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Science 13 October 1995:
Vol. 270. no. 5234, pp. 293 - 296
DOI: 10.1126/science.270.5234.293
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Reports

Titins: Giant Proteins in Charge of Muscle Ultrastructure and Elasticity

Siegfried Labeit and Bernhard Kolmerer

In addition to thick and thin filaments, vertebrate striated muscle contains a third filament system formed by the giant protein titin. Single titin molecules extend from Z discs to M lines and are longer than 1 micrometer. The titin filament contributes to muscle assembly and resting tension, but more details are not known because of the large size of the protein. The complete complementary DNA sequence of human cardiac titin was determined. The 82-kilobase complementary DNA predicts a 3-megadalton protein composed of 244 copies of immunoglobulin and fibronectin type III (FN3) domains. The architecture of sequences in the A band region of titin suggests why thick filament structure is conserved among vertebrates. In the I band region, comparison of titin sequences from muscles of different passive tension identifies two elements that correlate with tissue stiffness. This suggests that titin may act as two springs in series. The differential expression of the springs provides a molecular explanation for the diversity of sarcomere length and resting tension in vertebrate striated muscles.

European Molecular Biology Laboratory, P.O. Box 102209, 69012 Heidelberg, Germany. 


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Cardiac titin: an adjustable multi-functional spring.
H. Granzier and S. Labeit (2002)
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Passive tension of rat skeletal soleus muscle fibers: effects of unloading conditions.
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J Appl Physiol 92, 1465-1472
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Muscle-specific RING finger-1 interacts with titin to regulate sarcomeric M-line and thick filament structure and may have nuclear functions via its interaction with glucocorticoid modulatory element binding protein-1.
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J. Cell Biol. 157, 125-136
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Molecular Mechanics of Cardiac Titin's PEVK and N2B Spring Elements.
K. Watanabe, P. Nair, D. Labeit, M. S. Z. Kellermayer, M. Greaser, S. Labeit, and H. Granzier (2002)
J. Biol. Chem. 277, 11549-11558
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Transient association of titin and myosin with microtubules in nascent myofibrils directed by the MURF2 RING-finger protein.
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Y.-L. Yan, C. T. Miller, R. Nissen, A. Singer, D. Liu, A. Kirn, B. Draper, J. Willoughby, P. A. Morcos, A. Amsterdam, et al. (2002)
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N. Fukuda, D. Sasaki, S.'i. Ishiwata, and S. Kurihara (2001)
Circulation 104, 1639-1645
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Cardiac titin isoforms are coexpressed in the half-sarcomere and extend independently.
K. Trombitas, Y. Wu, D. Labeit, S. Labeit, and H. Granzier (2001)
Am J Physiol Heart Circ Physiol 281, H1793-H1799
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M. Kulke, C. Neagoe, B. Kolmerer, A. Minajeva, H. Hinssen, B. Bullard, and W. A. Linke (2001)
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J. Immunol. 167, 2130-2141
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Fishing out proteins that bind to titin.
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J. Cell Biol. 154, 21-24
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P. Young, E. Ehler, and M. Gautel (2001)
J. Cell Biol. 154, 123-136
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Titin, Thymoma, and Myasthenia Gravis.
J. A. Aarli (2001)
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Anti-Titin Antibodies in Myasthenia Gravis: Tight Association With Thymoma and Heterogeneity of Nonthymoma Patients.
A. M. Yamamoto, P. Gajdos, B. Eymard, C. Tranchant, J.-M. Warter, L. Gomez, C. Bourquin, J.-F. Bach, and H.-J. Garchon (2001)
Arch Neurol 58, 885-890
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H. Haravuori, A. Vihola, V. Straub, M. Auranen, I. Richard, S. Marchand, T. Voit, S. Labeit, H. Somer, L. Peltonen, et al. (2001)
Neurology 56, 869-877
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Stepwise unfolding of titin under force-clamp atomic force microscopy.
A. F. Oberhauser, P. K. Hansma, M. Carrion-Vazquez, and J. M. Fernandez (2001)
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D-Titin: A Giant Protein with Dual Roles in Chromosomes and Muscles.
C. Machado and D. J. Andrew (2000)
J. Cell Biol. 151, 639-652
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Desmin knockout muscles generate lower stress and are less vulnerable to injury compared with wild-type muscles.
M. Sam, S. Shah, J. Friden, D. J. Milner, Y. Capetanaki, and R. L. Lieber (2000)
Am J Physiol Cell Physiol 279, C1116-C1122
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Alterations in the Determinants of Diastolic Suction During Pacing Tachycardia.
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Circ. Res. 87, 235-240
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Series of Exon-Skipping Events in the Elastic Spring Region of Titin as the Structural Basis for Myofibrillar Elastic Diversity.
A. Freiburg, K. Trombitas, W. Hell, O. Cazorla, F. Fougerousse, T. Centner, B. Kolmerer, C. Witt, J. S. Beckmann, C. C. Gregorio, et al. (2000)
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Is the spring quality of muscle plastic?.
T. E. Reich, S. L. Lindstedt, P. C. LaStayo, and D. J. Pierotti (2000)
Am J Physiol Regulatory Integrative Comp Physiol 278, R1661-R1666
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A Novel Marker for Vertebrate Embryonic Heart, the EH-myomesin Isoform.
I. Agarkova, D. Auerbach, E. Ehler, and J.-C. Perriard (2000)
J. Biol. Chem. 275, 10256-10264
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The Vertebrate Body Axis: Evolution and Mechanical Function.
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The role of the cytoskeleton in heart failure.
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Cardiovasc Res 45, 273-278
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Antisense oligonucleotide experiments elucidate the essential role of titin in sarcomerogenesis in adult rat cardiomyocytes in long-term culture.
V Person, S Kostin, K Suzuki, S Labeit, and J Schaper (2000)
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Drosophila D-titin is required for myoblast fusion and skeletal muscle striation.
Y Zhang, D Featherstone, W Davis, E Rushton, and K Broadie (2000)
J. Cell Sci. 113, 3103-3115
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Differential Expression of Cardiac Titin Isoforms and Modulation of Cellular Stiffness.
O. Cazorla, A. Freiburg, M. Helmes, T. Centner, M. McNabb, Y. Wu, K. Trombitas, S. Labeit, and H. Granzier (2000)
Circ. Res. 86, 59-67
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A functional knock-out of titin results in defective myofibril assembly.
P. van der Ven, J. Bartsch, M Gautel, H Jockusch, and D. Furst (2000)
J. Cell Sci. 113, 1405-1414
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I-Band Titin in Cardiac Muscle Is a Three-Element Molecular Spring and Is Critical for Maintaining Thin Filament Structure.
W. A. Linke, D. E. Rudy, T. Centner, M. Gautel, C. Witt, S. Labeit, and C. C. Gregorio (1999)
J. Cell Biol. 146, 631-644
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3-Dimensional configuration of perimysial collagen fibres in rat cardiac muscle at resting and extended sarcomere lengths.
P. J Hanley, A. A Young, I. J LeGrice, S. G Edgar, and D. S Loiselle (1999)
J. Physiol. 517, 831-837
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Mechanically Driven Contour-Length Adjustment in Rat Cardiac Titin's Unique N2B Sequence : Titin Is an Adjustable Spring.
M. Helmes, K. Trombitas, T. Centner, M. Kellermayer, S. Labeit, W. A. Linke, and H. Granzier (1999)
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M. Herasse, Y. Ono, F. Fougerousse, E.-i. Kimura, D. Stockholm, C. Beley, D. Montarras, C. Pinset, H. Sorimachi, K. Suzuki, et al. (1999)
Mol. Cell. Biol. 19, 4047-4055
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Cardiac Myosin Binding Protein C.
S. Winegrad (1999)
Circ. Res. 84, 1117-1126
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Stretching single-domain proteins: Phase diagram and kinetics of force-induced unfolding.
D. K. Klimov and D. Thirumalai (1999)
PNAS 96, 6166-6170
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Biomechanics, One Molecule at a Time.
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Different Domains of the M-Band Protein Myomesin Are Involved in Myosin Binding and M-Band Targeting.
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Single-Molecule Biomechanics with Optical Methods.
A. D. Mehta, M. Rief, J. A. Spudich, D. A. Smith, and R. M. Simmons (1999)
Science 283, 1689-1695
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Familial Dilated Cardiomyopathy Locus Maps to Chromosome 2q31.
B. L. Siu, H. Niimura, J. A. Osborne, D. Fatkin, C. MacRae, S. Solomon, D. W. Benson, J. G. Seidman, and C. E. Seidman (1999)
Circulation 99, 1022-1026
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Initiation and maturation of I-Z-I bodies in the growth tips of transfected myotubes.
K Ojima, Z. Lin, Z. Zhang, T Hijikata, S Holtzer, S Labeit, H. Sweeney, and H Holtzer (1999)
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The NH2 Terminus of Titin Spans the Z-Disc: Its Interaction with a Novel 19-kD Ligand (T-cap) Is Required for Sarcomeric Integrity.
C. C. Gregorio, K. Trombitas, T. Centner, B. Kolmerer, G. Stier, K. Kunke, K. Suzuki, F. Obermayr, B. Herrmann, H. Granzier, et al. (1998)
J. Cell Biol. 143, 1013-1027
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Control of AMP deaminase 1 binding to myosin heavy chain.
I. Hisatome, T. Morisaki, H. Kamma, T. Sugama, H. Morisaki, A. Ohtahara, and E. W. Holmes (1998)
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