Nebulin regulates the assembly and lengths of the thin filaments in striated muscle

Journal of Cell Biology

Volumn 170, Issue 6, 2005, Pages 947-957

  McElhinny, Abigail S ^a   Schwach, Catherine ^a   Valichnac, Melinda ^a   Mount Patrick, Sarah ^a   Gregorio, Carol C ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LATRUNCULIN B; NEBULIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEPOLYMERIZATION; FETUS; HEART MUSCLE CELL; IMAGING; MUSCLE DEVELOPMENT; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; REGULATORY MECHANISM; RNA INTERFERENCE; SKELETAL MUSCLE; STAINING; TECHNOLOGY; THIN FILAMENT;

ACETIC ACIDS; ACTINS; ANIMALS; ANTIBODIES, MONOCLONAL; BICYCLO COMPOUNDS, HETEROCYCLIC; BLOTTING, WESTERN; CELLS, CULTURED; CHROMONES; DOSE-RESPONSE RELATIONSHIP, DRUG; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; FLUORESCENT DYES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICROSCOPY, FLUORESCENCE; MUSCLE DEVELOPMENT; MUSCLE PROTEINS; MUSCLE, SKELETAL; MYOBLASTS; MYOCYTES, CARDIAC; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; THIAZOLES; THIAZOLIDINES; TRANSFECTION; XANTHENES;

EID: 24944524470     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200502158     Document Type: Article

References (55)

1. Bang, M.L., R.E. Mudry, A.S. McElhinny, K. Trombitas, A.J. Geach, R. Yamasaki, H. Sorimachi, H. Granzier, C.C. Gregorio, and S. Labeit. 2001. Myopalladin, a novel 145-kilodalton sarcomeric protein with multiple roles in Z-disc and I-band protein assemblies. J. Cell Biol. 153:413-427.
2. Beall, C.J., M.A. Sepanski, and E.A. Fyrberg. 1989. Genetic dissection of Drosophila myofibril formation: effects of actin and myosin heavy chain null alleles. Genes Dev. 3:131-140.
3. Buday, L. 1999. Membrane-targeting of signalling molecules by SH2/SH3 domain-containing adaptor proteins. Biochim. Biophys. Acta. 1422:187-204.
4. Centner, T., F. Fougerousse, A. Freiburg, C. Witt, J.S. Beckmann, H. Granzier, K. Trombitas, C.C. Gregorio, and S. Labeit. 2000. Molecular tools for the study of titin's differential expression. Adv. Exp. Med. Biol. 481:35-49.
5. Chen, M.J., C.L. Shih, and K. Wang. 1993. Nebulin as an actin zipper. A twomodule nebulin fragment promotes actin nucleation and stabilizes actin filaments. J. Biol. Chem. 268:20327-20334.
6. Clark, K.A., A.S. McElhinny, M.C. Beckerle, and C.C. Gregorio. 2002. Striated muscle cytoarchitecture: an intricate web of form and function. Annu. Rev. Cell Dev. Biol. 18:637-706.
7. Donner, K., M. Sandbacka, V.L. Lehtokari, C. Wallgren-Pettersson, and K. Pelin. 2004. Complete genomic structure of the human nebulin gene and identification of alternatively spliced transcripts. Eur. J. Hum. Genet. 12:744-751.
8. Fock, U., and H. Hinssen. 2002. Nebulin is a thin filament protein of the cardiac muscle of the agnathans. J. Muscle Res. Cell Motil. 23:205-213.
9. Gonsior, S.M., M. Gautel, and H. Hinssen. 1998. A six-module human nebulin fragment bundles actin filaments and induces actin polymerization. J. Muscle Res. Cell Motil. 19:225-235.
10. Granzier, H.L.M., and K. Wang. 1993. Gel electrophoresis of giant proteins: solubilization and silver staining of titin and nebulin from single muscle fiber segments. Electrophoresis. 14:56-64.
11. Gregorio, C.C., and V.M. Fowler. 1995. Mechanisms of thin filament assembly in embryonic chick cardiac myocytes: tropomodulin requires tropomyosin for assembly. J. Cell Biol. 129:683-695.
12. Gregorio, C.C., A. Weber, M. Bondad, C.R. Pennise, and V.M. Fowler. 1995. Requirement of pointed-end capping by tropomodulin to maintain actin filament length in embryonic chick cardiac myocytes. Nature. 377:83-86.
13. Jin, J.P., and K. Wang. 1991. Nebulin as a giant actin-binding template protein in skeletal muscle sarcomere. Interaction of actin and cloned human nebulin fragments. FEBS Lett. 281:93-96.
14. Kazmierski, S.T., P.B. Antin, C.C. Witt, N. Huebner, A.S. McElhinny, S. Labeit, and C.C. Gregorio. 2003. The complete mouse nebulin gene sequence and the identification of cardiac nebulin. J. Mol. Biol. 328:835-846.
15. Kioka, N., K. Ueda, and T. Amachi. 2002. Vinexin, CAP/ponsin, ArgBP2: a novel adaptor protein family regulating cytoskeletal organization and signal transduction. Cell Struct. Funct. 27:1-7.
16. Labeit, S., and B. Kolmerer. 1995. The complete primary structure of human nebulin and its correlation to muscle structure. J. Mol. Biol. 248:308-315.
17. Linke, W.A., D.E. Rudy, T. Centner, M. Gautel, C. Witt, S. Labeit, and C.C. Gregorio. 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.
18. Littlefield, R., and V.M. Fowler. 1998. Defining actin filament length in striated muscle: rulers and caps or dynamic stability? Annu. Rev. Cell Dev. Biol. 14:487-525.
19. Littlefield, R., A. Almenar-Queralt, and V.M. Fowler. 2001. Actin dynamics at pointed ends regulates thin filament length in striated muscle. Nat. Cell Biol. 3:544-551.
20. Luther, P.K., R. Padron, S. Ritter, R. Craig, and J.M. Squire. 2003. Heterogeneity of Z-band structure within a single muscle sarcomere: implications for sarcomere assembly. J. Mol. Biol. 332:161-169.
21. Mardahl-Dumesnil, M., and V.M. Fowler. 2001. Thin filaments elongate from their pointed ends during myofibril assembly in Drosophila indirect flight muscle. J. Cell Biol. 155:1043-1053.
22. Mayer, B.J. 2001. SH3 domains: complexity in moderation. J. Cell Sci. 114: 1253-1263.
23. McElhinny, A.S., B. Kolmerer, V.M. Fowler, S. Labeit, and C.C. Gregorio. 2001. The N-terminal end of nebulin interacts with tropomodulin at the pointed ends of the thin filaments. J. Biol. Chem. 276:583-592.
24. McElhinny, A.S., K. Kakinuma, H. Sorimachi, S. Labeit, and C.C. Gregorio. 2002. 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. J. Cell Biol. 157:125-136.
25. McElhinny, A.S., S.T. Kazmierski, S. Labeit, and C.C. Gregorio. 2003. Nebulin: the nebulous, multifunctional giant of striated muscle. Trends Cardiovasc. Med. 13:195-201.
26. Michele, D.E., F.P. Albayya, and J.M. Metzger. 1999. Thin filament protein dynamics in fully differentiated adult cardiac myocytes: toward a model of sarcomere maintenance. J. Cell Biol. 145:1483-1495.
27. Millevoi, S., K. Trombitas, B. Kolmerer, S. Kostin, J. Schaper, K. Pelin, H. Granzier, and S. Labeit. 1998. Characterization of nebulette and nebulin and emerging concepts of their roles for vertebrate Z-discs. J. Mol. Biol. 282:111-123.
28. Mogami, K., P.T. O'Donnell, S.I. Bernstein, T.R. Wright, and C.P. Emerson Jr. 1986. Mutations of the Drosophila myosin heavy-chain gene: effects on transcription, myosin accumulation, and muscle function. Proc. Natl. Acad. Sci. USA. 83:1393-1397.
29. Moncman, C.L., and K. Wang. 1995. Nebulette: a 107 kD nebulin-like protein in cardiac muscle. Cell Motil. Cytoskeleton. 32:205-225.
30. Moncman, C.L., and K. Wang. 1996. Assembly of nebulin into the sarcomeres of avian skeletal muscle. Cell Motil. Cytoskeleton. 34:167-184.
31. Moncman, C.L., and K. Wang. 2002. Targeted disruption of nebulette protein expression alters cardiac myofibril assembly and function. Exp. Cell Res. 273:204-218.
32. Mudry, R.E., C.N. Perry, M. Richards, V.M. Fowler, and C.C. Gregorio. 2003. The interaction of tropomodulin with tropomyosin stabilizes thin filaments in cardiac myocytes. J. Cell Biol. 162:1057-1068.
33. Nwe, T.M., K. Maruyama, and Y. Shimada. 1999. Relation of nebulin and connectin (titin) to dynamics of actin in nascent myofibrils of cultured skeletal muscle cells. Exp. Cell Res. 252:33-40.
34. O'Donnell, P.T., and S.I. Bernstein. 1988. Molecular and ultrastructural defects in a Drosophila myosin heavy chain mutant: differential effects on muscle function produced by similar thick filament abnormalities. J. Cell Biol. 107:2601-2612.
35. Ojima, K., Z.X. Lin, M. Bang, S. Holtzer, R. Matsuda, S. Labeit, H.L. Sweeney, and H. Holtzer. 2000. Distinct families of Z-line targeting modules in the COOH-terminal region of nebulin. J. Cell Biol. 150:553-566.
36. Pfuhl, M., S.J. Winder, and A. Pastore. 1994. Nebulin, a helical actin binding protein. EMBO J. 13:1782-1789.
37. Robinson, T.F., and S. Winegrad. 1979. The measurement and dynamic implications of thin filament lengths in heart muscle. J. Physiol. 286:607-619.
38. Root, D.D., and K. Wang. 1994. Calmodulin-sensitive interaction of human nebulin fragments with actin and myosin. Biochemistry. 33:12581-12591.
39. Root, D.D., and K. Wang. 2001. High-affinity actin-binding nebulin fragments influence the actoS1 complex. Biochemistry. 40:1171-1186.
40. Roulier, E.M., C. Fyrberg, and E. Fyrberg. 1992. Perturbations of Drosophila α- actinin cause muscle paralysis, weakness, and atrophy but do not confer obvious nonmuscle phenotypes. J. Cell Biol. 116:911-922.
41. Schafer, D.A., C. Hug, and J.A. Cooper. 1995. Inhibition of CapZ during myofibrillogenesis alters assembly of actin filaments. J. Cell Biol. 128:61-70.
42. Schroeter, J.P., J.P. Bretaudiere, R.L. Sass, and M.A. Goldstein. 1996. Three-dimensional structure of the Z band in a normal mammalian skeletal muscle. J. Cell Biol. 133:571-583.
43. Shimada, Y., M. Komiyama, S. Begum, and K. Maruyama. 1996. Development of connectin/titin and nebulin in striated muscles of chicken. Adv. Biophys. 33:223-234.
44. Shimada, Y., H. Suzuki, and A. Konno. 1997. Dynamics of actin in cardiac myofibrils and fibroblast stress fibers. Cell Struct. Funct. 22:59-64.
45. Stedman, H., K. Browning, N. Oliver, M. Oronzi-Scott, K. Fischbeck, S. Sarkar, J. Sylvester, R. Schmickel, and K. Wang. 1988. Nebulin cDNAs detect a 25-kilobase transcript in skeletal muscle and localize to human chromosome 2. Genomics. 2:1-7.
46. Sussman, M.A., S. Baque, C.S. Uhm, M.P. Daniels, R.L. Price, D. Simpson, L. Terracio, and L. Kedes. 1998a. Altered expression of tropomodulin in cardiomyocytes disrupts the sarcomeric structure of myofibrils. Circ. Res. 82:94-105.
47. Sussman, M.A., S. Welch, N. Cambon, R. Klevitsky, T.E. Hewett, R. Price, S.A. Witt, and T.R. Kimball. 1998b. Myofibril degeneration caused by tropomodulin overexpression leads to dilated cardiomyopathy in juvenile mice. J. Clin. Invest. 101:51-61.
48. Suzuki, H., M. Komiyama, A. Konno, and Y. Shimada. 1998. Exchangeability of actin in cardiac myocytes and fibroblasts as determined by fluorescence photobleaching recovery. Tissue Cell. 30:274-280.
49. Trinick, J. 1994. Titin and nebulin protein rulers in muscle? Trends Biochem. Sci. 19:405-408.
50. van der Ven, P.F., J.W. Bartsch, M. Gautel, H. Jockusch, and D.O. Furst. 2000. A functional knock-out of titin results in defective myofibril assembly. J. Cell Sci. 113:1405-1414.
51. Wang, K., and C.L. Williamson. 1980. Identification of an N2-line protein of striated muscle. Proc. Natl. Acad. Sci. USA. 77:3254-3258.
52. Wang, K., and J. Wright. 1988. 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. 107:2199-2212.
53. Wang, K., M. Knipfer, Q.Q. Huang, A. van Heerden, L.C. Hsu, G. Gutierrez, X.L. Quian, and H. Stedman. 1996. Human skeletal muscle nebulin sequence encodes a blueprint for thin filament architecture. Sequence motifs and affinity profiles of tandem repeats and terminal SH3. J. Biol. Chem. 271:4304-4314.
54. Weber, A., C.C. Pennise, G.G. Babcock, and V.M. Fowler. 1994. Tropomodulin caps the pointed ends of actin filaments. J. Cell Biol. 127:1627-1635.
55. Zhang, J.Q., G. Luo, A.H. Herrera, B. Paterson, and R. Horowits. 1996. cDNA cloning of mouse nebulin. Evidence that the nebulin-coding sequence is highly conserved among vertebrates. Eur. J. Biochem. 239:835-841.