Hyperphosphorylation of mouse cardiac titin contributes to transverse aortic constriction-induced diastolic dysfunction

Circulation Research

Volumn 109, Issue 8, 2011, Pages 858-866

  Hudson, Bryan ^a   Hidalgo, Carlos ^a   Saripalli, Chandra ^a   Granzier, Henk ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

diastolic dysfunction; passive stiffness; titin

Indexed keywords

CONNECTIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; PROTEIN KINASE C;

ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA CONSTRICTION; ARTICLE; CONGESTIVE HEART FAILURE; CONTROLLED STUDY; DIASTOLIC DYSFUNCTION; HEART LEFT VENTRICLE; HEART MUSCLE COMPLIANCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MICROARRAY; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING;

ANIMALS; AORTIC DISEASES; HEART FAILURE, DIASTOLIC; MALE; MICE; MICE, INBRED C57BL; MUSCLE PROTEINS; MYOCARDIUM; PHOSPHORYLATION; PROTEIN KINASES; VENTRICULAR DYSFUNCTION, LEFT;

EID: 80053573173     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.111.246819     Document Type: Article

References (42)

1. Mann DL, ed. Heart failure: A companion to Braunwald's heart disease. Philadelphia, PA: Saunders; 2004.
2. Katz AM, Zile MR. New molecular mechanism in diastolic heart failure. Circulation. 2006;113:1922-1925.
3. Zile MR, Baicu CF, Bonnema DD. Diastolic heart failure: definitions and terminology. Prog Cardiovasc Dis. 2005;47:307-313. (Pubitemid 40884559)
4. Bursi F, Weston SA, Redfield MM, Jacobsen SJ, Pakhomov S, Nkomo VT, Meverden RA, Roger VL. Systolic and diastolic heart failure in the community. JAMA. 2006;296:2209-2216. (Pubitemid 44708051)
5. Kass DA, Bronzwaer JG, Paulus WJ. What mechanisms underlie diastolic dysfunction in heart failure? Circ Res. 2004;94:1533-1542. (Pubitemid 38856960)
6. Zile MR, Baicu CF, Gaasch WH. Diastolic heart failure-abnormalities in active relaxation and passive stiffness of the left ventricle. N Engl J Med. 2004;350:1953-1959.
7. Paulus WJ, van Ballegoij JJ. Treatment of heart failure with normal ejection fraction: an inconvenient truth! J Am Coll Cardiol. 2010;55: 526-537.
8. LeWinter MM, Granzier H. Cardiac titin: a multifunctional giant. Circulation. 2010;121:2137-2145.
9. Trombitás K, Redkar A, Centner T, Wu Y, Labeit S, Granzier H. Extensibility of isoforms of cardiac titin: variation in contour length of molecular subsegments provides a basis for cellular passive stiffness diversity. Biophys J. 2000;79:3226-3234.
10. Trombitás K, Wu Y, Labeit D, Labeit S, Granzier H. Cardiac titin isoforms are coexpressed in the half-sarcomere and extend independently. Am J Physiol Heart Circ Physiol. 2001;281:H1793-H1799.
11. Yamasaki R, Wu Y, McNabb M, Greaser M, Labeit S, Granzier H. Protein kinase A phosphorylates titin's cardiac-specific N2B domain and reduces passive tension in rat cardiac myocytes. Circ Res. 2002;90: 1181-1188. (Pubitemid 34786903)
12. Kruger M, Kotter S, Grutzner A, Lang P, Andresen C, Redfield MM, Butt E, dos Remedios CG, Linke WA. Protein kinase G modulates human myocardial passive stiffness by phosphorylation of the titin springs. Circ Res. 2009;104:87-94.
13. Borbely A, Falcao-Pires I, van Heerebeek L, Hamdani N, Edes I, Gavina C, Leite-Moreira AF, Bronzwaer JG, Papp Z, van der Velden J, Stienen GJ, Paulus WJ. Hypophosphorylation of the Stiff N2B titin isoform raises cardiomyocyte resting tension in failing human myocardium. Circ Res. 2009;104:780-786.
14. Anderson BR, Bogomolovas J, Labeit S, Granzier H. The Effects of PKCalpha Phosphorylation on the Extensibility of Titin's PEVK Element. J Struct Biol. 2010;170:270-277.
15. Hidalgo C, Hudson B, Bogomolovas J, Zhu Y, Anderson B, Greaser M, Labeit S, Granzier H. PKC phosphorylation of titin's PEVK element: a novel and conserved pathway for modulating myocardial stiffness. Circ Res. 2009;105:631-638.
16. Hudson BD, Hidalgo CG, Gotthardt M, Granzier HL. Excision of titin's cardiac PEVK spring element abolishes PKCalpha-induced increases in myocardial stiffness. J Mol Cell Cardiol. 2009;48:978-982.
17. Liao Y, Ishikura F, Beppu S, Asakura M, Takashima S, Asanuma H, Sanada S, Kim J, Ogita H, Kuzuya T, Node K, Kitakaze M, Hori M. Echocardiographic assessment of LV hypertrophy and function in aorticbanded mice: necropsy validation. Am J Physiol Heart Circ Physiol. 2002;282:H1703-H1708. (Pubitemid 34654838)
18. Radke MH, Peng J, Wu Y, McNabb M, Nelson OL, Granzier H, Gotthardt M. Targeted deletion of titin N2B region leads to diastolic dysfunction and cardiac atrophy. Proc Natl Acad Sci USA. 2007;104: 3444-3449. (Pubitemid 46364178)
19. Lahmers S, Wu Y, Call DR, Labeit S, Granzier H. Developmental control of titin isoform expression and passive stiffness in fetal and neonatal myocardium. Circ Res. 2004;94:505-513. (Pubitemid 38326286)
20. Buck D, Hudson BD, Ottenheijm CA, Labeit S, Granzier H. Differential splicing of the large sarcomeric protein nebulin during skeletal muscle development. J Struct Biol. 2010;170:325-333.
21. Chung CS, Granzier HL. Contribution of titin and extracellular matrix to passive pressure and measurement of sarcomere length in the mouse left ventricle. J Mol Cell Cardiol. 2011;50:731-739.
22. Krenz M, Robbins J. Impact of beta-myosin heavy chain expression on cardiac function during stress. J Am Coll Cardiol. 2004;44:2390-2397. (Pubitemid 39647615)
23. Little WC, Ohno M, Kitzman DW, Thomas JD, Cheng CP. Determination of left ventricular chamber stiffness from the time for deceleration of early left ventricular filling. Circulation. 1995;92:1933-1939.
24. Belin RJ, Sumandea MP, Allen EJ, Schoenfelt K, Wang H, Solaro RJ, de Tombe PP. Augmented protein kinase C-alpha-induced myofilament protein phosphorylation contributes to myofilament dysfunction in experimental congestive heart failure. Circ Res. 2007;101:195-204. (Pubitemid 47196587)
25. Giordano FJ. Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Invest. 2005;115:500-508. (Pubitemid 40322219)
26. Grutzner A, Garcia-Manyes S, Kotter S, Badilla CL, Fernandez JM, Linke WA. Modulation of titin-based stiffness by disulfide bonding in the cardiac titin N2-B unique sequence. Biophys J. 2009;97:825-834.
27. Granzier HL, Irving TC. Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments. Biophys J. 1995;68:1027-1044.
28. Wu Y, Cazorla O, Labeit D, Labeit S, Granzier H. Changes in titin and collagen underlie diastolic stiffness diversity of cardiac muscle. J Mol Cell Cardiol. 2000;32:2151-2162.
29. Xia Y, Lee K, Li N, Corbett D, Mendoza L, Frangogiannis NG. Characterization of the inflammatory and fibrotic response in a mouse model of cardiac pressure overload. Histochem Cell Biol. 2009;131:471-481.
30. Granzier HL, Radke MH, Peng J, Westermann D, Nelson OL, Rost K, King NM, Yu Q, Tschope C, McNabb M, Larson DF, Labeit S, Gotthardt M. Truncation of titin's elastic PEVK region leads to cardiomyopathy with diastolic dysfunction. Circ Res. 2009;105:557-564.
31. Fukuda N, Wu Y, Nair P, Granzier HL. Phosphorylation of titin modulates passive stiffness of cardiac muscle in a titin isoform-dependent manner. J Gen Physiol. 2005;125:257-271 (Pubitemid 40388308)
32. Owan TE, Hodge DO, Herges RM, Jacobsen SJ, Roger VL, Redfield MM. Trends in prevalence and outcome of heart failure with preserved ejection fraction. N Engl J Med. 2006;355:251-259. (Pubitemid 44079340)
33. Bradshaw AD, Baicu CF, Rentz TJ, Van Laer AO, Boggs J, Lacy JM, Zile MR. Pressure overload-induced alterations in fibrillar collagen content and myocardial diastolic function: role of secreted protein acidic and rich in cysteine (SPARC) in post-synthetic procollagen processing. Circulation. 2009;119:269-280.
34. van Deel ED, de Boer M, Kuster DW, Boontje NM, Holemans P, Sipido KR, van der Velden J, Duncker DJ. Exercise training does not improve cardiac function in compensated or decompensated left ventricular hypertrophy induced by aortic stenosis. J Mol Cell Cardiol. 2011;50: 1017-1025.
35. Wu Y, Bell SP, Trombitas K, Witt CC, Labeit S, LeWinter MM, Granzier H. Changes in titin isoform expression in pacing-induced cardiac failure give rise to increased passive muscle stiffness. Circulation. 2002;106:1384-1389. (Pubitemid 35013043)
36. Warren CM, Jordan MC, Roos KP, Krzesinski PR, Greaser ML. Titin isoform expression in normal and hypertensive myocardium. Cardiovasc Res. 2003;59:86-94. (Pubitemid 36776375)
37. Neagoe C, Kulke M, del Monte F, Gwathmey JK, de Tombe PP, Hajjar RJ, Linke WA. Titin isoform switch in ischemic human heart disease. Circulation. 2002;106:1333-1341. (Pubitemid 35013035)
38. Nagueh SF, Shah G, Wu Y, Torre-Amione G, King NM, Lahmers S, Witt CC, Becker K, Labeit S, Granzier HL. Altered titin expression, myocardial stiffness, and left ventricular function in patients with dilated cardiomyopathy. Circulation. 2004;110:155-162. (Pubitemid 38924583)
39. Makarenko I, Opitz CA, Leake MC, Neagoe C, Kulke M, Gwathmey JK, del Monte F, Hajjar RJ, Linke WA. Passive stiffness changes caused by upregulation of compliant titin isoforms in human dilated cardiomyopathy hearts. Circ Res. 2004;95:708-716. (Pubitemid 39331931)
40. Hamdani N, de Waard M, Messer AE, Boontje NM, Kooij V, van Dijk S, Versteilen A, Lamberts R, Merkus D, Dos Remedios C, Duncker DJ, Borbely A, Papp Z, Paulus W, Stienen GJ, Marston SB, van der Velden J. Myofilament dysfunction in cardiac disease from mice to men. J Muscle Res Cell Motil. 2008;29:189-201.
41. Nagayama T, Hsu S, Zhang M, Koitabashi N, Bedja D, Gabrielson KL, Takimoto E, Kass DA. Sildenafil stops progressive chamber, cellular, and molecular remodeling and improves calcium handling and function in hearts with pre-existing advanced hypertrophy caused by pressure overload. J Am Coll Cardiol. 2009;53:207-215.
42. House C, Wettenhall RE, Kemp BE. The influence of basic residues on the substrate specificity of protein kinase C. J Biol Chem. 1987;262:772-777. (Pubitemid 17005252)