Dilated and hypertrophic cardiomyopathy mutations in troponin and α-tropomyosin have opposing effects on the calcium affinity of cardiac thin filaments

Circulation Research

Volumn 101, Issue 12, 2007, Pages 1266-1273

  Robinson, Paul ^a   Griffiths, Peter J ^a   Watkins, Hugh ^a   Redwood, Charles S ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Calcium; Cardiomyopathy; Signaling; Troponin

Indexed keywords

2 [4' (IODOACETAMIDO)ANILINE]NAPHTHALENE 6 SULFONATE; ALPHA TROPOMYOSIN; ASPARTIC ACID; CALCIUM; CYSTEINE; FLUORESCENT DYE; SULFONIC ACID DERIVATIVE; TROPONIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CALCIUM BINDING; CONGESTIVE CARDIOMYOPATHY; CORRELATION ANALYSIS; HEART; HEART MUSCLE CELL; HYPERTROPHIC CARDIOMYOPATHY; IN VITRO STUDY; MUTANT; MUTATION; PRIORITY JOURNAL; SARCOPLASM; THIN FILAMENT; WILD TYPE;

ANIMALS; BINDING SITES; CALCIUM; CARDIOMYOPATHY, DILATED; CARDIOMYOPATHY, HYPERTROPHIC; HUMANS; MICROFILAMENTS; MUTATION; MYOCARDIAL CONTRACTION; RABBITS; TROPOMYOSIN; TROPONIN;

EID: 37349042936     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.107.156380     Document Type: Article

References (42)

1. Ashrafian H, Watkins H. Reviews of translational medicine and genomics in cardiovascular disease: new disease taxonomy and therapeutic implications cardiomyopathies: therapeutics based on molecular phenotype. J Am Coll Cardiol. 2007;49:1251-1264.
2. Richard P, Charron P, Carrier L, Ledeuil C, Cheav T, Pichereau C, Benaiche A, Isnard R, Dubourg O, Burban M, Gueffet JP, Millaire A, Desnos M, Schwartz K, Hainque B, Komajda M. Hypertrophic cardiomyopathy: distribution of disease genes, spectrum of mutations, and implications for a molecular diagnosis strategy. Circulation. 2003;107:2227-2232.
3. Thierfelder L, Watkins H, MacRae C, Lamas R, McKenna W, Vosberg HP, Seidman JG, Seidman CE. Alpha-tropomyosin and cardiac troponin T mutations cause familial hypertrophic cardiomyopathy: a disease of the sarcomere. Cell. 1994;77:701-712.
4. Watkins H, McKenna WJ, Thierfelder L, Suk HJ, Anan R, O'Donoghue A, Spirito P, Matsumori A, Moravec CS, Seidman JG, Seidman CE. Mutations in the genes for cardiac troponin T and alpha-tropomyosin in hypertrophic cardiomyopathy. N Engl J Med. 1995;332:1058-1064.
5. 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.
6. Deleted in proof.
7. Seidman JG, Seidman C. The genetic basis for cardiomyopathy: from mutation identification to mechanistic paradigms. Cell. 2001;104:557-567.
8. Kamisago M, Sharma SD, DePalma SR, Solomon S, Sharma P, McDonough B, Smoot L, Mullen MP, Woolf PK, Wigle ED, Seidman JG, Seidman CE. Mutations in sarcomere protein genes as a cause of dilated cardiomyopathy. N Engl J Med. 2000;343:1688-1696.
9. Li D, Czernuszewicz GZ, Gonzalez O, Tapscott T, Karibe A, Durand JB, Brugada R, Hill R, Gregoritch JM, Anderson JL, Quinones M, Bachinski LL, Roberts R. Novel cardiac troponin T mutation as a cause of familial dilated cardiomyopathy. Circulation. 2001;104:2188-2193.
10. Mogensen J, Murphy RT, Shaw T, Bahl A, Redwood C, Watkins H, Burke M, Elliott PM, McKenna WJ. Severe disease expression of cardiac troponin C and T mutations in patients with idiopathic dilated cardiomyopathy. J Am Coll Cardiol. 2004;44:2033-2040.
11. Olson TM, Kishimoto NY, Whitby FG, Michels VV. Mutations that alter the surface charge of alpha-tropomyosin are associated with dilated cardiomyopathy. J Mol Cell Cardiol. 2001;33:723-732.
12. Tobacman LS. Thin filament-mediated regulation of cardiac contraction. Annu Rev Physiol. 1996;58:447-481.
13. 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.
14. Hernandez OM, Housmans PR, Potter JD. Invited review: pathophysiology of cardiac muscle contraction and relaxation as a result of alterations in thin filament regulation. J Appl Physiol. 2001;90:1125-1136.
15. Mirza M, Marston S, Willott R, Ashley C, Mogensen J, McKenna W, Robinson P, Redwood C, Watkins H. Dilated cardiomyopathy mutations in three thin filament regulatory proteins result in a common functional phenotype. J Biol Chem. 2005;280:28498-28506.
16. Robinson P, Mirza M, Knott A, Abdulrazzak H, Willott R, Marston S, Watkins H, Redwood C. Alterations in thin filament regulation induced by a human cardiac troponin T mutant that causes dilated cardiomyopathy are distinct from those induced by troponin T mutants that cause hypertrophic cardiomyopathy. J Biol Chem. 2002;277:40710-40716.
17. Kataoka A, Hemmer C, Chase PB. Computational simulation of hypertrophic cardiomyopathy mutations in troponin I: influence of increased myofilament calcium sensitivity on isometric force, ATPase and [Ca2+]i. J Biomech. 2007;40:2044-2052.
18. Tobacman LS, Lin D, Butters C, Landis C, Back N, Pavlov D, Homsher E. Functional consequences of troponin T mutations found in hypertrophic cardiomyopathy. J Biol Chem. 1999;274:28363-28370.
19. Kobayashi T, Solaro RJ. Increased Ca2+ affinity of cardiac thin filaments reconstituted with cardiomyopathy-related mutant cardiac troponin I. J Biol Chem. 2006;281:13471-13477.
20. Elliott K, Watkins H, Redwood CS. Altered regulatory properties of human cardiac troponin I mutants that cause hypertrophic cardiomyopathy. J Biol Chem. 2000;275:22069-22074.
21. Bottinelli R, Coviello DA, Redwood CS, Pellegrino MA, Maron BJ, Spirito P, Watkins H, Reggiani C. A mutant tropomyosin that causes hypertrophic cardiomyopathy is expressed in vivo and associated with an increased calcium sensitivity. Circ Res. 1998;82:106-115.
22. Pardee JD, Spudich JA. Purification of muscle actin. Methods Enzymol. 1982;85(pt B):164-181.
23. Putkey JA, Liu W, Lin X, Ahmed S, Zhang M, Potter JD, Kerrick WG. Fluorescent probes attached to Cys 35 or Cys 84 in cardiac troponin C are differentially sensitive to Ca(2+)-dependent events in vitro and in situ. Biochemistry. 1997;36:970-978.
24. Redwood C, Lohmann K, Bing W, Esposito GM, Elliott K, Abdulrazzak H, Knott A, Purcell I, Marston S, Watkins H. Investigation of a truncated cardiac troponin T that causes familial hypertrophic cardiomyopathy: Ca(2+) regulatory properties of reconstituted thin filaments depend on the ratio of mutant to wild-type protein. Circ Res. 2000;86:1146-1152.
25. Rosenfeld SS, Taylor EW. Kinetic studies of calcium binding to regulatory complexes from skeletal muscle. J Biol Chem. 1985;260:252-261.
26. Davis JP, Norman C, Kobayashi T, Solaro RJ, Swartz DR, Tikunova SB. Effects of thin and thick filament proteins on calcium binding and exchange with cardiac troponin C. Biophys J. 2007;92:3195-3206.
27. Takeda S, Yamashita A, Maeda K, Maeda Y. Structure of the core domain of human cardiac troponin in the Ca(2+)-saturated form. Nature. 2003;424:35-41.
28. Szczesna D, Zhang R, Zhao J, Jones M, Guzman G, Potter JD. Altered regulation of cardiac muscle contraction by troponin T mutations that cause familial hypertrophic cardiomyopathy. J Biol Chem. 2000;275:624-630.
29. McKay RT, Pearlstone JR, Corson DC, Gagne SM, Smillie LB, Sykes BD. Structure and interaction site of the regulatory domain of troponin-C when complexed with the 96-148 region of troponin-I. Biochemistry. 1998;37:12419-12430.
30. 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.
31. Hinkle A, Tobacman LS. Folding and function of the troponin tail domain. Effects of cardiomyopathic troponin T mutations. J Biol Chem. 2003;278:506-513.
32. Blumenschein TM, Tripet BP, Hodges RS, Sykes BD. 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. 2001;276:36606-36612.
33. Biesiadecki BJ, Kobayashi T, Walker JS, John Solaro R, de Tombe PP. The troponin C G159D mutation blunts myofilament desensitization induced by troponin I Ser23/24 phosphorylation. Circ Res. 2007;100:1486-1493.
34. Preston LC, Lipscomb S, Robinson P, Mogensen J, McKenna WJ, Watkins H, Ashley CC, Redwood CS. Functional effects of the DCM mutant Gly159Asp Troponin C in skinned muscle fibres. Pflugers Arch. 2007;453:771-776.
35. Robertson SP, Johnson JD, Holroyde MJ, Kranias EG, Potter JD, Solaro RJ. The effect of troponin I phosphorylation on the Ca2+-binding properties of the Ca2+-regulatory site of bovine cardiac troponin. J Biol Chem. 1982;257:260-263.
36. Mirza M, Robinson P, Kremneva E, Copeland O, Nikolaeva O, Watkins H, Levitsky D, Redwood C, El-Mezgueldi M, Marston S. The effect of mutations in alpha-tropomyosin (E40K and E54K) that cause familial dilated cardiomyopathy on the regulatory mechanism of cardiac muscle thin filaments. J Biol Chem. 2007;282:13487-13497.
37. Holthauzen LM, Correa F, Farah CS. Ca2+-induced rolling of tropomyosin in muscle thin filaments: the alpha- and beta-band hypothesis revisited. J Biol Chem. 2004;279:15204-15213.
38. Smith GA, Dixon HB, Kirschenlohr HL, Grace AA, Metcalfe JC, Vandenberg JI. Ca2+ buffering in the heart: Ca2+ binding to and activation of cardiac myofibrils. Biochem J. 2000;346(pt 2):393-402.
39. Fatkin D, McConnell BK, Mudd JO, Semsarian C, Moskowitz IG, Schoen FJ, Giewat M, Seidman CE, Seidman JG. An abnormal Ca(2+) response in mutant sarcomere protein-mediated familial hypertrophic cardiomyopathy. J Clin Invest. 2000;106:1351-1359.
40. Miyamoto S, Howes AL, Adams JW, Dorn GW 2nd, Brown JH. Ca2+ dysregulation induces mitochondrial depolarization and apoptosis: role of Na+/Ca2+ exchanger and AKT. J Biol Chem. 2005;280:38505-38512.
41. Schmitt JP, Kamisago M, Asahi M, Li GH, Ahmad F, Mende U, Kranias EG, MacLennan DH, Seidman JG, Seidman CE. Dilated cardiomyopathy and heart failure caused by a mutation in phospholamban. Science. 2003; 299:1410-1413.
42. Du CK, Morimoto S, Nishii K, Minakami R, Ohta M, Tadano N, Lu QW, Wang YY, Zhan DY, Mochizuki M, Kita S, Miwa Y, Takahashi-Yanaga F, Iwamoto T, Ohtsuki I, Sasaguri T. Knock-in mouse model of dilated cardiomyopathy caused by troponin mutation. Circ Res. 2007;101:185-194.