Phosphorylation-dependent Conformational Transition of the Cardiac Specific N-Extension of Troponin I in Cardiac Troponin

Journal of Molecular Biology

Volumn 373, Issue 3, 2007, Pages 706-722

  Howarth, Jack W ^a   Meller, Jarek ^a   Solaro, R John ^b   Trewhella, Jill ^c,d   Rosevear, Paul R ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

^c UNIVERSITY OF UTAH   (United States)

^d UNIVERSITY OF SYDNEY   (Australia)

Author keywords

cardiac specific N extension of cardiac troponin I; cardiac troponin; modulation by phosphorylation; NMR; solution structure

Indexed keywords

CALCIUM; TROPONIN; TROPONIN I;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOINFORMATICS; CARBOXY TERMINAL SEQUENCE; MYOFILAMENT; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SEQUENCE ANALYSIS; X RAY CRYSTALLOGRAPHY;

EID: 34748818674     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.08.035     Document Type: Article

References (76)

1. van Eerd J.P., and Takahashi K. The amino acid sequence of bovine cardiac tamponin-C. Comparison with rabbit skeletal troponin-C. Biochem. Biophys. Res. Commun. 64 (1975) 122-127
2. Holroyde M.J., Robertson S.P., Johnson J.D., Solaro R.J., and Potter J.D. The calcium and magnesium binding sites on cardiac troponin and their role in the regulation of myofibrillar adenosine triphosphatase. J. Biol. Chem. 255 (1980) 11688-11693
3. Putkey J.A., Sweeney H.L., and Campbell S.T. Site-directed mutation of the trigger calcium-binding sites in cardiac troponin C. J. Biol. Chem. 264 (1989) 12370-12378
4. Strynadka N.C., Cherney M., Sielecki A.R., Li M.X., Smillie L.B., and James M.N. Structural details of a calcium-induced molecular switch: 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
5. Gagne S.M., Li M.X., and Sykes B.D. Mechanism of direct coupling between binding and induced structural change in regulatory calcium binding proteins. Biochemistry 36 (1997) 4386-4392
6. She M., Xing J., Dong W.J., Umeda P.K., and Cheung H.C. Calcium binding to the regulatory domain of skeletal muscle troponin C induces a highly constrained open conformation. J. Mol. Biol. 281 (1998) 445-452
7. Spyracopoulos L., Li M.X., Sia S.K., Gagne 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
8. Dong W.J., Xing J., Villain M., Hellinger M., Robinson J.M., Chandra M., et al. Conformation of the regulatory domain of cardiac muscle troponin C in its complex with cardiac troponin I. J. Biol. Chem. 274 (1999) 31382-31390
9. Abbott M.B., Dvoretsky A., Gaponenko V., and Rosevear P.R. Cardiac troponin I inhibitory peptide: location of interaction sites on troponin C. FEBS Letters 469 (2000) 168-172
10. Brown L.J., Sale K.L., Rouviere C., Song L., Zhang X., 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
11. Vinogradova M.V., Stone D.B., Malanina G.G., Karatzaferi C., Cooke R., Mendelson R.A., and Fletterick R.J. Ca(2+)-regulated structural changes in troponin. Proc. Natl Acad. Sci. USA 102 (2005) 5038-5043
12. Lindhout D.A., Boyko R.F., Corson D.C., Li M.X., and Sykes B.D. The role of electrostatics in the interaction of the inhibitory region of troponin I with troponin C. Biochemistry 44 (2005) 14750-14759
13. Tao T., Gong B.J., and Leavis P.C. Calcium-induced movement of troponin-I relative to actin in skeletal muscle thin filaments. Science 247 (1990) 1339-1341
14. Aihara T., Ueki S., Nakamura M., and Arata T. Calcium-dependent movement of troponin I between troponin C and actin as revealed by spin-labeling EPR. Biochem. Biophys. Res. Commun. 340 (2006) 462-468
15. Shitaka Y., Kimura C., Iio T., and Miki M. Kinetics of the structural transition of muscle thin filaments observed by fluorescence resonance energy transfer. Biochemistry 43 (2004) 10739-10747
16. Patchell V.B., Gallon C.E., Hodgkin M.A., Fattoum A., Perry S.V., and Levine B.A. The inhibitory region of troponin-I alters the ability of F-actin to interact with different segments of myosin. Eur. J. Biochem. 269 (2002) 5088-5100
17. Patchell V.B., Gallon C.E., Evans J.S., Gao Y., Perry V., and Levine B.A. The regulatory effects of tropomyosin and troponin I on the interaction of myosin loop regions with F-actin. J. Biol. Chem. 280 (2005) 14469-14475
18. Mittmann K., Jaquet K., and Heilmeyer L.M.G.J. A common motif of two adjacent phosphoserines in bovine, rabbit and human cardiac troponin I. FEBS Letters 273 (1990) 41-45
19. Kentish J.C., McCloskey D.T., Layland J., Palmer S., Leiden J.M., Martin A.F., and Solaro R.J. Phosphorylation of troponin I by protein kinase A accelerates relaxation and crossbridge cycle kinetics in mouse ventricular muscle. Circ. Res. 88 (2001) 1059-1065
20. 2+-regulatory site of bovine cardiac troponin. J. Biol. Chem. 257 (1982) 260-263
21. 2+ affinity of cardiac troponin C. J. Biol. Chem. 270 (1995) 30773-30780
22. Reiffert S.U., Jaquet K., Heilmeyer L.M.J., Ritchie M.D., and Geeves M.A. Bisphosphorylation of cardiac troponin I modulates the Ca(2+)-dependent binding of myosin subfragment S1 to reconstituted thin filaments. FEBS Letters 384 (1996) 43-47
23. Layland J., Grieve D.J., Cave A.C., Sparks E., Solaro R.J., and Shah A.M. Essential role of troponin I in the positive inotropic response to isoprenaline in mouse hearts contracting auxotonically. J. Physiol. (London) 556 (2004) 835-847
24. Sakthivel S., Finley N.L., Rosevear P.R., Lorenz J.N., Gulick J., Kim S., et al. In vivo and in vitro analysis of cardiac troponin I phosphorylation. J. Biol. Chem. 280 (2005) 703-714
25. 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
26. Abbott M.B., Gaponenko V., Abusamhadneh E., Finley N., Li G., Dvoretsky A., et al. Regulatory domain conformational exchange and linker region flexibility in cardiac troponin C bound to cardiac troponin I. J. Biol. Chem. 275 (2000) 20610-20617
27. Finley N., Abbott M.B., Abusamhadneh E., Gaponenko V., Dong W., Gasmi-Seabrook G., et al. NMR analysis of cardiac troponin C-troponin I complexes: effects of phosphorylation. FEBS Letters 453 (1999) 107-112
28. Gaponenko V., Abusamhadneh E., Abbott M.B., Finley N., Gasmi-Seabrook G., Solaro R.J., et al. Effects of troponin I phosphorylation on conformational exchange in the regulatory domain of cardiac troponin C. J. Biol. Chem. 274 (1999) 16681-16684
29. Ward D.G., Brewer S.M., Gallon C.E., Gao Y., Levine B.A., and Trayer I.P. NMR and mutagenesis studies on the phosphorylation region of human cardiac troponin I. Biochemistry 43 (2004) 5772-5781
30. Ferrieres G., Pugniere M., Mani J.C., Villard S., Laprade M., Doutre P., et al. Systematic mapping of regions of human cardiac troponin I involved in binding to cardiac troponin C: N- and C-terminal low affinity contributing regions. FEBS Letters 479 (2000) 99-105
31. 2+ -saturated form. Nature 424 (2003) 35-41
32. Wishart D.S., and Sykes B.D. Determination of secondary structure using chemical shift scales. J. Biomol. NMR 4 (1994) 171-180
33. Perrin C.L., Johnston E.R., Lollo C.P., and Kobrin P.A. NMR studies of base-catalyzed proton exchange in amides. J. Am. Chem. Soc. 103 (1981) 4691-4696
34. Perrin C.L., and Johnston E.R. Mechanisms of acid-catalyzed proton exchange in amides. J. Am. Chem. Soc. 103 (1981) 4697-4703
35. Tuchsen E., and Woodward C. Hydrogen exchange of primary amide protons in basic pancreatic trypsin inhibitor: evidence for NH2 group rotation in buried asparagine side chains. Biochemistry 26 (1987) 8073-8078
36. Tsikaris V., Sakarellos-Daitsiotis M., Tzovaras D., Sakarellos C., Orlewski P., Cung M.T., and Marraud M. Isomerization of the Xaa-Pro peptide bond induced by ionic interactions of arginine. Biopolymers 38 (1996) 673-682
37. Tsikaris V., Troganis A., Moussis V., Panou-Pomonis E., Sakarellos-Daitsiotis M., and Sakarellos C. Arg side-chain-backbone interactions evidenced in model peptides by 17O-NMR spectroscopy. Biopolymers 53 (2000) 135-139
38. Adzhubei A.A., and Sternberg M.J. Left-handed polyproline helices commonly occur in globular proteins. J. Mol. Biol. 229 (1993) 472-493
39. Andrew C.D., Warwicker J., Jones G.R., and Doig A.J. Effect of phoshporylation on helix stability as afunction of position. Biochemistry 41 (2002) 1897-1905
40. Ward D.G., Cornes M.P., and Trayer I.P. Structural consequences of cardiac troponin I phosphorylation. J. Biol. Chem. 277 (2002) 41795-41801
41. Schmidtmann A., Lindow C., Villard S., Heuser A., Mugge A., Gessner R., et al. Cardiac troponin C-L29Q, related to hypertrophic cardiomyopathy, hinders the transduction of the protein kinase A dependent phosphorylation signal from cardiac troponin I to C. FEBS J. 272 (2005) 6087-6097
42. Heller W.T., Finley N., Dong W.-J., Timmins P., Cheung H.C., Rosevear P.R., and Trewhella J. Small-angle neutron scattering with contrast variation reveals spatial relationships between the three subunits in the ternary cardiac troponin complex and the effects of troponin I phosphorlyation. Biochemistry 42 (2003) 7790-7800
43. Quirk P.G., Patchell V.B., Gao Y., Levine B.A., and Perry S.V. Sequential phosphorylation of adjacent serine residues on the N- terminal region of cardiac troponin-I: structure-activity implications of ordered phosphorylation. FEBS Letters 370 (1995) 175-178
44. Deng Y., Schmidtmann A., Redlich A., Westerdorf B., Jaquet K., and Thieleczek R. Effects of phosphorylation and mutation R145G on human cardiac troponin I function. Biochemistry 40 (2001) 14593-14602
45. Wattanapermpool J., Reiser P.J., and Solaro R.J. Troponin I isoforms and differential effects of acidic pH on soleus and cardiac myofilaments. Am. J. Physiol. 268 (1995) C323-C330
46. Luo Y., Leszyk J., Li B., Li Z., Gergely J., and Tao T. Troponin-I interacts with the Met47 region of skeletal muscle actin. Implications for the mechanism of thin filament regulation by calcium. J. Mol. Biol. 316 (2002) 429-434
47. Arad M., Penas-Lado M., Monserrat L., Maron B.J., Sherrid M., Ho C.Y., et al. Gene mutations in apical hypertrophic cardiomyopathy. Circulation 112 (2005) 2805-2811
48. Gomes A.V., Harada K., and Potter J.D. A mutation in the N-terminus of troponin I that is associated with hypertrophic cardiomyopathy affects the Ca(2+)-sensitivity, phosphorylation kinetics and proteolytic susceptibility of troponin. J. Mol. Cell. Cardiol. 39 (2005) 754-765
49. Borders C.L.J., Broadwater J.A., Bekeny P.A., Salmon J.E., Lee A.S., Eldridge A.M., and Pett V.B. A structural role for arginine in proteins: multiple hydrogen bonds to backbone carbonyl oxygens. Protein Sci. 3 (1994) 541-548
50. Dong W.J., Chandra M., Xing J., She M., Solaro R.J., and Cheung H.C. Phosphorylation-induced distance change in a cardiac muscle troponin I mutant. Biochemistry 36 (1997) 6754-6761
51. Reiffert S.U., Jaquet K., Heilmeyer Jr. L.M., and Herberg F.W. Stepwise subunit interaction changes by mono- and bisphosphorylation of cardiac troponin I. Biochemistry 37 (1998) 13516-13525
52. Mazhari S., Selser C., and Cremo C. Novel sensors of the regulatory switch on the regulatory light chain of smooth muscle myosin. J. Biol. Chem. 279 (2004) 39905-39914
53. Dong W., An J., Xing J., and Cheung H. Structural transition of the inhibitory region of troponin I within the regulated cardiac thin filament. Arch. Biochem. Biophys. 456 (2006) 135-142
54. Joughin B., Tiidor B., and Yaffe M. A computational method for the analysis and prediction of protein:phosphopeptide-binding sites. Protein Sci. 14 (2005) 131-139
55. Noland Jr. T.A., Raynor R.L., Jideama N.M., Guo X., Kazanietz M.G., Blumberg P.M., et al. Differential regulation of cardiac actomyosin S-1 MgATPase by protein kinase C isozyme-specific phosphorylation of specific sites in cardiac troponin I and its phosphorylation site mutants. Biochemistry 35 (1996) 14923-14931
56. Roman B.B., Goldspink P.H., Spaite E., Urboniene D., McKinney R., Geenen D.L., et al. Inhibition of PKC phosphorylation of cTnl improves cardiac performance in vivo. Am. J. Physiol. Heart Circ. Physiol. 286 (2004) H2089-H2095
57. Gomes A.V., and Potter J.D. Cellular and molecular aspects of familial hypertropic cardiomyopathy caused by mutations in the cardiac troponin I gene. Mol. Cell. Biochem. 263 (2004) 99-114
58. James J., Zhang Y., Osinka H., Sanbe A., Klevitsky R., Hewett T., and Robbins J. Transgenic modeling of a cardiac troponin I mutation linked to familial hypertrophic cardiomyopathy. Circ. Res. 87 (2000) 805-811
59. Elliott K., Watkins H., and Redwood C. Altered regulatory properties of human cardiac troponin I mutants that cause hypertrophic cardiomyopathy. J. Biol. Chem. 275 (2000) 22069-22074
60. Kruger M., Zittrich S., Redwood C., Blaudeck N., James J., Robbins J., et al. Effects of the mutation R145G in human cardiac troponin I on the kinetics of the contraction-relaxation cycle in isolated cardiac myofibrils. J. Physiol. 564 (2005) 347-357
61. Burkart E.M., Sumandea M.P., Kobayashi T., Nili M., Martin A.F., Homsher E., and Solaro R.J. Phosphorylation or glutamic acid substitution at protein kinase C sites on cardiac troponin I differentially depress myofilament tension and shortening velocity. J. Biol. Chem. 278 (2003) 11265-11271
62. Takimoto E., Soergel D.G., Janssen P.M., Stull L.B., Kass D.A., and Murphy A.M. Frequency- and afterload-dependent cardiac modulation in vivo by troponin I with constitutively active protein kinase A phosphorylation sites. Circ. Res. 94 (2004) 496-504
63. Wuthrich, K. (1986). NMR of Proteins and Nucleic Acids, John Wiley & Sons, New York.
64. Cornilescu G., Delaglio F., and Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13 (1999) 289-302
65. Schwieters C.D., Kuszewski J.J., Tjandra N., and Clore G.M. The Xplor-NIH NMR molecular structure determination package. J. Magn. Reson. 160 (2003) 65-73
66. Nilges M., Clore G., and Gronenborn A. Determination of three-dimensional structures of proteins from interproton distance data by dynamical simulated annealing from a random array of atoms. Circumventing problems associated with folding. FEBS Letters 239 (1988) 129-136
67. Rife J., Stallings S., Correll C., Dallas A., Steitz T., and Moore P. Comparison of the crystal and solution structures of two RNA oligonucleotides. Biophys. J. 76 (1999) 65-75
68. Laskowski R.A., Rullmannn J.A., MacArthur M.W., Kaptein R., and Thornton J.M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8 (1996) 477-486
69. Willard L., Ranjan A., Zhang H., Monzavi H., Boyko R.F., Sykes B.D., and Wishart D.S. VADAR: a web server for quantitative evaluation of protein structure quality. Nucl. Acids Res. 31 (2003) 3316-3319
70. Eyrich V., Marti-Renom M., Przybylski D., Madhusudhan M., Fiser A., Pazos F., et al. EVA: continuous automatic evaluation of protein structure prediction servers. Bioinformatics 17 (2001) 1242-1243
71. Jones D. Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 292 (1999) 195-202
72. Adamczak R., Porollo A., and Meller J. Combining prediction of secondary structures and solvent accessibility in proteins. Proteins: Struct. Funct. Genet. 59 (2005) 467-475
73. Adamczak R., Porollo A., and Meller J. Accurate prediction of solvent accessibility using neural networks-based regression. Proteins: Struct. Funct. Genet. 56 (2004) 753-767
74. Porollo A., Adamczak R., and Meller J. POLYVIEW: a flexible visualization tool for structural and functional annotations of proteins. Bioinformatics 20 (2004) 2460-2462
75. Heller W.T., Abusamhadneh E., Finley N., Rosevear P.R., and Trewhella J. The solution structure of a cardiac troponin C-troponin I-troponin T complex shows a somewhat compact troponin C interacting with an extended troponin I-troponin T component. Biochemistry 41 (2002) 15654-15663
76. Baker N., Sept D., Joseph S., Hoolst M., and McCammon J. Electrostatics of nanosystems: applications to microtubules and the ribosome. Proc. Natl Acad. Sci. USA 98 (2001) 10037-10041