Familial dilated cardiomyopathy mutations uncouple troponin i phosphorylation from changes in myofibrillar Ca2+ sensitivity

Cardiovascular Research

Volumn 99, Issue 1, 2013, Pages 65-73

  Memo, Massimiliano ^a   Leung, Man Ching ^a   Ward, Douglas G ^b   Dos Remedios, Cristobal ^c   Morimoto, Sachio ^d   Zhang, Lianfeng ^e   Ravenscroft, Gianina ^f   McNamara, Elyshia ^f   Nowak, Kristen J ^f   Marston, Steven B ^a   Messer, Andrew E ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c UNIVERSITY OF SYDNEY   (Australia)

^d KYUSHU UNIVERSITY   (Japan)

^e INSTITUTE OF LABORATORY ANIMAL SCIENCE   (China)

^f UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Ca2+ regulation of contractility; Familial dilated cardiomyopathy; In vitro motility assay; Mutations; Troponin phosphorylation

Indexed keywords

ALPHA TROPOMYOSIN; CALCIUM ION; CYCLIC AMP DEPENDENT PROTEIN KINASE; TROPONIN I; TROPONIN T;

ANIMAL TISSUE; ARTICLE; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; GENE MUTATION; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; THIN FILAMENT;

CA2+ REGULATION OF CONTRACTILITY; FAMILIAL DILATED CARDIOMYOPATHY; IN VITRO MOTILITY ASSAY; MUTATIONS; TROPONIN PHOSPHORYLATION;

ANIMALS; CALCIUM; CARDIOMYOPATHY, DILATED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GENOTYPE; HUMANS; MICE; MICE, TRANSGENIC; MODELS, MOLECULAR; MUTATION; MYOCARDIUM; MYOFIBRILS; PHENOTYPE; PHOSPHORYLATION; PROTEIN CONFORMATION; TROPOMYOSIN; TROPONIN I; TROPONIN T;

EID: 84879390656     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvt071     Document Type: Article

References (45)

1. Mogensen J, Murphy RT, Shaw T, Bahl A, Redwood C,Watkins H et al. Severe disease expression of cardiac troponin C and T mutations in patients with idiopathic dilated cardiomyopathy. J Am Coll Cardiol 2004;44:2033-2040 (Pubitemid 39473290)
2. Chang AN, Potter JD. Sarcomeric protein mutations in dilated cardiomyopathy. Heart Fail Rev 2005;10:225-235 (Pubitemid 43115832)
3. Menon SC, Olson TM, Michels V. Genetics of familial dilated cardiomyopathy. Prog Ped Cardiol 2008;25:57-67
4. Marston SB. How do mutations in contractile proteins cause the primary familial cardiomyopathies? J Cardiovasc Transl Res 2011;4:245-255
5. Tardiff JC. Sarcomeric proteins and familial hypertrophic cardiomyopathy: linking mutations in structural proteins to complex cardiovascular phenotypes. Heart Fail Rev 2005;10:237-248 (Pubitemid 43115833)
6. Kamisago M, Sharma SD, DePalma SR, Solomon S, Sharma P, Smoot L et al. Mutations in sarcomere protein genes as a cause of dilated cardiomyopathy. N Engl J Med 2000; 343:1688-1696
7. Moller DV, Andersen PS, Hedley P, Ersboll MK, Bundgaard H, Moolman-Smook J et al. The role of sarcomere gene mutations in patients with idiopathic dilated cardiomyopathy. Eur J Hum Genet: EJHG 2009;17:1241-1249
8. Herman DS, Lam L, Taylor MRG, Wang L, Teekakirikul P, Christodoulou D et al. Truncations of titin causing dilated cardiomyopathy. New Eng J Med 2012;366: 619-628
9. Mirza M, Marston S, Willott R, Ashley C, Mogensen J, McKenna W et al. Dilated cardiomyopathy mutations in three thin filament regulatory proteins result in a common functional phenotype. J Biol Chem 2005;280:28498-28506 (Pubitemid 41105750)
10. Robinson P, Griffiths PJ, Watkins H, Redwood CS. Dilated and hypertrophic cardiomyopathy mutations in troponin and alpha-tropomyosin have opposing effects on the calcium affinity of cardiac thin filaments. Circ Res 2007;101:1266-1273 (Pubitemid 350294643)
11. Dyer E, Jacques A, Hoskins A, Ward D, Gallon C, Messer A et al. Functional analysis of a unique troponin C mutation, Gly159Asp that causes familial dilated cardiomyopathy, studied in explanted heart muscle. Circ Heart Fail 2009;2:456-464
12. Matsumoto F, Maeda K, Chatake T, Maeda Y, Fujiwara S. Functional aberration of myofibrils by cardiomyopathy-causing mutations in the coiled-coil region of the troponin-core domain. Biochem Biophys Res Commun 2009;382:205-209
13. Debold EP, Saber W, Cheema Y, Bookwalter CS, Trybus KM, Warshaw DM et al. Human actin mutations associated with hypertrophic and dilated cardiomyopathies demonstrate distinct thin filament regulatory properties in vitro. J Mol Cell Cardiol 2010;48:286-292
14. 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
15. Layland J, Solaro RJ, Shah AM. Regulation of cardiac contractile function by troponin I phosphorylation. Cardiovasc Res 2005;66:12-21 (Pubitemid 40357865)
16. Little SC, Biesiadecki BJ, Kilic A, Higgins RSD, Janssen PML, Davis JP. The rates of Ca2+ dissociation and cross-bridge detachment from ventricular myofibrils as reported by a fluorescent cardiac troponin C. J Biol Chem 2012;287:27930-27940
17. Messer A, Gallon C, McKenna W, Elliott P, Dos Remedios C, Marston S. The use of phosphate-affinity SDS-PAGE to measure the troponin I phosphorylation site distribution in human heart muscle. Proteomics Clin Appl 2009;3:1371-1382
18. Messer AE, Jacques AM, Marston SB. Troponin phosphorylation and regulatory function in human heart muscle: dephosphorylation of Ser23/24 on troponin I could account for the contractile defect in end-stage heart failure. J Mol Cell Cardiol 2007; 42:247-259 (Pubitemid 44970468)
19. 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 (Pubitemid 46834761)
20. Dong W, Xing J, Ouyang Y, An J, Cheung HC. Structural kinetics of cardiac troponin C mutants linked to familial hypertrophic and dilated cardiomyopathy in troponin complexes. J Biol Chem 2008;283:3424-3432
21. SongW, Dyer E, Stuckey D, Leung M-C, Memo M, Mansfield C et al. Investigation of a transgenic mouse model of familial dilated cardiomyopathy. J Mol Cell Cardiol 2010;49: 380-389
22. Carballo S, Robinson P, Otway R, Fatkin D, Jongbloed JD, de Jonge N et al. Identification and functional characterization of cardiac troponin I as a novel disease gene in autosomal dominant dilated cardiomyopathy. Circ Res 2009;105:375-382
23. Juan F, Wei D, Xiongzhi Q, Ran D, Chunmei M, Lan H et al. The changes of the cardiac structure and function in cTnT R141W transgenic mice. Int J Cardiol 2008; 128:83-90 (Pubitemid 351916714)
24. Du CK, Morimoto S, Nishii K, Minakami R, Ohta M, Tadano N et al. Knock-In mouse model of dilated cardiomyopathy caused by troponin mutation. Circ Res 2007;101: 185-194 (Pubitemid 47196586)
25. 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 (Pubitemid 32538985)
26. Lakdawala NK, Dellefave L, Redwood CS, Sparks E, Cirino AL, Depalma S et al. Familial dilated cardiomyopathy caused by an alpha-tropomyosin mutation: the distinctive natural history of sarcomeric dilated cardiomyopathy. J Am Coll Cardiol 2010;55: 320-329
27. Mirza M, Robinson P, Kremneva E, Copeland O, Nikolaeva O, Watkins H et al. 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 (Pubitemid 47100552)
28. Knott A, Purcell IF, Marston S. In vitro motility analysis of thin filaments from failing and non-failing human hearts induces slower filament sliding and higher Ca2+-sensitivity. J Mol Cell Cardiol 2002;34:469-482 (Pubitemid 37163461)
29. Akkari PA, Song Y, Hitchcock-DeGregori S, Blechynden L, Laing N. Expression and biological activity of baculovirus generated wild-type human slow alpha tropomyosin and the Met9Arg mutant responsible for a dominant form of nemaline myopathy. Biochem Biophys Res Commun 2002;296:300-304
30. Layland J, Cave AC, Warren C, Grieve DJ, Sparks E, Kentish JC et al. Protection against endotoxemia-induced contractile dysfunction in mice with cardiac-specific expression of slow skeletal troponin I. FASEB J 2005;19:1137-1139 (Pubitemid 40946443)
31. Kinoshita E, Kinoshita-Kikuta E, Takiyama K, Koike T. Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol Cell Proteomics 2006;5:749-757
32. Kron SJ, Toyoshima YY, Uyeda TQP, Spudich JA. Assays for actin sliding movement over myosin coated surfaces. Methods Enzymol 1991;196:399-416
33. Fraser IDC, Marston SB. In Vitro motility analysis of actin-tropomyosin regulation by troponin and Ca2+: the thin filament is switched as a single cooperative unit. J Biol Chem 1995;270:7836-7841
34. Marston SB, Fraser IDC, Wu B, Roper G. A simple method for automatic tracking of actin filaments in the motility assay. J Musc Res Cell Motil 1996;17:497-506 (Pubitemid 26298532)
35. Morimoto S. Sarcomeric proteins and inherited cardiomyopathies. Cardiovasc Res 2008;77:659-666 (Pubitemid 351301864)
36. Pinto JR, Siegfried JD, Parvatiyar MS, Li D, Norton N, Jones MA et al. Functional characterization of TNNC1 rare variants identified in dilated cardiomyopathy. J Biol Chem 2011;286:34404-34412
37. Howarth JW, Meller J, Solaro RJ, Trewhella J, Rosevear PR. Phosphorylationdependent conformational transition of the cardiac specific N-extension of troponin I in cardiac troponin. J Mol Biol 2007;373:706-722 (Pubitemid 47488403)
38. Song W, Dyer E, Stuckey D, Copeland O, Leung M, Bayliss C et al. Molecular mechanism of the Glu99lys mutation in cardiac actin (ACTC gene) that causes apical hypertrophy in man and mouse. J Biol Chem 2011;286:27582-27593
39. Deng Y, Schmidtmann A, Kruse S, Filatov V, Heilmeyer LM Jr, Jaquet K et al. Phosphorylation of human cardiac troponin I G203S and K206Q linked to familial hypertrophic cardiomyopathy affects actomyosin interaction in different ways. J Mol Cell Cardiol 2003;35:1365-1374 (Pubitemid 37330094)
40. Jacques A, Hoskins A, Kentish J, Marston SB. From genotype to phenotype: a longitudinal study of a patient with hypertrophic cardiomyopathy due to a mutation in the MYBPC3 gene. J Musc Res Cell Motil 2009;29:239-246
41. Bayliss CR, Jacques AM, Leung M-C, Ward DG, Redwood CS, Gallon CE et al. Myofibrillar Ca2+-sensitivity is uncoupled from troponin I phosphorylation in hypertrophic obstructive cardiomyopathy due to abnormal troponin T. Cardiovasc Res 2013;97: 500-508
42. Vikhorev PG, Wilkinson R, Song W, Copeland O, Marston SB, Ferenczi MA. DCM-causing mutation E361G in actin slows myofibril relaxation kinetics and uncouples myofibril Ca2+-sensitivity from protein phosphorylation. Biophys J 2013;104:312a
43. Yasuda S, Coutu P, Sadayappan S, Robbins J, Metzger JM. Cardiac transgenic and gene transfer strategies converge to support an important role for troponin I in regulating relaxation in cardiac myocytes. Circ Res 2007;101:377-386 (Pubitemid 47267706)
44. Rajan S, Ahmed RP, Jagatheesan G, Petrashevskaya N, Boivin GP, Urboniene D et al. Dilated cardiomyopathy mutant tropomyosin mice develop cardiac dysfunction with significantly decreased fractional shortening and myofilament calcium sensitivity. Circ Res 2007;101:205-214 (Pubitemid 47196588)
45. Gramlich M, Michely B, Krohne C, Heuser A, Erdmann B, Klaassen S et al. Stress-induced dilated cardiomyopathy in a knock-in mouse model mimicking human titin-based disease. J Mol Cell Cardiol 2009;47:352-358.