Abstract
We examine how the stretch activation response of the Drosophila indirect flight muscles (IFM) is affected by the projectin mutation bent Dominant. IFM from flies heterozygous for this mutation (bent D / +) produce ~85% full length projectin and ~15% truncated projectin lacking the kinase domain and more C-terminal sequences. Passive stiffness and power output of mutant fibers is similar to that of wild-type (+/+) fibers, but the amplitude of the stretch activation response (delayed tension rise) was significantly reduced. Measurement of actomyosin kinetics by sinusoidal analysis revealed that the apparent rate constant of the delayed tension rise (2πb) increased in proportion to the decrease in amplitude, accounting for the near wild-type levels of power output and nearly normal flight ability. These results suggest that projectin plays a crucial role in stretch activation, possibly through its protein kinase activity, by modulating crossbridge recruitment and kinetics
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Ayme-Southgate A, Southgate R, Saide J, Benian GM, Pardue ML. Both synchronous and asynchronous muscle isoforms of projectin (the Drosophila bent locus product) contain functional kinase domain. J Cell Biol 1995;128:393–403.
Dickinson MH, Hyatt CJ, Lehmann F-O, Moore JR, Reedy MC, Simcox A, Tohtong R, Vigoreaux JO, Yamashita H, Maughan DW. Phosphorylation-dependent power output of transgenic flies: an integrated study. Biophys J 1997,73:3122–3134.
Domingo A, Gonzalez-Jurado J, Maroto M, Diaz C, Vinos J, Carrasco C, Cervera M, Marco R. 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 1998;19:393–403.
Granzier HLM, Wang K. Interplay between passive tension and strong and weak binding cross-bridges in insect indirect flight muscle. J Gen Physiol 1993;101:235–270.
Heierhorst J, Probst WC, Kohanski RA, Buku A, Weiss KR. Phosphorylation of myosin regulatory light chains by the molluscan twitchin kinase. Eur J Biochem 1995;233:426–431.
Heierhorst J, Probst WC, Vilim FS, Buku A, Weiss KR. Autophosphorylation of molluscan twitchin and interaction of its kinase domain with calcium/calmodulin. J Biol Chem 1994;269:21086–21093.
Huxley A. Muscular contraction. J Physiol (Lond) 1974;243:1–43.
Kawai M, Brandt PW. Sinusoidal analysis: a high resolution method for correlating biochemical reactions with physiological processes in activated skeletal muscles of rabbit, frog and crayfish. J Muscle Res Cell Motil1980;1:279–303.
Maroto M, Vinos J, Marco R, Cervera M. Autophosphorylating protein kinase activity in titin-like arthropod projectin. J Mol Biol 1992;224:287–291.
Nave R, Weber K. 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 Science 1990;95:535–544.
Pringle JWS. Stretch activation of muscle: function and mechanism. Proc R Soc Lond B 1978;201:107–130.
Reedy MC, Beall C. Ultrastructure of developing flight muscle in Drosophila. I. Assembly of myofibrils. Develop Biol 1993;160:443–465.
Saide JD. Identification of a connecting filament protein in insect fibrillar flight muscle. J Mol Biol 1981;153:661–679.
Saide JD, Chin-Bow S, Hogan-Sheldon J, Busquets-Turner L, Vigoreaux JO, Valgeirsdottir K, Pardue ML. Characterization of components of Z-bands in the fibrillar flight muscle of Drosophila melanogaster. J Cell Biol 1989;109:2157–2167.
Steiger GJ. Stretch activation and tension transients in cardiac, skeletal and insect flight muscle. In Insect flight muscle, RT Tregear, ed. North Holland: Amsterdam, 1977;221–268.
Tawada K, Kawai M. Covalent cross-linking of single fibers from rabbit psoas increases oscillatory power. Biophys J 1990;57:643–647.
Thorson J, White DCS. Distributed representations for actin-myosin interaction in the oscillatory contraction of muscle. Biophys J 1969;9:360–390.
Thorson J, White DCS. Role of cross-bridge distortion in the small-signal mechanical dynamics of insect and rabbit skeletal muscle. J Physiol (Great Britain)1983;343:59–84.
Tohtong R, Yamashita H, Graham M, Haeberle J, Simcox A, Maughan D. Impairment of muscle function caused by mutations of phosphorylation sites in myosin regulatory light chain. Nature 1995;374:650–655.
Tregear RT, Edwards RJ, Irving TC, Poole KJ, Reedy MC, Schmitz H, Towns-Andrews E, Reedy MK. X-ray diffraction indicates that active cross-bridges bind to actin target zones in insect flight muscle. Biophys J 1998;74:1439–1451.
Vemuri R, Lankford EB, Poetter K, Hassanzadeh S, Takeda K, Yu ZX; Ferrans VJ, Epstein ND. The stretch-activation response may be critical to the proper functioning of the mammalian heart. Proc Natl Acad Sci U S A 1999;96:1048–1053.
Vigoreaux JO, Hernandez C, Moore J, Ayer G, Maughan D. A genetic deficiency that spans the flightin gene of Drosophila melanogaster affects the ultrastructure and function of the flight muscles. J Exp Biol 1998;201:2033–2044.
Vigoreaux JO, Perry ML. Multiple isoelectric variants of flightin in Drosophila stretch-activated muscles are generated by temporally regulated phosphorylations. J Muscle Res Cell Motil 1994;15:607–616.
Vigoreaux JO, Saide JD, Pardue ML. Structurally different Drosophila striated muscles utilize distinct variants of Z band-associated proteins. J Muscle Res Cell Motil 1991;12:340–354.
Weitkamp B, Jurk K, Beinbrech G. Projectin-thin filament interactions and modulation of the sensitivity of the actomyosin ATPase to calcium by projectin kinase. J Biol Chem 1998;273:19802–19808.
White DCS. The elasticity of relaxed insect fibrillar flight muscle. J Physiol(Great Britain)1983;343:31–57.
Wray JS. Filament geometry and the activation of insect flight muscles. Nature 1979;280:325–326.
Zhao Y, Kawai M. The effect of the lattice spacing change on cross-bridge kinetics in chemically skinned rabbit psoas muscle fibers. Biophys J 1993;64:197–210.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2000 Springer Science+Business Media New York
About this chapter
Cite this chapter
Vigoreaux, J.O., Moore, J.R., Maughan, D.W. (2000). Role of the Elastic Protein Projectin in Stretch Activation and Work Output of Drosophila Flight Muscles. In: Granzier, H.L., Pollack, G.H. (eds) Elastic Filaments of the Cell. Advances in Experimental Medicine and Biology, vol 481. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-4267-4_14
Download citation
DOI: https://doi.org/10.1007/978-1-4615-4267-4_14
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4613-6916-5
Online ISBN: 978-1-4615-4267-4
eBook Packages: Springer Book Archive