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C. Elegans Model for Studying Tropomyosin and Troponin Regulations of Muscle Contraction and Animal Behavior

  • Hiroaki Kagawa
  • Tomohide Takaya
  • Razia Ruksana
  • Frederick Anokye-Danso
  • Md. Ziaul Amin
  • Hiromi Terami
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 592)

Abstract

There are two muscle tissues in the nematode Caenorhabditis elegans: the pharynx for feeding and the body wall for locomotion. These correspond to cardiac and skeletal muscles in vertebrates, respectively. Study of the muscle genes of C. elegans can be classified into three stages; first, mutant isolation and gene mapping, second, cloning and sequencing of the gene, and third, complete sequences of all genes. Many uncoordinated mutant animals have been isolated (Brenner, 1974; Waterston, 1988; Moerman and Fire, 1997) and the complete amino acid sequence of myosin heavy chain, twitchin, and paramyosin, (invertebrate specific core protein of thick filament), and were the first determined in any animals by analyzing the unc-54, unc-22, and unc-15 mutants, respectively (Karn et al., 1983; Benian et al., 1989; Kagawa et al., 1989). Tropomyosin and troponin components are also present but as with actin and myosin heavy chain in the worm, there are some differences in gene structure and sequence compared to those in other animals (Kagawa et al., 1995; Myers et al., 1996; Moerman and Fire, 1997). Deficiencies of body wall troponin C or tropomyosin in C. elegans cause the Pat (paralyzed arrest at embryonic two-fold stage) phenotype (Williams and Waterston, 1994; Terami et al., 1999) and those of troponin T cause Mup (muscle position abnormal) phenotype (Myers et al., 1996). After determining the complete genome sequences of the nematode (The C. elegans Sequence Consortium, 1998), we can find out how isoforms are related to each other. Only one troponin C gene, pat-10/tnc-1, is expressed in the body wall muscles and the gene defect causes a developmental arrest of the animals (Terami et al., 1999).

Keywords

Caenorhabditis Elegans Myosin Heavy Chain Body Wall Mutant Animal Nematode Caenorhabditis Elegans 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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14.4. References

  1. Anyanful, A., Sakube, Y., Takuwa, K., and Kagawa, H., 2001, The third and fourth tropomyosin isoforms of Caenorhabditis elegans are expressed in the pharynx and intestines and are essential for development and morphology, J. Mol. Biol. 313:525–537.PubMedCrossRefGoogle Scholar
  2. Benian, G. M., Kiff, J. E., Neckelmann, N., Moerman, D. G., and Waterston, W. H., 1989, Sequence of unusually large protein implicated in regulation of myosin activity in C. elegans, Nature 342:45–50.PubMedCrossRefGoogle Scholar
  3. Benoist, P., Mas, J. A., Marco, R., and Cervera, M., 1998, Different muscle-type expression of the Drosophila troponin T gene, J. Biol. Chem. 273:7538–7546.PubMedCrossRefGoogle Scholar
  4. Brenner, S., 1974, The genetics of Caenorhabditis elegans, Genetics 77:71–94.PubMedGoogle Scholar
  5. Burkeen, A. K., Maday, S. L., Rybicka, K. K., Sulcove, J. A., Ward, J., Huang, M. M., Barstead, R., Franzini-Armstrong, Allen, T. Stc., 2004, Disruption of Caenorhabditis elegans muscle structure and function caused by mutation troponin I, Biophys. J. 86:991–1001.PubMedCrossRefGoogle Scholar
  6. Domingo, A., Gonzalez-Jurado, J., Maroto, M., Diaz, C., Vinòs, J., Carrasco, C., Cervera, M., and Marco, R., 1998, Troponin T is a calcium-binding protein in insect muscle in vivo phosphorylation, muscle-specific isoforms and developmental profile in Drosophila melanogaster, J. Muscle Res. Cell Motil. 19:393–403.PubMedCrossRefGoogle Scholar
  7. Fyrberg, E., Fyrberg, C. C., Beall, C., and Saville, D. L., 1990, Drosophila melanogaster troponin T mutations engender three distinct syndromes of myofibrillar abnormalities, J. Mol. Biol. 216:657–675.PubMedCrossRefGoogle Scholar
  8. 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 for thick filament structure, J. Mol. Biol. 207:311–333.PubMedCrossRefGoogle Scholar
  9. Kagawa, H., Sugimoto, K., Matsumoto, S., Inoue, T., Imadzu, H., Takuwa, K., and Sakube, Y., 1995, Genome structure, mapping and expression of the tropomyosin gene tmy-1 of Caenorhabditis elegans, J. Mol. Biol. 251:603–613.PubMedCrossRefGoogle Scholar
  10. Kagawa, H., Takuwa, K., and Sakube, Y., 1997, Mutations and expressions of the tropomyosin gene and the troponin C gene of Caenorhabditis elegans, Cell Struct. Funct. 22:213–218.PubMedCrossRefGoogle Scholar
  11. Kamath, R. S., Fraser, A. G., Dong, Y., Poulin, G., Durbin, R., Gotta, M., Kanapin, A., Le Bot, N., Moreno, S., Sohrmann, M., Welchman, D. P., Zipperlen, P., and Ahringer, J., 2003, Systematical functional analysis of the Caenorhabditis elegans genome using RNAi, Nature 421:231–237.PubMedCrossRefGoogle Scholar
  12. Karn, J., Brenner, S., and Barnett, L., 1983, Protein structural domains in the Caenorhabditis elegans unc-54 myosin heavy chain gene are not separated by introns, Proc. Natl. Acad. Sci., USA 80:4253–4257.PubMedCrossRefGoogle Scholar
  13. Lewis, J. A., Wu, C.-H., Berg, H., and Levin, J. H., 1980, The genetics study levamisole resistance in the nematode Caenorhabditis elegans, Genetics 95:905–928.PubMedGoogle Scholar
  14. Moerman, D. G., and Fire, A., 1997, Muscle: Structure, function and development, in: C. elegans II, D. L. Riddle, T. Blumenthal, B. J. Meyer, and J. R. Priess, eds, Cold Spring Harbor Laboratory Press, New York, pp. 417–470.Google Scholar
  15. Myers, C. D., Goh, P. Y., Allen, T. S., Bucher, E. A., and Bogaert, T., 1996, Developmental genetics analysis of troponin T mutations in striated and nonstriated muscle cells of Caenorhabditis elegans, J. Cell Biol. 132:1061–1077.PubMedCrossRefGoogle Scholar
  16. Ohtsuki, I., Maruyama, K., and Ebashi, S., 1986, Regulatory and cytoskeletal proteins of vertebrate skeletal muscle, Adv. Protein Chem. 38:1–67.PubMedCrossRefGoogle Scholar
  17. Ono, S., and Ono, K., 2002, Tropomyosin inhibits ADF/cofilin-dependent actin filament dynamics, J. Cell Biol. 156:1065–1076.PubMedCrossRefGoogle Scholar
  18. Ono, K., and Ono, S., 2004, Tropomyosin and troponit are required for ovarian contraction in the Caenorhabditis elegans reproductive system, Mol. Biol. Cell 15:2782–2793.PubMedCrossRefGoogle Scholar
  19. Ruksana, R., Kuroda, K., Terami, H., Bando, T., Kitaoka, S., Takaya, T., Sakube, Y., and Kagawa, H., 2005, Tissue expression of four troponin I genes and their molecular interactions with two troponin C isoforms in Caenorhabditis elegans, Genes Cells 10:261–276.PubMedCrossRefGoogle Scholar
  20. Shiraishi, F., Kambara, M., and Ohtsuki, I., 1992, Replacement of troponin components in myofibrils, J. Biochem. (Tokyo) 111:61–65.Google Scholar
  21. Takeda, S., Yamashita, A., Maeda, K., and Maeda, Y., 2003, Structure of the core domain of human cardiac troponin in the Ca2+-saturated form, Nature 424:35–41.PubMedCrossRefGoogle Scholar
  22. Tanaka, H., Takeya, Y., Doi, T., Yumoto, F., Tanokura, M., Ohtsuki, I., Nishita, K., and Ojima, T., 2005, Comparative studies on the functional roles of N-and C-terminal regions of molluskan and vertebrate troponin I, FEBS J. 272:4475–4486.PubMedCrossRefGoogle Scholar
  23. Terami, H., Williams, B. D., Kitamura, S., Sakube, Y., Matsumoto, S., Doi, S., Obinata, T., and Kagawa, H., 1999, Genomic organization, expression and analysis of the Troponin C gene pat-10 of Caenorhabditis elegans, J. Cell Biol. 146:93–202.Google Scholar
  24. Terami, H. 2002 Molecular studies on body wall-and pharyngeal troponin C isoforms in Caenorhabditis elegans Ph. D thesis, Okayama UniversityGoogle Scholar
  25. The C. elegans Sequence Consortium, 1998, Genome sequence of the nematode C. elegans: A platform for investigating biology, Science 282:2012–2018.CrossRefGoogle Scholar
  26. Ueda, T, Katsuzaki, H., Terami, H., Ohtsuka, H., Kagawa, H., Murase, T., Kajiwara, Y., Yoshioka, O., and Iio, T., 2001, Calcium-binding of wild type and mutant troponin Cs of Caenorhabditis elegans, Biochim. Biophys. Acta 1548:220–228.PubMedGoogle Scholar
  27. Vassylyev, D. G., Takeda, S., Wakatsuki, S., Maeda, K., and Maeda, Y., 1998, Crystal structure of troponin C in complex with troponin I fragment at 2.3-A° resolution, Proc. Natl. Acad. Sci. USA 95:4847–4852.PubMedCrossRefGoogle Scholar
  28. Waterston, R. H., 1988, Muscle, in: The nematode Caenorhabditis elegans, W. B. Wood, ed., Cold Spring Harbor Laboratory Press, New York, pp. 281–335.Google Scholar
  29. White, S. P., Cohen, C., and Phillips, G. N. Jr, 1987, Structure of co-crystals of tropomyosin and troponin, Nature 325:826–828.PubMedCrossRefGoogle Scholar
  30. Williams, B. D., and Waterston, R. H., 1994, Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations, J. Cell Biol. 124:475–490.PubMedCrossRefGoogle Scholar
  31. WormBase; http://www.wormbase.org/ or WormBase, RNAi; http://www.wormbase.org/db/searches/rnai_search TNT; http://www.wormbase.org/db/misc/paper?name=WBPaper00010575;class=PaperGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Hiroaki Kagawa
    • 1
  • Tomohide Takaya
    • 1
  • Razia Ruksana
    • 1
  • Frederick Anokye-Danso
    • 1
  • Md. Ziaul Amin
    • 1
  • Hiromi Terami
    • 1
  1. 1.Division of Bioscience, Graduate School of Science and TechnologyOkayama UniversityJapan

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