The C terminus of cardiac troponin i stabilizes the Ca2+- activated state of tropomyosin on actin filaments

Circulation Research

Volumn 106, Issue 4, 2010, Pages 705-711

  Galińska, Agnieszka ^a   Hatch, Victoria ^a   Craig, Roger ^b   Murphy, Anne M ^c   Van Eyk, Jennifer E ^d   Wang, C L Albert ^e   Lehman, William ^a   Foster, D Brian ^a,d,e  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c Departments of Pediatrics   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e BOSTON BIOMEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

Cardiomyopathy; Myocardial stunning; Thin filament; Troponin

Indexed keywords

CALCIUM ION; MUTANT PROTEIN; TROPOMYOSIN; TROPONIN C; TROPONIN I; TROPONIN T;

ACTIN FILAMENT; ARTICLE; CARBOXY TERMINAL SEQUENCE; ELECTRON MICROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE; THREE DIMENSIONAL IMAGING;

ANIMALS; BINDING SITES; CALCIUM; CATTLE; HUMANS; IMAGING, THREE-DIMENSIONAL; MICROFILAMENTS; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; MUTATION; MYOCARDIAL CONTRACTION; MYOCARDIUM; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RABBITS; RECOMBINANT PROTEINS; TROPOMYOSIN; TROPONIN C; TROPONIN I; TROPONIN T;

EID: 77949366363     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.109.210047     Document Type: Article

References (46)

1. Morita H, Seidman J, Seidman CE. Genetic causes of human heart failure. J Clin Invest. 2005;115:518-526.
2. Bolli R, Marban E. Molecular and Cellular Mechanisms of Myocardial Stunning. Physiol Rev. 1999;79:609-634.
3. Kimura A, Harada H, Park JE, Nishi H, Satoh M, Takahashi M, Hiroi S, Sasaoka T, Ohbuchi N, Nakamura T, Koyanagi T, Hwang TH, Choo JA, Chung KS, Hasegawa A, Nagai R, Okazaki O, Nakamura H, Matsuzaki M, Sakamoto T, Toshima H, Koga Y, Imaizumi T, Sasazuki T. Mutations in the cardiac troponin I gene associated with hypertrophic cardiomyopathy. Nat Genet. 1997;16:379-382.
4. Mogensen J, Kubo T, Duque M, Uribe W, Shaw A, Murphy R, Gimeno JR, Elliott P, McKenna WJ. Idiopathic restrictive cardiomyopathy is part of the clinical expression of cardiac troponin I mutations. J Clin Invest. 2003;111:209-216.
5. Gao WD, Atar D, Liu Y, Perez NG, Murphy AM, Marban E. Role of troponin I proteolysis in the pathogenesis of stunned myocardium. Circ Res. 1997;80:393-399.
6. 2+-dependent proteolysis? Circ Res. 1996;78:455-465.
7. McDonough JL, Arrell DK, Van Eyk JE. Troponin I degradation and covalent complex formation accompanies myocardial ischemia/ reperfusion injury. Circ Res. 1999;84:9-20.
8. Van Eyk JE, Powers F, Law W, Larue C, Hodges RS, Solaro RJ. Breakdown and release of myofilament proteins during ischemia and ischemia/reperfusion in rat hearts: identification of degradation products and effects on the pCa-force relation. Circ Res. 1998;82:261-271.
9. Westfall MV, Solaro RJ. Alterations in myofibrillar function and protein profiles after complete global ischemia in rat hearts. Circ Res. 1992;70:302-313.
10. Kloner RA, Jennings RB. Consequences of brief ischemia: stunning, preconditioning, and their clinical implications: part 1. Circulation. 2001; 104:2981-2989.
11. Murphy AM, Kogler H, Georgakopoulos D, McDonough JL, Kass DA, Van Eyk JE, Marban E. Transgenic mouse model of stunned myocardium. Science. 2000;287:488-491.
12. McDonough JL, Labugger R, Pickett W, Tse MY, MacKenzie S, Pang SC, Atar D, Ropchan G, Van Eyk JE. Cardiac troponin I is modified in the myocardium of bypass patients. Circulation. 2001;103:58-64.
13. Kobayashi T, Jin L, de Tombe P. Cardiac thin filament regulation. Pflugers Arch. 2008;457:37-46.
14. Kobayashi T, Solaro RJ. Calcium, thin filaments, and the integrative biology of cardiac contractility. Annu Rev Physiol. 2005;67:39-67.
15. Lehman W, Craig R. Tropomyosin and the steric mechanism of muscle regulation. Adv Exp Med Biol. 2008;644:95-109.
16. Solaro RJ, Rosevear P, Kobayashi T. The unique functions of cardiac troponin I in the control of cardiac muscle contraction and relaxation. Biochem Biophys Res Commun. 2008;369:82-87.
17. 2+-regulated structural changes in troponin. Proc Natl Acad Sci USA. 2005;102:5038-5043.
18. 2+-saturated form. Nature. 2003;424:35-41.
19. Blumenschein TMA, Stone DB, Fletterick RJ, Mendelson RA, Sykes BD. Dynamics of the C-terminal region of TnI in the troponin complex in solution. Biophys J. 2006;90:2436-2444.
20. 2+ regulation of striated muscle. J Mol Biol. 2006;361:625-633.
21. 2+-activated states. J Mol Biol. 2006;357: 707-717.
22. Pirani A, Xu C, Hatch V, Craig R, Tobacman LS, Lehman W. Single particle analysis of relaxed and activated muscle thin filaments. J Mol Biol. 2005;346:761-772.
23. Moody C, Lehman W, Craig R. Caldesmon and the structure of smooth muscle thin filaments: electron microscopy of isolated thin filaments. J Mus Res Cell Motil. 1990;11:176-185.
24. Lehman W, Hatch V, Korman V, Rosol M, Thomas L, Maytum R, Geeves MA, Van Eyk JE, Tobacman LS, Craig R. Tropomyosin and actin isoforms modulate the localization of tropomyosin strands on actin filaments. J Mol Biol. 2000;302:593-606.
25. Egelman EH. A robust algorithm for the reconstruction of helical filaments using single-particle methods. Ultramicroscopy. 2000;85:225-234.
26. Owen C, DeRosier D. A 13-A map of the actin-scruin filament from the limulus acrosomal process J Cell Biol. 1993;123:337-344.
27. Milligan RA, Flicker PF. Structural relationships of actin, myosin, and tropomyosin revealed by cryo-electron microscopy. J Cell Biol. 1987;105:29-39.
28. Trachtenberg S, DeRosier DJ. Three-dimensional structure of the frozen-hydrated flagellar filament: the left-handed filament of Salmonella typhi-murium. J Mol Biol. 1987;195:581-601.
29. McKillop DF, Geeves MA. Regulation of the interaction between actin and myosin subfragment 1: evidence for three states of the thin filament. Biophys J. 1993;65:693-701.
30. Lehman W, Galinska-Rakoczy A, Hatch V, Tobacman LS, Craig R. Structural basis for the activation of muscle contraction by troponin and tropomyosin. J Mol Biol. 2009;388:673-681.
31. Galinska-Rakoczy A, Engel P, Xu C, Jung H, Craig R, Tobacman LS, Lehman W. Structural basis for the regulation of muscle contraction by troponin and tropomyosin. J Mol Biol. 2008;379:929-935.
32. Frank J, Radermacher M, Penczek P, Zhu J, Li Y, Ladjadj M, Leith A. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J Struct Biol. 1996;116:190-199.
33. Galkin VE, Orlova A, Lukoyanova N, Wriggers W, Egelman EH. Actin depolymerizing factor stabilizes an existing state of F-actin and can change the tilt of F-actin subunits. J Cell Biol. 2001;153:75-86.
34. Foster DB, Huang R, Hatch V, Craig R, Graceffa P, Lehman W, Wang CLA. Modes of caldesmon binding to actin: sites of caldesmon contact and modulation of interactions by caldesmon phosphorylation. J Biol Chem. 2004;279:53387-53394.
35. Foster DB, Noguchi T, VanBuren P, Murphy AM, Van Eyk JE. C-terminal truncation of cardiac troponin I causes divergent effects on ATPase and force: implications for the pathophysiology of myocardial stunning. Circ Res. 2003;93:917-924.
36. Tachampa K, Kobayashi T, Wang H, Martin AF, Biesiadecki BJ, Solaro RJ, de Tombe PP. Increased cross-bridge cycling kinetics after exchange of C-terminal truncated troponin I in skinned rat cardiac muscle. J Biol Chem. 2008;283:15114-15121.
37. Mathur MC, Kobayashi T, Chalovich JM. Some cardiomyopathy-causing troponin I mutations stabilize a functional intermediate actin state. Biophys J. 2009;96:2237-2244.
38. 2+ affinity of cardiac thin filaments reconstituted with cardiomyopathy-related mutant cardiac troponin I. J Biol Chem. 2006;281:13471-13477.
39. Kohler J, Chen Y, Brenner B, Gordon AM, Kraft T, Martyn DA, Regnier M, Rivera AJ, Wang C-K, Chase PB. Familial hypertrophic cardiomyopathy mutations in troponin I (K183A, G203S, K206Q) enhance filament sliding. Physiol Genomics. 2003;14:117-128.
40. Van Eyk JE, Hodges RS. The biological importance of each amino acid residue of the troponin I inhibitory sequence 104-115 in the interaction with troponin C and tropomyosin-actin. J Biol Chem. 1988;263:1726-1732.
41. 2+-dependent regulation of muscle contraction. J Mol Biol. 1997;271:728-750.
42. Holmes K, Lehman W. Gestalt-binding of tropomyosin to actin filaments. J Mus Res Cell Motil. 2008;29:213-219.
43. Gordon AM, Homsher E, Regnier M. Regulation of contraction in striated muscle. Physiol Rev. 2000;80:853-924.
44. Gao WD, Dai T, Nyhan D. Increased cross-bridge cycling rate in stunned myocardium. Am J Physiol Heart Circ Physiol. 2006;290:H886-H893.
45. Gao WD, Atar D, Backx PH, Marban E. Relationship between intracellular calcium and contractile force in stunned myocardium: direct evidence for decreased myofilament Ca2 + responsiveness and altered diastolic function in intact ventricular muscle. Circ Res. 1995;76:1036-1048.
46. Narolska NA, Piroddi N, Belus A, Boontje NM, Scellini B, Deppermann S, Zaremba R, Musters RJ, dos Remedios C, Jaquet K, Foster DB, Murphy AM, van Eyk JE, Tesi C, Poggesi C, van der Velden J, Stienen GJM. Impaired diastolic function after exchange of endogenous troponin I with C-terminal truncated troponin I in human cardiac muscle. Circ Res. 2006;99:1012-1020.