Structure and Dynamics of the Acidosis-Resistant A162H Mutant of the Switch Region of Troponin i Bound to the Regulatory Domain of Troponin C

Biochemistry

Volumn 54, Issue 23, 2015, Pages 3583-3593

  Pineda Sanabria, Sandra E ^a   Robertson, Ian M ^a   Sykes, Brian D ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MUSCLE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

CARDIAC MUSCLES; CARDIAC TROPONIN I; FORCE GENERATION; GAIN-OF FUNCTION; PHARMACOLOGICAL AGENTS; REGULATORY DOMAIN; STRUCTURAL STUDIES; STRUCTURE AND DYNAMICS;

HEART;

ALANINE; HISTIDINE; TROPONIN C; TROPONIN I; CALCIUM; CARBON; GLUTAMIC ACID; HYBRID PROTEIN; MUTANT PROTEIN; NITROGEN; PEPTIDE FRAGMENT; RECOMBINANT PROTEIN;

ACIDOSIS; ARTICLE; CONFORMATION; DIASTOLIC DYSFUNCTION; GENE MUTATION; HEART CONTRACTION; HEART PERFORMANCE; HUMAN; MOLECULAR DYNAMICS; MUSCLE CONTRACTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PH; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTON TRANSPORT; AMINO ACID SUBSTITUTION; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; KINETICS; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PROTEIN CONFORMATION; PROTEIN DOMAIN; SITE DIRECTED MUTAGENESIS;

AMINO ACID SUBSTITUTION; BINDING SITES; CALCIUM; CARBON RADIOISOTOPES; GLUTAMIC ACID; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; NITROGEN RADIOISOTOPES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECOMBINANT FUSION PROTEINS; RECOMBINANT PROTEINS; TROPONIN C; TROPONIN I;

EID: 84934969890     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b00178     Document Type: Article

References (34)

1. 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
2. Day, S. M., Westfall, M. V., Fomicheva, E. V., Hoyer, K., Yasuda, S., Cross, N. C. L., DAlecy, 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
3. Palpant, N. J., Day, S. M., Herron, T. J., Converso, K. L., and Metzger, J. M. (2008) Single histidine-substituted cardiac troponin I confers protection from age-related systolic and diastolic dysfunction Cardiovasc. Res. 80, 209-218
4. Kobayashi, T., Jin, L., and de Tombe, P. (2008) Cardiac thin filament regulation Pfluegers Arch. 457, 37-46
5. 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
6. Vinogradova, M. V., Stone, D. B., Malanina, G. G., Karatzaferi, C., Cooke, R., Mendelson, R. A., and Fletterick, R. J. (2005) Ca2+-regulated structural changes in troponin Proc. Natl. Acad. Sci. U.S.A.. 102, 5038-5043
7. 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
8. 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
9. Zhou, Z., Li, K., Rieck, D., Ouyang, Y., Chandra, M., and Dong, W. (2012) Structural dynamics of C-domain of cardiac troponin I protein in reconstituted thin filament J. Biol. Chem. 287, 7661-7674
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. 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
12. Robertson, I. M., Pineda-Sanabria, S. E., Holmes, P. C., and Sykes, B. D. (2014) Conformation of the critical pH sensitive region of troponin depends upon a single residue in troponin I Arch. Biochem. Biophys. 552-553, 40-49
13. Knowles, A. C., Irving, M., and Sun, Y. (2012) Conformation of the troponin core complex in the thin filaments of skeletal muscle during relaxation and active contraction J. Mol. Biol. 421, 125-137
14. Westfall, M. V. and Metzger, J. M. (2007) Single amino acid substitutions define isoform-specific effects of troponin I on myofilament Ca2+ and pH sensitivity J. Mol. Cell. Cardiol. 43, 107-118
15. 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
16. Pineda-Sanabria, S., Julien, O., and Sykes, B. D. (2014) Versatile cardiac troponin chimera for muscle protein structural biology and drug discovery ACS Chem. Biol. 9, 2121-2130
17. Zheng, L., Baumann, U., and Reymond, J. (2004) An efficient one-step site-directed and site-saturation mutagenesis protocol Nucleic Acids Res. 32, e115-e115
18. Baryshnikova, O., Williams, T., and Sykes, B. (2008) Internal pH indicators for biomolecular NMR J. Biomol. NMR 41, 5-7
19. 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
20. 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
21. Shen, Y., Delaglio, F., Cornilescu, G., and Bax, A. (2009) TALOS+: A hybrid method for predicting protein backbone torsion angles from NMR chemical shifts J. Biomol. NMR 44, 213-223
22. Schwieters, C. D., Kuszewski, J. J., and Marius Clore, G. (2006) Using Xplor-NIH for NMR molecular structure determination Prog. Nucl. Magn. Reson. Spectrosc. 48, 47-62
23. Bermejo, G. A., Clore, G. M., and Schwieters, C. D. (2012) Smooth statistical torsion angle potential derived from a large conformational database via adaptive kernel density estimation improves the quality of NMR protein structures Protein Sci. 21, 1824-1836
24. Spyracopoulos, L., Gagné, S. M., Li, M. X., and Sykes, B. D. (1998) Dynamics and thermodynamics of the regulatory domain of human cardiac troponin C in the apo- and calcium-saturated states Biochemistry. 37, 18032-18044
25. Robertson, S. P., Johnson, J. D., Holroyde, M. J., Kranias, E. G., Potter, J. D., and Solaro, R. J. (1982) The effect of troponin I phosphorylation on the Ca2+-binding properties of the Ca2+-regulatory site of bovine cardiac troponin J. Biol. Chem. 257, 260-263
26. Solaro, R. J., Rosevear, P., and Kobayashi, T. (2008) The unique functions of cardiac troponin I in the control of cardiac muscle contraction and relaxation Biochem. Biophys. Res. Commun. 369, 82-87
27. Hwang, P. M., Cai, F., Pineda-Sanabria, S. E., Corson, D. C., and Sykes, B. D. (2014) The cardiac-specific N-terminal region of troponin I positions the regulatory domain of troponin C Proc. Natl. Acad. Sci. U.S.A. 111, 14412-14417
28. Palpant, N. J., Houang, E. M., Delport, W., Hastings, K. E. M., Onufriev, A. V., Sham, Y. Y., and Metzger, J. M. (2010) Pathogenic peptide deviations support a model of adaptive evolution of chordate cardiac performance by troponin mutations Physiol. Genomics 42, 287-299
29. Smith, N., Witham, S., Sarkar, S., Zhang, J., Li, L., Li, C., and Alexov, E. (2012) DelPhi web server v2: Incorporating atomic-style geometrical figures into the computational protocol Bioinformatics 28, 1655-1657
30. Sarkar, S., Witham, S., Zhang, J., Zhenirovskyy, M., Rocchia, W., and Alexov, E. (2012) DelPhi web server: a comprehensive online suite for electrostatic calculations of biological macromolecules and their complexes Commun. Comput. Phys. 13, 269-284
31. 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
32. Palpant, N. J., Houang, E. M., Sham, Y. Y., and Metzger, J. M. (2012) pH-responsive titratable inotropic performance of histidine-modified cardiac troponin I Biophys. J. 102, 1570-1579
33. Palpant, N. J., DAlecy, L. G., and Metzger, J. M. (2009) Single histidine button in cardiac troponin I sustains heart performance in response to severe hypercapnic respiratory acidosis in vivo FASEB J. 23, 1529-1540
34. Thompson, B., Houang, E., Sham, Y., and Metzger, J. (2014) Molecular determinants of cardiac myocyte performance as conferred by isoform-specific TnI residues Biophys. J. 106, 2105-2114