The role of Akt/GSK-3β signaling in familial hypertrophic cardiomyopathy

Journal of Molecular and Cellular Cardiology

Volumn 46, Issue 5, 2009, Pages 739-747

  Luckey, Stephen W ^a   Walker, Lori A ^b   Smyth, Tyson ^a   Mansoori, Jason ^a   Messmer Kratzsch, Antke ^a   Rosenzweig, Anthony ^c   Olson, Eric N ^d   Leinwand, Leslie A ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c HARVARD STEM CELL INSTITUTE   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Akt; Cardiomyopathy; Familial hypertrophic cardiomyopathy; Glycogen synthase kinase 3 (GSK 3 ); Troponin T

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3; PROTEIN KINASE B; TROPONIN I; TROPONIN T;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DISEASE COURSE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FAMILIAL HYPERTROPHIC CARDIOMYOPATHY; GENE EXPRESSION; HEART MUSCLE FIBROSIS; HEART SIZE; HEART VENTRICLE SIZE; MISSENSE MUTATION; MOLECULE; MOUSE; MOUSE STRAIN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WILD TYPE;

AMINO ACID SUBSTITUTION; ANIMALS; BODY WEIGHT; CARDIOMYOPATHY, HYPERTROPHIC, FAMILIAL; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GLYCOGEN SYNTHASE KINASE 3; HEART VENTRICLES; HYPERTROPHY; MALE; MICE; MICE, MUTANT STRAINS; MUTATION; MYOCARDIUM; ORGAN SIZE; PHENOTYPE; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; TROPONIN T;

MUS; MUS MUSCULUS;

EID: 63349095616     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2009.02.010     Document Type: Article

References (42)

1. Richard P., Charron P., Carrier L., Ledeuil C., Cheav T., Pichereau C., et al. Hypertrophic cardiomyopathy: distribution of disease genes, spectrum of mutations, and implications for a molecular diagnosis strategy. Circulation 107 17 (2003) 2227-2232
2. Bonne G., Carrier L., Richard P., Hainque B., and Schwartz K. Familial hypertrophic cardiomyopathy: from mutations to functional defects. Circ Res 83 6 (1998) 580-593
3. Varnava A.M., Elliott P.M., Baboonian C., Davison F., Davies M.J., and McKenna W.J. Hypertrophic cardiomyopathy: histopathological features of sudden death in cardiac troponin T disease. Circulation 104 12 (2001) 1380-1384
4. Tardiff J.C., Factor S.M., Tompkins B.D., Hewett T.E., Palmer B.M., Moore R.L., et al. A truncated cardiac troponin T molecule in transgenic mice suggests multiple cellular mechanisms for familial hypertrophic cardiomyopathy. J Clin Invest 101 12 (1998) 2800-2811
5. Tardiff J.C., Hewett T.E., Palmer B.M., Olsson C., Factor S.M., Moore R.L., et al. Cardiac troponin T mutations result in allele-specific phenotypes in a mouse model for hypertrophic cardiomyopathy. J Clin Invest 104 4 (1999) 469-481
6. Ertz-Berger B.R., He H., Dowell C., Factor S.M., Haim T.E., Nunez S., et al. Changes in the chemical and dynamic properties of cardiac troponin T cause discrete cardiomyopathies in transgenic mice. Proc Natl Acad Sci U S A 102 50 (2005) 18219-18224
7. Sirenko S.G., Potter J.D., and Knollmann B.C. Differential effect of troponin T mutations on the inotropic responsiveness of mouse hearts-role of myofilament Ca2+ sensitivity increase. J Physiol 575 Pt 1 (2006) 201-213
8. Hernandez O.M., Szczesna-Cordary D., Knollmann B.C., Miller T., Bell M., Zhao J., et al. F110I and R278C troponin T mutations that cause familial hypertrophic cardiomyopathy affect muscle contraction in transgenic mice and reconstituted human cardiac fibers. J Biol Chem 280 44 (2005) 37183-37194
9. Knollmann B.C., Kirchhof P., Sirenko S.G., Degen H., Greene A.E., Schober T., et al. Familial hypertrophic cardiomyopathy-linked mutant troponin T causes stress-induced ventricular tachycardia and Ca2+-dependent action potential remodeling. Circ Res 92 4 (2003) 428-436
10. Montgomery D.E., Tardiff J.C., and Chandra M. Cardiac troponin T mutations: correlation between the type of mutation and the nature of myofilament dysfunction in transgenic mice. J Physiol 536 Pt 2 (2001) 583-592
11. Dorn II G.W., and Force T. Protein kinase cascades in the regulation of cardiac hypertrophy. J Clin Invest 115 3 (2005) 527-537
12. Morisco C., Zebrowski D., Condorelli G., Tsichlis P., Vatner S.F., and Sadoshima J. The Akt-glycogen synthase kinase 3beta pathway regulates transcription of atrial natriuretic factor induced by beta-adrenergic receptor stimulation in cardiac myocytes. J Biol Chem 275 19 (2000) 14466-14475
13. Antos C.L., McKinsey T.A., Frey N., Kutschke W., McAnally J., Shelton J.M., et al. Activated glycogen synthase-3 beta suppresses cardiac hypertrophy in vivo. Proc Natl Acad Sci U S A 99 2 (2002) 907-912
14. Matsui T., Li L., Wu J.C., Cook S.A., Nagoshi T., Picard M.H., et al. Phenotypic spectrum caused by transgenic overexpression of activated Akt in the heart. J. Biol. Chem. 277 25 (2002) 22896-22901
15. Shiojima I., and Walsh K. Regulation of cardiac growth and coronary angiogenesis by the Akt/PKB signaling pathway. Genes Dev 20 24 (2006) 3347-3365
16. Luckey S.W., Mansoori J., Fair K., Antos C.L., Olson E.N., and Leinwand L.A. Blocking cardiac growth in hypertrophic cardiomyopathy induces cardiac dysfunction and decreased survival only in males. Am J Physiol Heart Circ Physiol 292 2 (2007) H838-H845
17. Kobayashi T., Yang X., Walker L.A., Van Breemen R.B., and Solaro R.J. A non-equilibrium isoelectric focusing method to determine states of phosphorylation of cardiac troponin I: identification of Ser-23 and Ser-24 as significant sites of phosphorylation by protein kinase C. J Mol Cell Cardiol 38 1 (2005) 213-218
18. Scruggs S.B., Walker L.A., Lyu T., Geenen D.L., Solaro R.J., Buttrick P.M., et al. Partial replacement of cardiac troponin I with a non-phosphorylatable mutant at serines 43/45 attenuates the contractile dysfunction associated with PKCepsilon phosphorylation. J Mol Cell Cardiol 40 4 (2006) 465-473
19. Leinwand L.A. Sex is a potent modifier of the cardiovascular system. J Clin Invest 112 3 (2003) 302-307
20. Sumandea M.P., Burkart E.M., Kobayashi T., De Tombe P.P., and Solaro R.J. Molecular and integrated biology of thin filament protein phosphorylation in heart muscle. Ann N Y Acad Sci 1015 (2004) 39-52
21. Hill J.A., and Olson E.N. Cardiac plasticity. N Engl J Med 358 13 (2008) 1370-1380
22. Maass A.H., Ikeda K., Oberdorf-Maass S., Maier S.K., and Leinwand L.A. Hypertrophy, fibrosis, and sudden cardiac death in response to pathological stimuli in mice with mutations in cardiac troponin T. Circulation 110 15 (2004) 2102-2109
23. Izumo S., Nadal-Ginard B., and Mahdavi V. Protooncogene induction and reprogramming of cardiac gene expression produced by pressure overload. Proc Natl Acad Sci U S A 85 2 (1988) 339-343
24. Hinkle A., Goranson A., Butters C.A., and Tobacman L.S. Roles for the troponin tail domain in thin filament assembly and regulation. A deletional study of cardiac troponin T. J Biol Chem 274 11 (1999) 7157-7164
25. Tobacman L.S., Lin D., Butters C., Landis C., Back N., Pavlov D., et al. Functional consequences of troponin T mutations found in hypertrophic cardiomyopathy. J Biol Chem 274 40 (1999) 28363-28370
26. Javadpour M.M., Tardiff J.C., Pinz I., and Ingwall J.S. Decreased energetics in murine hearts bearing the R92Q mutation in cardiac troponin T. J Clin Invest 112 5 (2003) 768-775
27. Solaro R.J., Montgomery D.M., Wang L., Burkart E.M., Ke Y., Vahebi S., et al. Integration of pathways that signal cardiac growth with modulation of myofilament activity. J Nucl Cardiol 9 5 (2002) 523-533
28. de Tombe P.P., and Solaro R.J. Integration of cardiac myofilament activity and regulation with pathways signaling hypertrophy and failure. Ann Biomed Eng 28 8 (2000) 991-1001
29. Chandra M., Dong W.J., Pan B.S., Cheung H.C., and Solaro R.J. Effects of protein kinase A phosphorylation on signaling between cardiac troponin I and the N-terminal domain of cardiac troponin C. Biochemistry 36 43 (1997) 13305-13311
30. Kentish J.C., McCloskey D.T., Layland J., Palmer S., Leiden J.M., Martin A.F., et al. Phosphorylation of troponin I by protein kinase A accelerates relaxation and crossbridge cycle kinetics in mouse ventricular muscle. Circ Res 88 10 (2001) 1059-1065
31. Noland Jr. T.A., Guo X., Raynor R.L., Jideama N.M., Averyhart-Fullard V., Solaro R.J., et al. Cardiac troponin I mutants. Phosphorylation by protein kinases C and A and regulation of Ca(2+)-stimulated MgATPase of reconstituted actomyosin S-1. J Biol Chem 270 43 (1995) 25445-25454
32. Ke Y., Wang L., Pyle W.G., de Tombe P.P., and Solaro R.J. Intracellular localization and functional effects of P21-activated kinase-1 (Pak1) in cardiac myocytes. Circ Res 94 2 (2004) 194-200
33. Liu Q., and Hofmann P.A. Modulation of protein phosphatase 2a by adenosine A1 receptors in cardiomyocytes: role for p38 MAPK. Am J Physiol Heart Circ Physiol 285 1 (2003) H97-H103
34. 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 291 5 (2006) H2344-H2353
35. Jweied E.E., McKinney R.D., Walker L.A., Brodsky I., Geha A.S., Massad M.G., et al. Depressed cardiac myofilament function in human diabetes mellitus. Am J Physiol Heart Circ Physiol 289 6 (2005) H2478-H2483
36. van der Velden J., Papp Z., Zaremba R., Boontje N.M., de Jong J.W., Owen V.J., et al. Increased Ca2+-sensitivity of the contractile apparatus in end-stage human heart failure results from altered phosphorylation of contractile proteins. Cardiovasc Res 57 1 (2003) 37-47
37. Bodor G.S., Oakeley A.E., Allen P.D., Crimmins D.L., Ladenson J.H., and Anderson P.A. Troponin I phosphorylation in the normal and failing adult human heart. Circulation 96 5 (1997) 1495-1500
38. Zakhary D.R., Moravec C.S., Stewart R.W., and Bond M. Protein kinase A (PKA)-dependent troponin-I phosphorylation and PKA regulatory subunits are decreased in human dilated cardiomyopathy. Circulation 99 4 (1999) 505-510
39. McConnell B.K., Moravec C.S., and Bond M. Troponin I phosphorylation and myofilament calcium sensitivity during decompensated cardiac hypertrophy. Am J Physiol Heart Circ Physiol 274 2 (1998) H385-H396
40. Tomaselli G.F., and Zipes D.P. What causes sudden death in heart failure?. Circ Res 95 8 (2004) 754-763
41. Schillinger W., and Kogler H. Altered phosphorylation and Ca2+-sensitivity of myofilaments in human heart failure. Cardiovasc Res 57 1 (2003) 5-7
42. Gomes A.V., and Potter J.D. Molecular and cellular aspects of troponin cardiomyopathies. Ann N Y Acad Sci 1015 (2004) 214-224