Plasticity of cardiac titin/connectin in heart development

Journal of Muscle Research and Cell Motility

Volumn 26, Issue 6-8, 2005, Pages 333-342

  Opitz, Christiane A ^a   Linke, Wolfgang A ^b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CONNECTIN; ISOPROTEIN; MUSCLE PROTEIN; N2BA PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; CHICKEN; CONFERENCE PAPER; CONTROLLED STUDY; HEART DEVELOPMENT; HEART LEFT VENTRICLE; HEART MUSCLE; HEART RIGHT ATRIUM; MAMMAL; MOUSE; MUSCLE FIBRIL; NONHUMAN; PERINATAL DEVELOPMENT; PLASTICITY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; RAT; SARCOMERE; SIGNAL TRANSDUCTION; SWINE;

ANIMALS; ANIMALS, NEWBORN; CHICK EMBRYO; CHICKENS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEART VENTRICLES; MICE; MUSCLE CONTRACTION; MUSCLE PROTEINS; MUSCLE, SKELETAL; MYOFIBRILS; PROTEIN ISOFORMS; PROTEIN KINASES; RABBITS; RATS; SWINE;

MAMMALIA; SUS SCROFA;

EID: 33745726394     PISSN: 01424319     EISSN: 15732657     Source Type: Journal    
DOI: 10.1007/s10974-005-9040-7     Document Type: Conference Paper

References (80)

1. Agarkova I, Auerbach D, Ehler E and Perriard JC (2000) A novel marker for vertebrate embryonic heart, the EH-myomesin isoform. J Biol Chem 275: 10256-10264.
2. Anderson PA, Manring A, Glick KL and Crenshaw CC Jr (1982) Biophysics of the developing heart III. A comparison of the left ventricular dynamics of the foetal and neonatal lamb heart. Am J Obstet Gynecol 143: 195-203.
3. Bang ML, Centner T, Fornoff F, Geach AJ, Gotthardt M, McNabb M, Witt CC, Labeit D, Gregorio CC, Granzier H and Labeit S (2001) 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. Circ Res 89: 1065-1072.
4. Borg TK, Gay RE and Johnson LD (1982) Changes in the distribution of fibronectin and collagen during development of neonatal rat heart. Coll Relat Res 2: 211-218.
5. Cappelli V, Bottinelli R, Poggesi C, Moggio R and Reggiani C (1989) Shortening velocity and myosin and myofibrillar ATPase activity related to myosin isoenzyme composition during postnatal development in rat myocardium. Circ Res 65: 446-457.
6. Carrier L, Boheler KR, Chassagne C, de la Bastie D, Wisnewsky C, Lakatta EG and Schwartz K (1992) Expression of sarcomeric actin isogenes in the rat heart with development and senescence. Circ Res 70: 999-1005.
7. Carver W, Terracio L and Borg TK (1993) Expression and accumulation of interstitial collagen in the neonatal rat heart. Anat Rec 236: 511-520.
8. Cazorla O, Freiburg A, Helmes M, Centner T, McNabb M, Wu Y, Trombitas K, Labeit S and Granzier H (2000) Differential expression of cardiac titin isoforms and modulation of cellular stiffness. Circ Res 86: 59-67.
9. Cazorla O, Wu Y, Irving TC and Granzier H (2001) Titin-based modulation of calcium sensitivity of active tension in mouse skinned cardiac myocytes. Circ Res 88: 1028-1035.
10. Engelmann GL (1993) Coordinate gene expression during neonatal rat heart development. A possible role for the myocyte in extracellular matrix biogenesis and capillary angiogenesis. Cardiovasc Res 27: 1598-1605.
11. Fisher DJ and Towbin J (1988) Maturation of the heart. Clin Perinatol 15: 421-446.
12. Freiburg A, Trombitas K, Hell W, Cazorla O, Fougerousse F, Centner T, Kolmerer B, Witt C, Beckmann JS, Gregorio CC, Granzier H and Labeit S (2000) Series of exon-skipping events in the elastic spring region of titin as the structural basis for myofibrillar elastic diversity. Circ Res 86: 1114-1121.
13. Fukuda N, Sasaki D, Ishiwata S and Kurihara S (2001) Length dependence of tension generation in rat skinned cardiac muscle: role of titin in the Frank-Starling mechanism of the heart. Circulation 104: 1639-1645.
14. Fukuda N, Wu Y, Farman G, Irving TC and Granzier HL (2003) Titin isoform variance and length dependence of activation in skinned bovine cardiac muscle. J Physiol 553: 147-154.
15. Funatsu T, Kono E, Higuchi H, Kimura S, Ishiwata S, Yoshioka T, Maruyama K and Tsukita S (1993) Elastic filaments in situ in cardiac muscle: deep-etch replica analysis in combination with selective removal of actin and myosin filaments. J Cell Biol 120: 711-724.
16. Fürst DO, Osborn M, Nave R and Weber K (1988) 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 106: 1563-1572.
17. Gautel M, Lehtonen E and Pietruschka F (1996) Assembly of the cardiac I-band region of titin/connectin: expression of the cardiac-specific regions and their relation to the elastic segments. J Muscle Res Cell Motil 17: 449-461.
18. Godt RE, Fogaca RT, Silva IK and Nosek TM (1993) Contraction of developing avian heart muscle. Comp Biochem Physiol A Mol Integr Physiol 105: 213-218.
19. Grant DA and Walker AM (1996) Pleural and pericardial pressures limit foetal right ventricular output. Circulation 94: 555-561.
20. Grant DA, Fauhere JC, Eede KJ, Tyberg JV and Walker AM (2001) Left ventricular stroke volume in the foetal sheep is limited by extracardiac constraint and arterial pressure. J Physiol 535: 231-239.
21. Grant DA, Kondo CS, Maloney JE, Walker AM and Tyberg JV (1992) Pulmonary and pericardial limitations to diastolic filling of the left ventricle in lamb. Circulation 86: 1615-1621.
22. Granzier HL and Irving TC (1995) Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments. Biophys J 68: 1027-1044.
23. Granzier HL and Labeit S (2004) The giant protein titin: a major player in myocardial mechanics, signaling, and disease. Circ Res 94: 284-295.
24. Greaser ML, Berri M, Warren CM and Mozdziak PE (2002) Species variations in cDNA sequence and exon splicing patterns in the extensible I-band region of cardiac titin: relation to passive tension. J Muscle Res Cell Motil 23: 473-482.
25. Hattori A, Ishii T, Tatsumi R and Takahashi K (1995) Changes in the molecular types of connectin and nebulin during development of chicken skeletal muscle. Biochim Biophys Acta 1244: 179-184.
26. Hoh JF, McGrath PA and Hale PT (1978) Electrophoretic analysis of multiple forms of rat cardiac myosin: effects of hypophysectomy and thyroxine replacement. J Mol Cell Cardiol 10: 1053-1076.
27. Horowits R, Kempner ES, Bisher ME and Podolsky RJ (1986) A physiological role for titin and nebulin in skeletal muscle. Nature 323: 160-164.
28. Itoh Y, Suzuki T, Kimura S, Ohashi K, Higuchi H, Sawada H, Shimizu T, Shibata M and Maruyama K (1988) Extensible and less-extensible domains of connectin filaments in stretched vertebrate skeletal muscle sarcomeres as detected by immunofluorescence and immunoelectron microscopy using monoclonal antibodies. J Biochem 104: 504-508.
29. Kellermayer MS, Smith SB, Granzier HL and Bustamante C (1997) Folding-unfolding transitions in single titin molecules characterized with laser tweezers. Science 276: 1112-1116.
30. Kirkpatrick SE, Covell JW and Friedman WF (1973) A new technique for the continuous assessment of foetal and neonatal heart performance. Am J Obstet Gynecol 116: 963-972.
31. Kulke M, Fujita-Becker S, Rostkova E, Neagoe C, Labeit D, Manstein DJ, Gautel M and Linke WA (2001) Interaction between PEVK-titin and actin filaments: origin of a viscous force component in cardiac myofibrils. Circ Res 89: 874-881.
32. Labeit S and Kolmerer B (1995) Titins, giant proteins in charge of muscle ultrastructure and elasticity. Science 270: 293-296.
33. Lahmers S, Wu Y, Call DR, Labeit S and Granzier H (2004) Developmental control of titin isoform expression and passive stiffness in foetal and neonatal myocardium. Circ Res 94: 505-513.
34. Li H, Linke WA, Oberhauser AF, Carrion-Vazquez M, Kerkvliet JG, Lu H, Marszalek PE and Fernandez JM (2002) Reverse engineering of the giant muscle protein titin. Nature 418: 998-1002.
35. Lim SS, Woodroofe MN and Lemanski LF (1983) An analysis of contractile proteins in developing chick heart by SDS polyacrylamide gel electrophoresis and electron microscopy. J Embryol Exp Morphol 77: 1-14.
36. Linke WA and Fernandez JM (2002) Cardiac titin: Molecular basis of elasticity and cellular contribution to elastic and viscous stiffness components in myocardium. J Muscle Res Cell Motil 23: 483-497.
37. Linke WA and Leake MC (2004) Multiple sources of passive stress relaxation in muscle fibers. Phys Med Biol 49: 3613-3627.
38. Linke WA, Ivemeyer M, Labeit S, Hinssen H, Rüegg JC and Gautel M (1997) Actin-titin interaction in cardiac myofibrils: Probing a physiological role. Biophys J 73: 905-919.
39. Linke WA, Ivemeyer M, Mundel P, Stockmeier MR and Kolmerer B (1998) Nature of PEVK-titin elasticity in skeletal muscle. Proc Natl Acad Sci USA 95: 8052-8057.
40. Linke WA, Ivemeyer M, Olivieri N, Kolmerer B, Rüegg JC and Labeit S (1996) Towards a molecular understanding of the elasticity of titin. J Mol Biol 261: 62-71.
41. Linke WA, Popov VI and Pollack GH (1994) Passive and active tension in single cardiac myofibrils. Biophys J 67: 782-792.
42. Linke WA, Rudy DE, Centner T, Gautel M, Witt C, Labeit S and Gregorio CC (1999) I-band titin in cardiac muscle is a three-element molecular spring and is critical for maintaining thin filament structure. J Cell Biol 146: 631-644.
43. Lompré AM, Nadal-Ginard B and Mahdavi V (1984) Expression of the cardiac ventricular α- and β-myosin heavy chain genes is developmentally and hormonally regulated. J Biol Chem 260: 6437-6446.
44. Lyons GE, Schiaffino S, Sassoon D, Barton P and Buckingham M (1990) Developmental regulation of myosin gene expression in mouse cardiac muscle. J Cell Biol 111: 2427-2436.
45. Makarenko I, Opitz CA, Leake MC, Neagoe C, Kulke M, Gwathmey JK, del Monte F, Hajjar RJ and Linke WA (2004) Passive stiffness changes caused by upregulation of compliant titin isoforms in human dilated cardiomyopathy hearts. Circ Res 95: 708-716.
46. Maruyama K, Matsubara S, Natori R, Nonomura Y, Kimura S, Ohashi K, Murakami F, Handa S and Eguchi G (1977a) Connectin, an elastic protein of muscle: characterization and function. J Biochem (Tokyo) 82: 317-337.
47. Maruyama K, Murakami F and Ohashi K (1977b) Connectin, an elastic protein of muscle. Comparative Biochemistry. J Biochem (Tokyo) 82: 339-345.
48. Maruyama K, Natori R and Nonomura Y (1976) New elastic protein from muscle. Nature 262: 58-60.
49. Metzger DM, Michele DE, Rust EM, Borton AR and Westfall MV (2003) Sarcomere thin filament regulatory isoforms: Evidence of a dominant effect of slow skeletal troponin I on cardiac contraction. J Biol Chem 278: 13118-13123.
50. Miller MK, Granzier H, Ehler E and Gregorio CC (2004) The sensitive giant: the role of titin-based stretch sensing complexes in the heart. Trends Cell Biol 14: 119-126.
51. Minajeva A, Kulke M, Fernandez JM and Linke WA (2001) Unfolding of titin domains explains the viscoelastic behavior of skeletal myofibrils. Biophys J 80: 1442-1451.
52. 2+ regulation in developing rabbit cardiac muscle. Biochem Biophys Res Commun 267: 912-917.
53. Murphy AM (1996) Contractile protein phenotypic variation during development. Cardiovasc Res 31: E25-33.
54. Nagueh SF, Shah G, Wu Y, Torre-Amione G, King NM, Lahmers S, Witt CC, Becker K, Labeit S and Granzier HL (2004) Altered titin expression, myocardial stiffness, and left ventricular function in patients with dilated cardiomyopathy. Circulation 110: 155-162.
55. Neagoe C, Kulke M, del Monte F, Gwathmey JK, de Tombe PP, Hajjar R and Linke WA (2002) Titin isoform switch in ischemic human heart disease. Circulation 106: 1333-1341.
56. Neagoe C, Opitz CA, Makarenko I and Linke WA (2003) Gigantic variety: expression patterns of titin isoforms in striated muscles and consequences for myofibrillar passive stiffness. J Muscle Res Cell Motil 24: 175-189.
57. Opitz CA, Kulke M, Leake MC, Neagoe C, Hinssen H, Hajjar RJ and Linke WA (2003) Damped elastic recoil of the titin spring in myofibrils of human myocardium. Proc Natl Acad Sci USA 100: 12688-12693.
58. Opitz CA, Leake MC, Makarenko I, Benes V and Linke WA (2004) Developmentally regulated switching of titin size alters myofibrillar stiffness in the perinatal heart. Circ Res 94: 967-975.
59. Reiser PJ, Westfall MV, Schiaffino S and Solaro RJ (1994) Tension production and thin-filament protein isoforms in developing rat myocardium. Am J Physiol Heart Circ Physiol 267: H1589-H1596.
60. Rief M, Gautel M, Oesterhelt F, Fernandez JM and Gaub HE (1997) Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276: 1109-1112.
61. Sabry MA and Dhoot GK (1989) Identification of and changes in the expression of troponin T isoforms in developing avian and mammalian heart. J Mol Cell Cardiol 21: 85-91.
62. Saggin L, Ausoni S, Gorza L, Sartore S and Schiaffino S (1988) Troponin T switching in the developing rat heart. J Biol Chem 263: 18488-18492.
63. Saggin L, Gorza L, Ausoni S and Schiaffino S (1989) Troponin I switching in the developing heart. J Biol Chem 264: 16299-16302.
64. Siedner S, Kruger M, Schroeter M, Metzler D, Roell W, Fleischmann BK, Hescheler J, Pfitzer G and Stehle R (2003) Developmental changes in contractility and sarcomeric proteins from the early embryonic to the adult stage in the mouse heart. J Physiol 548: 493-505.
65. Tatsumi R and Hattori A (1995) Detection of giant myofibrillar proteins connectin and nebulin by electrophoresis in 2% polyacrylamide slab gels strengthened with agarose. Anal Biochem 224: 28-31.
66. Trinick J, Knight P and Whiting A (1984) Purification and properties of native titin. J Mol Biol 180: 331-356.
67. Trombitas K, Freiburg A, Centner T, Labeit S and Granzier H (1999) Molecular dissection of N2B cardiac titin's extensibility. Biophys J 77: 3189-3196.
68. Trombitas K, Jin JP and Granzier H (1995) The mechanically active domain of titin in cardiac muscle. Circ Res 77: 856-861.
69. Trombitas K, Wu Y, Labeit D, Labeit S and Granzier H (2001) Cardiac titin isoforms are coexpressed in the half-sarcomere and extend independently. Am J Physiol Heart Circ Physiol 281: H1793-H1799.
70. Trombitas K, Wu Y, McNabb M, Greaser M, Kellermayer MS, Labeit S and Granzier H (2003) Molecular basis of passive stress relaxation in human soleus fibers: assessment of the role of immunoglobulin-like domain unfolding. Biophys J 85: 3142-3153.
71. Tskhovrebova L and Trinick J (2003) Titin: properties and family relationships. Nat Rev Mol Cell Biol 4: 679-689.
72. Tskhovrebova L, Trinick J, Sleep JA and Simmons RM (1997) Elasticity and unfolding of single molecules of the giant muscle protein titin. Nature 387: 308-312.
73. Wang K, McClure J and Tu A (1979) Titin: major myofibrillar component of striated muscle. Proc Natl Acad Sci USA 76: 3698-3702.
74. Wang K, Ramirez-Mitchell R and Palter D (1984) Titin is an extraordinary long, flexible, and slender myofibrillar protein. Proc Natl Acad Sci USA 81: 3685-3689.
75. Warren CM, Jordan MC, Roos KP, Krzesinski PR and Greaser ML (2003) Titin isoform expression in normal and hypertensive myocardium. Cardiovasc Res 59: 86-94.
76. Warren CM, Krzesinski PR, Campbell KS, Moss RL and Greaser ML (2004) Titin isoform changes in rat myocardium during development. Mech Dev 121: 1301-1312.
77. Whalen RG and Sell SM (1980) Myosin from foetal hearts contains the skeletal muscle embryonic light chain. Nature 286: 731-733.
78. Wu Y, Bell SP, Trombitas K, Witt CC, Labeit S, LeWinter MM and Granzier H (2002) Changes in titin isoform expression in pacing-induced cardiac failure give rise to increased passive muscle stiffness. Circulation 106: 1384-1389.
79. Wu Y, Cazorla O, Labeit D, Labeit S and Granzier H (2000) Changes in titin and collagen underlie diastolic stiffness diversity of cardiac muscle. J Mol Cell Cardiol 32: 2151-2162.
80. Young P, Ehler E and Gautel M (2002) Obscurin, a giant sarcomeric Rho guanine nucleotide exchange factor protein involved in sarcomere assembly. J Cell Biol 154: 123-136.