Advertisement

Journal of Muscle Research & Cell Motility

, Volume 26, Issue 6–8, pp 467–477 | Cite as

In indirect flight muscles Drosophila projectin has a short PEVK domain, and its NH2-terminus is embedded at the Z-band

  • Agnes Ayme-Southgate
  • Judith Saide
  • Richard Southgate
  • Christophe Bounaix
  • Anthony Cammarato
  • Sunita Patel
  • Catherine Wussler
Article

Abstract

Insect indirect flight muscles (IFM) contain a third filament system made up of elastic connecting or C-filaments. The giant protein projectin is the main, if not the only, component of these structures. In this study we found that projectin is oriented within the IFM sarcomere with its NH2−terminus embedded in the Z-bands. We demonstrate that this protein has an elastic region that can be detected by the movement of specific epitopes following stretch. One possible elastic region is the PEVK-like domain located close to the NH2−terminus. The amino acid length of this region is short, and 52% of its residues are P, E, V or K. We propose a model in which projectin extends from the Z-band to the lateral borders of the A-band. The PEVK-like domain and a series of Ig domains spanning the intervening I-band may provide the elastic properties of projectin.

Keywords

Body Wall Muscle Indirect Flight Muscle Stretch Activation Elastic Filament Cardiac Titin 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

We want to thank Drs B. Bullard, and D. Kiehart for␣providing antibodies against various myofibrillar proteins. The work presented was supported by the National Institutes of Health/BRIN under Grant No. 8-P0RR16461A to AAS.

References

  1. Auber J, Couteaux R, (1963) Ultrasructure de la Strie Z dans des Muscles de Diptères. J Microsc 2:309–324Google Scholar
  2. Auber J, (1969) La Myofibrillogénèse du Muscle Strié. I. InsectesJ Microsc (Paris) 8:197–232Google Scholar
  3. 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, North Holland, pp 57–73Google Scholar
  4. Ayme-Southgate A, Vigoreaux JO, Benian GM, Pardue ML, (1991) Drosophila has a twitchin/titin-related gene that appears to encode projectinProc Natl Acad Sci USA 88:7973–7977PubMedCrossRefGoogle Scholar
  5. Ayme-Southgate A, Southgate R, Saide J, Benian G, Pardue ML, (1995) Both synchronous and asynchronous muscle isoforms of projectin (the Drosophila bent locus product) contain functional kinase domainsJ Cell Biol 128:393–403PubMedCrossRefGoogle Scholar
  6. Ayme-Southgate A, Bounaix C, Riebe TE, Southgate R, (2004) Assembly of the giant protein projectin during myofibrillogenesis in Drosophila indirect flight musclesBio Med Central Cell Biol5:17 (30 Apr 2004)Google Scholar
  7. Bernstein SI, O’Donnell PT, Cripps RM, (1993) Molecular genetics analysis of muscle development, structure and function in DrosophilaInt Rev Cytol 143:63–152PubMedCrossRefGoogle Scholar
  8. 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 lineJ Mol Biol 115:417–440PubMedCrossRefGoogle Scholar
  9. Bullard B, Goulding D, Ferguson C and Leonard K (2000) Links in the chain: the contribution of kettin to the elasticity of insect muscles. In: Pollack GH and Granzier H (eds.) Proceedings: Elastic Filaments of the Cell (pp. 207–220). Kluwer Academic/Plenum PublishersGoogle Scholar
  10. Candia Carnevali MD, De Eguileor M, Valvassori R, (1980) Z line morphology of functionally diverse insect skeletal musclesJ Submicrosc Cytol 12: 427–446Google Scholar
  11. Cazorla O, Freiburg A, Helmes M, Centner T, McNabb M, Wu Y, Trombitás K, Labeit S, Granzier H, (2000) Differential expression of cardiac titin isoforms and modulation of cellular stiffnessCirc Res 86:59–67PubMedGoogle Scholar
  12. Crossley AC, (1978) The morphology and development of the Drosophila muscular system. In: Asburner M, Wright TRF, (eds) The Genetics and Biology of Drosophila 2B. Academic Press, London, pp 499–559Google Scholar
  13. Daley J, Southgate R, Ayme-Southgate A, (1998) Structure of the projectin isoforms and implications for projectin assembly and functionsJ Mol Biol 279: 201–210PubMedCrossRefGoogle Scholar
  14. Deatherage JF, Cheng N, Bullard B, (1989) Arrangement of filaments and cross-links in the bee flight muscle Z disk by image analysis of oblique sectionsJ Cell Biol 108:1775–1782PubMedCrossRefGoogle Scholar
  15. Dickinson MH, Lighton JRB, (1995) Muscle efficiency and elastic storage in the flight motor of DrosophilaScience 268: 87–90PubMedGoogle Scholar
  16. Freiburg A, Trombitás 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 for myofibrillar elastic diversity. Circ Res 86:1114–1121PubMedGoogle Scholar
  17. 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 mutantsProc R Soc Lond B 249:33–40Google Scholar
  18. Gautel M, Goulding D, (1996) A molecular map of titin/connectin elasticity reveals two different mechanisms acting in seriesFEBS Lett 385:11–14PubMedCrossRefGoogle Scholar
  19. Granzier HL, Wang K, (1993a) Passive tension and stiffness of vertebrate skeletal and insect flight muscles: the contribution of weak cross-bridges and elastic filamentsBiophys J 65: 2141–2159Google Scholar
  20. Granzier HL, Wang K, (1993b) Interplay between passive tension and strong and weak binding crossbridges in insect indirect flight muscles: a functional dissection by gelsolin-mediated thin filament removalJ Gen Physiol 101:235–270CrossRefGoogle Scholar
  21. Granzier HL, Labeit D, Wu Y, Labeit S, (2002) Titin as a modular spring: emerging mechanisms for elasticity control by titin in cardiac physiology and pathophysiologyJ Muscle Res Cell Motil 23:457–471PubMedCrossRefGoogle Scholar
  22. Granzier HL, Labeit S, (2002) Cardiac titin: an adjustable multi-functional springJ Physiol 541:335–342PubMedCrossRefGoogle Scholar
  23. Granzier HL, Labeit S, (2004) The giant protein titin: a major player in myocardial mechanics, signaling, and diseaseCirc Res 94:284–295PubMedCrossRefGoogle Scholar
  24. Greaser ML, Wang S-M, Berri M, Mozdziak PE and Kumazawa Y (2000) Sequence and mechanical implications of cardiac PEVK. In: Pollack GH and Granzier H (eds.) Proceedings: Elastic Filaments of the Cell. Kluwer Academic/Plenum PublishersGoogle Scholar
  25. Gutierez-Cruz G, van Heerden A, Wang K, (2001) Modular motifs, structural folds and affinity profiles of pevk segments of human fetal skeletal muscle titinJ Biol Chem 10:7442–7449CrossRefGoogle Scholar
  26. Helmes M, Traombitas K, Centner T, Kellermayer M, Labeit S, Linke WA, Granzier, H (1999) Mechanically driven contour-length adjustement in rat cardiac titin's unique N2B sequence: titin is an adjustable springCirc Res 84:1339–1352PubMedGoogle Scholar
  27. 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 muscleJ Muscle Res Cell Motil 11:497–511PubMedCrossRefGoogle Scholar
  28. Jewell BR, Ruegg C, (1966) Oscillatory contraction of insect fibrillar muscle after glycerol extractionProc R Soc Lond B 164:428–459Google Scholar
  29. Kiehart DP, Feghali R, (1986) Cytoplasmic myosin from Drosophila melanogasterJ Cell Biol 103:1517–1525PubMedCrossRefGoogle Scholar
  30. Knudsen KA, (1985) Protein transferred to nitrocellulose for use as immunogens. Anal Biochem 147:285–288PubMedCrossRefGoogle Scholar
  31. Kulke M, Neagoe C, Kolmerer B, Minajeva A, Hinssen H, Bullard B, Linke WA, (2001) Kettin, a major source of myofibrillar stiffness in Drosophila indirect flight muscleJ Cell Biol 154:1045–1057PubMedCrossRefGoogle Scholar
  32. Labeit S, Kolmerer B, (1995) Titins: giant proteins in charge of muscle ultrastructure and elasticityScience 270:293–296PubMedGoogle Scholar
  33. 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 musclesEMBO J 9:3459–3467PubMedGoogle Scholar
  34. Lakey A, Ferguson C, Labeit S, Reedy M, Larkins A, Butcher G, Leonard K, Bullard B, (1993) Kettin, a large modular protein in the Z-Disc of insect musclesEMBO J 12:2863–2871PubMedGoogle Scholar
  35. Linke WA, Ivemeyer M, Olivieri N, Kolmerer B, Ruegg JC, Labeit S, (1996) Towards a molecular understanding of the elasticity of titinJ Mol Biol 261:62–71PubMedCrossRefGoogle Scholar
  36. Linke WA, Ivemeyer M, Mundel P, Stockmeier MR, Kolmerer B, (1998) Nature of PEVK-titin elasticity in skeletal muscleProc Natl Acad Sci USA 95:8052–8057PubMedCrossRefGoogle Scholar
  37. Linke WA, Rudy DE, Centner T, Gautel M, Witt CC, Labeit S, Gregorio CC, (1999) I-band titin in cardiac muscle is a three-element molecular spring and is critical for maintaining thin filament structureJ Cell Biol 246:631–644CrossRefGoogle Scholar
  38. Machado C, Sunkel CE, Andrew DJ (1998) Human autoantibodies reveal titin as a chromosomal proteinJ Cell Biol 141:321–333PubMedCrossRefGoogle Scholar
  39. Machado C, Andrews DJ, (2000) D-TITIN: a giant protein with dual roles in chromosomes and musclesJ Cell Biol 151:639–651PubMedCrossRefGoogle Scholar
  40. Moore JR, Vigoreaux JO, Maughan DW, (1999) The Drosophila projectin mutant, bentD, has reduced stretch activation and altered flight muscle kineticsJ Muscle Res Cell Motil 20:797–806PubMedCrossRefGoogle Scholar
  41. 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-titinJ Cell Sci 95:535–544PubMedGoogle Scholar
  42. Peckham M, White DCS, (1991) Mechanical properties of demembranated flight muscle fibers from a dragonflyJ Exp Biol 159:135–147Google Scholar
  43. Pringle FRS, (1978) Stretch activation of muscle: Function and mechanismProc R Soc Lond B 201:107–130PubMedCrossRefGoogle Scholar
  44. Saide JD, (1981) Identification of a connecting filament protein in insect fibrillar flight muscleJ Mol Biol 153:661–679PubMedCrossRefGoogle Scholar
  45. Saide JD, Chin-Bow S, Hogan-Sheldon J, Busquets-Turner L, Vigoreaux JO, Valgeirsdottir K, Pardue ML, (1989) Characterization of components of Z-bands in the fibrillar flight muscle of Drosophila melanogaster J Cell Biol 109:2157–2167PubMedCrossRefGoogle Scholar
  46. Saide JD, Chin-Bow S, Hogan-Sheldon J, Busquets-Turner L, (1990) Z-band proteins in the flight muscle and leg muscle of the honeybeeJ Muscle Res Cell Motil 11: 125–136PubMedCrossRefGoogle Scholar
  47. Saide J (2005) The insect Z-band. In: Vigoreaux J (ed.) Nature’s Versatile Engine: Insect Flight Muscle Inside and Out. Landes Bioscience, Georgetown, TXGoogle Scholar
  48. Southgate R, Ayme-Southgate A, (2001) Drosophila projectin contains a spring-like PEVK region which is alternatively splicedJ Mol Biol 313: 1037–1045CrossRefGoogle Scholar
  49. Squire JM, (1992) Muscle filament lattices and stretch activation: the match-mismatch model reassessedJ Muscle Res Cell Motil 13:183–189PubMedCrossRefGoogle Scholar
  50. Trombitas K (2000) Connecting filaments: a historical prospective. In: Pollack GH, Granzier H (eds.) Proceedings: Elastic Filaments of the Cell. Kluwer Academic/Plenum PublishersGoogle Scholar
  51. Trombitas K, Freiburg A, Centner T, Labeit S, Granzier H(1999) Molecular dissection of N2B cardiac titin's extensibilityBiophys J 6:3189–3196CrossRefGoogle Scholar
  52. Trombitas K, Tigyi-Sebe A, (1979) The continuity of thick filaments between sarcomeres in honeybee flight muscleNature 281:319–320PubMedCrossRefGoogle Scholar
  53. Trombitas K, Freiburg A, Greaser M, Labeit S and Granzier H (2000) From connecting filaments to co-expression of titin isoforms. In: Pollack GH, Granzier H (eds.) Proceedings: Elastic Filaments of the Cell. Kluwer Academic/Plenum PublishersGoogle Scholar
  54. Vigoreaux JO, Saide JD, Pardue ML, (1991) Structurally different Drosophila striated muscles utilize distinct variants of Z-band associated proteinsJ Muscle Res Cell Motil 12:340–354PubMedCrossRefGoogle Scholar
  55. Vigoreaux JO, Moore JR and Maughan DW (2000) Role of the elastic protein projectin in stretch activation and work output of Drosophila flight muscles. In: Pollack GH, Granzier H (eds.) Proceedings: Elastic Filaments of the Cell. Kluwer Academic/Plenum PublishersGoogle Scholar
  56. White DCS, (1983) The elasticity of relaxed insect fibrillar flight muscle. J Physiol 343:31–57PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Agnes Ayme-Southgate
    • 1
  • Judith Saide
    • 2
  • Richard Southgate
    • 1
  • Christophe Bounaix
    • 1
  • Anthony Cammarato
    • 2
    • 3
  • Sunita Patel
    • 2
    • 4
  • Catherine Wussler
    • 1
    • 5
  1. 1.Department of BiologyCollege of CharlestonCharlestonUSA
  2. 2.Department of PhysiologyBoston University School of MedicineBostonUSA
  3. 3.Department of BiologySan Diego State UniversitySan DiegoUSA
  4. 4.Division of HematologyBrigham and Women’s HospitalBostonUSA
  5. 5.Department of EducationTexas A&M UniversityTexasUSA

Personalised recommendations