Calcium sensitivity and the Frank-Starling mechanism of the heart are increased in titin N2B region-deficient mice

Journal of Molecular and Cellular Cardiology

Volumn 49, Issue 3, 2010, Pages 449-458

  Lee, Eun Jeong ^a   Peng, Jun ^a,d   Radke, Michael ^b   Gotthardt, Michael ^b,c   Granzier, Henk L ^a  

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

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c UNIVERSITY OF ARIZONA   (United States)

^d CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

Diastolic stiffness; Length dependent activation; Myofilament function

Indexed keywords

CALCIUM; CONNECTIN; CYCLIC AMP DEPENDENT PROTEIN KINASE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HEART CONTRACTION; HEART LEFT VENTRICLE VOLUME; HEART MUSCLE COMPLIANCE; HEART MUSCLE TENSION; ISOLATED HEART; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SARCOMERE LENGTH; STARLING LAW;

MUS;

EID: 77955277122     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2010.05.006     Document Type: Article

References (48)

1. Solaro R.J., Rarick H.M. Troponin and tropomyosin: proteins that switch on and tune in the activity of cardiac myofilaments. Circ Res 1998, 83:471-480.
2. de Tombe P.P., Mateja R.D., Tachampa K., Mou Y.A., Farman G.P., Irving T.C. Myofilament length dependent activation. J Mol Cell Cardiol 2010, 48:851-858.
3. Allen D.G., Kentish J.C. The cellular basis of the length-tension relation in cardiac muscle. J Mol Cell Cardiol 1985, 17:821-840.
4. Shiels H.A., White E. The Frank-Starling mechanism in vertebrate cardiac myocytes. J Exp Biol 2008, 211:2005-2013.
5. Kentish J.C., ter Keurs H.E., Ricciardi L., Bucx J.J., Noble M.I. Comparison between the sarcomere length-force relations of intact and skinned trabeculae from rat right ventricle. Influence of calcium concentrations on these relations. Circ Res 1986, 58:755-768.
6. Allen D.G., Blinks J.R. Calcium transients in aequorin-injected frog cardiac muscle. Nature 1978, 273:509-513.
7. Allen D.G., Kurihara S. The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle. J Physiol 1982, 327:79-94.
8. Terui T., Sodnomtseren M., Matsuba D., Udaka J., Ishiwata S., Ohtsuki I., Kurihara S., Fukuda N. Troponin and titin coordinately regulate length-dependent activation in skinned porcine ventricular muscle. J Gen Physiol 2008, 131:275-283.
9. Tachampa K., Wang H., Farman G.P., de Tombe P.P. Cardiac troponin I threonine 144: role in myofilament length dependent activation. Circ Res 2007, 101:1081-1083.
10. Cazorla O., Szilagyi S., Vignier N., Salazar G., Kramer E., Vassort G., Carrier L., Lacampagne A. Length and protein kinase A modulations of myocytes in cardiac myosin binding protein C-deficient mice. Cardiovasc Res 2006, 69:370-380.
11. Ait Mou Y., le Guennec J.Y., Mosca E., de Tombe P.P., Cazorla O. Differential contribution of cardiac sarcomeric proteins in the myofibrillar force response to stretch. Pflugers Arch 2008, 457:25-36.
12. Cazorla O., Vassort G., Garnier D., Le Guennec J.Y. Length modulation of active force in rat cardiac myocytes: is titin the sensor?. J Mol Cell Cardiol 1999, 31:1215-1227.
13. Cazorla O., Wu Y., Irving T.C., Granzier H. Titin-based modulation of calcium sensitivity of active tension in mouse skinned cardiac myocytes. Circ Res 2001, 88:1028-1035.
14. Fukuda N., Sasaki D., Ishiwata S., Kurihara S. Length dependence of tension generation in rat skinned cardiac muscle: role of titin in the Frank-Starling mechanism of the heart. Circulation 2001, 104:1639-1645.
15. Fukuda N., Wu Y., Farman G., Irving T.C., Granzier H. Titin isoform variance and length dependence of activation in skinned bovine cardiac muscle. J Physiol 2003, 553:147-154.
16. Fukuda N., Granzier H. Role of the giant elastic protein titin in the Frank-Starling mechanism of the heart. Curr Vasc Pharmacol 2004, 2:135-139.
17. Granzier H.L., Labeit S. The giant protein titin: a major player in myocardial mechanics, signaling, and disease. Circ Res 2004, 94:284-295.
18. Furst D.O., Osborn M., Nave R., Weber K. The organization of titin filaments in the half-sarcomere revealed by monoclonal antibodies in immunoelectron microscopy: a map of ten nonrepetitive epitopes starting at the Z line extends close to the M line. J Cell Biol 1988, 106:1563-1572.
19. Trombitas K., Jin J.P., Granzier H. The mechanically active domain of titin in cardiac muscle. Circ Res 1995, 77:856-861.
20. Radke M.H., Peng J., Wu Y., McNabb M., Nelson O.L., Granzier H., Gotthardt M. Targeted deletion of titin N2B region leads to diastolic dysfunction and cardiac atrophy. Proc Natl Acad Sci U S A 2007, 104:3444-3449.
21. van Heerebeek L., Hamdani N., Handoko M.L., Falcao-Pires I., Musters R.J., Kupreishvili K., Ijsselmuiden A.J., Schalkwijk C.G., Bronzwaer J.G., Diamant M., Borbely A., van der Velden J., Stienen G.J., Laarman G.J., Niessen H.W., Paulus W.J. Diastolic stiffness of the failing diabetic heart: importance of fibrosis, advanced glycation end products, and myocyte resting tension. Circulation 2008, 117:43-51.
22. Borbely A., Falcao-Pires I., van Heerebeek L., Hamdani N., Edes I., Gavina C., Leite-Moreira A.F., Bronzwaer J.G., Papp Z., van der Velden J., Stienen G.J., Paulus W.J. Hypophosphorylation of the Stiff N2B titin isoform raises cardiomyocyte resting tension in failing human myocardium. Circ Res 2009, 104:780-786.
23. Cazorla O., Freiburg A., Helmes M., Centner T., McNabb M., Wu Y., Trombitas K., Labeit S., Granzier H. Differential expression of cardiac titin isoforms and modulation of cellular stiffness. Circ Res 2000, 86:59-67.
24. 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. Biophys J 2000, 79:3226-3234.
25. 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.
26. 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.
27. Fukuda N., Wu Y., Nair P., Granzier H.L. Phosphorylation of titin modulates passive stiffness of cardiac muscle in a titin isoform-dependent manner. J Gen Physiol 2005, 125:257-271.
28. Kruger M., Kotter S., Grutzner A., Lang P., Andresen C., Redfield M.M., Butt E., dos Remedios C.G., Linke W.A. Protein kinase G modulates human myocardial passive stiffness by phosphorylation of the titin springs. Circ Res 2009, 104:87-94.
29. 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. 17 p following 638.
30. Fukuda N., Wu Y., Farman G., Irving T.C., Granzier H. Titin-based modulation of active tension and interfilament lattice spacing in skinned rat cardiac muscle. Pflugers Arch 2005, 449:449-457.
31. Warren C.M., Krzesinski P.R., Greaser M.L. Vertical agarose gel electrophoresis and electroblotting of high-molecular-weight proteins. Electrophoresis 2003, 24:1695-1702.
32. 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. Circ Res 2004, 94:505-513.
33. Granzier H.L., Pollack G.H. Effect of active pre-shortening on isometric and isotonic performance of single frog muscle fibres. J Physiol 1989, 415:299-327.
34. Fabiato A., Fabiato F. Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells. J Physiol (Paris) 1979, 75:463-505.
35. Gao W.D., Perez N.G., Marban E. Calcium cycling and contractile activation in intact mouse cardiac muscle. J Physiol 1998, 507(Pt 1):175-184.
36. Helmes M., Trombitas K., Centner T., Kellermayer M., Labeit S., Linke W.A., Granzier H. Mechanically driven contour-length adjustment in rat cardiac titin's unique N2B sequence: titin is an adjustable spring. Circ Res 1999, 84:1339-1352.
37. Trombitas K., Freiburg A., Centner T., Labeit S., Granzier H. Molecular dissection of N2B cardiac titin's extensibility. Biophys J 1999, 77:3189-3196.
38. Linke W.A., Stockmeier M.R., Ivemeyer M., Hosser H., Mundel P. Characterizing titin's I-band Ig domain region as an entropic spring. J Cell Sci 1998, 111(Pt 11):1567-1574.
39. Kellermayer M.S., Smith S.B., Bustamante C., Granzier H.L. Complete unfolding of the titin molecule under external force. J Struct Biol 1998, 122:197-205.
40. Konhilas J.P., Irving T.C., de Tombe P.P. Myofilament calcium sensitivity in skinned rat cardiac trabeculae: role of interfilament spacing. Circ Res 2002, 90:59-65.
41. Konhilas J.P., Irving T.C., de Tombe P.P. Length-dependent activation in three striated muscle types of the rat. J Physiol 2002, 544:225-236.
42. Yamasaki R., Berri M., Wu Y., Trombitas K., McNabb M., Kellermayer M.S., Witt C., Labeit D., Labeit S., Greaser M., Granzier H. Titin-actin interaction in mouse myocardium: passive tension modulation and its regulation by calcium/S100A1. Biophys J 2001, 81:2297-2313.
43. Linke W.A., Kulke M., Li H., Fujita-Becker S., Neagoe C., Manstein D.J., Gautel M., Fernandez J.M. PEVK domain of titin: an entropic spring with actin-binding properties. J Struct Biol 2002, 137:194-205.
44. Kulke M., Fujita-Becker S., Rostkova E., Neagoe C., Labeit D., Manstein D.J., Gautel M., Linke W.A. Interaction between PEVK-titin and actin filaments: origin of a viscous force component in cardiac myofibrils. Circ Res 2001, 89:874-881.
45. Campbell K.B., Taheri H., Kirkpatrick R.D., Slinker B.K. Single perturbed beat vs. steady-state beats for assessing systolic function in the isolated heart. Am J Physiol 1992, 262:H1631-H1639.
46. Kockskamper J., Khafaga M., Grimm M., Elgner A., Walther S., Kockskamper A., von Lewinski D., Post H., Grossmann M., Dorge H., Gottlieb P.A., Sachs F., Eschenhagen T., Schondube F.A., Pieske B. Angiotensin II and myosin light-chain phosphorylation contribute to the stretch-induced slow force response in human atrial myocardium. Cardiovasc Res 2008, 79:642-651.
47. Hanft L.M., McDonald K.S. Sarcomere length dependence of power output is increased after PKA treatment in rat cardiac myocytes. Am J Physiol Heart Circ Physiol 2009, 296:H1524-H1531.
48. Sarnoff S.J. Myocardial contractility as described by ventricular function curves; observations on Starling's law of the heart. Physiol Rev 1955, 35:107-122.