β1a490-508, a 19-residue peptide from C-terminal tail of Cav1.1 β1a subunit, potentiates voltage-dependent calcium release in adult skeletal muscle fibers

Biophysical Journal

Volumn 106, Issue 3, 2014, Pages 535-547

  Hernández Ochoa, Erick O ^a   Olojo, Rotimi O ^a   Rebbeck, Robyn T ^b   Dulhunty, Angela F ^b   Schneider, Martin F ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b Australian National University   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CA(V)1.1 PROTEIN, MOUSE; CALCIUM; CALCIUM CHANNEL L TYPE; RYANODINE RECEPTOR;

ANIMAL; ARTICLE; C57BL MOUSE; CALCIUM SIGNALING; CHEMISTRY; MEMBRANE POTENTIAL; METABOLISM; MOUSE; PHYSIOLOGY; PROTEIN BINDING; PROTEIN SUBUNIT; PROTEIN TERTIARY STRUCTURE; SKELETAL MUSCLE;

ANIMALS; CALCIUM; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MUSCLE FIBERS, SKELETAL; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 84893484194     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.11.4503     Document Type: Article

References (72)

1. B.M. Curtis, and W.A. Catterall Purification of the calcium antagonist receptor of the voltage-sensitive calcium channel from skeletal muscle transverse tubules Biochemistry 23 1984 2113 2118
2. 2+ channel Biochim. Biophys. Acta 1828 2013 1587 1597
3. B.M. Curtis, and W.A. Catterall Reconstitution of the voltage-sensitive calcium channel purified from skeletal muscle transverse tubules Biochemistry 25 1986 3077 3083
4. V. Flockerzi, and H.J. Oeken W. Trautwein Purified dihydropyridine- binding site from skeletal muscle T-tubules is a functional calcium channel Nature 323 1986 66 68
5. M. Takahashi, and M.J. Seagar W.A. Catterall Subunit structure of dihydropyridine-sensitive calcium channels from skeletal muscle Proc. Natl. Acad. Sci. USA 84 1987 5478 5482
6. W.A. Catterall Voltage-gated calcium channels Cold Spring Harb. Perspect. Biol. 3 2011 a003947
7. E. Rios, and G. Brum Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle Nature 325 1987 717 720
8. T. Tanabe, and H. Takeshima S. Numa Primary structure of the receptor for calcium channel blockers from skeletal muscle Nature 328 1987 313 318
9. P.R. Stanfield A calcium dependent inward current in frog skeletal muscle fibers Pflugers Arch. 368 1977 267 270
10. J.A. Sanchez, and E. Stefani Inward calcium current in twitch muscle fibers of the frog J. Physiol. 283 1978 197 209
11. M.F. Schneider, and W.K. Chandler Voltage dependent charge movement of skeletal muscle: a possible step in excitation-contraction coupling Nature 242 1973 244 246
12. 2+-permeable pore of the calcium release channel J. Biol. Chem. 262 1987 16636 16643
13. M. Inui, A. Saito, and S. Fleischer Purification of the ryanodine receptor and identity with feet structures of junctional terminal cisternae of sarcoplasmic reticulum from fast skeletal muscle J. Biol. Chem. 262 1987 1740 1747
14. B.A. Block, and T. Imagawa C. Franzini-Armstrong Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle J. Cell Biol. 107 1988 2587 2600
15. M.F. Schneider Control of calcium release in functioning skeletal muscle fibers Annu. Rev. Physiol. 56 1994 463 484
16. P. Horowicz, and M.F. Schneider Membrane charge movement in contracting and non-contracting skeletal muscle fibers J. Physiol. 314 1981 565 593
17. C.L. Huang Intramembrane charge movements in skeletal muscle Physiol. Rev. 68 1988 1197 1247
18. E. Ríos, and G. Pizarro Voltage sensor of excitation-contraction coupling in skeletal muscle Physiol. Rev. 71 1991 849 908
19. M.W. Berchtold, H. Brinkmeier, and M. Müntener Calcium ion in skeletal muscle: its crucial role for muscle function, plasticity, and disease Physiol. Rev. 80 2000 1215 1265
20. K.G. Beam, and P. Horowicz Excitation-contraction coupling in skeletal muscle A.G. Engel, C. Franzini-Armstrong, Myology 2004 McGraw-Hill New York 257 280
21. M.F. Schneider, and E.O. Hernandez-Ochoa Chapt. 57: Skeletal muscle excitation-contraction coupling J.A. Hill, E. Olson, Muscle: Fundamental Biology and Mechanisms of Disease [in two volumes] 2012 Academic Press, Elsevier London, UK 811 822
22. 2+ currents and alters channel inactivation properties J. Biol. Chem. 275 2000 14476 14481
23. 2+ release in mouse muscle fibers deficient in the DHP receptor γ1 subunit J. Gen. Physiol. 124 2004 605 618
24. B.E. Flucher, and G.J. Obermair M. Grabner The role of auxiliary dihydropyridine receptor subunits in muscle J. Muscle Res. Cell Motil. 26 2005 1 6
25. 2+ current kinetics in skeletal muscle but not targeting of α1S or excitation-contraction coupling J. Biol. Chem. 280 2005 2229 2237
26. M.P. Gach, and G. Cherednichenko P.D. Allen α2δ1 dihydropyridine receptor subunit is a critical element for excitation-coupled calcium entry but not for formation of tetrads in skeletal myotubes Biophys. J. 94 2008 3023 3034
27. R.G. Gregg, and A. Messing P.A. Powers Absence of the β subunit (cchb1) of the skeletal muscle dihydropyridine receptor alters expression of the α 1 subunit and eliminates excitation-contraction coupling Proc. Natl. Acad. Sci. USA 93 1996 13961 13966
28. 2+ channels Physiol. Rev. 90 2010 1461 1506
29. Y. Karunasekara, A.F. Dulhunty, and M.G. Casarotto The voltage-gated calcium-channel β subunit: more than just an accessory Eur. Biophys. J. 39 2009 75 81
30. 2+ current and excitation-contraction coupling by the dihydropyridine receptor β subunit Biophys. J. 76 1999 1744 1756
31. 2+ current and charge movements in skeletal myotubes promoted by the β-subunit of the dihydropyridine receptor in the absence of ryanodine receptor type 1 Biophys. J. 84 2003 942 959
32. M.C. García, and E. Carrillo J.A. Sánchez Short-term regulation of excitation-contraction coupling by the β1a subunit in adult mouse skeletal muscle Biophys. J. 89 2005 3976 3984
33. J. Schredelseker, and V. Di Biase M. Grabner The β 1a subunit is essential for the assembly of dihydropyridine-receptor arrays in skeletal muscle Proc. Natl. Acad. Sci. USA 102 2005 17219 17224
34. J. Schredelseker, and A. Dayal M. Grabner Proper restoration of excitation-contraction coupling in the dihydropyridine receptor β1-null zebrafish relaxed is an exclusive function of the β1a subunit J. Biol. Chem. 284 2009 1242 1251
35. 2+ channel β-subunit and ryanodine receptor type 1 strengthens excitation-contraction coupling Proc. Natl. Acad. Sci. USA 102 2005 19225 19230
36. M. Beurg, and C.A. Ahern R. Coronado Involvement of the carboxy-terminus region of the dihydropyridine receptor β1a subunit in excitation- contraction coupling of skeletal muscle Biophys. J. 77 1999 2953 2967
37. 2+ dependent excitation-contraction coupling in skeletal myotubes Biophys. J. 84 2003 220 237
38. R. Coronado, and C.A. Ahern D. Bhattacharya Functional equivalence of dihydropyridine receptor α1S and β1a subunits in triggering excitation-contraction coupling in skeletal muscle Biol. Res. 37 2004 565 575
39. R.T. Rebbeck, and Y. Karunasekara A.F. Dulhunty The β(1a) subunit of the skeletal DHPR binds to skeletal RyR1 and activates the channel via its 35-residue C-terminal tail Biophys. J. 100 2011 922 930
40. 2+ channel β1a subunit activates ryanodine receptor type 1 via a hydrophobic surface FASEB J. 26 2012 5049 5059
41. R.O. Olojo, E.O. Hernandez-Ochoa, and M.F. Schneider 19-Residue peptide from C-terminal tail of DHPR β1a subunit potentiates voltage-dependent calcium release in adult skeletal muscle fibers Biophys. J. 102 2012 362a
42. Y. Liu, and S.L. Carroll M.F. Schneider Calcium transients and calcium homeostasis in adult mouse fast-twitch skeletal muscle fibers in culture Am. J. Physiol. 272 1997 C1919 C1927
43. R.O. Olojo, and E.O. Hernández-Ochoa M.F. Schneider Effects of conformational peptide probe DP4 on bidirectional signaling between DHPR and RyR1 calcium channels in voltage-clamped skeletal muscle fibers Biophys. J. 100 2011 2367 2377
44. B.L. Prosser, and E.O. Hernández-Ochoa M.F. Schneider The Qγ component of intra-membrane charge movement is present in mammalian muscle fibers, but suppressed in the absence of S100A1 J. Physiol. 587 2009 4523 4541
45. O.P. Hamill, and A. Marty F.J. Sigworth Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches Pflugers Arch. 391 1981 85 100
46. 2+ transients in adult skeletal muscle fibers Biophys. J. 77 1999 2709 2716
47. B.L. Prosser, and E.O. Hernández-Ochoa M.F. Schneider Simultaneous recording of intramembrane charge movement components and calcium release in wild-type and S100A1-/- muscle fibers J. Physiol. 587 2009 4543 4559
48. R.O. Olojo, and A.P. Ziman C.W. Ward Mice null for calsequestrin 1 exhibit deficits in functional performance and sarcoplasmic reticulum calcium handling PLoS ONE 6 2011 e27036
49. M.G. Klein, and B.J. Simon M.F. Schneider Simultaneous recording of calcium transients in skeletal muscle using high- and low-affinity calcium indicators Biophys. J. 53 1988 971 988
50. L. Royer, S. Pouvreau, and E. Ríos Evolution and modulation of intracellular calcium release during long-lasting, depleting depolarization in mouse muscle J. Physiol. 586 2008 4609 4629
51. 2+ release from the sarcoplasmic reticulum compared in amphibian and mammalian skeletal muscle J. Gen. Physiol. 107 1996 1 18
52. J. Nakai, and R.T. Dirksen P.D. Allen Enhanced dihydropyridine receptor channel activity in the presence of ryanodine receptor Nature 380 1996 72 75
53. 2+ channels Biochim. Biophys. Acta 1828 2013 1530 1540
54. F. van Petegem, and K.A. Clark D.L. Minor Jr. Structure of a complex between a voltage-gated calcium channel β-subunit and an α-subunit domain Nature 429 2004 671 675
55. 2+ channels Nature 429 2004 675 680
56. D.C. Sheridan, and W. Cheng R. Coronado Involvement of a heptad repeat in the carboxyl terminus of the dihydropyridine receptor β1a subunit in the mechanism of excitation-contraction coupling in skeletal muscle Biophys. J. 87 2004 929 942
57. A. Dayal, and J. Schredelseker M. Grabner Skeletal muscle excitation-contraction coupling is independent of a conserved heptad repeat motif in the C-terminus of the DHPRβ(1a) subunit Cell Calcium 47 2010 500 506
58. 2+-calmodulin-dependent proteins for skeletal muscle plasticity J. Physiol. 589 2011 5021 5031
59. R.A. Bannister, and A. Polster A shortcut to a skeletal muscle DHPR knock-in? J. Physiol. 589 2011 4645 4646
60. D. Liu, and R. Hewawasam P.G. Board The inhibitory glutathione transferase M2-2 binding site is located in divergent region 3 of the cardiac ryanodine receptor Biochem. Pharmacol. 83 2012 1523 1529
61. E. Wium, A.F. Dulhunty, and N.A. Beard A skeletal muscle ryanodine receptor interaction domain in triadin PLoS ONE 7 2012 e43817
62. A. Dayal, and V. Bhat M. Grabner Domain cooperativity in the β1a subunit is essential for dihydropyridine receptor voltage sensing in skeletal muscle Proc. Natl. Acad. Sci. USA 110 2013 7488 7493
63. M.D. Stern, G. Pizarro, and E. Ríos Local control model of excitation-contraction coupling in skeletal muscle J. Gen. Physiol. 110 1997 415 440
64. N. Shirokova, J. García, and E. Ríos Local calcium release in mammalian skeletal muscle J. Physiol. 512 1998 377 384
65. C.C. Yin, L.M. Blayney, and F.A. Lai Physical coupling between ryanodine receptor-calcium release channels J. Mol. Biol. 349 2005 538 546
66. R.T. Rebbeck, and H. Willemse A.F. Dulhunty Interactions between dihydropyridine β1A subunit and ryanodine receptor isoforms Biophys. J. 104 2013 105a
67. 2+ release channels (ryanodine receptors) Science 281 1998 818 821
68. 2+ channels of skeletal muscle J. Physiol. 545 2002 407 419
69. S.W. Jones Calcium channels: when is a subunit not a subunit? J. Physiol. 545 2002 334
70. A.C. Dolphin β-subunits of voltage-gated calcium channels J. Bioenerg. Biomembr. 35 2003 599 620
71. 2+ channel β subunits with the α1 subunit interaction domain J. Biol. Chem. 270 1995 18088 18093
72. 2+ channel J. Biol. Chem. 287 2012 43853 43861