From myofibril to membrane; The transitional junction at the intercalated disc

Frontiers in Bioscience

Volumn 17, Issue 3, 2012, Pages 1035-1050

  Bennett, Pauline M ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Alpha actinin; Electron microscopy; Heart muscle; Intercalated disc; Review; Spectrin; Titin; Transitional junction; ZASP

Indexed keywords

ANIMAL; CELL MEMBRANE; ELECTRON MICROSCOPY; HEART MUSCLE; MOUSE; MUSCLE FIBRIL; PHYSIOLOGY; REVIEW; ULTRASTRUCTURE;

ANIMALS; CELL MEMBRANE; MICE; MICROSCOPY, ELECTRON; MYOCARDIUM; MYOFIBRILS;

EID: 84859249623     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/3972     Document Type: Article

References (104)

1. P. M. Bennett, A. M. Maggs, A. J. Baines and J. C. Pinder: The transitional junction: a new functional subcellular domain at the intercalated disc. Mol Biol Cell, 17(4), 2091-100 (2006). (Pubitemid 44011621)
2. J. G. Tidball and D. M. Quan: Reduction in myotendinous junction surface area of rats subjected to 4-day spaceflight. J Appl Physiol, 73(1), 59-64 (1992).
3. A. H. Herrera, B. Elzey, D. J. Law and R. Horowits: Terminal regions of mouse nebulin: sequence analysis and complementary localization with N-RAP. Cell Motil Cytoskeleton, 45(3), 211-22 (2000). (Pubitemid 30151740)
4. D. W. Fawcett and N. S. McNutt: The ultrastructure of the cat myocardium. I. Ventricular papillary muscle. J Cell Biol, 42(1), 1-45 (1969).
5. M. S. Forbes and N. Sperelakis: Intercalated discs of mammalian heart: a review of structure and function. Tissue Cell, 17(5), 605-48 (1985). (Pubitemid 16243839)
6. N. J. Severs, A. F. Bruce, E. Dupont and S. Rothery: Remodelling of gap junctions and connexin expression in diseased myocardium. Cardiovasc Res, 80(1), 9-19 (2008).
7. G. Sohl and K. Willecke: Gap junctions and the connexin protein family. Cardiovasc Res, 62(2), 228-32 (2004). (Pubitemid 38496536)
8. M. Delmar and W. J. McKenna: The cardiac desmosome and arrhythmogenic cardiomyopathies: from gene to disease. Circ Res, 107(6), 700-14 (2010).
9. F. Sheikh, R. S. Ross and J. Chen: Cell-cell connection to cardiac disease. Trends Cardiovasc Med, 19(6), 182-90 (2009).
10. W. W. Franke, S. Rickelt, M. Barth and S. Pieperhoff: The junctions that don't fit the scheme: special symmetrical cell-cell junctions of their own kind. Cell Tissue Res, 338(1), 1-17 (2009).
11. M. Yamaguchi, S. Yamano, M. Muguruma and R. M. Robson: Polarity and length of actin filaments at the fascia adherens of the cardiac intercalated disk. J Ultrastruct Mol Struct Res, 100(3), 235-44 (1988). (Pubitemid 19101864)
12. R. Horowits and R. J. Podolsky: The positional stability of thick filaments in activated skeletal muscle depends on sarcomere length: evidence for the role of titin filaments. J Cell Biol, 105(5), 2217-23 (1987). (Pubitemid 18019071)
13. H. L. Granzier and T. C. Irving: Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments. Biophys J, 68(3), 1027-44 (1995).
14. S. Labeit and B. Kolmerer: Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science, 270(5234), 293-6 (1995).
15. K. Wang, R. McCarter, J. Wright, J. Beverly and R. Ramirez-Mitchell: Regulation of skeletal muscle stiffness and elasticity by titin isoforms: a test of the segmental extension model of resting tension. Proc Natl Acad Sci USA, 88(16), 7101-5 (1991). (Pubitemid 21915097)
16. W. G. Pyle and R. J. Solaro: At the crossroads of myocardial signaling: the role of Z-discs in intracellular signaling and cardiac function. Circ Res, 94(3), 296-305 (2004). (Pubitemid 38240720)
17. G. Faulkner, G. Lanfranchi and G. Valle: Telethonin and other new proteins of the Z-disc of skeletal muscle. IUBMB Life, 51(5), 275-82 (2001). (Pubitemid 33010181)
18. P. K. Luther: The vertebrate muscle Z-disc: sarcomere anchor for structure and signalling. J Muscle Res Cell Motil, 30(5-6), 171-85 (2009).
19. D. Frank, C. Kuhn, H. A. Katus and N. Frey: The sarcomeric Z-disc: a nodal point in signalling and disease. J Mol Med, 84(6), 446-68 (2006). (Pubitemid 43801324)
20. K. A. Clark, A. S. McElhinny, M. C. Beckerle and C. C. Gregorio: Striated muscle cytoarchitecture: an intricate web of form and function. Annu Rev Cell Dev Biol, 18, 637-706 (2002). (Pubitemid 35387364)
21. M. H. Lu, C. DiLullo, T. Schultheiss, S. Holtzer, J. M. Murray, J. Choi, D. A. Fischman and H. Holtzer: The vinculin/sarcomeric-alpha-actinin/alpha-actin nexus in cultured cardiac myocytes. J Cell Biol, 117(5), 1007-22 (1992).
22. S. Balasubramanian, S. K. Mani, H. Kasiganesan, C. C. Baicu and D. Kuppuswamy: Hypertrophic stimulation increases beta-actin dynamics in adult feline cardiomyocytes. PLoS ONE, 5(7), e11470 (2010).
23. J. F. Casella, S. W. Craig, D. J. Maack and A. E. Brown: Cap Z(36/32), a barbed end actin-capping protein, is a component of the Z-line of skeletal muscle. J Cell Biol, 105(1), 371-9 (1987).
24. J. F. Casella, D. J. Maack and S. Lin: Purification and initial characterization of a protein from skeletal muscle that caps the barbed ends of actin filaments. J Biol Chem, 261(23), 10915-21 (1986). (Pubitemid 17210016)
25. A. Yamashita, K. Maeda and Y. Maeda: Crystal structure of CapZ: structural basis for actin filament barbed end capping. EMBO J, 22(7), 1529-38 (2003). (Pubitemid 36417402)
26. D. A. Schafer, Y. O. Korshunova, T. A. Schroer and J. A. Cooper: Differential localization and sequence analysis of capping protein beta-subunit isoforms of vertebrates. J Cell Biol, 127(2), 453-65 (1994).
27. C. L. Moncman and K. Wang: Nebulette: a 107 kD nebulin-like protein in cardiac muscle. Cell Motil Cytoskeleton, 32(3), 205-25 (1995).
28. C. L. Moncman and K. Wang: Functional dissection of nebulette demonstrates actin binding of nebulin-like repeats and Z-line targeting of SH3 and linker domains. Cell Motil Cytoskeleton, 44(1), 1-22 (1999). (Pubitemid 29416508)
29. C. T. Pappas, N. Bhattacharya, J. A. Cooper and C. C. Gregorio: Nebulin interacts with CapZ and regulates thin filament architecture within the Z-disc. Mol Biol Cell, 19(5), 1837-47 (2008).
30. B. Sjoblom, A. Salmazo and K. Djinovic-Carugo: Alpha-actinin structure and regulation. Cell Mol Life Sci, 65(17), 2688-701 (2008).
31. C. M. Hampton, D. W. Taylor and K. A. Taylor: Novel structures for alpha-actinin:F-actin interactions and their implications for actin-membrane attachment and tension sensing in the cytoskeleton. J Mol Biol, 368(1), 92-104 (2007). (Pubitemid 46441216)
32. D. S. Courson and R. S. Rock: Actin cross-link assembly and disassembly mechanics for alpha-Actinin and fascin. J Biol Chem, 285(34), 26350-7 (2010).
33. K. A. Taylor and D. W. Taylor: Formation of twodimensional complexes of F-actin and crosslinking proteins on lipid monolayers: demonstration of unipolar alphaactinin- F-actin crosslinking. Biophys J, 67(5), 1976-83 (1994). (Pubitemid 24342069)
34. K. Wang and J. Wright: Architecture of the sarcomere matrix of skeletal muscle: immunoelectron microscopic evidence that suggests a set of parallel inextensible nebulin filaments anchored at the Z line. J Cell Biol, 107(6 Pt 1), 2199-212 (1988). (Pubitemid 19015099)
35. A. Whiting, J. Wardale and J. Trinick: Does titin regulate the length of muscle thick filaments? J Mol Biol, 205(1), 263-8 (1989).
36. P. Young, C. Ferguson, S. Banuelos and M. Gautel: Molecular structure of the sarcomeric Z-disk: two types of titin interactions lead to an asymmetrical sorting of alphaactinin. EMBO J, 17(6), 1614-24 (1998). (Pubitemid 28119115)
37. H. Ohtsuka, H. Yajima, K. Maruyama and S. Kimura: Binding of the N-terminal 63 kDa portion of connectin/titin to alpha-actinin as revealed by the yeast two-hybrid system. FEBS Lett, 401(1), 65-7 (1997). (Pubitemid 27051259)
38. H. Sorimachi, A. Freiburg, B. Kolmerer, S. Ishiura, G. Stier, C. C. Gregorio, D. Labeit, W. A. Linke, K. Suzuki and S. Labeit: Tissue-specific expression and alpha-actinin binding properties of the Z-disc titin: implications for the nature of vertebrate Z-discs. J Mol Biol, 270(5), 688-95 (1997). (Pubitemid 27332059)
39. P. Young and M. Gautel: The interaction of titin and alphaactinin is controlled by a phospholipid-regulated intramolecular pseudoligand mechanism. EMBO J, 19(23), 6331-40 (2000).
40. M. Gautel, D. Goulding, B. Bullard, K. Weber and D. O. Furst: The central Z-disk region of titin is assembled from a novel repeat in variable copy numbers. J Cell Sci, 109 (Pt 11), 2747-54 (1996). (Pubitemid 26388359)
41. H. Ohtsuka, H. Yajima, K. Maruyama and S. Kimura: The N-terminal Z repeat 5 of connectin/titin binds to the C-terminal region of alpha-actinin. Biochem Biophys Res Commun, 235(1), 1-3 (1997). (Pubitemid 27302673)
42. R. A. Atkinson, C. Joseph, G. Kelly, F. W. Muskett, T. A. Frenkiel, D. Nietlispach and A. Pastore: Ca2+-independent binding of an EF-hand domain to a novel motif in the alphaactinin- titin complex. Nat Struct Biol, 8(10), 853-7 (2001). (Pubitemid 32923603)
43. R. A. Atkinson, C. Joseph, F. Dal Piaz, L. Birolo, G. Stier, P. Pucci and A. Pastore: Binding of alpha-actinin to titin: implications for Z-disk assembly. Biochemistry, 39(18), 5255- 64 (2000). (Pubitemid 30257063)
44. W. A. Linke, M. Ivemeyer, S. Labeit, H. Hinssen, J. C. Ruegg and M. Gautel: Actin-titin interaction in cardiac myofibrils: probing a physiological role. Biophys J, 73(2), 905- 19 (1997). (Pubitemid 27337625)
45. M. Kulke, S. Fujita-Becker, E. Rostkova, C. Neagoe, D. Labeit, D. J. Manstein, M. Gautel and W. A. Linke: Interaction between PEVK-titin and actin filaments: origin of a viscous force component in cardiac myofibrils. Circ Res, 89(10), 874- 81 (2001). (Pubitemid 34627892)
46. R. Yamasaki, M. Berri, Y. Wu, K. Trombitas, M. McNabb, M. S. Kellermayer, C. Witt, D. Labeit, S. Labeit, M. Greaser and H. Granzier: Titin-actin interaction in mouse myocardium: passive tension modulation and its regulation by calcium/S100A1. Biophys J, 81(4), 2297-313 (2001). (Pubitemid 32917177)
47. W. A. Linke, M. Kulke, H. Li, S. Fujita-Becker, C. Neagoe, D. J. Manstein, M. Gautel and J. M. Fernandez: PEVK domain of titin: an entropic spring with actinbinding properties. J Struct Biol, 137(1-2), 194-205 (2002). (Pubitemid 35430434)
48. A. J. te Velthuis and C. P. Bagowski: PDZ and LIM domain-encoding genes: molecular interactions and their role in development. ScientificWorldJournal, 7, 1470-92 (2007). (Pubitemid 47435428)
49. G. Faulkner, A. Pallavicini, E. Formentin, A. Comelli, C. Ievolella, S. Trevisan, G. Bortoletto, P. Scannapieco, M. Salamon, V. Mouly, G. Valle and G. Lanfranchi: ZASP: a new Z-band alternatively spliced PDZ-motif protein. J Cell Biol, 146(2), 465-75 (1999). (Pubitemid 29369781)
50. Q. Zhou, P. Ruiz-Lozano, M. E. Martone and J. Chen: Cypher, a striated muscle-restricted PDZ and LIM domaincontaining protein, binds to alpha-actinin-2 and protein kinase C. J Biol Chem, 274(28), 19807-13 (1999).
51. R. Passier, J. A. Richardson and E. N. Olson: Oracle, a novel PDZ-LIM domain protein expressed in heart and skeletal muscle. Mech Dev, 92(2), 277-84 (2000). (Pubitemid 30155922)
52. C. Huang, Q. Zhou, P. Liang, M. S. Hollander, F. Sheikh, X. Li, M. Greaser, G. D. Shelton, S. Evans and J. Chen: Characterization and in vivo functional analysis of splice variants of cypher. J Biol Chem, 278(9), 7360-5 (2003). (Pubitemid 36800739)
53. P. von Nandelstadh, M. Ismail, C. Gardin, H. Suila, I. Zara, A. Belgrano, G. Valle, O. Carpen and G. Faulkner: A class III PDZ binding motif in the myotilin and FATZ families binds enigma family proteins: a common link for Z-disc myopathies. Mol Cell Biol, 29(3), 822-34 (2009).
54. T. Klaavuniemi and J. Ylanne: Zasp/Cypher internal ZM-motif containing fragments are sufficient to co-localize with alpha-actinin-analysis of patient mutations. Exp Cell Res, 312(8), 1299-311 (2006).
55. T. Klaavuniemi, A. Kelloniemi and J. Ylanne: The ZASP-like motif in actinin-associated LIM protein is required for interaction with the alpha-actinin rod and for targeting to the muscle Z-line. J Biol Chem, 279(25), 26402-10 (2004). (Pubitemid 38798792)
56. F. Sheikh, M. L. Bang, S. Lange and J. Chen: "Z"eroing in on the role of Cypher in striated muscle function, signaling, and human disease. Trends Cardiovasc Med, 17(8), 258-62 (2007). (Pubitemid 350087695)
57. Q. Zhou, P. H. Chu, C. Huang, C. F. Cheng, M. E. Martone, G. Knoll, G. D. Shelton, S. Evans and J. Chen: Ablation of Cypher, a PDZ-LIM domain Z-line protein, causes a severe form of congenital myopathy. J Cell Biol, 155(4), 605-12 (2001). (Pubitemid 34289318)
58. G. Valle, G. Faulkner, A. De Antoni, B. Pacchioni, A. Pallavicini, D. Pandolfo, N. Tiso, S. Toppo, S. Trevisan and G. Lanfranchi: Telethonin, a novel sarcomeric protein of heart and skeletal muscle. FEBS Lett, 415(2), 163-8 (1997). (Pubitemid 27430060)
59. C. C. Gregorio, K. Trombitas, T. Centner, B. Kolmerer, G. Stier, K. Kunke, K. Suzuki, F. Obermayr, B. Herrmann, H. Granzier, H. Sorimachi and S. Labeit: The NH2 terminus of titin spans the Z-disc: its interaction with a novel 19-kD ligand (T-cap) is required for sarcomeric integrity. J Cell Biol, 143(4), 1013-27 (1998). (Pubitemid 28547400)
60. A. Mues, P. F. van der Ven, P. Young, D. O. Furst and M. Gautel: Two immunoglobulin-like domains of the Zdisc portion of titin interact in a conformation-dependent way with telethonin. FEBS Lett, 428(1-2), 111-4 (1998). (Pubitemid 28266840)
61. N. Pinotsis, M. Petoukhov, S. Lange, D. Svergun, P. Zou, M. Gautel and M. Wilmanns: Evidence for a dimeric assembly of two titin/telethonin complexes induced by the telethonin C-terminus. J Struct Biol, 155(2), 239-50 (2006). (Pubitemid 44278654)
62. M. Bertz, M. Wilmanns and M. Rief: The titintelethonin complex is a directed, superstable molecular bond in the muscle Z-disk. Proc Natl Acad Sci USA, 106(32), 13307-133310 (2009).
63. J. Wang, N. Shaner, B. Mittal, Q. Zhou, J. Chen, J. M. Sanger and J. W. Sanger: Dynamics of Z-band based proteins in developing skeletal muscle cells. Cell Motil Cytoskeleton, 61(1), 34-48 (2005). (Pubitemid 40604949)
64. J. W. Sanger, J. Wang, B. Holloway, A. du and J. M. Sanger: Myofibrillogenesis in skeletal muscle cells in zebrafish. Cell Motil Cytoskeleton, 66(8), 556-66 (2009).
65. R. Zhang, J. Yang, J. Zhu and X. Xu: Depletion of zebrafish Tcap leads to muscular dystrophy via disrupting sarcomere-membrane interaction, not sarcomere assembly. Hum Mol Genet, 18(21), 4130-40 (2009).
66. T. Sadikot, C. R. Hammond and M. B. Ferrari: Distinct roles for telethonin N-versus C-terminus in sarcomere assembly and maintenance. Dev Dyn, 239(4), 1124-35 (2010).
67. G. Faulkner, A. Pallavicini, A. Comelli, M. Salamon, G. Bortoletto, C. Ievolella, S. Trevisan, S. Kojic, F. Dalla Vecchia, P. Laveder, G. Valle and G. Lanfranchi: FATZ, a filamin-, actinin-, and telethonin-binding protein of the Zdisc of skeletal muscle. J Biol Chem, 275(52), 41234-42 (2000). (Pubitemid 32054956)
68. N. Frey and E. N. Olson: Calsarcin-3, a novel skeletal muscle-specific member of the calsarcin family, interacts with multiple Z-disc proteins. J Biol Chem, 277(16), 13998-4004 (2002). (Pubitemid 34968008)
69. N. Frey, J. A. Richardson and E. N. Olson: Calsarcins, a novel family of sarcomeric calcineurin-binding proteins. Proc Natl Acad Sci USA, 97(26), 14632-7 (2000). (Pubitemid 32016627)
70. F. Takada, D. L. Vander Woude, H. Q. Tong, T. G. Thompson, S. C. Watkins, L. M. Kunkel and A. H. Beggs: Myozenin: an alpha-actinin- and gamma-filamin-binding protein of skeletal muscle Z lines. Proc Natl Acad Sci USA, 98(4), 1595-600 (2001). (Pubitemid 32165544)
71. G. Luo, J. Q. Zhang, T. P. Nguyen, A. H. Herrera, B. Paterson and R. Horowits: Complete cDNA sequence and tissue localization of N-RAP, a novel nebulin-related protein of striated muscle. Cell Motil Cytoskeleton, 38(1), 75-90 (1997). (Pubitemid 27383301)
72. J. Q. Zhang, B. Elzey, G. Williams, S. Lu, D. J. Law and R. Horowits: Ultrastructural and biochemical localization of N-RAP at the interface between myofibrils and intercalated disks in the mouse heart. Biochemistry, 40(49), 14898-906 (2001). (Pubitemid 33136111)
73. K. Gehmlich, C. Geier, K. J. Osterziel, P. F. Van Der Ven and D. O. Furst: Decreased interactions of mutant muscle LIM protein (MLP) with N-RAP and alpha-actinin and their implication for hypertrophic cardiomyopathy. Cell Tissue Res, 317(2), 129-36 (2004). (Pubitemid 39070612)
74. S. A. Mohiddin, S. Lu, J. P. Cardoso, S. Carroll, S. Jha, R. Horowits and L. Fananapazir: Genomic organization, alternative splicing, and expression of human and mouse NRAP, a nebulin-related LIM protein of striated muscle. Cell Motil Cytoskeleton, 55(3), 200-12 (2003). (Pubitemid 36791302)
75. S. Lu, S. L. Carroll, A. H. Herrera, B. Ozanne and R. Horowits: New N-RAP-binding partners alpha-actinin, filamin and Krp1 detected by yeast two-hybrid screening: implications for myofibril assembly. J Cell Sci, 116(Pt 11), 2169-78 (2003). (Pubitemid 36722363)
76. S. Lu, D. E. Borst and R. Horowits: N-RAP expression during mouse heart development. Dev Dyn, 233(1), 201-12 (2005). (Pubitemid 40548039)
77. J. M. Ervasti: Costameres: the Achilles' heel of Herculean muscle. J Biol Chem, 278(16), 13591-4 (2003). (Pubitemid 36799888)
78. R. R. Kaprielian and N. J. Severs: Dystrophin and the cardiomyocyte membrane cytoskeleton in the healthy and failing heart. Heart Fail Rev, 5(3), 221-38 (2000).
79. A. J. Baines: The spectrin-ankyrin-4.1-adducin membrane skeleton: adapting eukaryotic cells to the demands of animal life. Protoplasma, 244(1-4), 99-131 (2010).
80. A. J. Baines and J. C. Pinder: The spectrin-associated cytoskeleton in mammalian heart. Front Biosci, 10, 3020-33 (2005). (Pubitemid 40910541)
81. P. M. Bennett, A. J. Baines, M. C. Lecomte, A. M. Maggs and J. C. Pinder: Not just a plasma membrane protein: in cardiac muscle cells alpha-II spectrin also shows a close association with myofibrils. J Muscle Res Cell Motil, 25(2), 119-26 (2004). (Pubitemid 39060886)
82. S. A. Stevenson, M. J. Cullen, S. Rothery, S. R. Coppen and N. J. Severs: High-resolution en-face visualization of the cardiomyocyte plasma membrane reveals distinctive distributions of spectrin and dystrophin. Eur J Cell Biol, 84(12), 961-71 (2005). (Pubitemid 41684151)
83. S. Kostin, S. Hein, E. Arnon, D. Scholz and J. Schaper: The cytoskeleton and related proteins in the human failing heart. Heart Fail Rev, 5(3), 271-80 (2000).
84. N. V. Hayes, C. Scott, E. Heerkens, V. Ohanian, A. M. Maggs, J. C. Pinder, E. Kordeli and A. J. Baines: Identification of a novel C-terminal variant of beta II spectrin: two isoforms of beta II spectrin have distinct intracellular locations and activities. J Cell Sci, 113 ( Pt 11), 2023-34 (2000). (Pubitemid 30386506)
85. T. J. Hund, O. M. Koval, J. Li, P. J. Wright, L. Qian, J. S. Snyder, H. Gudmundsson, C. F. Kline, N. P. Davidson, N. Cardona, M. N. Rasband, M. E. Anderson and P. J. Mohler: A beta(IV)-spectrin/CaMKII signaling complex is essential for membrane excitability in mice. J Clin Invest, 120(10), 3508-19 (2010).
86. Y. Zhang, W. G. Resneck, P. C. Lee, W. R. Randall, R. J. Bloch and J. A. Ursitti: Characterization and expression of a heart-selective alternatively spliced variant of alpha II-spectrin, cardi+, during development in the rat. J Mol Cell Cardiol, 48(6), 1050-9 (2010).
87. P. M. Taylor-Harris, L. A. Keating, A. M. Maggs, G. W. Phillips, E. J. Birks, R. C. Franklin, M. H. Yacoub, A. J. Baines and J. C. Pinder: Cardiac muscle cell cytoskeletal protein 4.1: analysis of transcripts and subcellular location- relevance to membrane integrity, microstructure, and possible role in heart failure. Mamm Genome, 16(3), 137-51 (2005). (Pubitemid 40569190)
88. V. Bennett and A. J. Baines: Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol Rev, 81(3), 1353-92 (2001). (Pubitemid 32606672)
89. J. J. Ipsaro and A. Mondragon: Structural basis for spectrin recognition by ankyrin. Blood, 115(20), 4093-101 (2010).
90. P. J. Mohler, I. Rivolta, C. Napolitano, G. LeMaillet, S. Lambert, S. G. Priori and V. Bennett: Nav1.5 E1053K mutation causing Brugada syndrome blocks binding to ankyrin-G and expression of Nav1.5 on the surface of cardiomyocytes. Proc Natl Acad Sci USA, 101(50), 17533-8 (2004). (Pubitemid 39657438)
91. N. Mohandas and P. G. Gallagher: Red cell membrane: past, present, and future. Blood, 112(10), 3939-48 (2008).
92. M. A. Stagg, E. Carter, N. Sohrabi, U. Siedlecka, G. K. Soppa, F. Mead, N. Mohandas, P. Taylor-Harris, A. Baines, P. Bennett, M. H. Yacoub, J. C. Pinder and C. M. Terracciano: Cytoskeletal protein 4.1R affects repolarization and regulates calcium handling in the heart. Circ Res, 103(8), 855-63 (2008).
93. A. J. Baines, P. M. Bennett, E. W. Carter and C. Terracciano: Protein 4.1 and the control of ion channels. Blood Cells Mol Dis, 42(3), 211-5 (2009).
94. J. C. Pinder and A. J. Baines: A protein accumulator. Nature, 406(6793), 253-4 (2000). (Pubitemid 30604391)
95. J. G. Tidball: The geometry of actin filamentmembrane associations can modify adhesive strength of the myotendinous junction. Cell Motil, 3(5-6), 439-47 (1983).
96. J. G. Tidball: Force transmission across muscle cell membranes. J Biomech, 24 Suppl 1, 43-52 (1991).
97. M. Yoshida, E. Sho, H. Nanjo, M. Takahashi, M. Kobayashi, K. Kawamura, M. Honma, M. Komatsu, A. Sugita, M. Yamauchi, T. Hosoi, Y. Ito and H. Masuda: Weaving hypothesis of cardiomyocyte sarcomeres: discovery of periodic broadening and narrowing of intercalated disk during volume-load change. Am J Pathol, 176(2), 660-78 (2010).
98. J. C. Perriard, A. Hirschy and E. Ehler: Dilated cardiomyopathy: a disease of the intercalated disc? Trends Cardiovasc Med, 13(1), 30-8 (2003). (Pubitemid 36120547)
99. M. Leu, E. Ehler and J. C. Perriard: Characterisation of postnatal growth of the murine heart. Anat Embryol (Berl), 204(3), 217-24 (2001). (Pubitemid 32938437)
100. E. Ehler, R. Horowits, C. Zuppinger, R. L. Price, E. Perriard, M. Leu, P. Caroni, M. Sussman, H. M. Eppenberger and J. C. Perriard: Alterations at the intercalated disk associated with the absence of muscle LIM protein. J Cell Biol, 153(4), 763-72 (2001). (Pubitemid 34286108)
101. M. J. Flick and S. F. Konieczny: The muscle regulatory and structural protein MLP is a cytoskeletal binding partner of betaI-spectrin. J Cell Sci, 113 ( Pt 9), 1553-64 (2000). (Pubitemid 30312504)
102. W. A. Linke, M. Ivemeyer, P. Mundel, M. R. Stockmeier and B. Kolmerer: Nature of PEVK-titin elasticity in skeletal muscle. Proc Natl Acad Sci USA, 95(14), 8052-7 (1998). (Pubitemid 28326064)
103. D. O. Furst, M. Osborn, R. Nave and K. Weber: 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(5), 1563-72 (1988).
104. W. A. Linke, M. Ivemeyer, N. Olivieri, B. Kolmerer, J. C. Ruegg and S. Labeit: Towards a molecular understanding of the elasticity of titin. J Mol Biol, 261(1), 62-71 (1996). (Pubitemid 26270783)