An embryonic myosin isoform enables stretch activation and cyclical power in Drosophila jump muscle

Biophysical Journal

Volumn 104, Issue 12, 2013, Pages 2662-2670

  Zhao, Cuiping ^a   Swank, Douglas M ^a  

^a RENSSELAER POLYTECHNIC INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA PROTEIN; ISOPROTEIN; MYOSIN HEAVY CHAIN;

ANIMAL; DROSOPHILA; METABOLISM; MUSCLE ISOMETRIC CONTRACTION; PHYSIOLOGY; SKELETAL MUSCLE;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; ISOMETRIC CONTRACTION; MUSCLE, SKELETAL; MYOSIN HEAVY CHAINS; PROTEIN ISOFORMS;

EID: 84879244400     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.04.057     Document Type: Article

References (56)

1. G.J. Steiger Stretch activation and tension transients in cardiac, skeletal and insect flight muscle R.T. Tregear, Insect Flight Muscle 1977 North Holland Amsterdam 221 268
2. J.W.S. Pringle The Croonian Lecture, 1977. Stretch activation of muscle: function and mechanism Proc. R. Soc. Lond. B Biol. Sci. 201 1978 107 130
3. R.K. Josephson, J.G. Malamud, and D.R. Stokes Asynchronous muscle: a primer J. Exp. Biol. 203 2000 2713 2722
4. G.J. Steiger Stretch activation and myogenic oscillation of isolated contractile structures of heart muscle Pflugers Arch. 330 1971 347 361
5. J.S. Wray Filament geometry and the activation of insect flight muscles Nature 280 1979 325 326
6. H.L.M. Granzier, and K. Wang Interplay between passive tension and strong and weak binding cross-bridges in insect indirect flight muscle. A functional dissection by gelsolin-mediated thin filament removal J. Gen. Physiol. 101 1993 235 270
7. N. Fukuda, and H.L. Granzier Titin/connectin-based modulation of the Frank-Starling mechanism of the heart J. Muscle Res. Cell Motil. 26 2005 319 323
8. R. Tohtong, and H. Yamashita D. Maughan Impairment of muscle function caused by mutations of phosphorylation sites in myosin regulatory light chain Nature 374 1995 650 653
9. M.H. Dickinson, and C.J. Hyatt D.W. Maughan Phosphorylation-dependent power output of transgenic flies: an integrated study Biophys. J. 73 1997 3122 3134
10. R.J. Perz-Edwards, and T.C. Irving M.K. Reedy X-ray diffraction evidence for myosin-troponin connections and tropomyosin movement during stretch activation of insect flight muscle Proc. Natl. Acad. Sci. USA 108 2011 120 125
11. B. Bullard, and A. Pastore Regulating the contraction of insect flight muscle J. Muscle Res. Cell Motil. 32 2011 303 313
12. J. Thorson, and D.C.S. White Role of cross-bridge distortion in the small- signal mechanical dynamics of insect and rabbit skeletal muscle J. Physiol. (Great Britain) 343 1983 59 84
13. S. Galler, T.L. Schmitt, and D. Pette Stretch activation, unloaded shortening velocity, and myosin heavy chain isoforms of rat skeletal muscle fibres J. Physiol. 478 1994 513 521
14. S. Galler, K. Hilber, and D. Pette Stretch activation and myosin heavy chain isoforms of rat, rabbit and human skeletal muscle fibres J. Muscle Res. Cell Motil. 18 1997 441 448
15. J.E. Stelzer, and S.L. Brickson R.L. Moss Role of myosin heavy chain composition in the stretch activation response of rat myocardium J. Physiol. 579 2007 161 173
16. C.E. Rozek, and N. Davidson Drosophila has one myosin heavy-chain gene with three developmentally regulated transcripts Cell 32 1983 23 34
17. S.I. Bernstein, and K. Mogami C.P. Emerson Jr. Drosophila muscle myosin heavy chain encoded by a single gene in a cluster of muscle mutations Nature 302 1983 393 397
18. D.M. Swank, and A.F. Knowles S.I. Bernstein The converter domain of myosin influences actin velocity and ATPase rate: an integrative analysis of the Drosophila exon 11 region Biophys. J. 78 2000 244A
19. D.M. Swank Mechanical analysis of Drosophila indirect flight and jump muscles Methods 56 2012 69 77
20. N. Zumstein, and O. Forman C.J. Elliott Distance and force production during jumping in wild-type and mutant Drosophila melanogaster J. Exp. Biol. 207 2004 3515 3522
21. G. Card, and M. Dickinson Performance trade-offs in the flight initiation of Drosophila J. Exp. Biol. 211 2008 341 353
22. M. Peckham, and J.E. Molloy D.C. White Physiological properties of the dorsal longitudinal flight muscle and the tergal depressor of the trochanter muscle of Drosophila melanogaster J. Muscle Res. Cell Motil. 11 1990 203 215
23. L. Wells, K.A. Edwards, and S.I. Bernstein Myosin heavy chain isoforms regulate muscle function but not myofibril assembly EMBO J. 15 1996 4454 4459
24. C.C. Eldred, and D.R. Simeonov D.M. Swank The mechanical properties of Drosophila jump muscle expressing wild-type and embryonic Myosin isoforms Biophys. J. 98 2010 1218 1226
25. A.F. Huxley, and R.M. Simmons Mechanical properties of the cross-bridges of frog striated muscle J. Physiol. 218 Suppl 1971 59P 60P
26. C. Yang, and C.N. Kaplan D.M. Swank The influence of myosin converter and relay domains on cross-bridge kinetics of Drosophila indirect flight muscle Biophys. J. 99 2010 1546 1555
27. Q. Wang, C. Zhao, and D.M. Swank Calcium and stretch activation modulate power generation in Drosophila flight muscle Biophys. J. 101 2011 2207 2213
28. B.M. Palmer, and T. Noguchi M.M. LeWinter Effect of cardiac myosin binding protein-C on mechanoenergetics in mouse myocardium Circ. Res. 94 2004 1615 1622
29. D.M. Swank, and A.F. Knowles S.I. Bernstein The myosin converter domain modulates muscle performance Nat. Cell Biol. 4 2002 312 316
30. D. Maughan, and J. Vigoreaux Nature's strategy for optimizing power generation in insect flight muscle Adv. Exp. Med. Biol. 565 2005 157 166 discussion 167, 371-157
31. S. Galler, and T.L. Schmitt D. Pette Stretch activation and isoforms of myosin heavy chain and troponin-T of rat skeletal muscle fibres J. Muscle Res. Cell Motil. 18 1997 555 561
32. O. Andruchova, and G.M. Stephenson S. Galler Myosin heavy chain isoform composition and stretch activation kinetics in single fibres of Xenopus laevis iliofibularis muscle J. Physiol. 574 2006 307 317
33. S. Galler, and E. Puchert D. Pette Kinetic properties of cardiac myosin heavy chain isoforms in rat Pflugers Arch. 445 2002 218 223
34. M.G. Hibberd, and J.A. Dantzig Y.E. Goldman Phosphate release and force generation in skeletal muscle fibers Science 228 1985 1317 1319
35. J.C. Rüegg, and M. Schädler G. Müller Effects of inorganic phosphate on the contractile mechanism Pflugers Arch. 325 1971 359 364
36. M. Kawai, and K. Güth J.C. Rüegg The effect of inorganic phosphate on the ATP hydrolysis rate and the tension transients in chemically skinned rabbit psoas fibers Pflugers Arch. 408 1987 1 9
37. E. Pate, and R. Cooke Addition of phosphate to active muscle fibers probes actomyosin states within the powerstroke Pflugers Arch. 414 1989 73 81
38. R. Cooke, and K. Franks E. Pate The inhibition of rabbit skeletal muscle contraction by hydrogen ions and phosphate J. Physiol. 395 1988 77 97
39. N.C. Millar, and E. Homsher The effect of phosphate and calcium on force generation in glycerinated rabbit skeletal muscle fibers. A steady-state and transient kinetic study J. Biol. Chem. 265 1990 20234 20240
40. J.A. Dantzig, and Y.E. Goldman E. Homsher Reversal of the cross-bridge force-generating transition by photogeneration of phosphate in rabbit psoas muscle fibres J. Physiol. 451 1992 247 278
41. V. Lombardi, and G. Piazzesi The contractile response during steady lengthening of stimulated frog muscle fibres J. Physiol. 431 1990 141 171
42. G. Wang, and M. Kawai Effect of temperature on elementary steps of the cross-bridge cycle in rabbit soleus slow-twitch muscle fibres J. Physiol. 531 2001 219 234
43. G. Piazzesi, and M. Reconditi V. Lombardi Temperature dependence of the force-generating process in single fibres from frog skeletal muscle J. Physiol. 549 2003 93 106
44. B. Colombini, and M. Nocella M.A. Bagni Cross-bridge properties during force enhancement by slow stretching in single intact frog muscle fibres J. Physiol. 585 2007 607 615
45. B. Colombini, and M. Nocella M.A. Bagni Effect of temperature on cross-bridge properties in intact frog muscle fibers Am. J. Physiol. Cell Physiol. 294 2008 C1113 C1117
46. C. Mansfield, and T.G. West M.A. Ferenczi Stretch of contracting cardiac muscle abruptly decreases the rate of phosphate release at high and low calcium J. Biol. Chem. 287 2012 25696 25705
47. J.E. Baker Free energy transduction in a chemical motor model J. Theor. Biol. 228 2004 467 476
48. S. Zhang, and S.I. Bernstein Spatially and temporally regulated expression of myosin heavy chain alternative exons during Drosophila embryogenesis Mech. Dev. 101 2001 35 45
49. S.I. Bernstein, and C.J. Hansen C.P. Emerson Jr. Alternative RNA splicing generates transcripts encoding a thorax-specific isoform of Drosophila melanogaster myosin heavy chain Mol. Cell. Biol. 6 1986 2511 2519
50. D.M. Swank, and A.F. Knowles S.I. Bernstein Variable N-terminal regions of muscle myosin heavy chain modulate ATPase rate and actin sliding velocity J. Biol. Chem. 278 2003 17475 17482
51. K.P. Littlefield, and D.M. Swank S.I. Bernstein The converter domain modulates kinetic properties of Drosophila myosin Am. J. Physiol. Cell Physiol. 284 2003 C1031 C1038
52. D.M. Swank, and W.A. Kronert D.W. Maughan Alternative N-terminal regions of Drosophila myosin heavy chain tune muscle kinetics for optimal power output Biophys. J. 87 2004 1805 1814
53. D.M. Swank, and J. Braddock D.W. Maughan An alternative domain near the ATP binding pocket of Drosophila myosin affects muscle fiber kinetics Biophys. J. 90 2006 2427 2435
54. D.M. Swank, V.K. Vishnudas, and D.W. Maughan An exceptionally fast actomyosin reaction powers insect flight muscle Proc. Natl. Acad. Sci. USA 103 2006 17543 17547
55. C. Yang, and S. Ramanath D.M. Swank Alternative versions of the myosin relay domain differentially respond to load to influence Drosophila muscle kinetics Biophys. J. 95 2008 5228 5237
56. D.V. Trivedi, and C. David C.M. Yengo Switch II mutants reveal coupling between the nucleotide- and actin-binding regions in myosin V Biophys. J. 102 2012 2545 2555