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Journal of Muscle Research & Cell Motility

, Volume 26, Issue 6–8, pp 435–447 | Cite as

Titin/connectin-related proteins in C. elegans: a review and new findings

  • Tracey M. Ferrara
  • Denise B. Flaherty
  • Guy M. Benian
Article

Keywords

Kinase Domain Myosin Light Chain Kinase Body Wall Muscle Pharyngeal Muscle Protein Kinase Domain 
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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Notes

Acknowledgements

We thank the following individuals for generating and sending to us unc-89 mutant alleles: Gary Moulder and Robert Barstead (Oklahoma Medical Research Foundation) for ok1116, Shohei Mitani (Tokyo Women’s Medical University) for tm752, and Laurent Segalat (University of Lyon) for five cx alleles. We thank Kim Gernert for helping us analyze some new aspects of the twitchin sequences. We are grateful to our lab colleagues, Kristie Mercer and Rachel Miller, for helpful comments and discussion. We also thank the NIH for their financial support (grant no. AR051466).

References

  1. Bagnato P, Barone V, Giacomello E, Rossi D, Sorrentino V, (2003) Binding of an ankyrin-1 isoform to obscurin suggests a molecular link between the sarcoplasmic reticulum and myofibrils in striated muscles J Cell Biol 160:245–253PubMedCrossRefGoogle Scholar
  2. Bang M-L, 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 ~700-kDa titin isoform, and its interaction with obscurin identify a novel Z-line to I-band linking system Circ Res 89:1065–1072PubMedGoogle Scholar
  3. Barral JM, Bauer CC, Ortiz I, Epstein HF, (1998) unc-45 mutations in C. elegans implicate a CRO1/She4p-like domain in myosin assembly J Cell Biol 143:1215–1225PubMedCrossRefGoogle Scholar
  4. Benian GM, Kiff JE, Neckelmann N, Moerman DG, Waterston RH, (1989) The sequence of twitchin: an unusually large protein implicated in regulation of myosin activity in C. elegans Nature 342:45–50PubMedCrossRefGoogle Scholar
  5. Benian GM, L’Hernault SW, Morris ME, (1993) Additional sequence complexity in the muscle gene, unc-22, and its encoded protein, twitchin, of C. elegans Genetics 134:1097–1104PubMedGoogle Scholar
  6. Benian GM, Tinley TL, Tang X, Borodovsky M, (1996) The C. elegans gene unc-89, required for muscle M-line assembly, encodes a giant modular protein composed of Ig and signal transduction domains J Cell Biol 132:835–848PubMedCrossRefGoogle Scholar
  7. Blomberg N, Baraldi E, Sattler M, Saraste M, Nilges M, (2000) Structure of a PH domain from the C. elegans muscle protein UNC-89 suggests a novel function Structure 8:1079–1087PubMedCrossRefGoogle Scholar
  8. Blumenthal T, Steward K, (1997) RNA processing and gene structure In: Riddle D, Blumentha T, Meyer BJ, Priess JR, (eds.). C. elegans II Cold Spring Harbor Laboratory Press New York pp. 117–145Google Scholar
  9. Borisov AB, Raeker MO, Kontrogianni-Konstantopoulos A, Yang K, Kurnit DM, Bloch RJ, Russell MW, (2003) Rapid response of cardiac obscurin gene cluster to aortic stenosis: differential activation of Rho-GEF and MLCK and involvement in hypertrophic growth Biochem Biophys Res Commun 310:910–918PubMedCrossRefGoogle Scholar
  10. Champagne MB, Edwards KA, Erickson HP, Kiehart DP, (2000) Drosophila stretchin-MLCK is a novel member of the titin/myosin light chain kinase family J Mol Biol 300:759–777PubMedCrossRefGoogle Scholar
  11. Chen M, Cheng A, Candotti F, Zhou Y-J, Hymel A, Fasth A, Notarangelo LD, O’Shea JJ, (2000) Complex effects of naturally occurring mutations in the JAK3 pseudokinase domain: evidence for interactions between the kinase and pseudokinase domains Mol Cell Biol 20:947–956PubMedCrossRefGoogle Scholar
  12. De Toledo M, Colombo K, Nagase T, Ohara O, Fort P, Blangy A, (2000) The yeast exchange assay, a new complementary method to screen for Dbl-like protein specificity: identification of a novel RhoA exchange factor FEBS Lett 480(2–3):287–292PubMedCrossRefGoogle Scholar
  13. Flaherty DB, Gernert KM, Shmeleva N, Tang X, Mercer KB, Borodovsky M, Benian GM, (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 323:533–549PubMedCrossRefGoogle Scholar
  14. Freiburg A, Trombitas K, Hell W, Cazorla O, Fougerousse F, Centner T, Kolmerer B, Witt C, Beckmann JS, Gregorio CC, Granzier H, Labeit S, (2000) Series of exon-skipping events in the elastic spring region of titin as the structural basis of myofibrillar elastic diversity Circ Res 86:1114–1121PubMedGoogle Scholar
  15. Fukuzawa A, Shimamura J, Takemori S, Kanzawa N, Yamaguchi M, Sun P, Maruyama K, Kimura S, (2001) Invertebrate connectin spans as much as 3.5 μm in the giant sarcomeres of crayfish claw muscle EMBO J 20:4826–4835PubMedCrossRefGoogle Scholar
  16. Funabara D, Watabe S, Mooers SU, Narayan S, Dudas C, Hartshorne DJ, Siegman MJ, Butler TM, (2003). Twitchin from molluscan catch muscle J Biol Chem 278:29308–29316PubMedCrossRefGoogle Scholar
  17. Gerull B, Gramlich M, Atherton J, McNabb M, Trombitas K, Sasse-Klaassen S, Seidman JG, Seidman C, Granzier H, Labeit S, Frenneaux M, Thierfelder L, (2002) Mutations of TTN, encoding the giant muscle filament titin, cause familial dilated cardiomyopathy Nat Gen 30:201–204CrossRefGoogle Scholar
  18. Granzier H, Labeit S, (2002) Cardiac titin: an adjustable multi-functional spring J Physiol 541.2:335–342CrossRefGoogle Scholar
  19. Greaser M, (2001) Identification of new repeating motifs in titin Proteins 43:145–149PubMedCrossRefGoogle Scholar
  20. Gutierrez-Cruz G, Van Heerden A, Wang K, (2001) Modular motif, structural folds and affinity profiles of PEVK segment of human fetal skeletal muscle titin J Biol Chem 276:7442–7449PubMedCrossRefGoogle Scholar
  21. Hackman P, Vihola A, Haravuori H, Marchand S, Sarparanta J, de Seze J, Labeit S, Witt C, Peltonen L, Richard I, Udd B, (2002) Tibial muscular dystrophy is a titinopathy caused by mutations in TTN, the gene encoding the giant skeletal-muscle protein titin Am J Hum Genet 71:492–500PubMedCrossRefGoogle Scholar
  22. Hakeda S, Endo S, Saigo K, (2000) Requirements of kettin, a giant muscle protein highly conserved in overall structure in evolution, for normal muscle function, viability, and flight activity of Drosophila J Cell Biol 148:101–114PubMedCrossRefGoogle Scholar
  23. Heierhorst J, Probst WC, Kohanski RA, Buku A, Weiss KR, (1995) Phosphorylation of myosin regulatory light chains by the molluscan twitchin kinase Eur J Biochem 233:426–431PubMedCrossRefGoogle Scholar
  24. Heierhorst J, Tang X, Lei J, Probst WC, Weiss KR, Kemp BE, Benian GM, (1996) Substrate specificity and inhibitor sensitivity of Ca2+/S100-dependent twitchin kinases Eur J Biochem 242:454–459PubMedCrossRefGoogle Scholar
  25. Hobert O, Moerman DG, Clark KA, Beckerle MC, Ruvkun G, (1999) A conserved LIM protein that affects muscular adherens junction integrity and mechanosensory function in C. elegans J Cell Biol 144:45–57PubMedCrossRefGoogle Scholar
  26. Hsieh C, Fukumoto S, Layne MD, Maemura K, Charles H, Patel A, Perrella MA, Lee M, (2000) Striated muscle preferentially expressed genes α and β are two serine/threonine protein kinases derived from the same gene as the aortic preferentially expressed Gene-1 J Biol Chem 275:36966–36973PubMedCrossRefGoogle Scholar
  27. Hu S-H, Parker MW, Lei J, Wilce MCJ, Benian GM, Kemp BE, (1994) Insights into autoregulation from the crystal structure of twitchin kinase Nature 369:581–584PubMedCrossRefGoogle Scholar
  28. Itoh-Satoh M, Takeharu H, Nishi H, Koga Y, Arimura T, Koyanagi T, Megumi T, Shigeru H, Ueda K, Nouchi T, Hiroe M, Marumo F, Imaizumi T, Yasunami M, Kimura A, (2002) Titin mutations as the molecular basis for dilated cardiomyopathy Biochem Biophys Res Comm 291:385–393PubMedCrossRefGoogle Scholar
  29. Kobe B, Heierhorst J, Feil SC, Parker MW, Benian GM, Weiss KR, Kemp BE, (1996) Giant protein kinases: domain interactions and structural basis of autoregulation EMBO J 15:6810–6821PubMedGoogle Scholar
  30. Kolmerer B, Clayton J, Benes V, Allen T, Ferguson C, Leonard K, Weber U, Knekt M, Ansorge W, Labeit S, Bullard B, (2000) Sequence and expression of the kettin gene in Drosophila melanogaster and Caenorhabditis elegans J Mol Biol 296(2):435–448PubMedCrossRefGoogle Scholar
  31. Kontrogianni-Konstantopoulos A, Jones EM, Van Rossum DB, Bloch RJ, (2003) Obscurin is a ligand for small ankyrin 1 in skeletal muscle Mol Biol Cell 14:1138–1148PubMedCrossRefGoogle Scholar
  32. 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–C217PubMedCrossRefGoogle Scholar
  33. Lei J, Tang X, Chambers TC, Pohl J, Benian GM, (1994) Protein kinase domain of twitchin has protein kinase activity and an autoinhibitory region J Biol Chem 269:21078–21085PubMedGoogle Scholar
  34. Linke WA, Granzier H, (1998) A spring tale: new facts on titin elasticity Biophys J 75:2613–2614PubMedCrossRefGoogle Scholar
  35. Liu J, Rost B, (2003) NORSp: predictions of long regions without regular secondary structure Nucl Acids Res 31:3833–3835PubMedCrossRefGoogle Scholar
  36. Liu J, Tan H, Rost B, (2002) Loopy proteins appear conserved in evolution J Mol Biol 322:53–64PubMedCrossRefGoogle Scholar
  37. Mercer KB, Flaherty DB, Miller RK, Qadota H, Tinley TL, Moerman DG, Benian GM, (2003) Caenorhabditis elegans UNC-98, a C2H2 Zn finger protein, is a novel partner of UNC-97/PINCH in muscle adhesion complexes Mol Biol Cell 14:2492–2507PubMedCrossRefGoogle Scholar
  38. Moerman DG, Benian GM, Waterston RH, (1986) Molecular cloning of the muscle gene unc-22 in C. elegans by Tc1 transposon tagging Proc Natl Acad Sci USA 83:2579–2583PubMedCrossRefGoogle Scholar
  39. Moerman DG, Benian GM, Barstead RJ, Schreifer L, Waterston RH, (1988) Identification and intracellular localization of the unc-22 gene product of C. elegans Genes Develop 2:93–105PubMedGoogle Scholar
  40. Moerman DG, Fire A, (1997) Muscle: structure, function and development In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR, (eds.) C. elegans II Cold Spring Harbor Laboratory Press Cold Spring Harbor, New York pp. 417–470Google Scholar
  41. Probst WC, Cropper EC, Heierhorst J, Hooper SL, Jaffe H, Vilim F, Beushausen S, Kupfermann I, Weiss KR, (1994) cAMP-dependent phosphorylation of Aplysia twitchin may mediate modulation of muscle contractions by neuropeptide cotransmitters Proc Natl Acad Sci USA 91:8487–8491PubMedCrossRefGoogle Scholar
  42. Rogalski TM, Gilbert MM, Devenport D, Norman KR, Moerman DG, (2003) DIM-1, a novel immunoglobulin superfamily protein in C. elegans, is necessary for maintaining body wall muscle integrity Genetics 163:905–915PubMedGoogle Scholar
  43. Russell MW, Raeker MO, Korytkowski KA, Sonneman KJ, (2002) Identification, tissue expression and chromosomal localization of human Obscurin-MLCK, a member of the titin and Dbl families of myosin light chain kinases Gene 282:237–246PubMedCrossRefGoogle Scholar
  44. Siegman MJ, Funabara D, Kinoshita S, Watabe S, Hartshorne DJ, Butler TM, (1998) Phosphorylation of a twitchin-related protein controls catch and calcium sensitivity of force production in invertebrate smooth muscle Proc Natl Acad Sci USA 95:5383–5388PubMedCrossRefGoogle Scholar
  45. Small TM, Flaherty DB, Mercer KB, Borodovsky M, Benian GM, (2001) A new isoform of UNC-89 with two MLCK-like protein kinase domains Mol Biol Cell 12:37aGoogle Scholar
  46. Small TM, Flaherty DB, Gernert K, Borodovsky M, Benian GM, (2003) Two new isoforms of UNC-89 (C. elegans obscurin) containing MLCK-like protein kinase domains Mol Biol Cell 14:46aGoogle Scholar
  47. Small TM, Gernert KM, Flaherty DB, Mercer KB, Borodovsky M, Benian GB, (2004) Three new isoforms of C. elegans UNC-89 containing MLCK-like protein kinase domains J Mol Biol 342:91–108PubMedCrossRefGoogle Scholar
  48. Southgate R, Ayme-Southgate A, (2001) Alternative splicing of an amino-terminal PEVK-like region generates multiple isoforms of Drosophila projectin J Mol Biol 313:1035–1043PubMedCrossRefGoogle Scholar
  49. Tabuchi K, Biederer T, Butz S, Sudhof TC, (2002) CASK participates in alternative tripartite complexes in which Mint 1 competes for binding with Caskin 1, a novel CASK-binding protein J Neurosc 22:4264–4273Google Scholar
  50. Teichmann SA, Chothia C, (2000) Immunoglobulin superfamily proteins in Caenorhabditis elegans J Mol Biol 296:1367–1383PubMedCrossRefGoogle Scholar
  51. Tskhovrebova L, Trinick J, (2003) Titin: properties and family relationships Nat Rev Mol Cell Biol 4:679–689PubMedCrossRefGoogle Scholar
  52. Waterston RH, Thomson JN, Brenner S, (1980) Mutants with altered muscle structure in C. elegans Dev Biol 77:271–302PubMedCrossRefGoogle Scholar
  53. Waterston RH, (1988) Muscle In: Wood WB, (ed.). The Nematode Caenorhabditis elegans Cold Spring Harbor Laboratory Press Cold Spring Harbor, New York 281–335Google Scholar
  54. Williams BD, Waterston RH, (1994) Genes critical for muscle development and function in C. elegans identified through lethal mutations J Cell Biol 124:475–490PubMedCrossRefGoogle Scholar
  55. Xu X, Meiler SE, Zhong TP, Mohideen M, Crossley DA, Burggren WW, Fishman MC, (2002) Cardiomyopathy in zebrafish due to mutation in an alternatively spliced exon of titin Nat Gen 30:205–209Google Scholar
  56. Young P, Ehler E, Gautel M, (2001) Obscurin, a giant sarcomeric Rho guanine nucleotide exchange factor protein involved in sarcomere assembly J Cell Biol 154:123–136PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Tracey M. Ferrara
    • 1
  • Denise B. Flaherty
    • 1
  • Guy M. Benian
    • 1
  1. 1.Department of PathologyEmory UniversityAtlantaUSA

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