S100A1 and calmodulin regulation of ryanodine receptor in striated muscle

Cell Calcium

Volumn 50, Issue 4, 2011, Pages 323-331

  Prosser, Benjamin L ^a   Hernández Ochoa, Erick O ^a   Schneider, Martin F ^a  

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

Author keywords

Calcium release; Calmodulin; Cardiac muscle; Dihydropyridine receptors; Excitation contraction coupling; Muscular contraction; Ryanodine receptor; RyR modulation; S100A1; Sarcoplasmic reticulum; Skeletal muscle; Transverse tubule; Voltage sensors

Indexed keywords

CALCIUM BINDING PROTEIN; CALCIUM CHANNEL L TYPE; CALCIUM ION; CALMODULIN; PROTEIN S100A1; RYANODINE RECEPTOR; RYANODINE RECEPTOR 1; RYANODINE RECEPTOR 2; RYANODINE RECEPTOR 3; UNCLASSIFIED DRUG;

BINDING COMPETITION; CALCIUM TRANSPORT; CHANNEL GATING; EXCITATION CONTRACTION COUPLING; HEART MUSCLE; IN VITRO STUDY; MUSCLE CONTRACTION; MUSCLE EXCITATION; MUSCLE FUNCTION; MUSCLE TWITCH; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR BINDING; REVIEW; SARCOPLASMIC RETICULUM; SKELETAL MUSCLE;

EID: 80053308273     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2011.06.001     Document Type: Review

References (84)

1. Schneider M.F., Chandler W.K. Voltage-dependent charge movement in skeletal muscle: a possible step in excitation-contraction coupling. Nature 1973, 242:244-247.
2. Horowicz P., Schneider M.F. Membrane charge moved at contraction theresholds in skeletal muscle fibres. J. Physiol. 1981, 314:595-633.
3. Rios E., Brum G. Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature 1987, 325:717-720.
4. Block B.A., Imagawa T., Campbell K.P., Franzini-Armstrong C. Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J. Cell Biol. 1988, 107:2587-2600.
5. Fahrenbach W.H. Sarcoplasmic reticulum: ultrastructure of the triadic junction. Science 1965, 147:1308-1309.
6. Cheng H., Lederer W.J. Calcium sparks. Physiol. Rev. 2008, 88:1491-1545.
7. 2+ channel using electron cryo-microscopy. J. Mol. Biol. 2003, 332:171-182.
8. 2+ release channels and their regulation by endogenous effectors. Annu. Rev. Physiol. 1994, 56:485-508.
9. Tanabe T., Beam K.G., Adams B.A., Niidome T., Numa S. Regions of the skeletal muscle dihydropyridine receptor critical for excitation-contraction coupling. Nature 1990, 346:567-569.
10. el Hayek R., Antoniu B., Wang J., Hamilton S.L., Ikemoto N. Identification of calcium release-triggering and blocking regions of the II-III loop of the skeletal muscle dihydropyridine receptor. J. Biol. Chem. 1995, 270:22116-22118.
11. Jayaraman T., Brillantes A.M., Timerman A.P., Fleischer S., Erdjument-Bromage H., Tempst P., Marks A.R. FK506 binding protein associated with the calcium release channel (ryanodine receptor). J. Biol. Chem. 1992, 267:9474-9477.
12. Meissner G. Evidence of a role for calmodulin in the regulation of calcium release from skeletal muscle sarcoplasmic reticulum. Biochemistry 1986, 25:244-251.
13. 2+ release channel (ryanodine receptor) of skeletal muscle. Biochemistry 1997, 36:11496-11503.
14. Marx S.O., Reiken S., Hisamatsu Y., Jayaraman T., Burkhoff D., Rosemblit N., Marks A.R. PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 2000, 101:365-376.
15. Yamaguchi N., Xu L., Pasek D.A., Evans K.E., Meissner G. Molecular basis of calmodulin binding to cardiac muscle Ca(2+) release channel (ryanodine receptor). J. Biol. Chem. 2003, 278:23480-23486.
16. Most P., Bernotat J., Ehlermann P., Pleger S.T., Reppel M., Borries M., Niroomand F., Pieske B., Janssen P.M., Eschenhagen T., Karczewski P., Smith G.L., Koch W.J., Katus H.A., Remppis A. S100A1: a regulator of myocardial contractility. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:13889-13894.
17. Maier L.S., Bers D.M. Calcium, calmodulin, and calcium-calmodulin kinase II: heartbeat to heartbeat and beyond. J. Mol. Cell Cardiol. 2002, 34:919-939.
18. Wagenknecht T., Berkowitz J., Grassucci R., Timerman A.P., Fleischer S. Localization of calmodulin binding sites on the ryanodine receptor from skeletal muscle by electron microscopy. Biophys. J. 1994, 67:2286-2295.
19. 2+ release channel. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:6128-6133.
20. 2+ release channel (ryanodine receptor). Biophys. J. 1995, 69:106-119.
21. Rodney G.G., Williams B.Y., Strasburg G.M., Beckingham K., Hamilton S.L. Regulation of RYR1 activity by Ca(2+) and calmodulin. Biochemistry 2000, 39:7807-7812.
22. 2+ release channel, ryanodine receptor. J. Biol. Chem. 2001, 276:22579-22585.
23. 2+ release channel. Biochemistry 1999, 38:8532-8537.
24. Meissner G. Regulation of mammalian ryanodine receptors. Front. Biosci. 2002, 7:d2072-d2080.
25. Xiong L.W., Newman R.A., Rodney G.G., Thomas O., Zhang J.Z., Persechini A., Shea M.A., Hamilton S.L. Lobe-dependent regulation of ryanodine receptor type 1 by calmodulin. J. Biol. Chem. 2002, 277:40862-40870.
26. 2+ release channel. J. Biol. Chem. 2003, 278:8348-8355.
27. 2+ release. Am. J. Physiol. Cell Physiol. 2008.
28. O'Connell K.M., Yamaguchi N., Meissner G., Dirksen R.T. Calmodulin binding to the 3614-3643 region of RyR1 is not essential for excitation-contraction coupling in skeletal myotubes. J. Gen. Physiol. 2002, 120:337-347.
29. Moore B.W. A soluble protein characteristic of the nervous system. Biochem. Biophys. Res. Commun. 1965, 19:739-744.
30. Zimmer D.B., Cornwall E.H., Landar A., Song W. The S100 protein family: history, function, and expression. Brain Res. Bull. 1995, 37:417-429.
31. Rustandi R.R., Baldisseri D.M., Inman K.G., Nizner P., Hamilton S.M., Landar A., Zimmer D.B., Weber D.J. Three-dimensional solution structure of the calcium-signaling protein apo-S100A1 as determined by NMR. Biochemistry 2002, 41:788-796.
32. Wright N.T., Varney K.M., Ellis K.C., Markowitz J., Gitti R.K., Zimmer D.B., Weber D.J. The three-dimensional solution structure of Ca(2+)-bound S100A1 as determined by NMR spectroscopy. J. Mol. Biol. 2005, 353:410-426.
33. Goch G., Vdovenko S., Kozlowska H., Bierzynski A. Affinity of S100A1 protein for calcium increases dramatically upon glutathionylation. FEBS J. 2005, 272:2557-2565.
34. Baudier J., Mochly-Rosen D., Newton A., Lee S.H., Koshland D.E., Cole R.D. Comparison of S100b protein with calmodulin: interactions with melittin and microtubule-associated tau proteins and inhibition of phosphorylation of tau proteins by protein kinase C. Biochemistry 1987, 26:2886-2893.
35. Wright N.T., Prosser B.L., Varney K.M., Zimmer D.B., Schneider M.F., Weber D.J. S100A1 and calmodulin compete for the same binding site on ryanodine receptor. J. Biol. Chem. 2008, 283:26676-26683.
36. Landar A., Rustandi R.R., Weber D.J., Zimmer D.B. S100A1 utilizes different mechanisms for interacting with calcium-dependent and calcium-independent target proteins. Biochemistry 1998, 37:17429-17438.
37. Inman K.G., Yang R., Rustandi R.R., Miller K.E., Baldisseri D.M., Weber D.J. Solution NMR structure of S100B bound to the high-affinity target peptide TRTK-12. J. Mol. Biol. 2002, 324:1003-1014.
38. Kato K., Kimura S. S100ao (alpha alpha) protein is mainly located in the heart and striated muscles. Biochim. Biophys. Acta 1985, 842:146-150.
39. Zimmer D.B., Landar A. Analysis of S100A1 expression during skeletal muscle and neuronal cell differentiation. J. Neurochem. 1995, 64:2727-2736.
40. Haimoto H., Kato K. S100a0 (alpha alpha) protein, a calcium-binding protein, is localized in the slow-twitch muscle fiber. J. Neurochem. 1987, 48:917-923.
41. 2+ release in murine skinned skeletal muscle fibers. J. Biol. Chem. 2003, 278:26356-26364.
42. Zimmer D.B., Song W., Zimmer W.E. Isolation of a rat S100 alpha cDNA and distribution of its mRNA in rat tissues. Brain Res. Bull. 1991, 27:157-162.
43. Adhikari B.B., Wang K. S100A1 modulates skeletal muscle contraction by desensitizing calcium activation of isometric tension, stiffness and ATPase. FEBS Lett. 2001, 497:95-98.
44. Maco B., Brezova A., Schafer B.W., Uhrik B., Heizmann C.W. Localization of the Ca(2+)-binding S100A1 protein in slow and fast skeletal muscles of the rat. Gen. Physiol. Biophys. 1997, 16:373-377.
45. Arcuri C., Giambanco I., Bianchi R., Donato R. Annexin V, annexin VI, S100A1 and S100B in developing and adult avian skeletal muscles. Neuroscience 2002, 109:371-388.
46. Prosser B.L., Wright N.T., Hernandez-Ochoa E.O., Varney K.M., Liu Y., Olojo R.O., Zimmer D.B., Weber D.J., Schneider M.F. S100A1 binds to the calmodulin-binding site of ryanodine receptor and modulates skeletal muscle excitation-contraction coupling. J. Biol. Chem. 2008, 283:5046-5057.
47. Most P., Remppis A., Pleger S.T., Katus H.A., Koch W.J. S100A1: a novel inotropic regulator of cardiac performance. Transition from molecular physiology to pathophysiological relevance. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 293:R568-R577.
48. 2+ release from isolated sarcoplasmic reticulum vesicles. FEBS Lett. 1989, 255:381-384.
49. Rhoads A.R., Friedberg F. Sequence motifs for calmodulin recognition. FASEB J. 1997, 11:331-340.
50. Wilder P.T., Lin J., Bair C.L., Charpentier T.H., Yang D., Liriano M., Varney K.M., Lee A., Oppenheim A.B., Adhya S., Carrier F., Weber D.J. Recognition of the tumor suppressor protein p53 and other protein targets by the calcium-binding protein S100B. Biochim. Biophys. Acta 2006, 1763:1284-1297.
51. Maximciuc A.A., Putkey J.A., Shamoo Y., Mackenzie K.R. Complex of calmodulin with a ryanodine receptor target reveals a novel, flexible binding mode. Structure 2006, 14:1547-1556.
52. Lau K., Chan M.Y., van Petegem F. Studies in the binding of calmodulin to skeletal and cardiac ryanodine receptors. Biophys. J. 2011, 100:188a.
53. 2+ release in skeletal muscle expressing ryanodine receptor impaired in regulation by calmodulin and S100A1. Am. J. Physiol. Cell Physiol. 2011, 300:C998-C1012.
54. Liu Y.W., Carroll S.L., Klein M.G., Schneider M.F. Calcium transients and calcium homeostasis in adult mouse fast-twitch skeletal muscle fibers in culture. Am. J. Physiol. Cell Physiol. 1997, 272:C1919-C1927.
55. Prosser B.L., Hernandez-Ochoa E.O., Lovering R.M., Andronache Z., Zimmer D.B., Melzer W., Schneider M.F. S100A1 promotes action potential-initiated calcium release flux and force production in skeletal muscle. Am. J. Physiol. Cell Physiol. 2010, 299:C891-C902.
56. -/- muscle fibres. J. Physiol. 2009, 587:4543-4559.
57. Prosser B.L., Hernandez-Ochoa E.O., Zimmer D.B., Schneider M.F. The Qgamma component of intra-membrane charge movement is present in mammalian muscle fibres, but suppressed in the absence of S100A1. J. Physiol. 2009, 587:4523-4541.
58. Melzer W., Rios E., Schneider M.F. A general procedure for determining the rate of calcium release from the sarcoplasmic reticulum in skeletal muscle fibers. Biophys. J. 1987, 51:849-863.
59. Hennig R., Lomo T. Firing patterns of motor units in normal rats. Nature 1985, 314:164-166.
60. 2+ sparks, demonstrated in cultured mammalian muscle. Am. J. Physiol. Cell Physiol. 2005.
61. 2+ sparks and T tubule reorganization in dedifferentiating adult mouse skeletal muscle fibers. Am. J. Physiol. Cell Physiol. 2007, 292:C1156-C1166.
62. 2+ entry in embryonic mouse skeletal muscle and decrease in frequency postnatally. Am. J. Physiol. Cell Physiol. 2003, 285:C686-C697.
63. Horowicz P., Schneider M.F. Membrane charge movement in contracting and non-contracting skeletal muscle fibres. J. Physiol. 1981, 314:565-593.
64. Bers D.M. Cardiac excitation-contraction coupling. Nature 2002, 415:198-205.
65. Tang W., Sencer S., Hamilton S.L. Calmodulin modulation of proteins involved in excitation-contraction coupling. Front. Biosci. 2002, 7:d1583-d1589.
66. Schaub M.C., Hefti M.A., Zaugg M. Integration of calcium with the signaling network in cardiac myocytes. J. Mol. Cell Cardiol. 2006, 41:183-214.
67. Meissner G. Molecular regulation of cardiac ryanodine receptor ion channel. Cell Calcium 2004, 35:621-628.
68. Kushnir A., Marks A.R. The ryanodine receptor in cardiac physiology and disease. Adv. Pharmacol. 2010, 59:1-30.
69. Kraus C., Rohde D., Weidenhammer C., Qiu G., Pleger S.T., Voelkers M., Boerries M., Remppis A., Katus H.A., Most P. S100A1 in cardiovascular health and disease: closing the gap between basic science and clinical therapy. J. Mol. Cell Cardiol. 2009, 47:445-455.
70. Lanner J.T., Georgiou D.K., Joshi A.D., Hamilton S.L. Ryanodine receptors: structure, expression, molecular details, and function in calcium release. Cold Spring Harb. Perspect. Biol. 2010, 2:a003996.
71. Balshaw D.M., Xu L., Yamaguchi N., Pasek D.A., Meissner G. Calmodulin binding and inhibition of cardiac muscle calcium release channel (ryanodine receptor). J. Biol. Chem. 2001, 276:20144-20153.
72. 2+ release channel (ryanodine receptor). Biophys. J. 2004, 86:797-804.
73. Yamaguchi N., Takahashi N., Xu L., Smithies O., Meissner G. Early cardiac hypertrophy in mice with impaired calmodulin regulation of cardiac muscle Ca release channel. J. Clin. Invest. 2007, 117:1344-1353.
74. Most P., Pleger S.T., Volkers M., Heidt B., Boerries M., Weichenhan D., Loffler E., Janssen P.M., Eckhart A.D., Martini J., Williams M.L., Katus H.A., Remppis A., Koch W.J. Cardiac adenoviral S100A1 gene delivery rescues failing myocardium. J. Clin. Invest. 2004, 114:1550-1563.
75. Brezova A., Heizmann C.W., Uhrik B. Immunocytochemical localization of S100A1 in mitochondria on cryosections of the rat heart. Gen. Physiol. Biophys. 2007, 26:143-149.
76. 2+-cycling in ventricular rat cardiomyocytes. J. Cell Sci. 2005, 118:421-431.
77. 2+-binding protein S100A1 in the heart leads to increased in vivo myocardial contractile performance. J. Biol. Chem. 2003, 278:33809-33817.
78. Volkers M., Loughrey C.M., Macquaide N., Remppis A., DeGeorge B.R., Wegner F.V., Friedrich O., Fink R.H., Koch W.J., Smith G.L., Most P. S100A1 decreases calcium spark frequency and alters their spatial characteristics in permeabilized adult ventricular cardiomyocytes. Cell Calcium 2007, 41:135-143.
79. Most P., Seifert H., Gao E., Funakoshi H., Volkers M., Heierhorst J., Remppis A., Pleger S.T., DeGeorge B.R., Eckhart A.D., Feldman A.M., Koch W.J. Cardiac S100A1 protein levels determine contractile performance and propensity toward heart failure after myocardial infarction. Circulation 2006, 114:1258-1268.
80. Kettlewell S., Most P., Currie S., Koch W.J., Smith G.L. S100A1 increases the gain of excitation-contraction coupling in isolated rabbit ventricular cardiomyocytes. J. Mol. Cell Cardiol. 2005, 39:900-910.
81. 2+ current in embryonic mouse and neonatal rat ventricular cardiomyocytes. J. Biol. Chem. 2005, 280:36019-36028.
82. Hernandez-Ochoa E.O., Prosser B.L., Wright N.T., Contreras M., Weber D.J., Schneider M.F. Augmentation of Cav1 channel current and action potential duration after uptake of S100A1 in sympathetic ganglion neurons. Am. J. Physiol. Cell Physiol. 2009, 297:C955-C970.
83. 2+ signaling in mouse cardiomyocytes with ablated S100A1 protein. Gen. Physiol. Biophys. 2009, 28:371-383.
84. Xu X., Yano M., Uchinoumi H., Hino A., Suetomi T., Ono M., Tateishi H., Oda T., Okuda S., Doi M., Kobayashi S., Yamamoto T., Ikeda Y., Ikemoto N., Matsuzaki M. Defective calmodulin binding to the cardiac ryanodine receptor plays a key role in CPVT-associated channel dysfunction. Biochem. Biophys. Res. Commun. 2010, 394:660-666.