Molecular effects of familial hypertrophic cardiomyopathy-related mutations in the TNT1 domain of cTnT

Journal of Molecular Biology

Volumn 421, Issue 1, 2012, Pages 54-66

  Manning, Edward P ^a   Tardiff, Jil C ^b   Schwartz, Steven D ^a,c  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^c University of Arizona   (United States)

Author keywords

calcium signaling; cardiac; molecular dynamics; thin filament; troponin

Indexed keywords

CALCIUM; TROPONIN T;

ARTICLE; CALCIUM BINDING; FAMILIAL HYPERTROPHIC CARDIOMYOPATHY; GENE MUTATION; GENE STRUCTURE; PHENOTYPE; PRIORITY JOURNAL;

EID: 84863513224     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.05.008     Document Type: Article

References (68)

1. Thierfelder L., Watkins H., MacRae C., Lamas R., McKenna W., and Vosberg H.P. Alpha-tropomyosin and cardiac troponin T mutations cause familial hypertrophic cardiomyopathy: a disease of the sarcomere Cell 77 1994 701 712
2. Kimura A., Harada H., Park J.E., Nishi H., Satoh M., and Takahashi M. Mutations in the cardiac troponin I gene associated with hypertrophic cardiomyopathy Nat. Genet. 16 1997 379 382 (Pubitemid 27323305)
3. Maron B.J. Hypertrophic cardiomyopathy: a systematic review JAMA 287 2002 1308 1320 (Pubitemid 34250486)
4. Watkins H., Conner D., Thierfelder L., Jarcho J.A., MacRae C., and McKenna W.J. Mutations in the cardiac myosin binding protein-C gene on chromosome 11 cause familial hypertrophic cardiomyopathy Nat. Genet. 11 1995 434 437
5. Tanigawa G., Jarcho J.A., Kass S., Solomon S.D., Vosberg H.P., Seidman J.G., and Seidman C.E. A molecular basis for familiar hypertrophic cardiomyopathy: an alpha/beta cardiac myosin heavy chain hybrid gene Cell 62 1990 991 998
6. Geisterfer-Lowrance A.A.T., Kass S., Tanigawa G., Vosberg H.P., McKenna W., Seidman C.E., and Seidman J.G. A molecular basis for familial hypertrophic cardiomyopathy: a beta cardiac myosin heavy chain gene missense mutation Cell 62 1990 999 1006
7. Alcalai R., Seidman J.G., and Seidman C.E. Genetic basis of hypertrophic cardiomyopathy: from bench to clinics J. Cardiovasc. Electrophysiol. 19 2008 104 110
8. Bonne G., Carrier L., Bercovici J., Cruaud C., Richard P., and Hainque B. Cardiac myosin binding protein-C gene splice acceptor site mutation is associated with familial hypertrophic cardiomyopathy Nat. Genet. 11 1995 438 440
9. Nakajima-Taniguchi C., Matsui H., Nagata S., Kishimito T., and Yamauchi-Takihara K. Novel missense mutation in alpha-tropomyosin gene found in Japanese patients with hypertrophic cardiomyopathy J. Mol. Cell. Cardiol. 27 1995 2053 2058
10. Poetter K., Jiang H., Hassanzadeh S., Master S.R., Chang A., and Dalakas M.C. Mutations in either the essential or regulatory light chains of myosin are associated with a rare myopathy in human heart and skeletal muscle Nat. Genet. 13 1996 63 69 (Pubitemid 26139295)
11. Watkins H., Seidman J.G., and Seidman C.E. Familial hypertrophic cardiomyopathy: a genetic model of cardiac hypertrophy Hum. Mol. Genet. 4 1995 1721 1727
12. Fatkin D., and Graham R.M. Molecular mechanisms of inherited cardiomyopathies Phys. Rev. 82 2002 945 980
13. Force T., Bonow R.O., Houser S.R., Solaro R.J., Hershberger R.E., and Adhikari B. Research priorities in hypertrophic cardiomyopathy: report of a working group of the National Heart, Lung, and Blood Institute Circulation 122 2010 1130 1133
14. Tardiff J.C. Thin filament mutations: developing an integrative approach Circ. Res. 108 2011 765 782
15. Tobacman L.S. Thin filament-mediated regulation of cardiac contraction Annu. Rev. Physiol. 58 1996 447 481 (Pubitemid 26106729)
16. Kobayashi T., and Solaro R.J. Calcium, thin filaments, and the integrative biology of cardiac contractility Annu. Rev. Physiol. 67 2005 39 67 (Pubitemid 40404485)
17. Gomes A.V., Barnes J.A., Harada K., and Potter J.D. Role of troponin T in disease Mol. Cell. Biochem. 263 2004 115 129 (Pubitemid 39256150)
18. Palm T., Graboski S., Hitchcock-DeGregori S.E., and Greenfield N.J. Disease-causing mutations in cardiac troponin T: identification of a critical tropomyosin-binding region Biophys. J. 81 2001 2827 2837 (Pubitemid 33020068)
19. Biesiadecki B.J., Chong S.M., Nosek T.M., and Jin J.P. Troponin T core structure and the regulatory NH2-terminal variable region Biochemistry 46 2007 1368 1379 (Pubitemid 46208484)
20. Schaertl S., Lehrer S.S., and Geeves M.A. Separation and characterization of the two functional regions of troponin involved in muscle thin filament regulation Biochemistry 34 1995 15890 15894
21. Pearlstone J.R., and Smillie L.B. Effects of troponin-I plus C on the binding of troponin-T and its fragments to alpha-tropomyosin J. Biol. Chem. 258 1983 2534 2542
22. Murakami K., Stewart M., Nozawa K., Tomii K., Kudou N., and Igarashi N. Structural basis for tropomyosin overlap in thin (actin) filaments and the generation of a molecular swivel by troponin-T Proc. Natl Acad. Sci. USA 105 2008 7200 7205 (Pubitemid 351754455)
23. Hinkle A., and Tobacman L.S. Folding and function of the troponin tail domain. Effects of cardiomyopathic troponin T mutations J. Biol. Chem. 278 2003 506 513 (Pubitemid 36043603)
24. Palm T., Greenfield N.J., and Hitchcock-DeGregori S.E. Tropomyosin ends determine the stability and functionality of overlap and troponin T complexes Biophys. J. 84 2003 3181 3189 (Pubitemid 36531765)
25. 2+-saturated form Nature 424 2003 35 41 (Pubitemid 36834832)
26. Manning E.P., Guinto P.J., and Tardiff J.C. 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
27. 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 (Pubitemid 47488403)
28. Solaro R.J., Moir A.J.G., and Perry S.V. Phosphorylation of troponin I and the inotropic effect of adrenaline in the perfused rabbit heart Nature 262 1976 615 617
29. 2+-activated state of tropomyosin on actin filaments Circ. Res. 106 2010 705 711
30. 2+-dependent photocrosslinking of tropomyosin residue 146 to residues 157-163 in the C-terminal domain of troponin I in reconstituted skeletal muscle thin filaments J. Mol. Biol. 389 2009 575 583
31. Hoffman R.M.B., and Sykes B.D. Isoform-specific variation in the intrinsic disorder of troponin I Proteins 73 2008 338 350
32. 2+ regulation of striated muscle J. Mol. Biol. 361 2006 625 633 (Pubitemid 44175378)
33. Manning E.P., Tardiff J.C., and Schwartz S.D. A model of calcium activation of the thin filament Biochemistry 50 2011 7405 7413
34. Kowlessur D., and Tobacman L.S. Low temperature dynamic mapping reveals unexpected order and disorder in troponin J. Biol. Chem. 285 2010 38978 38986
35. Kowlessur D., and Tobacman L.S. Troponin regulatory function and dynamics revealed by H/D exchange-mass spectrometry J. Biol. Chem. 285 2010 2686 2694
36. Nelson M.R., and Chazin W.J. Structures of EF-hand calcium binding proteins: diversity in the organization, packing and response to calcium binding BioMetals 11 1998 297 318 (Pubitemid 29121538)
37. Varughese J.F., Baxley T., Chalovich J.M., and Li Y. A computational and experimental approach to investigate bepridil binding with cardiac troponin J. Phys. Chem. B 115 2011 2392 2400
38. Poole K.J.V., Lorenz M., Evans G., Rosenbaum G., Pirani A., and Craig R. A comparison of muscle thin filament models obtained from electron microscopy reconstructions and low-angle X-ray fiber diagrams from non-overlap muscle J. Struct. Biol. 155 2006 273 284 (Pubitemid 44278649)
39. McKillop D.F.A., and Geeves M.A. Regulation of the interaction between actin and myosin subfragment 1: evidence for three states of the thin filament Biophys. J. 65 1993 693 701 (Pubitemid 23263882)
40. Watkins H., McKenna W.J., Thierfelder L., Suk H.J., Anan R., and O'Donoghue A. Mutations in the genes for cardiac troponin T and alpha-tropomyosin in hypertrophic cardiomyopathy N. Engl. J. Med. 332 1995 1058 1064
41. Forissier J.F., Carrier L., Farza H., Bonne G., Bercovici J., and Richard P. Codon 102 of the cardiac troponin T gene is a putative hot spot for mutations in familial hypertrophic cardiomyopathy Circulation 94 1996 3069 3073 (Pubitemid 26427467)
42. Moolman J.C., Corfield V.A., Posen B., Ngumbela K., Seidman C., Brink P.A., and Watkins H. Sudden death due to troponin T mutations J. Am. Coll. Cardiol. 29 1997 549 555 (Pubitemid 27116096)
43. Lombardi R., Bell A., Senthil V., Sidhu J., Noseda M., Roberts R., and Marian A.J. Differential interactions of thin filament proteins in two cardiac troponin T mouse models of hypertrophic and dilated cardiomyopathies Cardiovas. Res. 79 2008 109 117 (Pubitemid 351881942)
44. Haim T.E., Dowell C., Diamanti T., Scheuer J., and Tardiff J.C. Independent FHC-related cardiac troponin T mutations exhibit specific alterations in myocellular contractility and calcium kinetics J. Mol. Cell. Cardiol. 42 2007 1098 1110 (Pubitemid 46829199)
45. 2+ sensitivity of cardiac muscle contraction J. Biol. Chem. 279 2004 14488 14495 (Pubitemid 38618835)
46. Guinto P.J., Manning E.P., Schwartz S.D., and Tardiff J.C. Computational characterization of mutations in cardiac troponin T known to cause familial hypertrophic cardiomyopathy J. Theor. Comput. Chem. 6 2007 413 419
47. Ertz-Berger B., He H., Dowell C., Factor S., Haim T., and Nunez S. Changes in the chemical and dynamic properties of cardiac troponin T cause discrete cardiomyopathies in transgenic mice Proc. Natl Acad. Sci. USA 102 2005 18219 18224 (Pubitemid 41798528)
48. 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 (Pubitemid 27440950)
49. Wei B., and Jin J.P. Troponin T isoforms and posttranscriptional modifications: evolution, regulation and function Arch. Biochem. Biophys. 505 2011 144 154
50. Feng H.Z., Biesiadecki B.J., Yu Z.B., Hossain M.M., and Jin J.P. Restricted N-terminal truncation of cardiac troponin T: a novel mechanism for functional adaptation to energetic crisis J. Physiol. 586 2008 3537 3550 (Pubitemid 352003882)
51. Moore R.K., Guinto P.J., Dowell-Martino C., and Tardiff J.C. Functional and structural changes induced by cTnT-related FHC mutations in TNT1 alter actomyosin binding interactions. 2009 Biophysical Society Meeting Abstracts Biophys. J. 2010 Supplement 6a, Abstract, 34-Plat
52. Harada K., Takahashi-Yanaga F., Minakami R., Morimoto S., and Ohtsuki I. Functional consequences of the deletion mutation deletion Glu160 in human cardiac troponin T J. Biochem. 127 2000 263 268 (Pubitemid 30136909)
53. Maron B.J., Spirito P., Green K.J., Wesley Y.E., Bonow R.O., and Arce J. Noninvasive assessment of left ventricular diastolic function by pulsed Doppler echocardiography in patients with hypertrophic cardiomyopathy J. Am. Coll. Cardiol. 10 1987 733 742 (Pubitemid 17163095)
54. 2+ affinity of cardiac thin filaments reconstituted with cardiomyopathy-related mutant cardiac troponin I J. Biol. Chem. 281 2006 13471 13477 (Pubitemid 43855259)
55. Norman C., Tal J.A., Tikunova S.B., and Davis J.P. Modulation of the rate of cardiac muscle contraction by troponin C constructs with various calcium binding affinities Am. J. Physiol.: Heart Circ. Physiol. 293 2007 H2580 H2587
56. Brooks B.R., Brooks C.L. 3rd, Mackerell A.D. Jr, Nilsson L., Petrella R.J., and Roux B. CHARMM: the biomolecular simulation program J. Comput. Chem. 30 2009 1545 1614
57. Brooks B.R., Bruccoleri R.E., Olafson B.D., States D.J., Swaminathan S., and Karplus M. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations J. Comput. Chem. 4 1983 187 217
58. Chen J., Im W., and Brooks C.L. Balancing solvation and intramolecular interactions: toward a consistent generalized Born force field JACS 128 2006 3728 3736
59. Im W., Lee M.S., and Brooks C.L. Generalized Born model with a simple smoothing function J. Comput. Chem. 24 2003 1691 1702
60. 2+-activated states J. Mol. Biol. 357 2006 707 717
61. 2+-regulated structural changes in troponin Proc. Natl Acad. Sci. USA 102 2005 5038 5043
62. Bryson K., McGuffin L.J., Marsden R.L., Ward J.J., Ward J.S., Sodhi J.S., and Jones D.T. Protein structure prediction servers at University College London Nucleic Acids Res. 33 2005 W36 W38
63. Jones D.T. Protein secondary structure prediction based on position-specific scoring matrices J. Mol. Biol. 292 1999 195 202 (Pubitemid 29435759)
64. Frye J., Klenchin V.A., and Rayment I. Structure of the tropomyosin overlap complex from chicken smooth muscle: insight into the diversity of N-terminal recognition Biochemistry 49 2010 4908 4920
65. Greenfield N.J., Huang Y.J., Swapna G.V., Bhattacharya A., Rapp B., and Singh A. Solution NMR structure of the junction between tropomyosin molecules: implications for actin binding and regulation J. Mol. Biol. 364 2006 80 96 (Pubitemid 44634526)
66. Caves L.S., Evanseck J.D., and Karplus M. Locally accessible conformations of proteins: multiple molecular dynamics simulations of crambin Protein Sci. 7 1998 649 666 (Pubitemid 28130887)
67. Humphrey W., Dalke A., and Schulten K. VMD - Visual Molecular Dynamics J. Mol. Graphics 14 1996 33 38
68. Heinig M., and Frishman D. STRIDE: a web server for secondary structure assignment from known atomic coordinates of proteins Nucleic Acids Res. 32 2004 W500 W502