Thin filament incorporation of an engineered cardiac troponin C variant (L48Q) enhances contractility in intact cardiomyocytes from healthy and infarcted hearts

Journal of Molecular and Cellular Cardiology

Volumn 72, Issue , 2014, Pages 219-227

  Feest, Erik R ^a   Steven Korte, F ^a,b   Tu, An yue ^a   Dai, Jin ^a   Razumova, Maria V ^a   Murry, Charles E ^a,b   Regnier, Michael ^a,b  

^a University of Washington   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Adenovirus; Cardiomyocyte contractility; Cardiomyocytes; Gene therapy; Myocardial infarction

Indexed keywords

ADENOVIRUS VECTOR; CALCIUM ION; COMPLEMENTARY DNA; FURA 2; MUTANT PROTEIN; RECOMBINANT PROTEIN; TROPONIN C; CALCIUM;

ADULT; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING AFFINITY; CALCIUM BINDING; CALCIUM TRANSPORT; CARDIAC TRABECULAE; CONTROLLED STUDY; FEMALE; GENETIC TRANSDUCTION; HEART INFARCTION; HEART MUSCLE; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART MUSCLE RELAXATION; MUSCLE FIBRIL; MYOFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RAT; THIN FILAMENT; VIDEO MICROSCOPY; WESTERN BLOTTING; WILD TYPE; ACTION POTENTIAL; ADENOVIRIDAE; ANIMAL; FISCHER 344 RAT; GENE EXPRESSION; GENE THERAPY; GENE VECTOR; GENETICS; HEART CONTRACTION; METABOLISM; PATHOLOGY; PHYSIOLOGY; PRIMARY CELL CULTURE; PROTEIN ENGINEERING; VIDEORECORDING;

ACTION POTENTIALS; ADENOVIRIDAE; AMINO ACID SUBSTITUTION; ANIMALS; CALCIUM; FEMALE; GENE EXPRESSION; GENETIC THERAPY; GENETIC VECTORS; MYOCARDIAL CONTRACTION; MYOCARDIAL INFARCTION; MYOCARDIUM; MYOCYTES, CARDIAC; MYOFIBRILS; PRIMARY CELL CULTURE; PROTEIN ENGINEERING; RATS; RATS, INBRED F344; TRANSDUCTION, GENETIC; TROPONIN C; VIDEO RECORDING;

EID: 84901367922     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.03.015     Document Type: Article

References (59)

1. Benitah J.-P., Alvarez J.L., Gómez A.M. L-type Ca(2+) current in ventricular cardiomyocytes. J Mol Cell Cardiol 2010, 48:26-36.
2. Hobai I.A., O'Rourke B. Decreased sarcoplasmic reticulum calcium content is responsible for defective excitation-contraction coupling in canine heart failure. Circulation 2001, 103:1577-1584.
3. Piacentino V., Weber C.R., Chen X., Weisser-Thomas J., Margulies K.B., Bers D.M., et al. Cellular basis of abnormal calcium transients of failing human ventricular myocytes. Circ Res 2003, 92:651-658.
4. Sabbah H.N. Biologic rationale for the use of beta-blockers in the treatment of heart failure. Heart Fail Rev 2004, 9:91-97.
5. LeWinter M.M. Functional consequences of sarcomeric protein abnormalities in failing myocardium. Heart Fail Rev 2005, 10:249-257.
6. Palmer B.M. Thick filament proteins and performance in human heart failure. Heart Fail Rev 2005, 10:187-197.
7. Holt E., Tønnessen T., Lunde P.K., Semb S.O., Wasserstrom J.A., Sejersted O.M., et al. Mechanisms of cardiomyocyte dysfunction in heart failure following myocardial infarction in rats. J Mol Cell Cardiol 1998, 30:1581-1593.
8. Li P., Park C., Micheletti R., Li B., Cheng W., Sonnenblick E.H., et al. Myocyte performance during evolution of myocardial infarction in rats: effects of propionyl-L-carnitine. Am J Physiol 1995, 268:H1702-H1713.
9. Moreno-Gonzalez A., Korte F.S., Dai J., Chen K., Ho B., Reinecke H., et al. Cell therapy enhances function of remote non-infarcted myocardium. J Mol Cell Cardiol 2009, 47:603-613.
10. Belin R.J., Sumandea M.P., Kobayashi T., Walker L.A., Rundell V.L., Urboniene D., et al. Left ventricular myofilament dysfunction in rat experimental hypertrophy and congestive heart failure. Am J Physiol Heart Circ Physiol 2006, 291:H2344-H2353.
11. Belin R.J., Sumandea M.P., Allen E.J., Schoenfelt K., Wang H., Solaro R.J., et al. Augmented protein kinase C-alpha-induced myofilament protein phosphorylation contributes to myofilament dysfunction in experimental congestive heart failure. Circ Res 2007, 101:195-204.
12. Hamdani N., Kooij V., van Dijk S., Merkus D., Paulus W.J., Remedios C.D., et al. Sarcomeric dysfunction in heart failure. Cardiovasc Res 2007, 77:649-658.
13. Wolff M.R., Whitesell L.F., Moss R.L. Calcium sensitivity of isometric tension is increased in canine experimental heart failure. Circ Res 1995, 76:781-789.
14. Rubart M., Zipes D.P. Mechanisms of sudden cardiac death. J Clin Invest 2005, 115:2305-2315.
15. Kass D.a, Solaro R.J. Mechanisms and use of calcium-sensitizing agents in the failing heart. Circulation 2006, 113:305-315.
16. Wyskovsky W., Hauptner R., Suko J. Drug-induced calcium release from heavy sarcoplasmic reticulum of skeletal muscle. Biochim Biophys Acta 1988, 938:89-96.
17. Cleland J.G., Teerlink J.R., Senior R., Nifontov E.M., Mc Murray J.J.V., Lang C.C., et al. The effects of the cardiac myosin activator, omecamtiv mecarbil, on cardiac function in systolic heart failure: a double-blind, placebo-controlled, crossover, dose-ranging phase 2 trial. Lancet 2011, 378:676-683.
18. Shen Y.-T., Malik F.I., Zhao X., Depre C., Dhar S.K., Abarzúa P., et al. Improvement of cardiac function by a cardiac myosin activator in conscious dogs with systolic heart failure. Circ Heart Fail 2010, 3:522-527.
19. Malik F.I., Hartman J.J., Elias K.A., Morgan B.P., Rodriguez H., Brejc K., et al. Cardiac myosin activation: a potential therapeutic approach for systolic heart failure. Science 2011, 331:1439-1443.
20. Garg V, Frishman W.H. A new approach to inotropic therapy in the treatment of heart failure: cardiac myosin activators in treatment of HF. Cardiol Rev. May-Jun 2013, 21(3):155-159.
21. Wang D., Robertson I.M., Li M.X., McCully M.E., Crane M.L., Luo Z., et al. Structural and functional consequences of the cardiac troponin C L48Q Ca(2+)-sensitizing mutation. Biochemistry 2012, 51:4473-4487.
22. Tikunova S.B., Davis J.P. Designing calcium-sensitizing mutations in the regulatory domain of cardiac troponin C. J Biol Chem 2004, 279:35341-35352.
23. Kreutziger K.L., Piroddi N., McMichael J.T., Tesi C., Poggesi C., Regnier M. Calcium binding kinetics of troponin C strongly modulate cooperative activation and tension kinetics in cardiac muscle. J Mol Cell Cardiol 2011, 50:165-174.
24. Korte F.S., Feest E.R., Razumova M.V., Tu A.-Y., Regnier M. Enhanced Ca2+ binding of cardiac troponin reduces sarcomere length dependence of contractile activation independently of strong crossbridges. Am J Physiol Heart Circ Physiol 2012, 303:H863-H870.
25. Santana L.F., Kranias E.G., Lederer W.J. Calcium sparks and excitation-contraction coupling in phospholamban-deficient mouse ventricular myocytes. J Physiol 1997, 503(Pt 1):21-29.
26. Korte F.S., Dai J., Buckley K., Feest E.R., Adamek N., Geeves M.A., et al. Upregulation of cardiomyocyte ribonucleotide reductase increases intracellular 2 deoxy-ATP, contractility, and relaxation. J Mol Cell Cardiol 2011, 51:894-901.
27. Laflamme M.A., Chen K.Y., Naumova A.V., Muskheli V., Fugate J.a, Dupras S.K., et al. Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 2007, 25:1015-1024.
28. He T.C., Zhou S., da Costa L.T., Yu J., Kinzler K.W., Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci U S A 1998, 95:2509-2514.
29. Luo J., Deng Z.-L., Luo X., Tang N., Song W.-X., Chen J., et al. A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat Protoc 2007, 2:1236-1247.
30. Badrian B., Bogoyevitch M.A. Gene expression profiling reveals complex changes following MEK-EE expression in cardiac myocytes. Int J Biochem Cell Biol 2007, 39:349-365.
31. Badrian B., Bogoyevitch M.A. Changes in the transcriptional profile of cardiac myocytes following green fluorescent protein expression. DNA Cell Biol 2007, 26:727-736.
32. Li R.K., Jia Z.Q., Weisel R.D., Mickle D.A., Zhang J., Mohabeer M.K., et al. Cardiomyocyte transplantation improves heart function. Ann Thorac Surg 1996, 62:654-660. [discussion 660-1].
33. Müller-Ehmsen J., Whittaker P., Kloner R.A., Dow J.S., Sakoda T., Long T.I., et al. Survival and development of neonatal rat cardiomyocytes transplanted into adult myocardium. J Mol Cell Cardiol 2002, 34:107-116.
34. Scorsin M., Hagege A.A., Marotte F., Mirochnik N., Copin H., Barnoux M., et al. Does transplantation of cardiomyocytes improve function of infarcted myocardium?. Circulation 1997, 96. [II-188-93].
35. Huwer H., Winning J., Vollmar B., Welter C., Löhbach C., Menger M.D., et al. Long-term cell survival and hemodynamic improvements after neonatal cardiomyocyte and satellite cell transplantation into healed myocardial cryoinfarcted lesions in rats. Cell Transplant 2003, 12:757-767.
36. Sacconi L., Ferrantini C., Lotti J., Coppini R., Yan P., Loew L.M., et al. Action potential propagation in transverse-axial tubular system is impaired in heart failure. Proc Natl Acad Sci U S A 2012, 109:5815-5819.
37. Cazorla O., Lucas A., Poirier F., Lacampagne A., Lezoualc'h F. The cAMP binding protein Epac regulates cardiac myofilament function. Proc Natl Acad Sci U S A 2009, 106:14144-14149.
38. Sheehan K.A., Arteaga G.M., Hinken A.C., Dias F.A., Ribeiro C., Wieczorek D.F., et al. Functional effects of a tropomyosin mutation linked to FHC contribute to maladaptation during acidosis. J Mol Cell Cardiol 2011, 50:442-450.
39. Kawashima H., Satoh H., Saotome M., Urushida T., Katoh H., Hayashi H. Protein phosphatase inhibitor-1 augments a protein kinase A-dependent increase in the Ca2+ loading of the sarcoplasmic reticulum without changing its Ca2+ release. Circ J 2009, 73:1133-1140.
40. Shah A.M., Prendergast B.D., Grocott-Mason R., Lewis M.J., Paulus W.J. The influence of endothelium-derived nitric oxide on myocardial contractile function. Int J Cardiol 1995, 50:225-231.
41. Vogelpohl I., Vetter R., Heger J., Ebermann L., Euler G., Schultheiss H.-P., et al. Transgenic overexpression of heart-specific adenine nucleotide translocase 1 positively affects contractile function in cardiomyocytes. Cell Physiol Biochem 2011, 27:121-128.
42. Feest E.R., Tu A., Luo C., Nowakowski S.G., Regnier M. Effect of varying mutant troponin C content on contractile properties of striated muscle. Biophys J 2009, 96:228a.
43. Dong W.J., Jayasundar J.J., An J., Xing J., Cheung H.C. Effects of PKA phosphorylation of cardiac troponin I and strong crossbridge on conformational transitions of the N-domain of cardiac troponin C in regulated thin filaments. Biochemistry 2007, 46:9752-9761.
44. De Tombe P.P., Belus A., Piroddi N., Scellini B., Walker J.S., Martin A.F., et al. Myofilament calcium sensitivity does not affect cross-bridge activation-relaxation kinetics. Am J Physiol Regul Integr Comp Physiol 2007, 292:R1129-R1136.
45. Fentzke R.C., Buck S.H., Patel J.R., Lin H., Wolska B.M., Stojanovic M.O., et al. Impaired cardiomyocyte relaxation and diastolic function in transgenic mice expressing slow skeletal troponin I in the heart. J Physiol 1999, 517(Pt 1):143-157.
46. Feng H.-Z., Hossain M.M., Huang X.-P., Jin J.-P. Myofilament incorporation determines the stoichiometry of troponin I in transgenic expression and the rescue of a null mutation. Arch Biochem Biophys 2009, 487:36-41.
47. Lim C.C., Yang H., Yang M., Wang C.-K., Shi J., Berg E.a, et al. A novel mutant cardiac troponin C disrupts molecular motions critical for calcium binding affinity and cardiomyocyte contractility. Biophys J 2008, 94:3577-3589.
48. Arteaga G.M., Warren C.M., Milutinovic S., Martin A.F., Solaro R.J. Specific enhancement of sarcomeric response to Ca2+ protects murine myocardium against ischemia-reperfusion dysfunction. Am J Physiol Heart Circ Physiol 2005, 289:H2183-H2192.
49. Maron B.J., Towbin J.A., Thiene G., Antzelevitch C., Corrado D., Arnett D., et al. Contemporary definitions and classification of the cardiomyopathies: an American Heart Association Scientific Statement from the Council on Clinical Cardiology, Heart Failure and Transplantation Committee; Quality of Care and Outcomes Research and Function. Circulation 2006, 113:1807-1816.
50. Elliott P., Andersson B., Arbustini E., Bilinska Z., Cecchi F., Charron P., et al. Classification of the cardiomyopathies: a position statement from the European Society Of Cardiology Working Group on Myocardial and Pericardial Diseases. Eur Heart J 2008, 29:270-276.
51. Maron B.J. Hypertrophic cardiomyopathy: a systematic review. JAMA 2002, 287:1308-1320.
52. Morimoto S., Lu Q.-W., Harada K., Takahashi-Yanaga F., Minakami R., Ohta M., et al. Ca(2+)-desensitizing effect of a deletion mutation Delta K210 in cardiac troponin T that causes familial dilated cardiomyopathy. Proc Natl Acad Sci U S A 2002, 99:913-918.
53. Lu Q.-W., Morimoto S., Harada K., Du C.-K., Takahashi-Yanaga F., Miwa Y., et al. Cardiac troponin T mutation R141W found in dilated cardiomyopathy stabilizes the troponin T-tropomyosin interaction and causes a Ca2+ desensitization. J Mol Cell Cardiol 2003, 35:1421-1427.
54. 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.
55. Rajan S., Ahmed R.P.H., Jagatheesan G., Petrashevskaya N., Boivin G.P., 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.
56. Du C.K., 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.
57. Baudenbacher F., Schober T., Pinto J.R., Sidorov V.Y., Hilliard F., Solaro R.J., et al. Myofilament Ca2+ sensitization causes susceptibility to cardiac arrhythmia in mice. J Clin Invest 2008, 118:3893-3903.
58. Solaro R.J., Gambassi G., Warshaw D.M., Keller M.R., Spurgeon H.A., Beier N., et al. Stereoselective actions of thiadiazinones on canine cardiac myocytes and myofilaments. Circ Res 1993, 73:981-990.
59. White J., Lee J.A., Shah N., Orchard C.H. Differential effects of the optical isomers of EMD 53998 on contraction and cytoplasmic Ca2+ in isolated ferret cardiac muscle. Circ Res 1993, 73:61-70.