Role of the fetal and α/β exons in the function of fast skeletal troponin T isoforms: Correlation with altered Ca2+ regulation associated with development

Journal of Molecular Biology

Volumn 352, Issue 1, 2005, Pages 58-71

  Chaudhuri, Tathagata ^a   Mukherjea, Monalisa ^a   Sachdev, Sanjay ^b,d   Randall, Jeffrey D ^a,e   Sarkar, Satyapriya ^a,b,c  

^a TUFTS UNIVERSITY   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c TUFTS UNIVERSITY   (United States)

^d ROSWELL PARK CANCER INSTITUTE   (United States)

^e US Genomics   (United States)

Author keywords

Ca2+ regulation; Fast skeletal muscle troponin T isoforms; Fetal and peptides; Recombinant troponin T variants

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CALCIUM ION; COMPLEMENTARY DNA; ISOPROTEIN; NUCLEOTIDE; PEPTIDE DERIVATIVE; PROTEIN SUBUNIT; RECOMBINANT PROTEIN; TROPONIN T;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DEVELOPMENTAL STAGE; ENZYME ACTIVITY; EXON; FETUS; FETUS DEVELOPMENT; GENE CONSTRUCT; GENETIC HETEROGENEITY; HUMAN; IN VITRO STUDY; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SKELETON; THIN FILAMENT; WILD TYPE;

MAMMALIA;

EID: 23944436842     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.06.066     Document Type: Article

References (74)

1. A.M. Gordon, E. Homsher, and M. Regnier Regulation of contraction in striated muscle Physiol. Rev. 80 2000 853 924
2. L.D. Yates, and M.L. Greaser Troponin subunit stoichiometry and content in rabbit skeletal muscle and myofibrils J. Biol. Chem. 258 1983 5770 5774
3. L.D. Yates, and M.L. Greaser Quantitative determination of myosin and actin in rabbit skeletal muscle J. Mol. Biol. 168 1983 123 141
4. C.S. Farah, and F.C. Reinach The troponin complex and regulation of muscle contraction FASEB J. 9 1995 755 767
5. P.C. Leavis, and J. Gergely Thin filament proteins and thin filament-linked regulation of vertebrate muscle contraction CRC Crit. Rev. Biochem. 16 1984 235 305
6. A.S. Zot, and J.D. Potter Structural aspects of troponin-tropomyosin regulation of skeletal muscle contraction Annu. Rev. Biophys. Biophys. Chem. 16 1987 535 539
7. G.N. Phillips Jr, J.P. Fillers, and C. Cohen Tropomyosin crystal structure and muscle regulation J. Mol. Biol. 192 1986 111 131
8. S.V. Perry Troponin I: Inhibitor or facilitator Mol. Cell. Biochem. 190 1999 9 32
9. O. Herzberg, and M.N.G. James Structure of the calcium regulatory muscle protein troponin-C at 2.8 Å resolution Nature 313 1985 653 659
10. M. Sundaralingam, R. Bergstrom, G. Strasburg, S.T. Rao, M. Greaser, and B.C. Wang Molecular struture of troponin C from chicken skeletal muscle at 3 Å resolution Science 227 1985 945 948
11. 2+- induced conformational transition of troponin C J. Biol. Chem. 261 1986 2638 2644
12. C.M. Shipsky, and B.D. Sykes NMR solution structure of calcium-saturated skeletal muscle troponin C Biochemistry 34 1995 15953 15964
13. S.M. Gagne, S. Tsuda, M.X. Li, L.B. Smillie, and B.D. Sykes Structures of the troponin C regulatory domains in the apo and calcium-saturated states Nature Struct. Biol. 2 1995 784 789
14. 2+ switch in the calmodulin superfamily Structure 5 1997 1695 1711
15. N.C.J. Stryuadka, M. Cherney, A.R. Sielecki, M.X. Li, L.B. Smillie, and M.N.G. James 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
16. M.X. Li, I. Spyracopoulos, and B.D. Sykes Binding of cardiac troponin -1147-163 induces a structural opening in human cardiac troponin-C Biochemistry 38 1999 8289 8298
17. 2+-dependent interactions between the c-helix of troponin-C and troponin I: photocrosslinking and fluorescence studies using a recombinant troponin-C J. Biol. Chem. 265 1990 4953 4957
18. D.G. Vassylyeu, S. Takada, S. Wakatsuki, K. Maeda, and Y. Maeda Crystal structure of troponin C in complex with troponin I fragment at 2-3 Å resolution Proc. Natl Acad. Sci. USA 95 1998 4847 4852
19. 2+- triggered conformational transition in troponin C Proc. Natl Acad. Sci. USA 89 1992 11814 11817
20. Z. Grabarek, R.Y. Tan, J. Wang, T. Tao, and J. Gergely Inhibition of mutant troponin C activity by an intra-domain disulphide bond Nature 345 1990 132 135
21. K. Fujimori, M. Sorenson, O. Herzberg, J. Moult, and F.C. Reinach Probing the calcium-induced conformational transition of troponin-C with site-directed mutants Nature 345 1990 182 184
22. 2- and COOH-terminal regions of skeletal muscle troponin I J. Biol. Chem. 269 1994 5230 5240
23. P.K. Jha, C.J. Mao, and S. Sarkar Photocrosslinking of rabbit skeletal troponin I deletion mutants with troponin C and its thiol mutants: the inhibitory region enhances binding of troponin I fragments to troponin C Biochemistry 35 1996 11026 11035
24. Y. Luo, J.L. Wu, B. Li, K. Langsetmo, J. Gergely, and T. Tao Photo cross linking of benzophenone-labeled single cysteine troponin I mutants to other thin filament proteins J. Mol. Biol. 296 2000 899 910
25. R.T. McKay, J.R. Pearlstone, D.C. Corson, S.M. Gagne, L.B. Smillie, and B.D. Sykes Structure and interaction site of the regulatory domain of troponin-C when complexed with the 96-148 region of troponin-I Biochemistry 37 1998 12419 12430
26. R.T. McKay, B.P. Tripet, J.R. Pearlstone, L.B. Smillie, and B.D. Sykes Defining the region of troponin-I that binds to troponin-C Biochemistry 38 1999 5478 5489
27. 2+. troponin C, troponin I derived from small-angle scattering date: implications for regulation Biochemistry 33 1994 12800 12806
28. 2+- bound complex: a small-angle X-ray and neutron scattering study Biochemistry 33 1994 8233 8239
29. 2+ on the in situ structures of troponin C and troponin I: a neutron scattering study J. Mol. Biol. 281 1998 689 704
30. S.V. Perry Troponin T: genetics, properties and function J. Muscle Res. Cell Motil. 19 1998 575 602
31. 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
32. 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
33. 2+ sensitivity and cooperativity J. Biol. Chem. 258 1983 2534 2542
34. J.R. Pearlstone, and L.B. Smillie The binding site of skeletal α tropomyosin on troponin-T Can. J. Biochem. 55 1977 1032 1038
35. J.R. Brisson, K. Golosinska, L.B. Smillie, and B.D. Sykes Interaction of tropomyosin and troponin T: a proton nuclear magnetic resonance study Biochemistry 25 1986 4548 4555
36. T.M. Blumenschein, B.P. Tripet, R.S. Hodges, and B.D. Sykes Mapping the interacting regions between troponins T and C. Binding of TnT and TnI peptides to TnC and NMR mapping of the TnT-binding site on TnC J. Biol. Chem. 276 2001 36606 36612
37. C.S. Chong, and R.S. Hodges Photochemical crosslinking between rabbit skeletal troponin subunits J. Biol. Chem. 257 1982 11667 11672
38. 2+ sensitivity of the reconstituted regulatory system Biochemistry 35 1996 16573 16580
39. 2- and COOH-terminal domains of troponin T: ATPase activation and binding to troponin I and C J. Biol. Chem. 273 1998 10594 10601
40. R. Stefancsik, P.K. Jha, and S. Sarkar Identification and mutagenesis of a highly conserved domain in troponin T responsible for troponin I binding: potential role for coiled coil interaction Proc. Natl Acad. Sci. USA 95 1998 957 962
41. S. Mukhopadhyay, K. Langsetmo, W.F. Stafford, G.D. Henry, J.D. Baleja, and S. Sarkar Identification of a region of fast skeletal troponin T required for stabilization of the coiled-coil formation with troponin I J. Biol. Chem. 280 2005 538 547
42. S. Takeda, A. Yamashita, K. Maeda, and Y. Maeda Structure of the core domain of human cardiac troponin in the Ca(2+)-saturated form Nature 424 2003 35 41
43. 2+ regulated structural changes in troponin Proc. Natl Acad. Sci. USA 102 2005 5038 5043
44. J.R. Pearlstone, and L.B. Smillie The interaction of rabbit skeletal muscle troponin T fragments with troponin I Can. J. Biochem. Cell Biol. 63 1985 212 218
45. Z. Grabarek, W. Drabikowski, P.C. Leavis, S.S. Rosenfeld, and J. Gergely Proteolytic fragments of troponin C: interactions with the other troponin subunits and biological activity J. Biol. Chem. 256 1981 13121 13127
46. J. Leszyk, J.H. Collins, P.C. Leavis, and T. Tao Crosslinking of rabbit skeletal muscle troponin subunits: labeling of cysteine-98 of troponin C with 4-maleimidobenzophenone and analysis of products formed in the binary complex with troponin T and the ternary complex with troponins I and T Biochemistry 27 1988 6983 6987
47. L. Mesnard, D. Logeart, S. Taviaux, S. Diriong, J.J. Mercadier, and F. Samson Human cardiac Troponin T: cloning and expression of new isoforms in the normal and failing heart Circ. Res. 76 1995 687 692
48. F. Samson, P.J. de Jong, B.J. Trask, P. Koza-Taylor, M.C. Speer, and T. Potter Assignment of the human slow skeletal troponin T gene to 19q13.4 using somatic cell hybrids and fluorescence in situ hybridization analysis Genomics 4 1992 1374 1375
49. C. Mao, A.P. Baumgartner, P.K. Jha, T.H. Huang, and S. Sarkar Assignment of the human fast skeletal troponin T gene (TNNT3) to chromosome 11p15.5: evidence for the presence of 11pter in a monochromosome 9 somatic cell hybrid in NIGMS mapping panel 2 Genomics 31 1996 385 388
50. R.E. Breitbart, and B. Nadal-Ginard Complete nucleotide sequence of the fast skeletal troponin T gene. Alternatively spliced exons exhibit unusual interspecies divergence J. Mol. Biol. 188 1986 313 324
51. M.M. Briggs, and F. Schachat Physiologically regulated alternative splicing patterns of fast troponin T RNA are conserved in mammals Am. J. Physiol. 270 1996 C298 C305
52. R. Stefancsik, J.D. Randall, C. Mao, and S. Sarkar Structure and sequence of the human fast skeletal troponin T (TNNT3) gene: insight into the evolution of the gene and the origin of the developmentally regulated isoforms Comp. Funct. Genom. 4 2003 609 625
53. M.M. Briggs, and F. Schachat Origin of fetal troponin T: developmentally regulated splicing of a new exon in the fast troponin T gene Dev. Biol. 158 1993 503 509
54. 2+ sensitivity and inhibition of force development. Insights into the role of troponin T isoforms in the heart J. Biol. Chem. 277 2002 35341 35349
55. S.M. MacFarland, J.P. Jin, and F.V. Brozovich Troponin T isoforms modulate calcium dependence of the kinetics of the cross-bridge cycle: studies using a transgenic mouse line Arch. Biochem. Biophys. 405 2002 241 246
56. L.S. Tobacman Thin filament-mediated regulation of cardiac contraction Annu. Rev. Physiol. 58 1996 447 481
57. J.P. Jin, A. Chen, O. Ogut, and Q.Q. Huang Conformational modulation of slow skeletal muscle troponin T by an NH(2)-terminal metal-binding extension Am. J. Physiol. Cell Physiol. 279 2000 C1067 C1077
58. 2-terminal variable region Biochemistry 39 2000 11702 11713
59. 2-terminal variable region and functional effects Biochemistry 37 1998 14519 14528
60. P.A. Anderson, N.N. Malouf, A.E. Oakeley, E.D. Pagani, and P.D. Allen Troponin T isoform expression in humans. A comparison among normal and failing adult heart, fetal heart, and adult and fetal skeletal muscle Circ. Res. 69 1991 1226 1233
61. J. Gulati, A.B. Akella, S.D. Nikolic, V. Starc, and F. Siri Shifts in contractile regulatory protein subunits troponin T and troponin I in cardiac hypertrophy Biochem. Biophys. Res. Commun. 202 1994 384 390
62. Q.-L. Wu, P.K. Jha, M.K. Raychowdhury, Y. Du, P.C. Leavis, and S. Sarkar Isolation and characterization of human fast skeletal β troponin T cDNA: comparative sequence analysis of isoforms and insight into the evolution of members of a multigene family DNA Cell Biol. 13 1994 217 233
63. 2-terminal residues of rabbit skeletal troponin T strengthens binding of troponin to immobilized tropomyosin J. Biol. Chem. 266 1991 12432 12438
64. 2-terminal truncation of skeletal muscle troponin T does not alter the Ca2+ sensitivity of thin filament assembly J. Biol. Chem. 270 1995 25455 25460
65. O. Ogut, and J.P. Jin Cooperative interaction between developmentally regulated troponin T and tropomyosin isoforms in the absence of F-actin J. Biol. Chem. 275 2000 26089 26095
66. B.S. Pan, and J.D. Potter Two genetically expressed troponin T fragments representing alpha and beta isoforms exhibit functional differences J. Biol. Chem. 267 1992 23052 23056
67. P.J. Reiser, M.L. Greaser, and R.L. Moss Developmental changes in troponin T isoform expression and tension production in chicken single skeletal muscle fibres J. Physiol. 449 1992 573 588
68. O. Ogut, H. Granzier, and J.P. Jin Acidic and basic troponin T isoforms in mature fast-twitch skeletal muscle and effect on contractility Am. J. Physiol. 1999 C1162 C1170
69. F.H. Schachat, M.S. Diamond, and P.W. Brandt Effect of different troponin T-tropomyosin combinations on thin filament activation J. Mol. Biol. 198 1987 551 554
70. S.N. Ho, H.D. Hunt, R.M. Horton, J.K. Pullen, and L.R. Pease Site-directed mutagenesis by overlap extension using the polymerase chain reaction Gene 77 1989 51 59
71. L.B. Smillie Preparation and identification of α- and β-tropomyosins Methods Enzymol. 85 1982 234 241
72. J.D. Pardee, and J.A. Spudich Purification of muscle actin Methods Cell Biol. 24 1982 271 289
73. S. Margossian, and S. Lowey Preparation of myosin and its subfragments from rabbit skeletal muscle Methods Enzymol. 85 1982 55 71
74. D. Bers, C. Patton, and R. Nuccitelli A practical guide to the preparation of calcium buffers Methods Cell Biol. 40 1999 4 28