Skip to main content
SpringerLink
Log in

The genetics and molecular biology of the titin/connectin-like proteins of invertebrates

  • Chapter
  • First Online:
Reviews of Physiology, Biochemistry and Pharmacology

Part of the book series: Reviews of Physiology, Biochemistry and Pharmacology ((REVIEWS,volume 138))

Abstract

A substantial amount of information has been gathered about the structure and function of twitchin/titin-related proteins in the invertebrates. This has been obtained through sequence analysis and the analysis of loss-offunction phenotypes in C. elegans and Drosophila. Nevertheless, a number of fascinating questions remain, including: (i) Why are these invertebrate proteins all of approx. 700–800 kDa? In terms of sarcomeric organization, what is the significance of this size? (ii) Why do three of these proteins consist of a mixture of Ig and Fn domains, whereas UNC-89 contains only Ig domains? This is even more interesting because the structures of Ig and Fn domains are very similar (118). What is the significance of the repeating pattern of groups of Ig and Fn domains (e.g. Fn-Fn-Ig)? (iii) How are twitchin and the synchronous muscle isoform of projectin situated on the surface of thick filaments? That is, do they form polymers or are they located at discrete locations with intervening gaps? (iv) What is the mechanism by which the fundamentally similar projectin isoforms get localized to different sarcomeric locations? (v) If the data on Aplysia twitchin can be extended to the muscles of other invertebrates, what is the mechanism by which twitchin inhibits the rate of relaxation? How does phosphorylation of twitchin relieve this inhibition? (vi) What are the substrates for the protein kinase domains of nematode twitchin and insect projectin? If rMLCs are indeed the substrates, how would and why does this phosphorylation take place for the IFM isoform of projectin, which resides primarily in the I band? If rMLCs are the substrates, given the stoichiometry of approx. 1∶50 for twitchin:myosin, and the likely fixed position of twitchin along the thick filament, how does phosphorylation of just a few rMLCs result in a physiological effect (e.g. inhibition of relaxation)? What is the true activator for the twitchin and projectin kinases? (vii) How does UNC-89 participate in M-line assembly? (viii) What are the biochemical and physiological functions of intestinal brush border twitchin? A number of investigators will enjoy pursuing these and other questions for some time in the future.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Squire J (1981) The structure and basis of muscular contraction. Plenum Press, New York

    Google Scholar 

  2. Auber J, Couteaux R (1963) Ultrasructure de la strie Z dans des muscles de Dipteres. J Microscopie 2:309–324

    Google Scholar 

  3. Saide JD, Ullrick WC (1974) Purification and properties of the isolated honeybee Z-disc. J Mol Biol 87:671–683

    PubMed  CAS  Google Scholar 

  4. Ashhurst DE (1977) The Z-line:its structure and evidence for the presence of connecting filaments. In:Tregear RT (ed) Insect Flight Muscle:Proceedings of the Oxford Symposium. Elsevier, Amsterdam, pp 57–73

    Google Scholar 

  5. Trombitas T, Tigyi-Sebe A (1977) Fine structure and mechanical properties of insect muscle gels to nitrocellulose sheets:procedure and some applications. In:Tregear RT (ed) Insect Flight Muscle:Proceedings of the Oxford Symposium. Elsevier, Amsterdam, pp 79–90

    Google Scholar 

  6. Candia Carnevali MD, De Eguileor M, Valvassori R (1980) Z line morphology of functionally diverse insect skeletal muscles. J Submicrosc Cytol 12:427–446

    Google Scholar 

  7. Deatherage JF, Cheng N, Bullard B (1989) Arrangement of filaments and crosslinks in the bee flight muscle Z disk by image analysis of oblique sections. J Cell Biol 108:1775–1782

    PubMed  CAS  Google Scholar 

  8. Wang K, McClure J, Tu A (1979) Titin:major myofibrillar components of striated muscle. Proc Natl Acad Sci USA 76:3698–3702

    PubMed  CAS  Google Scholar 

  9. Maruyama K, Kimura S, Ohashi K, Kuwano Y (1981) Connectin, an elastic protein of muscle. Identification of “titin” with connectin. J Biochem 89:701–709

    PubMed  CAS  Google Scholar 

  10. 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 and Devel 2:93–105

    CAS  Google Scholar 

  11. Benian GM, Kiff JE, Nickelmann N, Moerman DG, Waterston RH (1989) Sequence of an unusually large protein implicated in regulation of myosin activity in C. elegans. Nature 342:45–50

    PubMed  CAS  Google Scholar 

  12. 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 91:8487–8491

    PubMed  CAS  Google Scholar 

  13. Bullard B, Hammond KS, Luke BM (1977) The site of paramyosin in insect flight muscle and the presence of an unidentified protein between myosin filaments and Z line. J Mol Biol 115:417–440

    PubMed  CAS  Google Scholar 

  14. Saide JD (1981) Identification of a connecting filament protein in insect fibrillar flight muscle. J Mol Biol 153:661–679

    PubMed  CAS  Google Scholar 

  15. Hu DH, Kimura S, Maruyama K (1986) Sodium dodecyl sulfate-gel electrophoresis of connectin-like high molecular weight proteins of various types of vertebrate and invertebrate muscles. J Biochem 99:485–492

    Google Scholar 

  16. Locker RH, Wild DJC (1986) A comparative study of high molecular weight proteins in various types of muscle across the animal kingdom. J Biochem 99:1473–1484

    PubMed  CAS  Google Scholar 

  17. Saide JD, Chin-Bow S, Hogan-Sheldon J, Busquets-Turner L, Vigoreaux JO, Valgeirsdottir K, Pardue ML (1989) Characterization of components of Zbands in the fibrillar flight muscle of Drosophila melanogaster. J Cell Biol 109:2157–2167

    PubMed  CAS  Google Scholar 

  18. Lakey A, Ferguson C, Labeit S, Reedy M, Larkins A, Butcher G, Leonard K, Bullard B (1990) Identification and localization of high molecular weight proteins in insect flight and leg muscles. EMBO J 9:3459–3467

    PubMed  CAS  Google Scholar 

  19. Hu DH, Matsuno A, Terakado K, Matsuura T, Kimura S, Maruyama K (1990) Projectin is an invertebrate connectin (titin):isolation from crayfish claw muscle and localization in crayfish claw muscle and insect flight muscle. J Muscle Res Cell Motil 11:497–511

    PubMed  CAS  Google Scholar 

  20. Nave R, Weber K (1990) A myofibrillar protein of insect muscle related to vertebrate titin connects Z band and A band:purification and molecular characterization of invertebrate mini-titin. J Cell Sci 95:535–544

    PubMed  CAS  Google Scholar 

  21. Maroto M, Vinos J, Marco R, Cervera M (1992) Autophosphorylating protein kinase activity of titin-like arthropod projectin. J Mol Biol 224:287–291

    PubMed  CAS  Google Scholar 

  22. Vibert P, Edelstein SM, Castellani L, Elliot BW (1993) Mini-titins in striated and smooth molluscan muscles:structure, location and immunological crossreactivity. J Muscle Res and Cell Motil 14:598–607

    CAS  Google Scholar 

  23. Matsuno A, Takano-Ohmuro H, Itoh Y, Matsuura T, Shibata M, Nakae A, Kaminuma T, Maruyama K (1989) Anti-connectin monoclonal antibodies that react with the unc-22 gene product bind dense bodies of Caenorhabditis nematode body wall muscle cells. Tissue and Cell 21:495–505

    Google Scholar 

  24. Vigoreaux JO, Saide JD, Pardue ML (1991) Structurally different Drosophila striated muscles utilize distinct variants of Z-band associated proteins. J Muscle Res Cell Motil 12:340–354

    PubMed  CAS  Google Scholar 

  25. 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 134:1097–1104

    PubMed  CAS  Google Scholar 

  26. Labeit S, Barlow DP, Gautel M, Gibson T, Holt J, Hsieh C-L, Francke U, Leonard K, Wardale J, Whiting A, Trinick J (1990) A regular pattern of two types of 100 residue motif in the sequence of titin. Nature 345:273–276

    PubMed  CAS  Google Scholar 

  27. Labeit S, Gautel M, Lakey A, Trinick J (1992) Towards a molecular understanding of titin. EMBO J 11:1711–1716

    PubMed  CAS  Google Scholar 

  28. Labeit S, Kolmerer B (1995) Titins:Giant proteins in charge of muscle ultrastructure and elasticity. Science 270:293–296

    PubMed  CAS  Google Scholar 

  29. Ayme-Southgate A, Vigoreaux JO, Benian GM, Pardue ML (1991) Drosophila has a twitchin/titin-related gene that appears to encode projectin. Proc Natl Acad Sci USA 88:7973–7977

    PubMed  CAS  Google Scholar 

  30. Ayme-Southgate A, Southgate R, Saide J, Benian GM, Pardue ML (1995) Both synchronous and asynchronous muscle isoforms of projectin (the Drosophila bent locus product) contain functional kinase domains. J Cell Biol 128:393–403

    PubMed  CAS  Google Scholar 

  31. Fyrberg CC, Labeit S, Bullard B, Leonard K, Fyrberg EA (1992) Drosophila projectin:relatedness to titin and twitchin and correlation with lethal(4)102Cda and bent-dominant mutants. Proc R Soc Lond B 249:33–40

    Google Scholar 

  32. Olson NJ, Pearson RB, Needleman DS, Hurwitz MY, Kemp BE, Means AR (1990) Regulatory and structural motifs of chicken gizzard myosin light chain kinase. Proc Natl Acad Sci USA 87:2284–2288

    PubMed  CAS  Google Scholar 

  33. Shoemaker MO, Lau W, Shattuck RL, Kwiatkowski AP, Martrisian PE, Guerra-Santos L, Wilson E, Lukas TJ, Van Eldik LJ, Watterson DM (1990) Use of DNA sequence and mutant analyses and antisense oligodeoxynucleotides to examine the molecular basis of nonmuscle myosin light chain kinase autoinhibition, calmodulin recognition and activity. J Cell Biol 111:1107–1125

    PubMed  CAS  Google Scholar 

  34. Gallagher PJ, Herring BP (1991) The carboxyl terminus of the smooth muscle myosin light chain kinase is expressed as an independent protein, telokin. J Biol Chem 266:23945–23952

    PubMed  CAS  Google Scholar 

  35. Collinge M, Martrisian PE, Zimmer WE, Shattuck RL, Lukas TJ, Van Eldik LJ, Watterson DM (1992) Structure and expression of a calcium-binding protein gene contained within a calmodulin-regulated protein kinase gene. Mol Cell Biol 12:2359–2371

    PubMed  CAS  Google Scholar 

  36. Einheber S, Fischman DA (1990) Isolation and characterization of a cDNA clone encoding avian skeletal muscle C-protein:an intracellular member of the immunoglobulin superfamily. Proc Natl Acad Sci USA 87:2157–2161

    PubMed  CAS  Google Scholar 

  37. Vaughan KT, Weber FE, Einheber S, Fischman DA (1993) Molecular cloning of chicken myosin-binding protein H (86 kDa protein) reveals extensive homology with MYBP-C (C-protein) with conserved immunoglobulin C2 and fibronectin type III motifs. J Biol Chem 268:3670–3676

    PubMed  CAS  Google Scholar 

  38. Price MG, Gomer RH (1993) Skelemin, a cytoskeletal M-disc periphery protein, contains motifs of adhesion/recognition and intermediate filament proteins. J Biol Chem 268:21800–21810

    PubMed  CAS  Google Scholar 

  39. Noguchi J, Yanagisawa M, Imamura M, Kasuya Y, Sakurai T, Tanaka T, Masaki T (1992) Complete primary structure and tissue expression of chicken pectoralis M-protein. J Biol Chem 267:20302–20310

    PubMed  CAS  Google Scholar 

  40. Vinkemeier U, Obermann W, Weber K, Furst DO (1993) The globular head domain of titin extends into the center of the sarcomeric M band:cDNA cloning, epitope mapping and immunoelectron microscopy of two titin-associated proteins. J Cell Sci 106:319–330

    PubMed  CAS  Google Scholar 

  41. Lakey A, Labeit S, Gautel M, Ferguson C., Barlow DP, Leonard K, Bullard B (1993) Kettin, a large modular protein in the Z-disc of insect muscles. EMBO J 12:2863–2871

    PubMed  CAS  Google Scholar 

  42. Holden HM, Ito M, Hartshorne DJ, Rayment I (1992) X-ray structure determination of telokin, the C-terminal domain of myosin light chain kinase, at 2.8 A resolution. J Mol Biol 227:840–851

    PubMed  CAS  Google Scholar 

  43. Pfuhl M, Pastore A (1995) Tertiary structure of an immunoglobulin-like domain from the giant muscle protein titin:a new member of the I set. Structure 3:391–401

    PubMed  CAS  Google Scholar 

  44. Improta S, Politou A, Pastore A (1996) Immunoglobulin-like modules from titin I-band:extensible components of muscle elasticity. Structure 4:323–337

    PubMed  CAS  Google Scholar 

  45. Fong S, Hammill SJ, Proctor M, Freund SMV, Benian GM, Chothia C, Bycroft M, Clarke J (1996) Structure and stability of an immunoglobulin superfamily domain from twitchin, a muscle protein of the nematode C. elegans. J Mol Biol 264:624–639

    PubMed  CAS  Google Scholar 

  46. Shirinsky VP, Vorotnikov AV, Birukov KG, Nanaev AK, Collinge M, Lukas TJ, Sellers JR, Watterson DM (1993) A kinase-related protein stabilizes unphosphorylated smooth muscle myosin minifilaments in the presence of ATP. J Biol Chem 268:16578–16583

    PubMed  CAS  Google Scholar 

  47. Okagaki T, Weber FE, Fischman DA, Vaughan KT, Mikawa T, Reinach FC (1993) The major myosin-binding domain of skeletal muscle MyBP-C (C-protein) resides in the COOH-terminal, immunoglobulin C2 motif. J Cell Biol 123:619–626

    PubMed  CAS  Google Scholar 

  48. Freiburg A, Gautel M (1996) A molecular map of the interactions between titin and myosin-binding protein C:implications for sarcomeric assembly in familial hypertrophic cardiomyopathy. Eur J Biochem 235:317–323

    PubMed  CAS  Google Scholar 

  49. Crossley AC (1978) The morphology and development of the Drosophila muscular system. In:Asburner M, Wright TRF (eds) The Genetics and Biology of Drosophila. Academic Press, London, pp 499–559

    Google Scholar 

  50. Pringle FRS (1978) Stretch activation of muscle:function and mechanism. Proc R Soc Lond B 201:107–130

    Google Scholar 

  51. Jewell BR, Ruegg C (1966) Oscillatory contraction of insect fibrillar muscle after glycerol extraction. Proc R Soc Lond B 164:428–459

    Google Scholar 

  52. Wray JS (1979) Filament geometry and the activation of insect flight muscle. Nature 280:325–326

    Google Scholar 

  53. Squire JM (1992) Muscle filament lattices and stretch activation:the matchmismatch model reassessed. J Muscle Res Cell Motil 13:183–189

    PubMed  CAS  Google Scholar 

  54. Lei J, Tang X, Chambers T, Pohl J, Benian GM (1994) The protein kinase domain of twitchin has protein kinase activity and an autoinhibitory region. J Biol Chem 269:21078–21085

    PubMed  CAS  Google Scholar 

  55. Hu S-H, Parker MW, Lei J, Wilce MCJ, Benian GM, Kemp BE (1994) Intrasteric regulation of protein kinases:insights from the crystal structure of twitchin kinase. Nature 369:581–584

    PubMed  CAS  Google Scholar 

  56. Hochman B (1971) Analysis of chromosome 4 in Drosophila melanogaster. II. Ethylmethanesulfonate induced lethals. Genetics 67:235–252

    PubMed  CAS  Google Scholar 

  57. Hochman B (1974) Analysis of a whole chromosome in Drosophila. Cold Spr Harb Symp Quant Biol 38:581–589

    CAS  Google Scholar 

  58. Trinick J (1994) Titin and nebulin:protein rulers in muscle? Trends in Bio Sci 19:405–409

    CAS  Google Scholar 

  59. Whiting A, Wardale J, Trinick J (1989) Does titin regulate the length of muscle thick filaments? J Mol Biol 205:263–268

    PubMed  CAS  Google Scholar 

  60. Fulton AB, Isaacs WB (1991) Titin, a huge, elastic sarcomeric protein with a probable role in morphogenesis. BioEssays 13:157–161

    PubMed  CAS  Google Scholar 

  61. Waterston RH, Thomson JN, Brenner S (1980) Mutants with altered muscle structure in C. elegans. Devel Biol 77:271–302

    CAS  Google Scholar 

  62. Moerman DG, Baillie DL (1979) Genetic organization in Caenorhabditis elegans:Fine structure analysis of the unc-22 gene. Genetics 91:95–104

    PubMed  Google Scholar 

  63. Moerman DG, Plurad S, Waterston RH, Baillie DL (1982) Mutations in the unc54 myosin heavy chain gene of C. elegans that alter contractility but not muscle structure. Cell 29:773–781

    PubMed  CAS  Google Scholar 

  64. Moerman DG, Benian GM, Waterston RH (1986) Molecular cloning of the muscle gene unc-22 in C. elegans by Tcl transposon tagging. Proc Natl Acad Sci USA 83:2579–2583

    PubMed  CAS  Google Scholar 

  65. Benian GM, L’Hernault SW, Fox LA, Tucker CY, Sale WS (1991) Structure of twitchin: An unusually large sarcomeric protein of C. elegans. J Cell Biol 115 (3,2):29a

    Google Scholar 

  66. Nave R, Furst D, Vinkemeier U, Weber K (1991) Purification and physical properties of nematode mini-titins and their relation to twitchin. J Cell Sci 98:491–496

    PubMed  CAS  Google Scholar 

  67. Vibert P, York ML, Castellani L, Edelstein S, Elliott B, Nyitray L (1996) Structure and distribution of mini-titins. Adv Biophys 33:199–209

    PubMed  CAS  Google Scholar 

  68. Kiff JE, Moerman DG, Schriefer LA, Waterston RH (1988) Transposon induced deletions in unc-22 of C. elegans associated with almost normal gene activity. Nature 331:631–633

    PubMed  CAS  Google Scholar 

  69. Koenig M, Beggs AH, Moyer M, Scherpf S, Heindrich K…(30)… Kunkel LM (1989) The molecular basis for Duchenne versus Becker muscular dystrophy:correlation of severity with type of deletion. Am J Hum Genet 45:498–506

    PubMed  CAS  Google Scholar 

  70. 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 24:6810–6821

    Google Scholar 

  71. Heierhorst J, Probst WC, Vilim FS, Buku A, Weiss KR (1994) Autophosphorylation of molluscan twitchin and interaction of its kinase domain with calcium/calmodulin. J Biol Chem 269:21086–21093

    PubMed  CAS  Google Scholar 

  72. 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 233:426–431

    PubMed  CAS  Google Scholar 

  73. Heierhorst J, Tang X, Lei J, Kemp B, Weiss K, Benian GM (1996) Substrate requirements, inhibition by naphthylene sulfonates, and distinct calmodulin affinities of twitchin kinases. Eur J Biochem 242:454–459

    PubMed  CAS  Google Scholar 

  74. Heierhorst J, Mann RM, Kemp BE (1997) Interaction of the recombinant S100A1 protein with twitchin kinase, and comparison with other Ca2+binding proteins. Eur J Biochem (in press)

    Google Scholar 

  75. Heierhorst J, Kobe B, Feil SC, Parker MW, Benian GM, Weiss KR, Kemp BE (1996) Ca+2 / S100 regulation of giant protein kinases. Nature 380:636–639

    PubMed  CAS  Google Scholar 

  76. Zimmer DB, Cornwall EH, Landar A, Song W (1995) The S100 protein family:history, function and expression. Brain Res Bull 37:417–429

    PubMed  CAS  Google Scholar 

  77. Knappeis GG, Carlsen F (1968) The ultrastructure of the M-line in skeletal muscle. J Cell Biol 38:202–211

    PubMed  CAS  Google Scholar 

  78. Luther P, Squire J (1978) Three-dimensional structure of the vertebrate muscle M-region. J Mol Biol 125:313–324

    PubMed  CAS  Google Scholar 

  79. Strehler EE, Carlsson E, Eppenberger HM, Thornell L-E (1983) Ultrastructural localization of M-band proteins in chicken breast muscle as revealed by combined immunocytochemistry and ultramicrotomy. J Mol Biol 166:141–158

    PubMed  CAS  Google Scholar 

  80. Gautel M, Leonard K, Labeit S (1993) Phosphorylation of KSP motifs in the Cterminal region of titin in differentiating myoblasts. EMBO J 12:3827–3834

    PubMed  CAS  Google Scholar 

  81. Obermann WMJ, Gautel M, Steiner F, van der Ven PFM, Weber K, Furst DO (1996) The structure of the sarcomeric M band:localization of defined domains of myomesin, M-protein and the 250 kD carboxy-terminal region of titin by immunoelectron microscopy. J Cell Biol 134:1441–1453

    PubMed  CAS  Google Scholar 

  82. Bullard B, Leonard K (1996) Modular proteins of insect muscle. Adv Biophys 33:211–221

    PubMed  CAS  Google Scholar 

  83. Waterston RH (1988) Muscle. In:Wood WB (ed) The Nematode Caenorhabditis elegans. Cold Spring Harbor Press, Cold Spring Harbor, NY, pp 281–335

    Google Scholar 

  84. Francis GR, Waterston RH (1985) Muscle organization in Caenorhabditis elegans:Localization of proteins implicated in thin filament attachment and I-band organization. J Cell Biol 101:1532–1549

    PubMed  CAS  Google Scholar 

  85. Benian GM, Tinley TL, Tang X, Borodovsky M (1996) The C. elegans gene unc89, required for muscle M-line assembly, encodes a giant modular protein composed of Ig and signal transduction domains. J Cell Biol 132:835–848

    PubMed  CAS  Google Scholar 

  86. Miller DM, Ortiz I, Berliner GC, Epstein HF (1983) Differential localization of two myosins within nematode thick filaments. Cell 34:477–490

    PubMed  CAS  Google Scholar 

  87. Maruyama IN, Miller DM, Brenner S (1989) Myosin heavy chain gene amplification as a suppressor mutation in C. elegans. Mol Gen Genet 219:113–118

    PubMed  CAS  Google Scholar 

  88. Myers MW, Lazzarini RA, Lee VM-Y, Schlaepfer WW, Nelson DL (1987) The human mid-size neurofilament subunit:a repeated protein sequence and the relationship of its gene to the intermediate filament gene family. EMBO J 6:1617–1626

    PubMed  CAS  Google Scholar 

  89. Lees JF, Shneidman PS, Skuntz SF, Carden MJ, Lazzarini RA (1988) The structure and organization of the human heavy neurofilament subunit (NF-H) and the gene encoding it. EMBO J 7:1947–1955

    PubMed  CAS  Google Scholar 

  90. Hirokawa N, Glicksman MA, Willard MB (1984) Organization of mammalian neurofilament polypeptides within the neuronal cytoskeleton. J Cell Biol 98:1523–1536

    PubMed  CAS  Google Scholar 

  91. Nakagawa T, Chen J, Zhang Z, Kanai Y, Hirokawa N (1995) Two distinct functions of the carboxyl-terminal tail domain of NF-M upon neurofilament assembly:cross-bridge formation and longitudinal elongation of filaments. J Cell Biol 129:411–429

    PubMed  CAS  Google Scholar 

  92. Lew J, Wang JH (1995) Neuronal cdc2-like kinase. Trends Biochem Sci 20:33–37

    PubMed  CAS  Google Scholar 

  93. Nixon RA, Sihag RK (1991) Neurofilament phosphorylation:a new look at regulation and function. Trends Neurosci 14:501–506

    PubMed  CAS  Google Scholar 

  94. Gautel M, Goulding D, Bullard B, Weber K, Furst DO (1996) The central Z-disk region of titin is assembled from a novel repeat in variable copy numbers. J Cell Sci 109:2747–2754

    PubMed  CAS  Google Scholar 

  95. Moreno S, Nurse P (1990) Substrates for p34cdc2:in vivo veritas? Cell 61:549–551

    PubMed  CAS  Google Scholar 

  96. Cohen GB, Ren R, Baltimore D (1995) Modular binding domains in signal transduction proteins. Cell 80:237–248

    PubMed  CAS  Google Scholar 

  97. Zheng Y, Cerione R, Bender A (1994) Control of the yeast bud site assembly GTPase CDC42. J Biol Chem 269:2369–2372

    PubMed  CAS  Google Scholar 

  98. Hart MJ, Eva A, Evans T, Aaronson SA, Cerione RA (1991) Catalysis of guanine nucleotide exchange on the CDC42Hs protein by the dbl oncogene product. Nature 354:311–314

    PubMed  CAS  Google Scholar 

  99. Takai Y, Sasaki T, Tanaka K, Nakanishi H (1995) Rho as a regulator of the cytoskeleton. Trends Biochem Sci 20:227–231

    PubMed  CAS  Google Scholar 

  100. Gibson TJ, Hyvonen M, Musacchio A, Saraste M, Birney E (1994) PH domain:the first anniversary. Trends Biochem Sci 19:349–353

    PubMed  CAS  Google Scholar 

  101. Harlan JE, Hajduk PJ, Yoon HS, Fesik SW (1994) Pleckstrin homology domains bind to phosphatidylinositol-4,5-bisphosphate. Nature 371:168–170

    PubMed  CAS  Google Scholar 

  102. Hyvonen M, Macias MJ, Nilges M, Oschkinat H, Saraste M, Wilmanns M (1995) Structure of the binding site of inositol phosphates in a PH domain. EMBO J 14:4676–4685

    PubMed  CAS  Google Scholar 

  103. Gettner SN, Kenyon C, Reichardt LF (1995) Characterizaiton of bpat-3 heterodimers, a family of essential integrin receptors in C. elegans. J Cell Biol 129:1127–1141

    PubMed  CAS  Google Scholar 

  104. Rogalski TM, Williams BD, Mullen GP, Moerman DG (1993) Products of the unc-52 gene in C. elegans are homologous to the core protein of the mammalian basement membrane heparan sulfate proteoglycan. Genes Dev 7:1471–1484

    PubMed  CAS  Google Scholar 

  105. Francis GR, Waterston RH (1991) Muscle cell attachment in C. elegans. J Cell Biol 114:465–479

    PubMed  CAS  Google Scholar 

  106. Williams BD, Waterston RH (1994) Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations. J Cell Biol 124:475–490

    PubMed  CAS  Google Scholar 

  107. Hresko MC, Williams BD, Waterston RH (1994) Assembly of body wall muscle and muscle cell attachment structures in Caenorhabditis elegans. J Cell Biol 124:491–506

    PubMed  CAS  Google Scholar 

  108. Miller DM, Shakes DC (1995) Immunofluroescence microscopy. In:Epstein HF, Shakes DC (eds) C. elegans:Modern Biological Analysis of an Organism. Academic Press, San Diego, pp 365–394

    Google Scholar 

  109. Bretscher A (1991) Microfilament structure and function in the cortical cytoskeleton. Ann Rev Cell Biol 7:337–374

    PubMed  CAS  Google Scholar 

  110. Heintzelman MB, Mooseker MS (1992) Assembly of the intestinal brush border cytoskeleton. Curr Top Dev Biol 26:93–122

    PubMed  CAS  Google Scholar 

  111. Mamajiwalla SN, Fath KR, Burgess DR (1992) Development of the chicken intestinal epithelium. Curr Top Dev Biol 26:123–143

    PubMed  CAS  Google Scholar 

  112. Keller T, Mooseker MS (1982) Ca+2-calmodulin-dependent phosphorylation of myosin, and its role in brush border contraction in vitro. J Cell Biol 95:943–959

    PubMed  CAS  Google Scholar 

  113. Madara JL (1989) Loosening tight junctions. Lessons from the intestine. J Clin Invest 83:1089–1094

    PubMed  CAS  Google Scholar 

  114. Eilertsen KJ, Keller TCS (1992) Identification and characterization of two huge protein components of the brush border cytoskeleton:evidence for a cellular isoform of titin. J Cell Biol 119:549–557

    PubMed  CAS  Google Scholar 

  115. White J (1988) The Anatomy. In:Wood WB (ed) The Nematode Caenorhabitis elegans. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 81–122

    Google Scholar 

  116. Bullard B, Leonard K (1996) Modular proteins of insect muscles. Adv Biophys 33:211–221

    PubMed  CAS  Google Scholar 

  117. Cheng N, Deatherage JF (1989) Three-dimensional reconstruction of the Z disk of sectioned bee flight muscle. J Cell Biol 108:1761–1774

    PubMed  CAS  Google Scholar 

  118. Main AL, Harvey TS, Baron M, Boyd J, Campbell ID (1992) The threedimensional structure of the tenth type III module of fibronectin:an insight into RGD-mediated interactions. Cell 71:671–678

    PubMed  CAS  Google Scholar 

  119. Daley J, Southgate R, Ayme-Southgate A (1998) Structure of the Drosophila projectin protein: isoforms and implication for projectin filament assembly. J Mol Biol 279(1):201–210

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departments of Pathology and Cell Biology, Emory University, 30322, Atlanta, GA

    G. M. Benian & T. L. Tinley

  2. Department of Molecular Biology, Lehigh University, 18015, Bethleham, PA

    A. Ayme-Southgate

Authors
  1. G. M. Benian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Ayme-Southgate
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. L. Tinley
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

Copyright information

© 1999 Springer-Verlag

About this chapter

Cite this chapter

Benian, G.M., Ayme-Southgate, A., Tinley, T.L. (1999). The genetics and molecular biology of the titin/connectin-like proteins of invertebrates. In: Reviews of Physiology, Biochemistry and Pharmacology. Reviews of Physiology, Biochemistry and Pharmacology, vol 138. Springer, Berlin, Heidelberg. https://doi.org/10.1007/BFb0119629

Download citation

  • DOI: https://doi.org/10.1007/BFb0119629

  • Published:

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-540-65484-1

  • Online ISBN: 978-3-540-49231-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation