Versatile cardiac troponin chimera for muscle protein structural biology and drug discovery

ACS Chemical Biology

Volumn 9, Issue 9, 2014, Pages 2121-2130

  Pineda Sanabria, Sandra E ^a   Julien, Olivier ^a,b   Sykes, Brian D ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; MUSCLE PROTEIN; TROPONIN C; TROPONIN I; BEPRIDIL; CALCIUM; DRUG; N (6 AMINOHEXYL) 5 CHLORO 1 NAPHTHALENESULFONAMIDE; RECOMBINANT PROTEIN; SULFONAMIDE; THROMBIN;

ARTICLE; CHIMERA; DRUG DEVELOPMENT; ISOTOPE LABELING; PROTEIN AGGREGATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SOLUBILITY; CHEMISTRY; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PROTEIN CONFORMATION; SPECTROFLUOROMETRY;

BEPRIDIL; CALCIUM; DRUG DISCOVERY; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHARMACEUTICAL PREPARATIONS; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SPECTROMETRY, FLUORESCENCE; SULFONAMIDES; THROMBIN; TROPONIN C; TROPONIN I;

EID: 84912574169     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb500249j     Document Type: Article

References (52)

1. Gordon, A. M., Homsher, E., and Regnier, M. (2000) Regulation of contraction in striated muscle. Physiol. Rev. 80, 853-924.
2. Kobayashi, T., Jin, L., and de Tombe, P. (2008) Cardiac thin filament regulation. Pflügers Arch 457, 37-46.
3. Li, M., Wang, X., and Sykes, B. (2004) Structural based insights into the role of troponin in cardiac muscle pathophysiology. J. Muscle Res. Cell Motil. 25, 559-579.
4. Takeda, S., Yamashita, A., Maeda, K., and Maeda, Y. (2003) Structure of the core domain of human cardiac troponin in the Ca2+-saturated form. Nature 424, 35-41.
5. Li, M. X., Spyracopoulos, L., and Sykes, B. D. (1999) Binding of cardiac troponin-I147-163 induces a structural opening in human cardiac troponin-C. Biochemistry 38, 8289-8298.
6. Spyracopoulos, L., Li, M. X., Sia, S. K., Gagné, S. M., Chandra, M., Solaro, R. J., and Sykes, B. D. (1997) Calcium-induced structural transition in the regulatory domain of human cardiac troponin C. Biochemistry 36, 12138-12146.
7. Lassalle, M. W. (2010) Defective dynamic properties of human cardiac troponin mutations. Biosci. Biotechnol. Biochem. 74, 82-91.
8. Blumenschein, T. M. A., Stone, D. B., Fletterick, R. J., Mendelson, R. A., and Sykes, B. D. (2006) Dynamics of the C-terminal region of TnI in the troponin complex in solution. Biophys. J. 90, 2436-2444.
9. Julien, O., Mercier, P., Allen, C. N., Fisette, O., Ramos, C. H. I., Lagüe, P., Blumenschein, T. M. A., and Sykes, B. D. (2011) Is there nascent structure in the intrinsically disordered region of troponin I? Proteins 79, 1240-1250.
10. Robertson, I. M., Holmes, P. C., Li, M. X., Pineda-Sanabria, S. E., Baryshnikova, O. K., and Sykes, B. D. (2012) Elucidation of isoform-dependent pH sensitivity of troponin I by NMR spectroscopy. J. Biol. Chem. 287, 4996-5007.
11. Dargis, R., Pearlstone, J. R., Barrette-Ng, I., Edwards, H., and Smillie, L. B. (2002) Single mutation (A162H) in human cardiac troponin I corrects acid pH sensitivity of Ca2+-regulated actomyosin S1 ATPase. J. Biol. Chem. 277, 34662-34665.
12. Day, S. M., Westfall, M. V., Fomicheva, E. V., Hoyer, K., Yasuda, S., Cross, N. C. L., D'Alecy, L. G., Ingwall, J. S., and Metzger, J. M. (2006) Histidine button engineered into cardiac troponin I protects the ischemic and failing heart. Nat. Med. 12, 181-189.
13. Pineda-Sanabria, S. E., Robertson, I. M., Li, M. X., and Sykes, B. D. (2013) Interaction between the regulatory domain of cardiac troponin C and the acidosis-resistant cardiac troponin I A162H. Cardiovasc. Res. 97, 481-489.
14. Overington, J. P., Al-Lazikani, B., and Hopkins, A. L. (2006) How many drug targets are there? Nat. Rev. Drug Discovery 5, 993-996.
15. Endoh, M. (2008) Cardiac Ca2+ signaling and Ca2+ sensitizers. Circ. J. 72, 1915-1925.
16. Robertson, I. M., Sun, Y., Li, M. X., and Sykes, B. D. (2010) A structural and functional perspective into the mechanism of Ca2+-sensitizers that target the cardiac troponin complex. J. Mol. Cell. Cardiol. 49, 1031-1041.
17. Wang, X., Li, M. X., and Sykes, B. D. (2002) Structure of the regulatory N-domain of human cardiac troponin C in complex with human cardiac troponin I147-163 and bepridil. J. Biol. Chem. 277, 31124-31133.
18. Haikala, H., Kaivola, J., Nissinen, E., Wall, P., Levijoki, J., and Lindén, I. (1995) Cardiac troponin C as a target protein for a novel calcium sensitizing drug, levosimendan. J. Mol. Cell. Cardiol. 27, 1859-1866.
19. 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 Kilpeläinen, I. (2001) Binding of levosimendan, a calcium sensitizer, to cardiac troponin C. J. Biol. Chem. 276, 9337-9343.
20. Papp, Z., Édes, I., Fruhwald, S., De Hert, S. G., Salmenperä, M., Leppikangas, H., Mebazaa, A., Landoni, G., Grossini, E., Caimmi, P., Morelli, A., Guarracino, F., Schwinger, R. H. G., Meyer, S., Algotsson, L., Wikström, B. G., Jörgensen, K., Filippatos, G., Parissis, J. T., González, M. J. G., Parkhomenko, A., Yilmaz, M. B., Kivikko, M., Pollesello, P., and Follath, F. (2012) Levosimendan: Molecular mechanisms and clinical implications: Consensus of experts on the mechanisms of action of levosimendan. Int. J. Cardiol. 159, 82-87.
21. Oleszczuk, M., Robertson, I. M., Li, M. X., and Sykes, B. D. (2010) Solution structure of the regulatory domain of human cardiac troponin C in complex with the switch region of cardiac troponin I and W7: The basis of W7 as an inhibitor of cardiac muscle contraction. J. Mol. Cell. Cardiol. 48, 925-933.
22. Porumb, T., Yau, P., Harvey, T. S., and Ikura, M. (1994) A calmodulin-target peptide hybrid molecule with unique calcium-binding properties. Protein Eng. 7, 109-115.
23. Westfall, M. V., and Metzger, J. M. (2001) Troponin I isoforms and chimeras: Tuning the molecular switch of cardiac contraction. Physiology 16, 278-281.
24. Rezvanpour, A., Phillips, J. M., and Shaw, G. S. (2009) Design of high-affinity S100-target hybrid proteins. Protein Sci. 18, 2528-2536.
25. Zhou, H., and Gilson, M. K. (2009) Theory of free energy and entropy in noncovalent binding. Chem. Rev. 109, 4092-4107.
26. Zhou, H. (2001) The affinity-enhancing roles of flexible linkers in two-domain DNA-binding proteins. Biochemistry 40, 15069-15073.
27. Fielding, L. (2007) NMR methods for the determination of protein-ligand dissociation constants. Prog. Nucl. Magn. Reson. Spectrosc. 51, 219-242.
28. Macomber, R. S. (1992) An introduction to NMR titration for studying rapid reversible complexation. J. Chem. Educ. 69, 375.
29. Robertson, I., Boyko, R., and Sykes, B. (2011) Visualizing the principal component of 1H,15N-HSQC NMR spectral changes that reflect protein structural or functional properties: Application to troponin C. J. Biomol. NMR 51, 115-122.
30. Zhou, H. (2006) Quantitative relation between intermolecular and intramolecular binding of pro-rich peptides to SH3 domains. Biophys. J. 91, 3170-3181.
31. Li, M. X., Gagné, S. M., Spyracopoulos, L., Kloks, C. P. A. M., Audette, G., Chandra, M., Solaro, R. J., Smillie, L. B., and Sykes, B. D. (1997) NMR studies of Ca2+ binding to the regulatory domains of cardiac and E41A skeletal muscle troponin C reveal the importance of site I to energetics of the induced structural changes. Biochemistry 36, 12519-12525.
32. Pan, B. S., and Solaro, R. J. (1987) Calcium-binding properties of troponin C in detergent-skinned heart muscle fibers. J. Biol. Chem. 262, 7839-7849.
33. Wang, Y. P., and Fuchs, F. (1994) Length, force, and Ca(2+)-troponin C affinity in cardiac and slow skeletal muscle. Am. J. Physiol. 266, C1077-82.
34. Wolska, B. M., Keller, R. S., Evans, C. C., Palmiter, K. A., Phillips, R. M., Muthuchamy, M., Oehlenschlager, J., Wieczorek, D. F., de Tombe, P. P., and Solaro, R. J. (1999) Correlation between myofilament response to Ca2+ and altered dynamics of contraction and relaxation in transgenic cardiac cells that express β-tropomyosin. Circ. Res. 84, 745-751.
35. Kischel, P., Bastide, B., Potter, J. D., and Mounier, Y. (2000) The role of the Ca(2+) regulatory sites of skeletal troponin C in modulating muscle fibre reactivity to the Ca(2+) sensitizer bepridil. Br. J. Pharmacol. 131, 1496-1502.
36. Lindert, S., Kekenes-Huskey, P., Huber, G., Pierce, L., and McCammon, J. A. (2012) Dynamics and calcium association to the N-terminal regulatory domain of human cardiac troponin C: A multiscale computational study. J. Phys. Chem. B 116, 8449-8459.
37. Robinson, J. M., Cheung, H. C., and Dong, W. (2008) The cardiac Ca2+-sensitive regulatory switch, a system in dynamic equilibrium. Biophys. J. 95, 4772-4789.
38. Li, M. X., Hoffman, R. M. B., and Sykes, B. D. (2006) Interaction of cardiac troponin C and troponin I with W7 in the presence of three functional regions of cardiac troponin I. Biochemistry 45, 9833-9840.
39. Voet, A., Banwell, E. F., Sahu, K. K., Heddle, J. G., and Zhang, K. Y. (2013) Protein interface pharmacophore mapping tools for small molecule protein: Protein interaction inhibitor discovery. Curr. Top. Med. Chem. 13, 989-1001.
40. Barile, E., and Pellecchia, M. (2014) NMR-based approaches for the identification and optimization of inhibitors of protein-protein interactions. Chem. Rev. 114, 4749-4763.
41. Gonzalez-Ruiz, D., and Gohlke, H. (2006) Targeting protein-protein interactions with small molecules: Challenges and perspectives for computational binding epitope detection and ligand finding. Curr. Med. Chem. 13, 2607-2625.
42. Morelli, X., Bourgeas, R., and Roche, P. (2011) Chemical and structural lessons from recent successes in protein-protein interaction inhibition (2P2I). Curr. Opin. Chem. Biol. 15, 475-481.
43. Blumenschein, T. M. A., Stone, D. B., Fletterick, R. J., Mendelson, R. A., and Sykes, B. D. (2005) Calcium-dependent changes in the flexibility of the regulatory domain of troponin C in the troponin complex. J. Biol. Chem. 280, 21924-21932.
44. Li, M., Saude, E., Wang, X., Pearlstone, J., Smillie, L., and Sykes, B. (2002) Kinetic studies of calcium and cardiac troponin I peptide binding to human cardiac troponin C using NMR spectroscopy. Eur. Biophys. J. 31, 245-256.
45. Li, M. X., Gagne, S. M., Tsuda, S., Kay, C. M., Smillie, L. B., and Sykes, B. D. (1995) Calcium binding to the regulatory N-domain of skeletal muscle troponin C occurs in a stepwise manner. Biochemistry 34, 8330-8340.
46. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293.
47. Johnson, B. A., and Blevins, R. A. (1994) NMR view: A computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4, 603-614.
48. Pierson, E. S., Miller, D. D., Callaham, D. A., Shipley, A. M., Rivers, B. A., Cresti, M., and Hepler, P. K. (1994) Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: Effect of BAPTA-type buffers and hypertonic media. Plant Cell. 6, 1815-1828.
49. Linse, S., Helmersson, A., and Forsén, S. (1991) Calcium binding to calmodulin and its globular domains. J. Biol. Chem. 266, 8050-8054.
50. Davis, J. P., Norman, C., Kobayashi, T., Solaro, R. J., Swartz, D. R., and Tikunova, S. B. (2007) Effects of thin and thick filament proteins on calcium binding and exchange with cardiac troponin C. Biophys. J. 92, 3195-3206.
51. Marti-Renom, M. A., Stuart, A. C., Fiser, A., Sanchez, R., Melo, F., and Sali, A. (2000) Comparative protein structure modeling of genes and genomes. Annu. Rev. Biophys. Biomol. Struct. 29, 291-325.
52. Hoffman, R. M. B., Li, M. X., and Sykes, B. D. (2005) The binding of W7, an inhibitor of striated muscle contraction, to cardiac troponin C. Biochemistry 44, 15750-15759.