Tuning the molecular giant titin through phosphorylation: Role in health and disease

Trends in Cardiovascular Medicine

Volumn 23, Issue 5, 2013, Pages 165-171

  Hidalgo, Carlos ^a   Granzier, Henk ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

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

CONGESTIVE CARDIOMYOPATHY; ENZYME PHOSPHORYLATION; HEART DISEASE; HEART EJECTION FRACTION; HEART FAILURE; HEART MUSCLE CELL; HEART MUSCLE COMPLIANCE; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; SARCOMERE;

ANIMALS; CONNECTIN; HEART DISEASES; HUMANS; MYOCARDIAL CONTRACTION; MYOCARDIUM; OXIDATION-REDUCTION; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN KINASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; VENTRICULAR FUNCTION;

EID: 84878871182     PISSN: 10501738     EISSN: 18732615     Source Type: Journal    
DOI: 10.1016/j.tcm.2012.10.005     Document Type: Review

References (46)

1. Bang M.L., Centner T., Fornoff F., Geach A.J., Gotthardt M., McNabb M., et al. The complete gene sequence of titin, expression of an unusual approximately 700-kDa titin isoform, and its interaction with obscurin identify a novel Z-line to I-band linking system. Circulation Research 2001, 89(11):1065-1072.
2. 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. Circulation Research 2007, 101(2):195-204.
3. Bishu K., Hamdani N., Mohammed S.F., Kruger M., Ohtani T., Ogut O., et al. Sildenafil and B-type natriuretic peptide acutely phosphorylate titin and improve diastolic distensibility in vivo. Circulation 2011, 124(25):2882-2891.
4. Borbely A., Falcao-Pires I., van Heerebeek L., Hamdani N., Edes I., Gavina C., et al. Hypophosphorylation of the Stiff N2B titin isoform raises cardiomyocyte resting tension in failing human myocardium. Circulation Research 2009, 104(6):780-786.
5. Borbely A., van der Velden J., Papp Z., Bronzwaer J.G., Edes I., Stienen G.J., et al. Cardiomyocyte stiffness in diastolic heart failure. Circulation 2005, 111(6):774-781.
6. Cazorla O., Freiburg A., Helmes M., Centner T., McNabb M., Wu Y., et al. Differential expression of cardiac titin isoforms and modulation of cellular stiffness. Circulation Research 2000, 86(1):59-67.
7. Couchonnal L.F., Anderson M.E. The role of calmodulin kinase II in myocardial physiology and disease. Physiology (Bethesda) 2008, 23:151-159.
8. Fujita H., Labeit D., Gerull B., Labeit S., Granzier H.L. Titin isoform-dependent effect of calcium on passive myocardial tension. American Journal of Physiology Heart and Circulatory Physiology 2004, 287(6):H2528-H2534.
9. Fukuda N., Wu Y., Nair P., Granzier H.L. Phosphorylation of titin modulates passive stiffness of cardiac muscle in a titin isoform-dependent manner. Journal of General Physiology 2005, 125(3):257-271.
10. Gautel M., Goulding D., Bullard B., Weber K., Furst D.O. The central Z-disk region of titin is assembled from a novel repeat in variable copy numbers. Journal of Cell Science 1996, 109(Pt. 11):2747-2754.
11. Gautel M., Leonard K., Labeit S. Phosphorylation of KSP motifs in the C-terminal region of titin in differentiating myoblasts. EMBO Journal 1993, 12(10):3827-3834.
12. Granzier H.L., Irving T.C. Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments. Biophysical Journal 1995, 68(3):1027-1044.
13. Greaser M.L., Berri M., Warren C.M., Mozdziak P.E. Species variations in cDNA sequence and exon splicing patterns in the extensible I-band region of cardiac titin: relation to passive tension. Journal of Muscle Research and Cell Motility 2002, 23(5-6):473-482.
14. Greaser M.L., Krzesinski P.R., Warren C.M., Kirkpatrick B., Campbell K.S., Moss R.L. Developmental changes in rat cardiac titin/connectin: transitions in normal animals and in mutants with a delayed pattern of isoform transition. Journal of Muscle Research and Cell Motility 2005, 26(6-8):325-332.
15. Grieve D.J., Shah A.M. Oxidative stress in heart failure. More than just damage. European Heart Journal 2003, 24(24):2161-2163.
16. Grutzner A., Garcia-Manyes S., Kotter S., Badilla C.L., Fernandez J.M., Linke W.A. Modulation of titin-based stiffness by disulfide bonding in the cardiac titin N2-B unique sequence. Biophysical Journal 2009, 97(3):825-834.
17. Hidalgo C., Hudson B., Bogomolovas J., Zhu Y., Anderson B., Greaser M., et al. PKC phosphorylation of titin's PEVK element: a novel and conserved pathway for modulating myocardial stiffness. Circulation Research 2009, 105(7):631-638. 617 p. following 638.
18. Hidalgo C.G., Methawasin M., Chung C., Bogomolavas J., Gasch A., Labeit S., et al. The multifunctional calcium/calmodulin-dependent protein kinase II delta (CaMKIId) phosphorylates titin N2B and PEVK spring elements. Biophysical Journal 2012, 102(3):559a.
19. Horowits R., Podolsky R.J. The positional stability of thick filaments in activated skeletal muscle depends on sarcomere length: evidence for the role of titin filaments. Journal of Cell Biology 1987, 105(5):2217-2223.
20. Hudson B., Hidalgo C., Saripalli C., Granzier H. Hyperphosphorylation of mouse cardiac titin contributes to transverse aortic constriction-induced diastolic dysfunction. Circulation Research 2011, 109(8):858-866.
21. Hudson B.D., Hidalgo C.G., Gotthardt M., Granzier H.L. Excision of titin's cardiac PEVK spring element abolishes PKCalpha-induced increases in myocardial stiffness. Journal of Molecular and Cellular Cardiology 2010, 48(5):972-978.
22. Kellermayer M.S., Smith S.B., Bustamante C., Granzier H.L. Complete unfolding of the titin molecule under external force. Journal of Structural Biology 1998, 122(1-2):197-205.
23. Kruger M., Kotter S., Grutzner A., Lang P., Andresen C., Redfield M.M., et al. Protein kinase G modulates human myocardial passive stiffness by phosphorylation of the titin springs. Circulation Research 2009, 104(1):87-94.
24. Kruger M., Linke W.A. Protein kinase-A phosphorylates titin in human heart muscle and reduces myofibrillar passive tension. Journal of Muscle Research and Cell Motility 2006, 27(5-7):435-444.
25. Labeit D., Watanabe K., Witt C., Fujita H., Wu Y., Lahmers S., et al. Calcium-dependent molecular spring elements in the giant protein titin. Proceedings of the National Academy of Sciences of the United States of America 2003, 100(23):13716-13721.
26. Labeit S., Kolmerer B. Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science 1995, 270(5234):293-296.
27. Lahmers S., Wu Y., Call D.R., Labeit S., Granzier H. Developmental control of titin isoform expression and passive stiffness in fetal and neonatal myocardium. Circulation Research 2004, 94(4):505-513.
28. LeWinter M.M., Wu Y., Labeit S., Granzier H. Cardiac titin: structure, functions and role in disease. Clinica Chimica Acta 2007, 375(1-2):1-9.
29. Makarenko I., Opitz C.A., Leake M.C., Neagoe C., Kulke M., Gwathmey J.K., et al. Passive stiffness changes caused by upregulation of compliant titin isoforms in human dilated cardiomyopathy hearts. Circulation Research 2004, 95(7):708-716.
30. Molkentin J.D., Dorn G.W. Cytoplasmic signaling pathways that regulate cardiac hypertrophy. Annual Review of Physiology 2001, 63:391-426.
31. Nagueh S.F., Shah G., Wu Y., Torre-Amione G., King N.M., Lahmers S., et al. Altered titin expression, myocardial stiffness, and left ventricular function in patients with dilated cardiomyopathy. Circulation 2004, 110(2):155-162.
32. Neagoe C., Kulke M., del Monte F., Gwathmey J.K., de Tombe P.P., Hajjar R.J., et al. Titin isoform switch in ischemic human heart disease. Circulation 2002, 106(11):1333-1341.
33. Nedrud J., Labeit S., Gotthardt M., Granzier H. Mechanics on myocardium deficient in the N2B region of titin: the cardiac-unique spring element improves efficiency of the cardiac cycle. Biophysical Journal 2011, 101(6):1385-1392.
34. Raskin A, Lange. S, Banares K, Lyon RC, Zieseniss A, Lee L.K. et al.2012; A novel mechanism involving four and a half lim domain protein-1 and extracellular-signal-regulated kinase-2 regulates titin phosphorylation and mechanics Journal of Biological Chemistry.
35. Sebestyen M.G., Wolff J.A., Greaser M.L. Characterization of a 5.4kb cDNA fragment from the Z-line region of rabbit cardiac titin reveals phosphorylation sites for proline-directed kinases. Journal of Cell Science 1995, 108(Pt. 9):3029-3037.
36. Selby D.E., Palmer B.M., LeWinter M.M., Meyer M. Tachycardia-induced diastolic dysfunction and resting tone in myocardium from patients with a normal ejection fraction. Journal of the American College of Cardiology 2011, 58(2):147-154.
37. Sheikh F., Raskin A., Chu P.H., Lange S., Domenighetti A.A., Zheng M., et al. An FHL1-containing complex within the cardiomyocyte sarcomere mediates hypertrophic biomechanical stress responses in mice. Journal of Clinical Investigation 2008, 118(12):3870-3880.
38. Trombitas K., Freiburg A., Centner T., Labeit S., Granzier H. Molecular dissection of N2B cardiac titin's extensibility. Biophysical Journal 1999, 77(6):3189-3196.
39. Trombitas 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. Biophysical Journal 2000, 79(6):3226-3234.
40. Trombitas K., Wu Y., Labeit D., Labeit S., Granzier H. Cardiac titin isoforms are coexpressed in the half-sarcomere and extend independently. American Journal of Physiology Heart and Circulatory Physiology 2001, 281(4):H1793-1799.
41. Tskhovrebova L., Trinick J. Flexibility and extensibility in the titin molecule: analysis of electron microscope data. Journal of Molecular Biology 2001, 310(4):755-771.
42. van Heerebeek L, Franssen CP, Hamdani N, Verheugt FW, Somsen GA, Paulus WJ. Molecular and cellular basis for diastolic dysfunction. Current Heart Failure Reports 2012;9(4):293-302.
43. Watanabe K., Muhle-Goll C., Kellermayer M.S., Labeit S., Granzier H. Different molecular mechanics displayed by titin's constitutively and differentially expressed tandem Ig segments. Journal of Structural Biology 2002, 137(1-2):248-258.
44. Wu Y., Peng J., Campbell K.B., Labeit S., Granzier H. Hypothyroidism leads to increased collagen-based stiffness and re-expression of large cardiac titin isoforms with high compliance. Journal of Molecular and Cellular Cardiology 2007, 42(1):186-195.
45. 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. Circulatory Research 2002, 90(11):1181-1188.
46. Zile M.R., Gottdiener J.S., Hetzel S.J., McMurray J.J., Komajda M., McKelvie R., et al. Prevalence and significance of alterations in cardiac structure and function in patients with heart failure and a preserved ejection fraction. Circulation 2011, 124(23):2491-2501.