I. Wolner et al
Inhibition of skeletal muscle ryanodine receptor
533
HOHENEGGER, M. & SUKO, J. (1993). Phosphorylation of the purified
cardiac ryanodine receptor by exogenous and endogenous protein
kinases. Biochem J., 296, 303–308.
SCOOTE, M. & WILLIAMS, A.J. (2002). The cardiac ryanodine receptor
(calcium release channel): emerging role in heart failure and
arrhythmia pathogenesis. Cardiovasc. Res., 56, 359–372.
KASSACK, M.U., BRAUN, K., GANSO, M., ULLMANN, H., NICKEL,
P., BOING, B., MULLER, G. & LAMBRECHT, G. (2004). Structure–
activity relationships of analogues of NF449 confirm NF449 as the
most potent and selective known P2X1 receptor antagonist. Eur. J.
Med. Chem., 39, 345–357.
KASSACK, M. & NICKEL, P. (1996). Rapid, highly sensitive gradient
narrow-bore high-performance liquid chromatographic determina-
tion of suramin and its analogues. J. Chromatogr. B. Biomed. Appl.,
686, 275–284.
KLINGER, M., BOFILL-CARDONA, E., MAYER, B., NANOFF, C.,
FREISSMUTH, M. & HOHENEGGER, M. (2001). Suramin and the
suramin analogue NF307 discriminate among calmodulin-binding
sites. Biochem. J., 355, 827–833.
KLINGER, M., FREISSMUTH, M., NICKEL, P., STABLER-SCHWARZBART,
M., KASSACK, M., SUKO, J. & HOHENEGGER, M. (1999). Suramin
and suramin analogs activate skeletal muscle via a calmodulin
binding site. Mol. Pharmacol., 55, 462–472.
MEISSNER, G. (1994). Ryanodine receptor/Ca2+ release channel and
their regulation by endogenous effectors. Ann. Rev. Physiol., 56,
485–508.
MOORE, C.P., RODNEY, G., ZHANG, J.Z., SANTACRUZ-TOLOZA, L.,
STRASBURG, G. & HAMILTON, S.L. (1999). Apocalmodulin and
Ca2+ calmodulin bind to the same region on the skeletal muscle
Ca2+ release channel. Biochemistry, 38, 8532–8537.
SITSAPESAN, R. & WILLIAMS, A.J. (1996). Modification of the
conductance and gating properties of ryanodine receptors by
suramin. J. Membr. Biol., 153, 93–103.
SMITH, J.S., ROUSSEAU, E. & MEISSNER, G. (1989). Calmodulin
modulation of single sarcoplasmic reticulum Ca2+-release channels
from cardiac and skeletal muscle. Circ. Res., 64, 352–359.
SUKO, J., HELLMANN, G. & DROBNY, H. (2001). Short- and long-
term functional alterations of the skeletal muscle calcium release
channel (ryanodine receptor) by suramin: apparent dissociation of
single channel current recording and [3H]ryanodine binding. Mol.
Pharmacol., 59, 543–556.
SUTKO, J.L. & AIREY, J.A. (1996). Ryanodine receptor Ca2+ release
channels: does diversity in form equal diversity in function? Physiol.
Rev., 76, 1027–1071.
TRIPATHY, A., XU, L., MANN, G.
& MEISSNER, G. (1995).
Calmodulin activation and inhibition of skeletal muscle
Ca2+ release channel (ryanodine receptor). Biophys. J., 69,
106–119.
VOOGD, T.E., VANSTERKENBURG, E.L., WILTING, J. & JANSSEN,
L.H. (1993). Recent research on the biological activity of suramin.
Pharmacol. Rev., 45, 177–203.
WEHRENS, X.H.
& MARKS, A.R. (2003). Altered function and
regulation of cardiac ryanodine receptors in cardiac disease. Trends
Biochem. Sci., 28, 671–678.
PAPINENI, R.V., O’CONNELL, K.M., ZHANG, H., DIRKSEN, R.T. &
HAMILTON, S.L. (2002). Suramin interacts with the calmodulin
binding site on the ryanodine receptor, RYR1. J. Biol. Chem., 277,
49167–49174.
PLANK, B., WYSKOVSKY, W., HOHENEGGER, M., HELLMANN, G.
& SUKO, J. (1988). Inhibition of calcium release from skeletal
muscle sarcoplasmic reticulum by calmodulin. Biochim. Biophys.
Acta, 938, 79–88.
RODNEY, G.G., KROL, J., WILLIAMS, B., BECKINGHAM, K. &
HAMILTON, S.L. (2001). The carboxy-terminal calcium binding
sites of calmodulin control calmodulin’s switch from an activator to
an inhibitor of RYR1. Biochemistry, 40, 12430–12435.
RODNEY, G.G., WILLIAMS, B.Y., STRASBURG, G.M., BECKINGHAM,
K. & HAMILTON, S.L. (2000). Regulation of RYR1 activity by Ca2+
and calmodulin. Biochemistry, 39, 7807–7812.
WYSKOVSKY, W., HOHENEGGER, M., PLANK, B., HELLMANN, G.,
KLEIN, S. & SUKO, J. (1990). Activation and inhibition of the
calcium-release channel of isolated skeletal muscle heavy sarco-
plasmic reticulum. Models of the calcium-release channel. Eur. J.
Biochem., 194, 549–559.
XIONG, L.W., NEWMAN, R.A., RODNEY, G.G., THOMAS, O.,
ZHANG, J.Z., PERSECHINI, A., SHEA, M.A. & HAMILTON, S.L.
(2002). Lobe-dependent regulation of ryanodine receptor type 1 by
calmodulin. J. Biol. Chem., 277, 40862–40870.
YAMAGUCHI, N., XU, L., PASEK, D.A., EVANS, K.E. & MEISSNER,
G. (2003). Molecular basis of calmodulin binding to cardiac muscle
Ca2+ release channel (ryanodine receptor). J. Biol. Chem., 278,
23480–23486.
SAMSO, M.
&
Ca2+-calmodulin bind to neighboring locations on the ryanodine
WAGENKNECHT, T. (2002). Apocalmodulin and
(Received June 10, 2005
Accepted July 1, 2005
Published online 1 August 2005)
receptor. J. Biol. Chem., 277, 1349–1353.
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