Caenorhabditis elegans UNC-96 is a new component of M-lines that interacts with UNC-98 and paramyosin and is required in adult muscle for assembly and/or maintenance of thick filaments

Molecular Biology of the Cell

Volumn 17, Issue 9, 2006, Pages 3832-3847

  Mercer, Kristina B ^a   Miller, Rachel K ^a,b   Tinley, Tina L ^a,b   Sheth, Seema ^a   Qadota, Hiroshi ^a   Benian, Guy M ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; GENOMIC DNA; PARAMYOSIN; PROTEIN; UNC 96 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CROSS LINKING; ELECTRON MICROSCOPY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; IMMUNOFLUORESCENCE MICROSCOPY; MOLECULAR CLONING; MUSCLE FIBRIL; MYOFILAMENT; MYOPATHY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SARCOMERE; TRANSGENE; TWO HYBRID SYSTEM; WESTERN BLOTTING; YEAST;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CARRIER PROTEINS; GENES, HELMINTH; MICROFILAMENTS; MOLECULAR SEQUENCE DATA; MOVEMENT; MUSCLE PROTEINS; MUSCLES; MUTATION; MYOFIBRILS; PEPTIDES; PHENOTYPE; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; TEMPERATURE; TROPOMYOSIN;

CAENORHABDITIS ELEGANS;

EID: 33748289980     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-02-0144     Document Type: Article

References (68)

1. Barral, J. M., Bauer, C. C., Ortiz, I., and Epstein, H. F. (1998). Unc-45 mutations in Caenorhabditis elegans implicate a CRO1/She4p-like domain in myosin assembly. J. Cell Biol. 143, 1215-1225.
2. Barral, J. M., Hutagalung, A H., Brinker, A., Hartl, F. U., and Epstein, H. F. (2002). Role of the myosin assembly protein UNC-45 as a molecular chaperone for myosin. Science 295, 669-671.
3. Barstead, R. J., and Waterston, R. H. (1991). Vinculin is essential for muscle function in the nematode. J. Cell Biol. 114, 715-724.
4. Benian, G. M., Kiff, J. E., Neckelmann, N., Moerman, D. G., and Waterston, R. H. (1989). The sequence of twitchin: an unusually large protein implicated in regulation of myosin activity in C. elegans. Nature 342, 45-50.
5. Benian, G. M., L'Hernault, S. W., and Morris, M. E. (1993). Additional sequence complexity in the muscle gene, unc-22, and its encoded protein, twitchin, of C. elegans. Genetics 134, 1097-1104.
6. Benian, G. M., Tinley, T. L., Tang, X., and Borodovsky, M. (1996). The C. elegans gene unc-89, required for muscle M-line assembly, encodes a giant modular protein composed of immunoglobulin and signal transduction domains. J. Cell Biol. 132, 835-848.
7. Bodine, S. C., et al. (2001). Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294, 1704-1708.
8. Broday, L., Kolotuev, I., Didier, C., Bhoumik, A., Podbilewicz, B., and Ronai, Z. (2004). The LIM domain protein UNC-95 is required for the assembly of muscle attachment structures and is regulated by the RING finger protein RNF-5 in C. elegans. J. Cell Biol. 165, 857-867.
9. Centner, T., et al. (2001). J. Mol. Biol. 306, 717-726.
10. Deitiker, P. R., and Epstein, H. F. (1993). Thick filament substructures in C. elegans: evidence for two populations of paramyosin. J. Cell Biol. 123, 303-311.
11. Didier, C., et al. (2003). RNF5, a RING finger protein that regulates cell motility by targeting paxillin ubiquitination and altered localization. Mol. Cell Biol. 23, 5331-5345.
12. Epstein, H. F., Berliner, G. C., Casey, D. L., and Ortiz, I. (1988). Purified thick filaments form the nematode C. elegans: evidence for multiple proteins associated with core structures. J. Cell Biol. 106, 1985-1995.
13. Epstein, H. F., Casey, D. L., and Ortiz, I. (1993). Myosin and paramyosin of Caenorhabditis elegans embryos assemble into nascent structures distinct from thick filaments and multi-filament assemblages. J. Cell Biol. 122, 845-858.
14. Epstein, H. F., Lu, G. Y., Deitiker, P. R., Ortiz, I., and Schmid, M. F. (1995). Preliminary three-dimensional model for nematode thick filament core. J. Struct. Biol. 115, 163-174.
15. Epstein, H. F., Miller, D. M., Ortiz, I., and Berliner, G. C. (1985). Myosin and paramyosin are organized around a newly identified core structure. J. Cell Biol. 100, 904-915.
16. Epstein, H. F., Waterston, R. H., and Brenner, S. (1974). A mutant affecting the heavy chain of myosin in C. elegans. J. Mol. Biol. 90, 291-300.
17. Ferrara, T. M., Flaherty, D. B., and Benian, G. M. (2005). Titin/connectin-related proteins in C. elegans: a review and new findings. J. Muse. Res. Cell Motil. 26, 435-447.
18. Flaherty, D. B., Gernert, K. M., Shmeleva, N., Tang, X., Mercer, K. B., Borodovsky, M., and Benian, G. M. (2002). Titins in C. elegans with unusual features: coiled-coil domains, novel regulation of kinase activity and two new possible elastic regions. J. Mol. Biol. 323, 533-549.
19. Francis, G. R., and Waterston, R. H. (1985). Muscle organization in C. elegans: localization of proteins implicated in thin filament attachment and I-band organization. J. Cell Biol. 101, 1532-1549.
20. Gengyo-Ando, K., and Kagawa, H. (1991). Single charge change on the helical surface of the paramyosin rod dramatically disrupts thick filament assembly in Caenorhabditis elegans. J. Mol. Biol. 219, 429-441.
21. Gettner, S. N., Kenyon, C., and Reichardt, L. F. (1995). Characterization of βPAT-3 heterodimers, a family of essential integrin receptors in C. elegans. J. Cell Biol. 129, 1127-1141.
22. Gotthardt, M., Hammer, R. E., Hubner, N., Monti, J., Witt, C. C., McNabb, M., Richardson, J. A., Granzier, H., Labeit, S., and Herz, J. (2003). Conditional expression of mutant M-line titins results in cardiomyopathy with altered sarcomere structure. J. Biol. Chem. 278, 6059-6065.
23. Grater, F., Shen, J., Jiang, H., Gautel, M., and Grubmuller, H. (2005). Mechanically induced titin kinase activation studied by force-probe molecular dynamics simulations. Biophys. J. 88, 790-804.
24. Gregorio, C. C., and Antin, P. B. (2000). To the heart of myofibril assembly. Trends Cell Biol. 10, 355-362.
25. Hannak, E., Oegema, K., Kirkham, M., Gonczy, P., Habermann, B., and Hyman, A. A. (2002). The kinetically dominant assembly pathway for centrosomal asters in C. elegans is γ-tubulin dependent. J. Cell Biol. 157, 591-602.
26. Hill, K. L., Harfe, B. D., Dobbins, C. A., and L'Hernault, S. W. (2000). dpy-18 encodes an alpha-subunit of prolyl-4-hydroxylase in C. elegans. Genetics 155, 1139-1148.
27. Hobert, O., Moerman, D. G., Clark, K. A., Beckerle, M. C., and Ruvkun, G. (1999). A conserved LIM protein that affects muscular adherens junction integrity and mechanosensory function in C. elegans. J. Cell Biol. 144, 45-57.
28. Hoppe, T., Cassata, G., Barral, J. M., Springer, W., Hutagalung, A. H., Epstein, H. F., and Baumeister, R. (2004). Regulation of the myosin-directed chaperone UNC-45 by a novel E3/E4-multiubiquirylation complex in C. elegans. Cell 118, 337-349.
29. Hresko, M. C., Williams, B. D., and Waterston, R. H. (1994). Assembly of body wall muscle and muscle cell attachment structures in C. elegans. J. Cell Biol. 124, 491-506.
30. Ito, H., Fukuda, Y., Murata, K., and Kimura, A. (1983). Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168.
31. James, P., Halladay, J., and Craig, E. A. (1996). Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144, 1425-1436.
32. Kagawa, H., Gengyo, K., McLachlan, A. D., Brenner, S., and Karn, J. (1989). Paramyosin gene (unc-15) of Caenorhabditis elegans: molecular cloning, nucleotide sequence and models of thick filament structure. J. Mol. Biol. 207, 311-333.
33. Kamath, R. S., and Ahringer, J. (2003). Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30, 313-321.
34. Knappeis, G. G., and Carlsen, F. (1968). The ultrastructure of the M line in skeletal muscle. J. Cell Biol. 38, 202-211.
35. Lange, S., et al. (2005). The kinase domain of titin controls muscle gene expression and protein turnover. Science 308, 1599-1603.
36. Lin, X., Qadota, H., Moerman, D. G., and Williams, B. D. (2003). C. elegans PAT-6/actopaxin plays a critical role in the assembly of integrin adhesion complexes in vivo. Curr. Biol. 13, 922-932.
37. Liu, F., Ortiz, I., Hutagalung, A., Bauer, C. C., Cook, R. G., and Epstein, H. F. (2000). Differential assembly of α- and γ-filagenins into thick filaments in Caenorhabditis elegans. J. Cell Sci. 113, 4001-4012.
38. Luther, P., and Squire, J. (1978). Three-dimensional structure of the vertebrate muscle M-region. J. Mol. Biol. 125, 313-324.
39. Mackinnon, A. C., Qadota, H., Norman, K. R., Moerman, D. G., and Williams, B. D. (2002). C. elegans PAT-4/ILK functions as an adaptor protein within integrin adhesion complexes. Curr. Biol. 12, 787-797.
40. Maruyama, I. N., Miller, D. M., and Brenner, S. (1989). Myosin heavy chain gene amplification as a suppressor mutation in Caenorhabditis elegans. Mol. Gen. Genet. 219, 113-118.
41. Mercer, K. B., Flaherty, D. B., Miller, R. K., Qadota, H., Tinley, T. L., Moerman, D. G., and Benian, G. M. (2003). C. elegans UNC-98, a C2H2 Zn finger protein, is a novel partner of UNC-97/PINCH in muscle adhesion complexes. Mol. Biol. Cell 14, 2492-2507.
42. Miller, D. M., Ortiz, I., Berliner, G. C., and Epstein, H. F. (1983). Differential localization of two myosins within nematode thick filaments. Cell 34, 477-490.
43. Miller, D. M., Stockdale, F. E., and Karn, J. (1986). Immunological identification of the genes encoding the four myosin heavy chain isoforms of Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 83, 2305-2309.
44. Minamide, L. S., and Bamburg, J. R. (1990). A filter paper dye-binding assay for quantitative determination of protein without interference from reducing agents or detergents. Anal. Biochem. 190, 66-70.
45. Mitch, W. E., and Goldberg, A. L. (1996). Mechanisms of muscle wasting: the role of the ubiquitin-proteasome pathway. N. Engl. J. Med. 335, 1897-1905.
46. Moerman, D. G., Benian, G. M., Barstead, R. J., Schreifer, L., and Waterston, R. H. (1988). Identification and intracellular localization of the unc-22 gene product of C. elegans. Genes Devel. 2, 93-105.
47. Moerman, D. G., and Fire, A. (1997). Muscle: structure, function and development. In: C. elegans II., ed. D. L. Riddle, T. Blumenthal, B. J. Meyer, and J. R. Priess, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 417-470.
48. Moerman, D. G., and Williams, B. D. (2006). Sarcomere assembly in C. elegans muscle. In: WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook. 1.81.1. http://www.wormbook.org.
49. Moulder, G. L., Huang, M. M., Waterston, R. H., and Barstead, R. J. (1996). Talin requires β-integrin, but not vinculin, for its assembly into focal adhesion-like structures in the nematode C. elegans. Mol. Biol. Cell 7, 1181-1193.
50. Muller, S. A., Haner, M., Ortiz, I., Aebi, U., and Epstein, H. F. (2001). STEM analysis of Caenorhabditis elegans muscle thick filaments: evidence for microdifferentiated substructures. J. Mol. Biol. 305, 1035-1044.
51. Nonet, M. L., Grundahl, K., Meyer, B. J., and Rand, J. B. (1993). Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell 73, 1291-1305.
52. Ono, S. (2001). The C. elegans unc-78 gene encodes a homologue of actin-interacting protein 1 required for organized assembly of muscle actin filaments. J. Cell Biol. 152, 1313-1319.
53. Riddle, D. L., and Brenner, S. (1978). Indirect suppression in C. elegans. Genetics 89, 299-314.
54. Rogalski, T. M., Mullen, G. P., Gilbert, M. M., Williams, B. D., and Moerman, D. G. (2000). The UNC-112 gene in C. elegans encodes a novel component of cell-matrix adhesion structures required for integrin localization in the muscle cell membrane. J. Cell Biol. 150, 253-264.
55. Rogalski, T. M., Williams, B. D., Mullen, G. P., and Moerman, D. G. (1993). Products of the unc-52 gene in C. elegans are homologous to the core protein of the mammalian basement membrane heparin sulfate proteoglycan. Genes Dev. 7, 1471-1484.
56. Schachat, F., Garcea, R. L., and Epstein, H. F. (1978). Myosins exist as homodimers of heavy chains: demonstration with specific antibody purified by nematode mutant myosin affinity chromatography. Cell 15, 405-411.
57. Simmer, F., Tijsterman, M., Parrish, S., Koushika, S. P., Nonet, M. L., Fire, A., Ahringer, J., and Plasterk, R.H.A. (2002). Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Curr. Biol. 12, 1317-1319.
58. Small, T. M., Gernert, K. M., Flaherty, D. B., Mercer, K. B., Borodovsky, M., and Benian, G. M. (2004). Three new isoforms of C. elegans UNC-89 containing MLCK-like protein kinase domains. J. Mol. Biol. 342, 91-108.
59. Soto, M. C., Qadota, H., Kasuya, K., Inoue, M., Tsuboi, D., Mello, C. C., and Kaibuchi, K. (2002). The GEX-2 and GEX-3 proteins are required for tissue morphogenesis and cell migrations in C. elegans. Genes Dev. 16, 620-632.
60. Tsuboi, D., Qadota, H., Kasuya, K., Amano, M., and Kaibuchi, K. (2002). Isolation of the interacting molecules with GEX-3 by a novel functional screening. Biochem. Biophys. Res. Commun. 292, 697-701.
61. Waterston, R. H. (1988). Muscle. In: The Nematode Caenorhabditis elegans, ed. W. B. Wood, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 281-335.
62. Waterston, R. H. (1989). The minor myosin heavy chain, MHC A, of Caenorhabditis elegans is necessary for the initiation of thick filament assembly. EMBO J. 8, 3429-3436.
63. Waterston, R. H., Epstein, H. F., and Brenner, S. (1974). Paramyosin of Caenorhabditis elegans. J. Mol. Biol. 90, 285-290.
64. Waterston, R. H., Fishpool, R. M., and Brenner, S. (1977). Mutants affecting paramyosin in Caenorhabditis elegans. J. Mol. Biol. 117, 679-697.
65. Waterston, R. H., Thomson, J. N., and Brenner, S. (1980). Mutants with altered muscle structure in C. elegans. Dev. Biol. 77, 271-302.
66. Weiner, O. D., Servant, G., Welch, M. D., Mitchison, T. J., Sedat, J. W., and Bourne, H. R. (1999). Spatial control of actin polymerization during neutrophil chemotaxis. Nat. Cell Biol. 1, 75-81.
67. Williams, B. D., and Waterston, R. H. (1994). Genes critical for muscle development and function in C. elegans identified through lethal mutations. J. Cell Biol. 124, 475-490.
68. Zengel, J. M., and Epstein, H. F. (1980). Identification of genetic elements associated with muscle structure in C. elegans. Cell Motil. 1, 73-97.