Modulation of sarcoplasmic reticulum Ca2+ release in skeletal muscle expressing ryanodine receptor impaired in regulation by calmodulin and S100A1

American Journal of Physiology - Cell Physiology

Volumn 300, Issue 5, 2011, Pages

  Yamaguchi, Naohiro ^a   Prosser, Benjamin L ^b   Ghassemi, Farshid ^a   Xu, Le ^a   Pasek, Daniel A ^a   Eu, Jerry P ^c   Hernández Ochoa, Erick O ^b   Cannon, Brian R ^b   Wilder, Paul T ^b   Lovering, Richard M ^b   Weber, David ^b   Melzer, Werner ^d   Schneider, Martin F ^b   Meissner, Gerhard ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

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

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF ULM   (Germany)

Author keywords

Ca2+ release channel; Excitation contraction coupling; RyR1 L3625D; Ryr1D D mouse

Indexed keywords

CALCIUM BINDING PROTEIN; CALMODULIN; PROTEIN S100A1; RYANODINE RECEPTOR; UNCLASSIFIED DRUG;

ACTION POTENTIAL; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM TRANSPORT; COMPLEX FORMATION; EXON; FLEXOR MUSCLE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SARCOPLASMIC RETICULUM; SKELETAL MUSCLE;

ACTION POTENTIALS; ANIMALS; CALCIUM; CALMODULIN; FEMALE; MALE; MICE; MUSCLE CONTRACTION; MUSCLE STRENGTH; MUSCLE, SKELETAL; PROTEIN BINDING; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; S100 PROTEINS; SARCOPLASMIC RETICULUM;

MUS;

EID: 79955559201     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00370.2010     Document Type: Article

References (52)

1. Balshaw DM, Xu L, Yamaguchi N, Pasek DA, Meissner G. Calmodulin binding and inhibition of cardiac muscle calcium release channel (ryanodine receptor). J Biol Chem 276: 20144-20153, 2001.
2. Balshaw DM, Yamaguchi N, Meissner G. Modulation of intracellular calcium release channels by calmodulin. J Membr Biol 185: 1-8, 2002.
3. Baylor SM, Hollingworth S. Sarcoplasmic reticulum calcium release compared in slow-twitch and fast-twitch fibres of mouse muscle. J Physiol 551: 125-138, 2003.
4. Bronson SK, Plaehn EG, Kluckman KD, Hagaman JR, Maeda N, Smithies O. Single-copy transgenic mice with chosen-site integration. Proc Natl Acad Sci USA 93: 9067-9072, 1996.
5. Bunting M, Bernstein KE, Greer JM, Capecchi MR, Thomas KR. Targeting genes for self-excision in the germ line. Genes Dev 15: 1524-1528, 1999.
6. Du XJ, Cole TJ, Tenis N, Gao XM, Kontgen F, Kemp BE, Heierhorst J. Impaired cardiac contractility response to hemodynamic stress in S100A1-deficient mice. Mol Cell Biol 22: 2821-2829, 2002.
7. Fill M, Copello JA. Ryanodine receptor calcium release channels. Physiol Rev 82: 893-922, 2002.
8. Franzini-Armstrong C, Protasi F. Ryanodine receptors of striated muscles: a complex channel capable of multiple interactions. Physiol Rev 77: 699-729, 1997.
9. Harkins AB, Kurebayashi N, Baylor SM. Resting myoplasmic free calcium in frog skeletal muscle fibers estimated with fluo-3. Biophys J 65: 865-881, 1993.
10. Kettlewell S, Most P, Currie S, Koch WJ, Smith GL. S100A1 increases the gain of excitation-contraction coupling in isolated rabbit ventricular cardiomyocytes. J Mol Cell Cardiol 39: 900-910, 2005.
11. Kraus C, Rohde D, Weidenhammer C, Qiu G, Pleger ST, Voelkers M, Boerries M, Remppis A, Katus HA, Most P. S100A1 in cardiovascular health and disease: closing the gap between basic science and clinical therapy. J Mol Cell Cardiol 47: 445-455, 2009.
12. Ledbetter MW, Preiner JK, Louis CF, Mickelson JR. Tissue distribution of ryanodine receptor isoforms and alleles determined by reverse transcription polymerase chain reaction. J Biol Chem 269: 31544-31551, 1994.
13. Liu Y, Carroll SL, Klein MG, Schneider MF. Calcium transients and calcium homeostasis in adult mouse fast-twitch skeletal muscle fibers in culture. Am J Physiol Cell Physiol 272: C1919-C1927, 1997.
14. Lovering RM, De Deyne PG. Contractile function, sarcolemma integrity, and the loss of dystrophin after skeletal muscle eccentric contractioninduced injury. Am J Physiol Cell Physiol 286: C230-C238, 2004.
15. 2+-binding S100A1 protein in slow and fast skeletal muscles of the rat. Gen Physiol Biophys 16: 373-377, 1997.
16. Markowitz J, Rustandi RR, Varney KM, Wilder PT, Udan R, Wu SL, Horrocks WD, Weber DJ. Calcium-binding properties of wild-type and EF-hand mutants of S100B in the presence and absence of a peptide derived from the C-terminal negative regulatory domain of p53. Biochemistry 44: 7305-7314, 2005.
17. Maximciuc AA, Putkey JA, Shamoo Y, MacKenzie KR. Complex of calmodulin with the ryanodine receptor target reveals a novel, flexible binding mode. Structure 14: 1547-1556, 2006.
18. Meissner G. Regulation of mammalian ryanodine receptors. Front Biosci 7: d2072-d2080, 2002.
19. Melzer W, Rios E, Schneider MF. The removal of myoplasmic free calcium following calcium release in frog skeletal muscle. J Physiol 372: 261-292, 1986.
20. Melzer W, Rios E, Schneider MF. A general procedure for determining the rate of calcium release from the sarcoplasmic reticulum in skeletal muscle fibers. Biophys J 51: 849-863, 1987.
21. 2+ binding protein S100A1 in the heart leads to increased in vivo myocardial contractile performance. J Biol Chem 278: 33809-33817, 2003.
22. O'Connell KM, Yamaguchi N, Meissner G, Dirksen RT. Calmodulin binding to the 3614-3643 region of RyR1 is not essential for excitationcontraction coupling in skeletal myotubes. J Gen Physiol 120: 337-347, 2002.
23. Pleger ST, Most P, Boucher M, Soltys S, Chuprun JK, Pleger W, Gao E, Dasgupta A, Rengo G, Remppis A, Katus HA, Eckhart AD, Rabinowitz JE, Koch WJ. Stable myocardial-specific AAV6-S100A1 gene therapy results in chronic functional heart failure rescue. Circulation 115: 2506-2515, 2007.
24. Prosser BL, Hernandez-Ochoa EO, Lovering RM, Andronache Z, Zimmer DB, Melzer W, Schneider MF. S100A1 promotes action potential-initiated calcium release flux and force production in skeletal muscle. Am J Physiol Cell Physiol 299: C891-C902, 2010.
25. Prosser BL, Hernandez-Ochoa EO, Zimmer DB, Schneider MF. The Qgamma component of intra-membrane charge movement is present in mammalian muscle fibres, but suppressed in the absence of S100A1. J Physiol 587: 4523-4541, 2009.
26. Prosser BL, Hernandez-Ochoa EO, Zimmer DB, Schneider MF. Simultaneous recording of intramembrane charge movement components and calcium release in wild-type and S100A1-/-muscle fibres. J Physiol 587: 4543-4559, 2009.
27. Prosser BL, Wright NT, Hernandez-Ochoa EO, Varney KM, Liu Y, Olojo R, Zimmer DB, Weber DJ, Schneider MF. S100A1 binds to the calmodulin-binding site of ryanodine receptor and modulates skeletal muscle excitation-contraction coupling. J Biol Chem 283: 5046-5057, 2008.
28. 2+-binding protein S100A1 in human cardiomyopathy. Biochim Biophys Acta 1313: 253-257, 1996.
29. 2+ release. Am J Physiol Cell Physiol 294: C1288-C1297, 2008.
30. Rodney GG, Moore CP, Williams BY, Zhang JZ, Krol J, Pedersen SE, Hamilton SL. Calcium binding to calmodulin leads to an N-terminal shift in its binding site on the ryanodine receptor. J Biol Chem 276: 2069-2074, 2001.
31. Radzyukevich TL, Cougnon MH, Moseley AE, Heiny JA. Developmental induction of DHPR alpha 1s and RYR1 gene expression does not require neural or mechanical signals. J Muscle Res Cell Motil 2004: 87-94, 2004.
32. 2+-calmodulin bind to neighboring locations on the ryanodine receptor. J Biol Chem 277: 1349-1353, 2002.
33. Schneider MF, Chandler WK. Voltage dependent charge movement in skeletal muscle: a possible step in excitation-contraction coupling. Nature 242: 244-246, 1973.
34. Schoenmakers TJ, Visser GJ, Flik G, Theuvenet AP. CHELATOR: an improved method for computing metal ion concentrations in physiological solutions. Biotechniques 12: 870-879, 1992.
35. Schuhmeier RP, Dietze B, Ursu D, Lehmann-Horn F, Melzer W. Voltage-activated calcium signals in myotubes loaded with high concentrations of EGTA. Biophys J 84: 1065-1078, 2003.
36. 2+ fluxes in skeletal myotubes determined using a removal model analysis. J Gen Physiol 123: 33-51, 2004.
37. 2+ release from the sarcoplasmic reticulum compared in amphibian and mammalian skeletal muscle. J Gen Physiol 107: 1-18, 1996.
38. Sun J, Xin C, Eu JP, Stamler JS, Meissner G. Cysteine-3635 is responsible for skeletal muscle ryanodine receptor modulation by NO. Proc Natl Acad Sci USA 98: 11158-11162, 2001.
39. Sutko JL, Airey JA, Welch W, Ruest L. The pharmacology of ryanodine and related compounds. Pharmacol Rev 49: 53-98, 1997.
40. Takeshima H, Iino M, Takekura H, Nishi M, Kuno J, Minowa O, Takano H, Noda T. Excitation-contraction uncoupling and muscular degeneration in mice lacking functional skeletal muscle ryanodine-receptor gene. Nature 369: 556-559, 1994.
41. Takeshima H, Komazaki S, Hirose K, Nishi M, Noda T, Iino M. Embryonic lethality and abnormal cardiac myocytes in mice lacking ryanodine receptor type 2. EMBO J 1998: 3309-3316, 1998.
42. Timmer J, Müller T, Melzer W. Numerical methods to determine calcium release flux from calcium transients in muscle cells. Biophys J 74: 1694-1707, 1998.
43. 2+ release channel (ryanodine receptor) of skeletal muscle. Biochemistry 36: 11496-11503, 1997.
44. Tsoporis JN, Marks A, Zimmer DB, McMahon C, Parker TG. The myocardial protein S100A1 plays a role in the maintenance of normal gene expression in the adult heart. Mol Cell Biochem 242: 27-33, 2003.
45. Volkers M, Loughrey CM, Macquaide N, Remppis A, DeGeorge BR Jr, Wegner FV, Friedrich O, Fink RH, Koch WJ, Smith GL, Most P. S100A1 decreases calcium spark frequency and alters their spatial characteristics in permeabilized adult ventricular cardiomyocytes. Cell Calcium 41: 135-143, 2007.
46. Wright NT, Cannon BR, Zimmer DB, Weber DJ. S100A1: structure, function, and therapeutic potential. Curr Chem Biol 3: 138-145, 2009.
47. Wright NT, Prosser BL, Varney KM, Zimmer DB, Schneider MF, Weber DJ. S100A1 and calmodulin compete for the same binding site on ryanodine receptor. J Biol Chem 283: 26676-26683, 2008.
48. 2+ release channels (ryanodine receptors) by multiple mechanisms. J Biol Chem 274: 32680-32691, 1999.
49. 2+ release channel. J Clin Invest 117: 1344-1353, 2007.
50. 2+ release channel, ryanodine receptor. J Biol Chem 276: 22579-22585, 2001.
51. Yamaguchi N, Xu L, Pasek DA, Evans KE, Chen SR, Meissner G. Calmodulin regulation and identification of calmodulin binding region of type-3 ryanodine receptor calcium release channel. Biochemistry 44: 15074-15081, 2005.
52. Zimmer DB. Examination of the calcium-modulated protein S100 alpha and its target proteins in adult and developing skeletal muscle. Cell Motil Cytoskeleton 20: 325-237, 1991.