Nebulin interacts with CapZ and regulates thin filament architecture within the Z-disc

Molecular Biology of the Cell

Volumn 19, Issue 5, 2008, Pages 1837-1847

  Pappas, Christopher T ^b   Bhattacharya, Nandini ^c   Cooper, John A ^c   Gregorio, Carol C ^a,b  

^a UNIVERSITY OF ARIZONA   (United States)

^b University of Arizona   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; NEBULIN; PROTEIN CAPZ; SMALL INTERFERING RNA; TRYPTOPHAN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DEPOLYMERIZATION; FLUORESCENCE; MOLECULAR MODEL; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RAT; REDUCTION; SARCOMERE; SKELETAL MUSCLE; THIN FILAMENT;

AMINO ACID SEQUENCE; ANIMALS; BINDING, COMPETITIVE; BIOLOGICAL ASSAY; CAPZ ACTIN CAPPING PROTEIN; CHICKENS; FLUORESCENCE; GENE EXPRESSION REGULATION; MICE; MICROFILAMENTS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUSCLE FIBERS; MUSCLE PROTEINS; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RATS; SARCOMERES;

EID: 48249127189     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-07-0690     Document Type: Article

References (52)

1. Almenar-Queralt, A., Gregorio, C. C., and Fowler, V. M. (1999). Tropomodulin assembles early in myofibrillogenesis in chick skeletal muscle: evidence that thin filaments rearrange to form striated myofibrils. J. Cell Sci. 112, 1111-1123.
2. Ao, X., and Lehrer, S. S. (1995). Phalloidin unzips nebulin from thin filaments in skeletal myofibrils. J. Cell Sci. 108, 3397-3403.
3. Babcock, G., and Fowler, V. M. (1994). Isoform specific interaction of tropomodulin with skeletal muscle and erythrocyte tropomyosins. J. Biol. Chem. 269, 27510-27518.
4. Bang, M. L., Gregorio, C., and Labeit, S. (2002). Molecular dissection of the interaction of desmin with the C-terminal region of nebulin. J. Struct. Biol. 137, 119-127.
5. Bang, M. L., Li, X., Littlefield, R., Bremner, S., Thor, A., Knowlton, K. U., Lieber, R. L., and Chen, J. (2006). Nebulin-deficient mice exhibit shorter thin filament lengths and reduced contractile function in skeletal muscle. J. Cell Biol. 173, 905-916.
6. Bang, M. L., Mudry, R. E., McElhinny, A. S., Trombitas, K., Geach, A. J., Yamasaki, R., Sorimachi, H., Granzier, H., Gregorio, C. C., and Labeit, S. (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.
7. Bukatina, A. E., Sonkin, B. Y., Alievskaya, L. L., and Yashin, V. A. (1984). Sarcomere structures in the rabbit psoas muscle as revealed by fluorescent analogs of phalloidin. Histochemistry 81, 301-304.
8. Caldwell, J. E., Heiss, S. G., Mermall, V., and Cooper, J. A. (1989). Effects of CapZ, an actin capping protein of muscle, on the polymerization of actin. Biochemistry 28, 8506-8514.
9. Casella, J. F., and Torres, M. A. (1994). Interaction of Cap Z with actin. The NH2-terminal domains of the alpha 1 and beta subunits are not required for actin capping, and alpha 1 beta and alpha 2 beta heterodimers bind differentially to actin. J. Biol. Chem. 269, 6992-6998.
10. Cooper, J. A. (1987). Effects of cytochalasin and phalloidin on actin. J. Cell Biol. 105, 1473-1478.
11. Fock, U., and Hinssen, H. (2002). Nebulin is a thin filament protein of the cardiac muscle of the agnathans. J. Muscle Res. Cell Motil. 23, 205-213.
12. Fowler, V. M., McKeown, C. R., and Fischer, R. S. (2006). Nebulin: does it measure up as a ruler? Curr. Biol. 16, R18-R20.
13. Fyrberg, C., Ketchum, A., Ball, E., and Fyrberg, E. (1998). Characterization of lethal Drosophila melanogaster alpha-actinin mutants. Biochem. Genet. 36, 299-310.
14. Gregorio, C. C., and Fowler, V. M. (1995). Mechanisms of thin filament assembly in embryonic chick cardiac myocytes: tropomodulin requires tropomyosin for assembly. J. Cell Biol. 129, 683-695.
15. Hart, M. C., and Cooper, J. A. (1999). Vertebrate isoforms of actin capping protein beta have distinct functions in vivo. J. Cell Biol. 147, 1287-1298.
16. Herrera, A. H., Elzey, B., Law, D. J., and Horowits, R. (2000). Terminal regions of mouse nebulin: sequence analysis and complementary localization with N-RAP. Cell Motil. Cytoskeleton 45, 211-222.
17. Horowits, R. (2006). Nebulin regulation of actin filament lengths: new angles. Trends Cell Biol. 16, 121-124.
18. Jin, J. P., and Wang, K. (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.
19. Kazmierski, S. T., Antin, P. B., Witt, C. C., Huebner, N., McElhinny, A. S., Labeit, S., and Gregorio, C. C. (2003). The complete mouse nebulin gene sequence and the identification of cardiac nebulin. J. Mol. Biol. 328, 835-846.
20. Labeit, S., and Kolmerer, B. (1995). The complete primary structure of human nebulin and its correlation to muscle structure. J. Mol. Biol. 248, 308-315.
21. Lin-Jones, J., and Hauschka, S. D. (1997). Skeletal and cardiac α-actin isoforms exhibit unanticipated temporal and tissue-specific gene expression patterns in developing avian limbs and embryos. Dev. Biol. 189, 322-334.
22. Littlefield, R., and Fowler, V. M. (1998). Defining actin filament length in striated muscle: rulers and caps or dynamic stability? Annu. Rev. Cell Dev. Biol. 14, 487-525.
23. Luther, P. K., Barry, J. S., and Squire, J. M. (2002). The three-dimensional structure of a vertebrate wide (slow muscle) Z-band: lessons on Z-band assembly. J. Mol. Biol. 315, 9-20.
24. McElhinny, A. S., Kazmierski, S. T., Labeit, S., and Gregorio, C. C. (2003). Nebulin: the nebulous, multifunctional giant of striated muscle. Trends Cardiovasc. Med. 13, 195-201.
25. McElhinny, A. S., Kolmerer, B., Fowler, V. M., Labeit, S., and Gregorio, C. C. (2001). The N-terminal end of nebulin interacts with tropomodulin at the pointed ends of the thin filaments. J. Biol. Chem. 276, 583-592.
26. McElhinny, A. S., Schwach, C., Valichnac, M., Mount-Patrick, S., and Gregorio, C. C. (2005). Nebulin regulates the assembly and lengths of the thin filaments in striated muscle. J. Cell Biol. 170, 947-957.
27. Millevoi, S., Trombitas, K., Kolmerer, B., Kostin, S., Schaper, J., Pelin, K., Granzier, H., and Labeit, S. (1998). Characterization of nebulette and nebulin and emerging concepts of their roles for vertebrate Z-discs. J. Mol. Biol. 282, 111-123.
28. Moncman, C. L., and Wang, K. (2000). Architecture of the thin filament-Z-line junction: lessons from nebullete and nebulin homologies. J. Muscle Res. Cell Motil. 21, 153-169.
29. Narita, A., Takeda, S., Yamashita, A., Maeda, Y. (2006). Structural basis of actin filament capping at the barbed-end: a cryo-electron microscopy study. EMBO J. 25, 5626-5633.
30. Nave, R., Furst, D. O., and Weber, K. (1990). Interaction of alpha-actinin and nebulin in vitro. Support for the existence of a fourth filament system in skeletal muscle. FEBS Lett. 269, 163-166.
31. Ohtsuki, I. (1975). Distribution of troponin components in the thin filament studied by immunoelectron microscopy. J. Biochem. 77, 633-639.
32. Palmgren, S., Ojala, P. J., Wear, M. A., Cooper, J. A., and Lappalainen, P. (2001). Interactions with PIP2, ADP-actin monomers, and capping protein regulate the activity and localization of yeast twinfilin. J. Cell Biol. 155, 251-260.
33. Pfuhl, M., Winder, S. J., and Pastore, A. (1994). Nebulin, a helical actin binding protein. EMBO J. 13, 1782-1789.
34. Rowe, R.W.D. (1973). The ultrastructure of Z discs from white, intermediate, and red fibers of mammalian striated muscles. J. Cell Biol. 57, 261-277.
35. Schafer, D. A., Hug, C., and Cooper, J. A. (1995). Inhibition of CapZ during myofibrillogenesis alters assembly of actin filaments. J. Cell Biol. 128, 61-70.
36. Schafer, D. A., Korshunova, Y. O., Schroer, T. A., and Cooper, J. A. (1994). Differential localization and sequence analysis of capping protein beta-subunit isoforms of vertebrates. J. Cell Biol. 127, 453-465.
37. Seeley, M., Huang, W., Chen, Z., Wolff, W. O., Lin, X., Xu, X. (2007). Depletion of zebrafish titin reduces cardiac contractility by disrupting the assembly of Z-discs and A-bands. Circ. Res. 100, 238-245.
38. Stromer, M. H., and Goll, D. E. (1972). Studies on purified-actinin. II. Electron microscopic studies on the competitive binding of -actinin and tropomyosin to Z-line extracted myofibrils. J. Mol. Biol. 67, 489-494.
39. Szczesna, D., and Lehrer, S. S. (1993). The binding of fluorescent phallotoxins to actin in myofibrils. J. Muscle Res. Cell Motil. 14, 594-597.
40. Trinick, J. (1994). Titin and nebulin protein rulers in muscle? Trends Biochem. Sci. 19, 405-408.
41. Urbanik, E., and Ware, B. R. (1989). Actin filament capping and cleaving activity of cytochalasins B, D, E, and H. Arch. Biochem. Biophys. 269, 181-187.
42. Wang, K., Knipfer, M., Huang, Q. Q., van Heerden, A., Hsu, L. C., Gutierrez, G., Quian, X. L., and Stedman, H. (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.
43. Wang, K., and Williamson, C. L. (1980). Identification of an N2-line protein of striated muscle. Proc. Natl. Acad. Sci. USA 77, 3254-3258.
44. Wang, K., and Wright, J. (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.
45. Wear, M. A., and Cooper, J. A. (2004). Capping protein binding to S100B: implications for the tentacle model for capping the actin filament barbed end. J. Biol. Chem. 279, 14382-14390.
46. Wear, M. A., Yamashita, A., Kim, K., Maeda, Y., and Cooper, J. A. (2003). How capping protein binds the barbed end of the actin filament. Curr. Biol. 13, 1531-1537.
47. Wilson, P., Fuller, E., and Forer, A. (1987). Irradiations of rabbit myofibrils with an ultraviolet microbeam. II. Phalloidin protects actin in solution but not in myofibrils from depolymerization by ultraviolet light. Biochem. Cell Biol. 65, 376-385.
48. Witt, C. C., Burkart, C., Labeit, D., McNabb, M., Wu, Y., Granzier, H., and Labeit, S. (2006). Nebulin regulates thin filament length, contractility, and Z-disc structure in vivo. EMBO J. 25, 3843-3855.
49. Wright, J., Huang, Q. Q., and Wang, K. (1993). Nebulin is a full-length template of actin filaments in the skeletal muscle sarcomere: an immunoelectron microscopic study of its orientation and span with site-specific monoclonal antibodies. J. Muscle Res. Cell Motil. 14, 476-483.
50. Yamashita, A., Maeda, K., and Maeda, Y. (2003). Crystal structure of CapZ: structural basis for actin filament barbed end capping. EMBO J. 22, 1529-1538.
51. Zhukarev, V., Sanger, J. M., Sanger, J. W., Goldman, Y. E., and Shuman, H. (1997). Distribution and orientation of rhodamine-phalloidin bound to thin filaments in skeletal and cardiac myofibrils. Cell Motil. Cytoskeleton 37, 363-377.
52. Zou, P., Pinotsis, N., Lange, S., Song, Y. H., Popov, A., Mavridis, I., Mayans, O. M., Gautel, M., Wilmanns, M. (2006). Palindromic assembly of the giant muscle protein titin in the sarcomeric Z-disc. Nature 439, 229-233.