The tropomyosin binding region of cardiac troponin T modulates crossbridge recruitment dynamics in rat cardiac muscle fibers

Journal of Molecular Biology

Volumn 425, Issue 9, 2013, Pages 1565-1581

  Gollapudi, Sampath K ^a   Gallon, Clare E ^b   Chandra, Murali ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF EXETER MEDICAL SCHOOL   (United Kingdom)

Author keywords

allosteric interaction; cardiac troponin T; contractile dynamics; regulatory proteins; thin filament activation

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CALCIUM ION; TROPOMYOSIN; TROPONIN; TROPONIN T; TROPONIN T1; TROPONIN T2; UNCLASSIFIED DRUG;

ALLOSTERISM; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HEART; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART RATE; MOLECULAR DYNAMICS; MUSCLE LENGTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; THIN FILAMENT; TISSUE SPECIFICITY;

RATTUS;

EID: 84876415331     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.01.028     Document Type: Article

References (54)

1. 2- and COOH-terminal domains of Troponin T. ATPase activation and binding to troponin I and troponin C J. Biol. Chem. 273 1998 10594 10601
2. D.M. Oliveira, C.R. Nakaie, A.D. Sousa, C.S. Farah, and F.C. Reinach Mapping the domain of troponin T responsible for the activation of actomyosin ATPase activity. Identification of residues involved in binding to actin J. Biol. Chem. 275 2000 27513 27519
3. 2 + regulation of muscle contraction J. Biol. Chem. 270 1995 2557 2562
4. B.S. Pan, A.M. Gordon, and J.D. Potter Deletion of the first 45 NH2-terminal residues of rabbit skeletal troponin T strengthens binding of troponin to immobilized tropomyosin J. Biol. Chem. 266 1991 12432 12438
5. D.H. Heeley, K. Golosinska, and L.B. Smillie The effects of troponin T fragments T1 and T2 on the binding of nonpolymerizable tropomyosin to F-actin in the presence and absence of troponin I and troponin C J. Biol. Chem. 262 1987 9971 9978
6. J.R. Pearlstone, and L.B. Smillie The binding site of skeletal alpha-tropomyosin on troponin-T Can. J. Biochem. 55 1977 1032 1038
7. E.P. Manning, P.J. Guinto, and J.C. Tardiff Correlation of molecular and functional effects of mutations in cardiac troponin T linked to familial hypertrophic cardiomyopathy: an integrative in silico/in vitro approach J. Biol. Chem. 287 2012 14515 14523
8. M. Chandra, M.L. Tschirgi, I. Rajapakse, and K.B. Campbell Troponin T modulates sarcomere length-dependent recruitment of cross-bridges in cardiac muscle Biophys. J. 90 2006 2867 2876
9. S.S. Lehrer, and M.A. Geeves The muscle thin filament as a classical cooperative/allosteric regulatory system J. Mol. Biol. 277 1998 1081 1089
10. A. Hinkle, and L.S. Tobacman Folding and function of the troponin tail domain. Effects of cardiomyopathic troponin T mutations J. Biol. Chem. 278 2003 506 513
11. T. Palm, S. Graboski, S.E. Hitchcock-DeGregori, and N.J. Greenfield Disease-causing mutations in cardiac troponin T: identification of a critical tropomyosin-binding region Biophys. J. 81 2001 2827 2837
12. M. Regnier, A.J. Rivera, C.K. Wang, M.A. Bates, P.B. Chase, and A.M. Gordon Thin filament near-neighbour regulatory unit interactions affect rabbit skeletal muscle steady-state force-Ca(2 +) relations J. Physiol. 540 2002 485 497
13. R. Maytum, M.A. Geeves, and S.S. Lehrer A modulatory role for the troponin T tail domain in thin filament regulation J. Biol. Chem. 277 2002 29774 29780
14. L.S. Tobacman, M. Nihli, C. Butters, M. Heller, V. Hatch, and R. Craig The troponin tail domain promotes a conformational state of the thin filament that suppresses myosin activity J. Biol. Chem. 277 2002 27636 27642
15. 2 + sensitivity and cooperativity J. Biol. Chem. 258 1983 2534 2542
16. D.E. Montgomery, J.C. Tardiff, and M. Chandra Cardiac troponin T mutations: correlation between the type of mutation and the nature of myofilament dysfunction in transgenic mice J. Physiol. 536 2001 583 592
17. J.E. Stelzer, J.R. Patel, M.C. Olsson, D.P. Fitzsimons, L.A. Leinwand, and R.L. Moss Expression of cardiac troponin T with COOH-terminal truncation accelerates cross-bridge interaction kinetics in mouse myocardium Am. J. Physiol. Heart Circ. Physiol. 287 2004 H1756 H1761
18. D. Szczesna, R. Zhang, J. Zhao, M. Jones, G. Guzman, and J.D. Potter Altered regulation of cardiac muscle contraction by troponin T mutations that cause familial hypertrophic cardiomyopathy J. Biol. Chem. 275 2000 624 630
19. F. Takahashi-Yanaga, I. Ohtsuki, and S. Morimoto Effects of troponin T mutations in familial hypertrophic cardiomyopathy on regulatory functions of other troponin subunits J. Biochem. 130 2001 127 131
20. T.E. Gillis, D.A. Martyn, A.J. Rivera, and M. Regnier Investigation of thin filament near-neighbour regulatory unit interactions during force development in skinned cardiac and skeletal muscle J. Physiol. 580 2007 561 576
21. A.M. Gordon, E. Homsher, and M. Regnier Regulation of contraction in striated muscle Physiol. Rev. 80 2000 853 924
22. J.P. Konhilas, T.C. Irving, and P.P. de Tombe Length-dependent activation in three striated muscle types of the rat J. Physiol. 544 2002 225 236
23. K.B. Campbell, M.V. Razumova, R.D. Kirkpatrick, and B.K. Slinker Nonlinear myofilament regulatory processes affect frequency-dependent muscle fiber stiffness Biophys. J. 81 2001 2278 2296
24. K.B. Campbell, M.V. Razumova, R.D. Kirkpatrick, and B.K. Slinker Myofilament kinetics in isometric twitch dynamics Ann. Biomed. Eng. 29 2001 384 405
25. K.B. Campbell, M. Chandra, R.D. Kirkpatrick, B.K. Slinker, and W.C. Hunter Interpreting cardiac muscle force-length dynamics using a novel functional model Am. J. Physiol. Heart Circ. Physiol. 286 2004 H1535 H1545
26. X.Q. Huang, and W. Miller A time-efficient, linear-space local similarity algorithm Adv. Appl. Math. 12 1991 337 357
27. M. Chandra, D.E. Montgomery, J.J. Kim, and R.J. Solaro The N-terminal region of troponin T is essential for the maximal activation of rat cardiac myofilaments J. Mol. Cell. Cardiol. 31 1999 867 880
28. M.A. Andrade, P. Chacon, J.J. Merelo, and F. Moran Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network Protein Eng. 6 1993 383 390
29. J.J. Merelo, M.A. Andrade, A. Prieto, and F. Morán Proteinotopic feature maps Neurocomputing 6 1994 443 454
30. L. Whitmore, and B.A. Wallace Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases Biopolymers 89 2008 392 400
31. P.P. de Tombe, and G.J. Stienen Protein kinase A does not alter economy of force maintenance in skinned rat cardiac trabeculae Circ. Res. 76 1995 734 741
32. G.J. Stienen, R. Zaremba, and G. Elzinga ATP utilization for calcium uptake and force production in skinned muscle fibres of Xenopus laevis J. Physiol. 482 1995 109 122
33. M. Chandra, M.L. Tschirgi, and J.C. Tardiff Increase in tension-dependent ATP consumption induced by cardiac troponin T mutation Am. J. Physiol. Heart Circ. Physiol. 289 2005 H2112 H2119
34. B. Brenner, and E. Eisenberg Rate of force generation in muscle: correlation with actomyosin ATPase activity in solution Proc. Natl Acad. Sci. USA 83 1986 3542 3546
35. 2 + on cross-bridge turnover kinetics in skinned single rabbit psoas fibers: implications for regulation of muscle contraction Proc. Natl Acad. Sci. USA 85 1988 3265 3269
36. Y. Ishii, and S. Lehrer Two-site attachment of troponin to pyrene-labeled tropomyosin J. Biol. Chem. 266 1991 6894 6903
37. 2 + in the presence of troponin-C J. Biol. Chem. 257 1982 10587 10592
38. J.R. Pearlstone, and L.B. Smillie Identification of a second binding region on rabbit skeletal troponin-T for α-tropomyosin FEBS Lett. 128 1981 119 122
39. R. Mamidi, S.L. Mallampalli, D.F. Wieczorek, and M. Chandra Identification of two new regions in the N-Terminal region of cardiac troponin T that have divergent effects on cardiac contractile function J. Physiol. 591 2012 1217 1234
40. C. Communal, M. Sumandea, P. de Tombe, J. Narula, R.J. Solaro, and R.J. Hajjar Functional consequences of caspase activation in cardiac myocytes Proc. Natl Sci. Acad. USA 99 2002 6252 6256
41. S.K. Gollapudi, R. Mamidi, S.L. Mallampalli, and M. Chandra The N-terminal extension of cardiac troponin T stabilizes the blocked state of cardiac thin filament Biophys. J. 103 2012 940 948
42. M.P. Sumandea, S. Vahebi, C.A. Sumandea, M.L. Garcia-Cazarin, J. Staidle, and E. Homsher Impact of cardiac troponin T N-terminal deletion and phosphorylation on myofilament function Biochemistry 48 2009 7722 7731
43. A.S. Mak, and L.B. Smillie Structural interpretation of the two-site binding of troponin on the muscle thin filament J. Mol. Biol. 149 1981 541 550
44. S.P. White, C. Cohen, and G.N. Phillips Jr. Structure of co-crystals of tropomyosin and troponin Nature 325 1987 826 828
45. S. Schaertl, S.S. Lehrer, and M.A. Geeves Separation and characterization of the two functional regions of troponin involved in muscle thin filament regulation Biochemistry 34 1995 15890 15894
46. K. Campbell Rate constant of muscle force redevelopment reflects cooperative activation as well as cross-bridge kinetics Biophys. J. 72 1997 254 262
47. 2 +-saturated form Nature 424 2003 35 41
48. 2 +-regulated structural changes in troponin Proc. Natl Acad. Sci. USA 102 2005 5038 5043
49. D.E. Montgomery, J.C. Tardiff, and M. Chandra Cardiac troponin T mutations: correlation between the type of mutation and the nature of myofilament dysfunction in transgenic mice J. Physiol. (Lond.) 536 2001 583 592
50. 2-terminal peptide in myofilament activation J. Biol. Chem. 269 1994 15210 15216
51. B.S. Pan, and R.G. Johnson Jr Interaction of cardiotonic thiadiazinone derivatives with cardiac troponin C J. Biol. Chem. 271 1996 817 823
52. B.J. Placek, and L.M. Gloss The N-terminal tails of the H2A-H2B histones affect dimer structure and stability Biochemistry 41 2002 14960 14968
53. A. Fabiato, and F. Fabiato Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells J. Physiol. (Paris) 75 1979 463 505
54. M. Chandra, M.L. Tschirgi, S.J. Ford, B.K. Slinker, and K.B. Campbell Interaction between myosin heavy chain and troponin isoforms modulate cardiac myofiber contractile dynamics Am. J. Physiol. Regul. Integr. Comp. Physiol. 293 2007 R1595 R1607