Interaction of cardiac troponin with cardiotonic drugs: A structural perspective

Biochemical and Biophysical Research Communications

Volumn 369, Issue 1, 2008, Pages 88-99

  Li, Monica X ^a   Robertson, Ian M ^a   Sykes, Brian D ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Calcium sensitizers; Cardiac muscle contraction; Cardiotonic drugs; Myofilament; Troponin

Indexed keywords

5 [1 (3,4 DIMETHOXYBENZOYL) 1,2,3,4 TETRAHYDRO 6 QUINOLYL] 3,6 DIHYDRO 6 METHYL 2H 1,3,4 THIADIAZIN 2 ONE; ANAPOE; BEPRIDIL; CALCIUM ION; CARDIOTONIC AGENT; CI 913; CYCLIC AMP DEPENDENT PROTEIN KINASE; DETERGENT; IMAZODAN; LEVOSIMENDAN; N (6 AMINOHEXYL) 5 CHLORO 1 NAPHTHALENESULFONAMIDE; TROPONIN; TROPONIN C; TROPONIN I; UNCLASSIFIED DRUG;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; DRUG BINDING SITE; DRUG MECHANISM; DRUG PROTEIN BINDING; DRUG STRUCTURE; HEART CONTRACTION; HEART MUSCLE CONTRACTILITY; HEART MUSCLE RELAXATION; HUMAN; MYOFILAMENT; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION;

ANIMALS; CALCIUM; CALCIUM SIGNALING; CARDIOTONIC AGENTS; HEART; HEART DISEASES; HUMANS; MYOCARDIAL CONTRACTION; STRUCTURE-ACTIVITY RELATIONSHIP; TROPONIN;

EID: 40849131184     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2007.12.108     Document Type: Article

References (84)

1. Farah C.S., and Reinach F.C. The troponin complex and regulation of muscle contraction. FASEB J. 9 (1995) 755-767
2. Kobayashi T., and Solaro R.J. Calcium, thin filaments, and the integrative biology of cardiac contractility. Annu. Rev. Physiol. 67 (2005) 39-67
3. Li M.X., Wang X., and Sykes B.D. Structural based insights into the role of troponin in cardiac muscle pathophysiology. J. Muscle Res. Cell Motil. 25 (2004) 559-579
4. Herzberg O., and James M.N.G. Structure of the calcium regulatory muscle protein troponin-C at 2.8 A resolution. Nature 313 (1985) 653-659
5. Sundaralingam M., Bergstrom R., Strasburg G., Rao S.T., Roychowdhury P., Greaser M., and Wang B.C. Molecular structure of troponin C from chicken skeletal muscle at 3-Å resolution. Science 227 (1985) 945-948
6. 2+ -induced conformational transition of troponin C. J. Biol. Chem. 261 (1986) 2638-2644
7. Slupsky C.M., and Sykes B.D. NMR solution structure of calcium-saturated skeletal muscle troponin C. Biochemistry 34 (1995) 15953-15964
8. Gagné S.M., Tsuda S., Li M.X., Smillie L.B., and Sykes B.D. Structures of the troponin C regulatory domains in the apo and calcium-saturated states. Nat. Struct. Biol. 2 (1995) 784-789
9. Strynadka N.C.J., Cherney M., Sielecki A.R., Li M.X., Smillie L.B., and James M.N.G. Structural details of a calcium-induced molecular swith: X-ray crystallographic analysis of the calcium-saturated N-terminal domain of troponin C at 1.75 Å resolution. J. Mol. Biol. 273 (1997) 238-255
10. 2+ -swith in the calmodulin superfamily. Structure 5 (1997) 1695-1711
11. Sia S.K., Li M.X., Spyracopoulos L., Gagné S.M., Liu W., Putkey J.A., and Sykes B.D. NMR structure of cardiac troponin C reveals an unexpected closed regulatory domain. J. Biol. Chem. 272 (1997) 18216-18221
12. Spyracopoulos L., Li M.X., Sia S.K., Gagné S.M., Chandra M., Solaro R.J., and Sykes B.D. Calcium-induced structural transition in the regulatory domain of human cardiac troponin C. Biochemistry 36 (1997) 12138-12146
13. Li M.X., Spyracopoulos L., and Sykes B.D. Binding of cardiac troponin-I 147-163 induces a structural opening in human cardiac troponin-C. Biochemistry 38 (1999) 8289-8298
14. Mercier P., Ferguson R.E., Corrie J.E., Trenthem D.R., and Sykes B.D. Structure and dynamics of rhodamine labeled N-domain of skeletal troponin C in complex with with skeletal troponin I 115-131. Biochemistry 42 (2003) 4333-4348
15. 2+ and troponin I peptide binding to the E41A mutant of the N-domain of skeletal troponin C. Biochemistry 39 (2000) 12731-12738
16. McKay R.T., Tripet B.P., Hodges R.S., and Sykes B.D. Interaction of the second binding region of troponin I with the regulatory domain of skeletal muscle troponin-C as determined by NMR spectroscopy. J. Biol. Chem. 272 (1997) 28494-28500
17. McKay R.T., Tripet B.P., Pearlstone J.R., Smillie L.B., and Sykes B.D. Defining the region of troponin-I that binds to troponin-C. Biochemistry 38 (1999) 5478-5489
18. McKay R.T., Pearlstone J.R., Corson D.C., Gagné S.M., Smillie L.B., and Sykes B.D. Structure and interaction site of the regulatory domain of troponin-C when complexed with the 96-148 region of troponin-I. Biochemistry 37 (1998) 12419-12430
19. Gasmi-Seabrook G.M., Howarth J.W., Finley N., Abusamhadneh E., Gaponenko V., Brito R.M., Solaro R.J., and Rosevear P.R. Solution structures of the C-terminal domain of cardiac troponin C free and bound to the N-terminal domain of cardiac troponin I. Biochemistry 38 (1999) 8313-8322
20. Campbell A.P., and Sykes B.D. Interaction of troponin I and troponin C: use of the two-dimensional nuclear magnetic resonance transferred nuclear overhauser effect to determine the structure of the inhibitory troponin I peptide when bound to skeletal troponin C. J. Mol. Biol. 222 (1991) 405-421
21. Hernandez G., Blumenthal D.K., Kennedy M.A., Unkefer C.J., and Trewhella J. Troponin I inhibitory peptide (96-115) has an extended conformation when bound to skeletal muscle troponin C. Biochemistry 38 (1999) 6911-6917
22. Brito R.M., Putkey J.A., Strynadka N.C., James M.N., and Rosevear P.R. Comparative NMR studies on cardiac troponin C and a mutant incapable of binding calcium at site II. Biochemistry 30 (1991) 10236-10245
23. Brito R.M., Krudy G.A., Negele J.C., Putkey J.A., and Rosevear P.R. Calcium plays distinctive structural roles in the N- and C-terminal domains of cardiac troponin C. J. Biol. Chem. 268 (1993) 20966-20973
24. Krudy G.A., Brito R.M., Putkey J.A., and Rosevear P.R. Conformational changes in the metal-binding sites of cardiac troponin C induced by calcium binding. Biochemistry 31 (1992) 1595-1602
25. Krudy G.A., Kleerekoper Q., Guo X., Howarth J.W., Solaro R.J., and Rosevear P.R. NMR studies delineating spatial relationships within the cardiac troponin I-troponin C complex. J. Biol. Chem. 269 (1994) 23731-23735
26. Howarth J.W., Krudy G.A., Lin X., Putkey J.A., and Rosevear P.R. An NMR and spin label study of the effects of binding calcium and troponin I inhibitory peptide to cardiac troponin C. Protein Sci. 4 (1995) 671-680
27. Lin X., Krudy G.A., Howarth J., Brito R.M., Rosevear P.R., and Putkey J.A. Assignment and calcium dependence of methionyl epsilon C and epsilon H resonances in cardiac troponin C. Biochemistry 33 (1994) 14434-14442
28. Finley N., Abbott M.B., Abusamhadneh E., Gaponenko V., Dong W., Gasmi-Seabrook G., Howarth J.W., Rance M., Solaro R.J., Cheung H.C., and Rosevear P.R. NMR analysis of cardiac troponin C-troponin I complexes: effects of phosphorylation. FEBS Lett. 453 (1999) 107-112
29. Kleerekoper Q., Howarth J.W., Guo X., Solaro R.J., and Rosevear P.R. Cardiac troponin I induced conformational changes in cardiac troponin C as monitored by NMR using site-directed spin and isotope labeling. Biochemistry 34 (1995) 13343-13352
30. Abbott M.B., Gaponenko V., Abusamhadneh E., Finley N., Li G., Dvoretsky A., Rance M., Solaro R.J., and Rosevear P.R. Regulatory domain conformational exchange and linker region flexibility in cardiac troponin C bound to cardiac troponin I. J. Biol. Chem. 275 (2000) 20610-20617
31. Abbott M.B., Dvoretsky A., Gaponenko V., and Rosevear P.R. Cardiac troponin I inhibitory peptide: location of interaction sites on troponin C. FEBS Lett. 469 (2000) 168-172
32. Abbott M.B., Dong W.J., Dvoretsky A., DaGue B., Caprioli R.M., Cheung H.C., and Rosevear P.R. Modulation of cardiac troponin C-cardiac troponin I regulatory interactions by the amino-terminus of cardiac troponin I. Biochemistry 40 (2001) 5992-6001
33. Vassylyev D.G., Takeda S., Wakatsuki S., Maeda K., and Maeda Y. Crystal structure of troponin C in complex with troponin I fragment at 2.3-Å resolution. Proc. Natl. Acad. Sci. USA 95 (1998) 4847-4852
34. Lindhout D.A., and Sykes B.D. Structure and dynamics of the C-domain of human cardiac troponin C in complex with the inhibitory region of human cardiac troponin I. J. Biol. Chem. 278 (2003) 27024-27034
35. 2+-saturated form. Nature 424 (2003) 35-41
36. 2+-regulated structural changes in troponin. Proc Natl Acad Sci USA 102 (2005) 5038-5043
37. Brown L.J., Sale K.L., Hills R., Rouviere C., Song L.K., Zhang X.J., and Fajer P.G. Structure of the inhibitory region of troponin by site directed spin labeling electron paramagnetic resonance. Proc. Natl. Acad. Sci. USA 99 (2002) 12765-12770
38. Pearlstone J.R., and Smillie L.B. The interaction of rabit skeletal muscle troponin-T fragments with troponin I. Can. J. Biochem. Cell Biol. 63 (1985) 212-218
39. Gaponenko V., Abusamhadneh E., Abbott M.B., Finley N., Gasmi-Seabrook G., Solaro R.J., Rance M., and Rosevear P.R. Effects of troponin I phosphorylation on conformational exchange in the regulatory domain of cardiac troponin C. J. Biol. Chem. 274 (1999) 16681-16684
40. Ward D.G., Brewer S.M., Comes M.P., and Trayer I.P. A cross-linking study of the N-terminal extension of human cardiac troponin I. Biochemistry 42 (2003) 10324-10332
41. Howarth J.W., Meller J., Solaro R.J., Trewhella J., and Rosevear P.R. Phosphorylation-dependent conformational transition of the cardiac specific N-extension of troponin I in cardiac troponin. J. Mol. Biol. 373 (2007) 706-722
42. Blumenschein T.M., Stone D.B., Fletterick R.J., Mendelson R.A., and Sykes B.D. Calcium-dependent changes in the flexibility of the regulatory domain of troponin C in the troponin complex. J. Biol. Chem. 280 (2005) 21924-21932
43. 2+-regulated muscle relaxation at interaction sites of troponin with actin and tropomyosin. J. Mol. Biol. 352 (2005) 178-201
44. 2+ and myosin-induced activation of heart muscle. J. Mol. Biol. 340 (2004) 295-305
45. Blumenschein T.M., Stone D.B., Fletterick R.J., Mendelson R.A., and Sykes B.D. Dynamics of the C-terminal region of TnI in the troponin complex in solution. Biophys. J. 90 (2006) 2436-2444
46. Hoffman R.M.B., Blumenschein T.M., and Sykes B.D. An interplay between protein disorder and structure confers the Ca2+ regulation of striated muscle. J. Mol. Biol. 361 (2006) 625-633
47. 2+-sensitizers-update 2001, Cardiovasc. Drug Ther. 15 (2001) 397-403
48. 2+ sensitizers rescue patients from chronic congestive heart failure. Br. J. Pharmacol. 150 (2007) 826-828
49. 2+ sensitizer, levosimendan, to recombinant human cardiac troponin C. A molecular modelling, fluorescence probe, and proton nuclear magnetic resonance study. J. Biol. Chem. 269 (1994) 28584-28590
50. Sorsa T., Pollesello P., and Solaro R.J. The contractile apparatus as a target for drugs against heart failure: interaction of levosimendan, a calcium sensitizer, with cardiac troponin C. Mol. Cell. Biochem. 266 (2004) 87-107
51. Kass D.A., and Solaro R.J. Mechanisms and use of calcium-sensitizing agents in the failing heart. Circulation 113 (2006) 305-315
52. Cramb G., and Dow J.W. Two site binding of bepridil an modulation of adenylate cyclase in cardiac sarcolemmal membranes. Biochim. Biophys. Acta 736 (1983) 99-108
53. 2+ binding by bepridil. J. Pharmacol. Exp. Ther. 238 (1986) 502-507
54. MacLachlan L.K., Reid D.G., Mitchell R.C., Salter C.J., and Smith S.J. Binding of a calcium sensitizer, bepridil, to cardiac troponin C. A fluorescence stopped-flow kinetic, circular dichroism, and proton nuclear magnetic resonance study. J. Biol. Chem. 265 (1990) 9764-9770
55. Kleerekoper Q., Liu W., Choi D., and Putkey J.A. Identification of binding sites for bepridil and trifluoperazine on cardiac troponin C. J. Biol. Chem. 273 (1998) 8153-8160
56. Abusamhadneh E., Abbott M.B., Dvoretsky A., Finley N., Sasi S., and Rosevear P.R. Interaction of bepridil with the cardiac troponin C/troponin I complex. FEBS Lett. 506 (2001) 51-54
57. Li Y., Love M.L., Putkey J.A., and Cohen C. Bepridil opens the regulatory N-terminal lobe of cardiac troponin C. Proc. Natl. Acad. Sci. USA 97 (2000) 5140-5145
58. 147-163 and bepridil. J. Biol. Chem. 277 (2002) 31124-31133
59. Levin R.M., and Weiss B. Specificity of the binding of trifluoperazine to the calcium-dependent activator of phosphodiesterase and to a series of other calcium-binding proteins. Biochim. Biophys. Acta. 540 (1978) 197-204
60. Herzig J.W., Tkachuk V.A., Baldenkov G.N., Feoktistov I.A., Menshikov M.Y., and Quast U. Calmodulin and troponin C as targets for drug action. Biomed. Biochim. Acta 46 (1987) S440-S443
61. Kurebayashi N., and Ogawa Y. Increase by trifluoperazine in calcium sensitivity of myofibrils in a skinned fibre from frog skeletal muscle. J. Physiol. 403 (1988) 407-424
62. Silver P.J., Pinto P.B., and Dachiw J. Modulation of vascular and cardiac contractile protein regulatory mechanisms by calmodulin inhibitors and related compounds. Biochem. Pharmacol. 35 (1986) 2545-2551
63. Sorsa T., Heikkinen S., Abbott M.B., Abusamhadneh E., Laakso T., Tilgmann C., Serimaa R., Annila A., Rosevear P.R., Drakenberg T., Pollesello P., and Kilpelainen I. Binding of levosimendan, a calcium sensitizer, to cardiac troponin C. J. Biol. Chem. 276 (2001) 9337-9343
64. Kleerekoper Q., and Putkey J.A. Drug binding to cardiac troponin C. J. Biol. Chem. 274 (1999) 23932-23939
65. Sorsa T., Pollesello P., Permi P., Drakenberg T., and Kilpelainen I. Interaction of levosimendan with cardiac troponin C in the presence of cardiac troponin I peptides. J. Mol. Cell. Cardiol. 35 (2003) 1055-1061
66. Levijoki J., Pollesello P., Kaivola J., Tilgmann C., Sorsa T., Annila A., Kilpelainen I., and Haikala H. Further evidence for the cardiac troponin C mediated calcium sensitization by levosimendan: structure-response and binding analysis with analogs of levosimnedan. J. Mol. Cell. Cardiol. 32 (2000) 479-491
67. Robertson I.M., Reinke S.N., Li M.X., and Sykes B.D. Interaction of the regulatory domain of cardiac troponin C with a variety of cardiotonic drugs. Biophys. J. 92 (2007) 628a
68. Adhikari B.B., and Wang K. Interplay of troponin- and myosin-based pathways of calcium activation in skeletal and cardiac muscle: the use of W7 as an inhibitor of thin filament activation. Biophys. J. 86 (2004) 359-370
69. Hoffman R.M.B., Li M.X., and Sykes B.D. The binding of W7, an inhibitor of striated muscle contraction, to cardiac troponin C. Biochemistry 44 (2005) 15750-15759
70. Li M.X., Hoffman R.M.B., and Sykes B.D. Interaction of cardiac troponin C with calmodulin antagonist W7 in the presence of three functional regions of cardiac troponin I. Biochemistry 45 (2006) 9833-9840
71. Lues I., Beier N., Jonas R., Klockow M., and Haeusler G. The two mechanisms of action of racemic cardiotonic EMD 53998, calcium sensitization and phosphodiesterase inhibition, reside in different enantiomers. J. Cardiovasc. Pharmacol. 21 (1993) 883-892
72. Solaro R.J., Gambassi G., Warshaw D.M., Keller M.R., Spurgeon H.A., Beier N., and Lakatta E.G. Stereoselective actions of thiadiazinones on canine cardiac myocytes and myofilaments. Circ. Res. 73 (1993) 981-990
73. Haeusler G., Jonas R., Minck K.O., Schliep H.J., Schelling P., Weygandt H., and Lues I. In vivo evidence of positive inotropism of EMD 57033 through calcium sensitization. J. Cardiovasc. Pharmacol. 29 (1997) 647-655
74. Senzaki H., Isoda T., Paolocci N., Ekelund U., Hare J.M., and Kass D.A. Improved mechanoenergetics and cardiac rest and reserve function of in vivo failing heart by calcium sensitizer EMD 57033. Circulation 101 (2000) 1040-1048
75. 2+ in stunned myocardium. Eur. J. Pharmacol. 403 (2000) 99-109
76. de Zeeuw S., Trines S.A., Krams R., Verdouw P.D., and Duncker D.J. Cardiovascular profile of the calcium sensitizer EMD 57033 in open- chest anaesthetized pigs with regionally stunned myocardium. Br. J. Pharmacol. 129 (2000) 1413-1422
77. Tsutsui H., Kinugawa S., Ide T., Hayashidani S., Suematsu N., Satoh S., Nakamura R., Egashira K., and Takeshita A. Positive inotropic effects of calcium sensitizers on normal and failing cardiac myocytes. J. Cardiovasc. Pharmacol. 37 (2001) 16-24
78. Slinker B.K., Wu Y., Green H.W.I., Kirkpatrick R.D., and Campbell K.B. Overall cardiac functional effect of positive inotropic drugs with differing effects on relaxation. J. Cardiovasc. Pharmacol. 36 (2000) 1-13
79. Trines S.A., Smits C.A., van der Moer J., Slager C.J., Verdouw P.D., and Krams R. Calcium sensitizer EMD 57033, but not the beta1-adrenoreceptor agonist dobutamine, increases mechanical efficiency in stunned myocardium. J. Cardiovasc. Pharmacol. 39 (2002) 61-72
80. Soergel D.G., Georgakopoulos D., Stull L.B., Kass D.A., and Murphy A.M. Augmented systolic response to the calcium sensitizer EMD 57033 in a transgenic model with troponin I truncation. Am. J. Physiol. Heart Circ. Physiol. 286 (2004) H1785-H1792
81. Pan B.-S., and Johnson J.R.G. Interaction of cardiotonic thiadiazinone derivatives with cardiac troponin C. J. Biol. Chem. 271 (1996) 817-823
82. 2+ sensitizer EMD 57033 and cardiac troponin I inhibitory peptide. Biochemistry 39 (2000) 8782-8790
83. 2+ sensitizing drug EMD 57033. J. Biol. Chem. 276 (2001) 25456-25466
84. Burkart E.M., Arteaga G.M., Sumandea M.P., Prabhakar R., Wieczorek D.F., and Solaro R.J. Altered signaling surrounding the C-lobe of cardiac troponin C in myofilaments containing an alpha tropomyosin mutation linked to familial hypertrophic cardiomyopathy. J. Mol. Cell. Cardiol. 35 (2003) 1285-1293