- 0.02, 0.51 +/- 0.03, and 0.61 +/- 0.03 Po were 90 +/- 6, 140 +/- 6, and 182 +/- 9 ms, respectively. After phosphorylation of RLC, the half-times for relaxation from 0.36 +/- 0.03 Po, 0.59 +/- 0.03 Po, and 0.65 +/- 0.02 Po were 197 +/- 35 ms, 184 +/- 35 ms, and 179 +/- 22 ms. This slowing of relaxation rates from steady-state forces less than 0.50 Po was also observed when bundles of fibers were bathed with N-ethylmaleimide-modified myosin S-1, a strongly binding cross-bridge derivative of S1. These results suggest that phosphorylation of RLC slows relaxation, most likely by slowing the apparent rate of transition of cross-bridges from strongly bound (force-generating) to weakly bound (non-force-generating) states, and reduces or eliminates Ca2+ and cross-bridge activation-dependent changes in relaxation rates.

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References

Watterson J, Schaub M, Locher R, Di Pierri S, KUTZER M . Temperature-induced transitions in the conformation of intermediates in the hydrolytic cycle of myosin. Eur J Biochem. 1975; 56(1):79-90. DOI: 10.1111/j.1432-1033.1975.tb02209.x. View

Godt R, LINDLEY B . Influence of temperature upon contractile activation and isometric force production in mechanically skinned muscle fibers of the frog. J Gen Physiol. 1982; 80(2):279-97. PMC: 2228673. DOI: 10.1085/jgp.80.2.279. View

Barany K, Barany M . Phosphorylation of the 18,000-dalton light chain of myosin during a single tetanus of frog muscle. J Biol Chem. 1977; 252(14):4752-4. View

Manning D, Stull J . Myosin light chain phosphorylation-dephosphorylation in mammalian skeletal muscle. Am J Physiol. 1982; 242(3):C234-41. DOI: 10.1152/ajpcell.1982.242.3.C234. View

Klug G, Botterman B, Stull J . The effect of low frequency stimulation on myosin light chain phosphorylation in skeletal muscle. J Biol Chem. 1982; 257(9):4688-90. View

EDMAN K, Flitney F . Laser diffraction studies of sarcomere dynamics during 'isometric' relaxation in isolated muscle fibres of the frog. J Physiol. 1982; 329:1-20. PMC: 1224764. DOI: 10.1113/jphysiol.1982.sp014287. View

Moss R, Giulian G, Greaser M . Effects of EDTA treatment upon the protein subunit composition and mechanical properties of mammalian single skeletal muscle fibers. J Cell Biol. 1983; 96(4):970-8. PMC: 2112315. DOI: 10.1083/jcb.96.4.970. View

Nagamoto H, Yagi K . Properties of myosin light chain kinase prepared from rabbit skeletal muscle by an improved method. J Biochem. 1984; 95(4):1119-30. DOI: 10.1093/oxfordjournals.jbchem.a134700. View

Winkelmann D, LOWEY S . Probing myosin head structure with monoclonal antibodies. J Mol Biol. 1986; 188(4):595-612. DOI: 10.1016/s0022-2836(86)80009-2. View

10.

Brenner B . Effect of Ca2+ on cross-bridge turnover kinetics in skinned single rabbit psoas fibers: implications for regulation of muscle contraction. Proc Natl Acad Sci U S A. 1988; 85(9):3265-9. PMC: 280185. DOI: 10.1073/pnas.85.9.3265. View

11.

Schoenberg M . The kinetics of weakly- and strongly-binding crossbridges: implications for contraction and relaxation. Adv Exp Med Biol. 1988; 226:189-202. View

12.

Williams Jr D, Greene L, Eisenberg E . Cooperative turning on of myosin subfragment 1 adenosinetriphosphatase activity by the troponin-tropomyosin-actin complex. Biochemistry. 1988; 27(18):6987-93. DOI: 10.1021/bi00418a048. View

13.

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. View

14.

Metzger J, Greaser M, Moss R . Variations in cross-bridge attachment rate and tension with phosphorylation of myosin in mammalian skinned skeletal muscle fibers. Implications for twitch potentiation in intact muscle. J Gen Physiol. 1989; 93(5):855-83. PMC: 2216237. DOI: 10.1085/jgp.93.5.855. View

15.

Sweeney H, Stull J . Alteration of cross-bridge kinetics by myosin light chain phosphorylation in rabbit skeletal muscle: implications for regulation of actin-myosin interaction. Proc Natl Acad Sci U S A. 1990; 87(1):414-8. PMC: 53274. DOI: 10.1073/pnas.87.1.414. View

16.

Swartz D, Moss R . Influence of a strong-binding myosin analogue on calcium-sensitive mechanical properties of skinned skeletal muscle fibers. J Biol Chem. 1992; 267(28):20497-506. View

17.

Metzger J, Moss R . Myosin light chain 2 modulates calcium-sensitive cross-bridge transitions in vertebrate skeletal muscle. Biophys J. 1992; 63(2):460-8. PMC: 1262169. DOI: 10.1016/S0006-3495(92)81614-4. View

18.

Sweeney H, Bowman B, Stull J . Myosin light chain phosphorylation in vertebrate striated muscle: regulation and function. Am J Physiol. 1993; 264(5 Pt 1):C1085-95. DOI: 10.1152/ajpcell.1993.264.5.C1085. View

19.

Rayment I, Rypniewski W, Smith R, Tomchick D, Benning M, Winkelmann D . Three-dimensional structure of myosin subfragment-1: a molecular motor. Science. 1993; 261(5117):50-8. DOI: 10.1126/science.8316857. View

20.

Zhang R, Zhao J, Mandveno A, Potter J . Cardiac troponin I phosphorylation increases the rate of cardiac muscle relaxation. Circ Res. 1995; 76(6):1028-35. DOI: 10.1161/01.res.76.6.1028. View