Molecular identification and localization of cellular titin, a novel titin isoform in the fibroblast stress fiber

Cell Motility and the Cytoskeleton

Volumn 64, Issue 6, 2007, Pages 418-433

  Cavnar, Peter J ^a   Olenych, Scott G ^a   Keller III, Thomas C S ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

actinin; Cellular titin; Sarcomere; Stress fibers; Titin

Indexed keywords

ALPHA ACTININ; C TITIN; CONNECTIN; MYOSIN; UNCLASSIFIED DRUG;

ARTICLE; BRUSH BORDER; CHICKEN; CONTROLLED STUDY; FIBROBLAST; GENE SEQUENCE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; MEGAKARYOBLAST; MOLECULAR BIOLOGY; MUSCLE CELL; MUSCLE STRESS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; SKIN FIBROBLAST; THROMBOCYTE FUNCTION; WESTERN BLOTTING;

ANIMALS; BLOOD PLATELETS; BLOTTING, WESTERN; EXONS; FIBROBLASTS; GENE EXPRESSION REGULATION; HUMANS; MICE; MICROFILAMENTS; MUNTJACS; MUSCLE PROTEINS; NIH 3T3 CELLS; PROTEIN ISOFORMS; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STRESS FIBERS;

CERVIDAE; MUNTIACUS MUNTJAK; ORYCTOLAGUS CUNICULUS;

EID: 34249021781     PISSN: 08861544     EISSN: 10970169     Source Type: Journal    
DOI: 10.1002/cm.20193     Document Type: Article

References (59)

1. Atkinson RA, Joseph C, Dal PF, Birolo L, Stier G, Pucci P, Pastore A. 2000. Binding of α-actinin to titin: Implications for Z-disk assembly. Biochemistry 39:5255-5264.
2. Bang ML, Centner T, Fornoff F, Geach AJ, Gotthardt M, McNabb M, Witt CC, Labeit D, Gregorio CC, Granzier H, 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.
3. Chi RJ, Olenych SG, Kim K, Keller TC, III. 2005. Smooth muscle α-actinin interaction with smitin. Int J Biochem Cell Biol 37:1470-1482.
4. Coulis G, Sentandreu MA, Bleimling N, Gautel M, Benyamin Y, Ouali A. 2004. Myofibrillar tightly bound calcium in skeletal muscle fibers: A possible role of this cation in titin strands aggregation. FEBS Lett 556:271-275.
5. Eilertsen KJ, Keller TC, III. 1992. Identification and characterization of two huge protein components of the brush border cytoskeleton: Evidence for a cellular isoform of titin. J Cell Biol 119:549-557.
6. Eilertsen KJ, Kazmierski ST, Keller TC, III. 1994. Cellular titin localization in stress fibers and interaction with myosin II filaments in vitro. J Cell Biol 126:1201-1210.
7. Eilertsen KJ, Kazmierski ST, Keller TC, III. 1997. Interaction of α- actinin with cellular titin. Eur J Cell Biol 74:361-364.
8. Faulkner G, Pallavicini A, Comelli A, Salamon M, Bortoletto G, Ievolella C, Trevisan S, Kojic' S, Dalla VF, Laveder P, Valle G, Lanfranchi G. 2000. FATZ, a filamin-, actinin-, and telethonin-binding protein of the Z-disc of skeletal muscle. J Biol Chem 275:41234-41242.
9. Forbes JG, Jin AJ, Ma K, Gutierrez-Cruz G, Tsai WL, Wang K. 2005. Titin PEVK segment: Charge-driven elasticity of the open and flexible polyampholyte. J Muscle Res Cell Motil 26:291-301.
10. Fugman DA, Witte DP, Jones CL, Aronow BJ, Lieberman MA. 1990. In vitro establishment and characterization of a human megakaryoblastic cell line. Blood 75:1252-1261.
11. Furst DO, Vinkemeier U, Weber K. 1992. Mammalian skeletal muscle C-protein: Purification from bovine muscle, binding to titin and the characterization of a full-length human cDNA. J Cell Sci 102 (Part 4):769-778.
12. Gautel M, Goulding D, Bullard B, Weber K, Furst DO. 1996. The central Z-disk region of titin is assembled from a novel repeat in variable copy numbers. J Cell Sci 109 (Part 11):2747-2754.
13. Granzier H, Labeit S. 2002. Cardiac titin: An adjustable multi-functional spring. J Physiol 541:335-342.
14. Granzier H, Helmes M, Cazorla O, McNabb M, Labeit D, Wu Y, Yamasaki R, Redkar A, Kellermayer M, Labeit S, Trombitas K. 2000. Mechanical properties of titin isoforms. Adv Exp Med Biol 481:283-300.
15. Grater F, Shen J, Jiang H, Gautel M, Grubmuller H. 2005. Mechanically induced titin kinase activation studied by force-probe molecular dynamics simulations. Biophys J 88:790-804.
16. Gregorio CC, Perry CN, McElhinny AS. 2005. Functional properties of the titin/connectin-associated proteins, the muscle-specific RING finger proteins (MURFs), in striated muscle. J Muscle Res Cell Motil 26:389-400.
17. Gregorio CC, Trombitas K, Centner T, Kolmerer B, Stier G, Kunke K, Suzuki K, Obermayr F, Herrmann B, Granzier H, Sorimachi H, Labeit S. 1998. 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 143:1013-1027.
18. Gutierrez-Cruz G, Van Heerden AH, Wang K. 2001. Modular motif, structural folds and affinity profiles of the PEVK segment of human fetal skeletal muscle titin. J Biol Chem 276:7442-7449.
19. Helmes M, Trombitas K, Centner T, Kellermayer M, Labeit S, Linke WA, Granzier H. 1999. Mechanically driven contour-length adjustment in rat cardiac titin's unique N2B sequence: Titin is an adjustable spring. Circ Res 84:1339-1352.
20. Hoshijima M. 2006. Mechanical stress-strain sensors embedded in cardiac cytoskeleton: Z disk, titin, and associated structures. Am J Physiol Heart Circ Physiol 290:H1313-H1325.
21. Hotulainen P, Lappalainen P. 2006. Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J Cell Biol 173:383-394.
22. Houmeida A, Holt J, Tskhovrebova L, Trinick J. 1995. Studies of the interaction between titin and myosin. J Cell Biol 131:1471-1481.
23. Katoh K, Kano Y, Masuda M, Onishi H, Fujiwara K. 1998. Isolation and contraction of the stress fiber. Mol Biol Cell 9:1919-1938.
24. Keller TC, III. 1995. Structure and function of titin and nebulin. Curr Opin Cell Biol 7:32-38.
25. Keller TC, III, Eilertsen K, Higginbotham M, Kazmierski S, Kim KT, Velichkova M. 2000. Role of titin in nonmuscle and smooth muscle cells. Adv Exp Med Biol 481:265-277.
26. Kim K, Keller TC, III. 2002. Smitin, a novel smooth muscle titin-like protein, interacts with myosin filaments in vivo and in vitro. J Cell Biol 156:101-111.
27. Kontrogianni-Konstantopoulos A, Bloch RJ. 2005. Obscurin: A multi-tasking muscle giant. J Muscle Res Cell Motil 26:419-426.
28. Kontrogianni-Konstantopoulos A, Catino DH, Strong JC, Randall WR, Bloch RJ. 2004. Obscurin regulates the organization of myosin into A bands. Am J Physiol Cell Physiol 287:C209-C217.
29. Kontrogianni-Konstantopoulos A, Catino DH, Strong JC, Sutter S, Borisov AB, Pumplin DW, Russell MW, Bloch RJ. 2006. Obscurin modulates the assembly and organization of sarcomeres and the sarcoplasmic reticulum. FASEB J 20:2102-2111.
30. Labeit S, Kolmerer B. 1995. Titins: Giant proteins in charge of muscle ultrastructure and elasticity. Science 270:293-296.
31. Labeit S, Lahmers S, Burkart C, Fong C, McNabb M, Witt S, Witt C, Labeit D, Granzier H. 2006. Expression of distinct classes of titin isoforms in striated and smooth muscles by alternative splicing, and their conserved interaction with filamins. J Mol Biol 362:664-681.
32. Langanger G, Moeremans M, Daneels G, Sobieszek A, De BM, De MJ. 1986. The molecular organization of myosin in stress fibers of cultured cells. J Cell Biol 102:200-209.
33. Lange S, Xiang F, Yakovenko A, Vihola A, Hackman P, Rostkova E, Kristensen J, Brandmeier B, Franzen G, Hedberg B, Gunnarsson LG, Hughes SM, Marchand S, Sejersen T, Richard I, Edstrom L, Ehler E, Udd B, Gautel M. 2005. The kinase domain of titin controls muscle gene expression and protein turnover. Science 308:1599-1603.
34. Linke WA, Ivemeyer M, Olivieri N, Kolmerer B, Ruegg JC, Labeit S. 1996. Towards a molecular understanding of the elasticity of titin. J Mol Biol 261:62-71.
35. Linke WA, Ivemeyer M, Labeit S, Hinssen H, Ruegg JC, Gautel M. 1997. Actin-titin interaction in cardiac myofibrils: Probing a physiological role. Biophys J 73:905-919.
36. Linke WA, Rudy DE, Centner T, Gautel M, Witt C, Labeit S, 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.
37. Ma K, Wang K. 2003. Malleable conformation of the elastic PEVK segment of titin: Non-co-operative interconversion of polyproline II helix, β-turn and unordered structures. Biochem J 374:687-695.
38. Ma K, Forbes JG, Gutierrez-Cruz G, Wang K. 2006. Titin as a giant scaffold for integrating stress and Src homology domain 3-mediated signaling pathways: The clustering of novel overlap ligand motifs in the elastic PEVK segment. J Biol Chem 281:27539-27556.
39. Mayans O, van der Ven PF, Wilm M, Mues A, Young P, Furst DO, Wilmanns M, Gautel M. 1998. Structural basis for activation of the titin kinase domain during myofibrillogenesis. Nature 395:863-869.
40. Miller G, Musa H, Gautel M, Peckham M. 2003. A targeted deletion of the C-terminal end of titin, including the titin kinase domain, impairs myofibrillogenesis. J Cell Sci 116:4811-4819.
41. Muhle-Goll C, Habeck M, Cazorla O, Nilges M, Labeit S, Granzier H. 2001. Structural and functional studies of titin's fn3 modules reveal conserved surface patterns and binding to myosin S1-a possible role in the Frank-Starling mechanism of the heart. J Mol Biol 313:431-447.
42. Nicholas G, Thomas M, Langley B, Somers W, Patel K, Kemp CF, Sharma M, Kambadur R. 2002. Titin-cap associates with, and regulates secretion of, Myostatin. J Cell Physiol 193:120-131.
43. Obermann WM, Gautel M, Weber K, Furst DO. 1997. Molecular structure of the sarcomeric M band: Mapping of titin and myosin binding domains in myomesin and the identification of a potential regulatory phosphorylation site in myomesin. EMBO J 16:211-220.
44. Ojima K, Ono Y, Hata S, Koyama S, Doi N, Sorimachi H. 2005. Possible functions of p94 in connectin-mediated signaling pathways in skeletal muscle cells. J Muscle Res Cell Motil 26:409-417.
45. Peterson LJ, Rajfur Z, Maddox AS, Freel CD, Chen Y, Edlund M, Otey C, Burridge K. 2004. Simultaneous stretching and contraction of stress fibers in vivo. Mol Biol Cell 15:3497-3508.
46. Sandquist JC, Swenson KI, Demali KA, Burridge K, Means AR. 2006. Rho kinase differentially regulates phosphorylation of nonmucle myosin II isoforms A and B during cell rounding and migration. J Biol Chem 281:35873-35883.
47. Sanger JW, Sanger JM, Jockusch BM. 1983. Differences in the stress fibers between fibroblasts and epithelial cells. J Cell Biol 96:961-969.
48. Sorimachi H, Freiburg A, Kolmerer B, Ishiura S, Stier G, Gregorio CC, Labeit D, Linke WA, Suzuki K, Labeit S. 1997. Tissue-specific expression and α-actinin binding properties of the Z-disc titin: Implications for the nature of vertebrate Z-discs. J Mol Biol 270:688-695.
49. Trinick J. 1994. Titin and nebulin: Protein rulers in muscle? Trends Biochem Sci 19:405-409.
50. Tskhovrebova L, Trinick J. 2003. Titin: Properties and family relationships. Nat Rev Mol Cell Biol 4:679-689.
51. Turnacioglu KK, Mittal B, Dabiri GA, Sanger JM, Sanger JW. 1997. Zeugmatin is part of the Z-band targeting region of titin. Cell Struct Funct 22:73-82.
52. Wang SM, Greaser ML. 1985. Immunocytochemical studies using a monoclonal antibody to bovine cardiac titin on intact and extracted myofibrils. J Muscle Res Cell Motil 6:293-312.
53. Warren CM, Krzesinski PR, Campbell KS, Moss RL, Greaser ML, 2004. Titin isoform changes in rat myocardium during development. Mech Dev 121:1301-1312.
54. Witt CC, Oliyieri N, Centner T, Kolmerer B, Millevoi S, Morell J, Labeit D, Labeit S, Jockusch H, Pastore A. 1998. A survey of the primary structure and the interspecies conservation of I-band titin's elastic elements in vertebrates. J Struct Biol 122:206-215.
55. Young P, Gautel M. 2000. The interaction of titin and α-actinin is controlled by a phospholipid-regulated intramolecular pseudo-ligand mechanism. EMBO J 19:6331-6340.
56. Young P, Ferguson C, Banuelos S, Gautel M. 1998. Molecular structure of the sarcomeric Z-disk: Two types of titin interactions lead to an asymmetrical sorting of α-actinin. EMBO J 17:1614-1624.
57. Young P, Ehler E, Gautel M. 2001. Obscurin, a giant sarcomeric Rho guanine nucleotide exchange factor protein involved in sarcomere assembly. J Cell Biol 154:123-136.
58. Zastrow MS, Flaherty DB, Benian GM, Wilson KL. 2006. Nuclear titin interacts with A- and B-type lamins in vitro and in vivo. J Cell Sci 119:239-249.
59. Zou P, Pinotsis N, Lange S, Song YH, Popov A, Mavridis I, Mayans OM, Gautel M, Wilmanns M. 2006. Palindromic assembly of the giant muscle protein titin in the sarcomeric Z-disk. Nature 439:229-233.