Tension and force-resistant attachment are essential for myofibrillogenesis in drosophila flight muscle

Current Biology

Volumn 24, Issue 7, 2014, Pages 705-716

  Weitkunat, Manuela ^a   Kaya Çopur, Aynur ^a   Grill, Stephan W ^b,c   Schnorrer, Frank ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b MAX PLANCK INSTITUT FÜR PHYSIK KOMPLEXER SYSTEME   (Germany)

^c MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; VERTEBRATA;

ANATOMY AND HISTOLOGY; ANIMAL; BIOMECHANICS; DROSOPHILA; FLYING; MUSCLE; MUSCLE DEVELOPMENT; PHYSIOLOGY;

ANIMALS; BIOMECHANICAL PHENOMENA; DROSOPHILA; FLIGHT, ANIMAL; MUSCLE DEVELOPMENT; MUSCLES;

EID: 84898059200     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2014.02.032     Document Type: Article

References (54)

1. F. Schnorrer, and B.J. Dickson Muscle building; mechanisms of myotube guidance and attachment site selection Dev. Cell 7 2004 9 20
2. R. Schweitzer, E. Zelzer, and T. Volk Connecting muscles to tendons: tendons and musculoskeletal development in flies and vertebrates Development 137 2010 2807 2817
3. S. Lange, E. Ehler, and M. Gautel From A to Z and back? Multicompartment proteins in the sarcomere Trends Cell Biol. 16 2006 11 18
4. H.E. Huxley The mechanism of muscular contraction Science 164 1969 1356 1365
5. N. Yoshinaga, J.F. Joanny, J. Prost, and P. Marcq Polarity patterns of stress fibers Phys. Rev. Lett. 105 2010 238103
6. F. Schnorrer, I. Kalchhauser, and B.J. Dickson The transmembrane protein Kon-tiki couples to Dgrip to mediate myotube targeting in Drosophila Dev. Cell 12 2007 751 766
7. G. Wolfstetter, and A. Holz The role of LamininB2 (LanB2) during mesoderm differentiation in Drosophila Cell. Mol. Life Sci. 69 2012 267 282
8. B. Estrada, S.S. Gisselbrecht, and A.M. Michelson The transmembrane protein Perdido interacts with Grip and integrins to mediate myotube projection and attachment in the Drosophila embryo Development 134 2007 4469 4478
9. N.H. Brown, S.L. Gregory, and M.D. Martin-Bermudo Integrins as mediators of morphogenesis in Drosophila Dev. Biol. 223 2000 1 16
10. C. Bökel, and N.H. Brown Integrins in development: moving on, responding to, and sticking to the extracellular matrix Dev. Cell 3 2002 311 321
11. M. Leptin, T. Bogaert, R. Lehmann, and M. Wilcox The function of PS integrins during Drosophila embryogenesis Cell 56 1989 401 408
12. A. Prokop, M.D. Martín-Bermudo, M. Bate, and N.H. Brown Absence of PS integrins or laminin A affects extracellular adhesion, but not intracellular assembly, of hemiadherens and neuromuscular junctions in Drosophila embryos Dev. Biol. 196 1998 58 76
13. E. Ehler, and M. Gautel The sarcomere and sarcomerogenesis Adv. Exp. Med. Biol. 642 2008 1 14
14. J.W. Sanger, J. Wang, Y. Fan, J. White, and J.M. Sanger Assembly and dynamics of myofibrils J. Biomed. Biotechnol. 2010 2010 858606
15. G.L. Crawford, and R. Horowits Scaffolds and chaperones in myofibril assembly: putting the striations in striated muscle Biophys. Rev. 3 2011 25 32
16. A. Du, J.M. Sanger, and J.W. Sanger Cardiac myofibrillogenesis inside intact embryonic hearts Dev. Biol. 318 2008 236 246
17. K.T. Tokuyasu Immunocytochemical studies of cardiac myofibrillogenesis in early chick embryos. III. Generation of fasciae adherentes and costameres J. Cell Biol. 108 1989 43 53
18. T. Volk, L.I. Fessler, and J.H. Fessler A role for integrin in the formation of sarcomeric cytoarchitecture Cell 63 1990 525 536
19. J.W. Bloor, and N.H. Brown Genetic analysis of the Drosophila alphaPS2 integrin subunit reveals discrete adhesive, morphogenetic and sarcomeric functions Genetics 148 1998 1127 1142
20. M. Schwander, M. Leu, M. Stumm, O.M. Dorchies, U.T. Ruegg, J. Schittny, and U. Müller Beta1 integrins regulate myoblast fusion and sarcomere assembly Dev. Cell 4 2003 673 685
21. J.C. Sparrow, and F. Schöck The initial steps of myofibril assembly: integrins pave the way Nat. Rev. Mol. Cell Biol. 10 2009 293 298
22. E. Ehler, B.M. Rothen, S.P. Hämmerle, M. Komiyama, and J.C. Perriard Myofibrillogenesis in the developing chicken heart: assembly of Z-disk, M-line and the thick filaments J. Cell Sci. 112 1999 1529 1539
23. H. Holtzer, T. Hijikata, Z.X. Lin, Z.Q. Zhang, S. Holtzer, F. Protasi, C. Franzini-Armstrong, and H.L. Sweeney Independent assembly of 1.6 microns long bipolar MHC filaments and I-Z-I bodies Cell Struct. Funct. 22 1997 83 93
24. Y. Rui, J. Bai, and N. Perrimon Sarcomere formation occurs by the assembly of multiple latent protein complexes PLoS Genet. 6 2010 e1001208
25. A. Zemel, and A. Mogilner Motor-induced sliding of microtubule and actin bundles Phys. Chem. Chem. Phys. 11 2009 4821 4833
26. B.M. Friedrich, E. Fischer-Friedrich, N.S. Gov, and S.A. Safran Sarcomeric pattern formation by actin cluster coalescence PLoS Comput. Biol. 8 2012 e1002544
27. C. Grashoff, B.D. Hoffman, M.D. Brenner, R. Zhou, M. Parsons, M.T. Yang, M.A. McLean, S.G. Sligar, C.S. Chen, T. Ha, and M.A. Schwartz Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics Nature 466 2010 263 266
28. M. Dickinson Insect flight Curr. Biol. 16 2006 R309 R314
29. C. Schönbauer, J. Distler, N. Jährling, M. Radolf, H.-U. Dodt, M. Frasch, and F. Schnorrer Spalt mediates an evolutionarily conserved switch to fibrillar muscle fate in insects Nature 479 2011 406 409
30. J. Fernandes, M. Bate, and K. Vijayraghavan Development of the indirect flight muscles of Drosophila Development 113 1991 67 77
31. D. Dutta, S. Anant, M. Ruiz-Gomez, M. Bate, and K. Vijayraghavan Founder myoblasts and fibre number during adult myogenesis in Drosophila Development 131 2004 3761 3772
32. J.J. Fernandes, S.E. Celniker, and K. Vijayraghavan Development of the indirect flight muscle attachment sites in Drosophila: role of the PS integrins and the stripe gene Dev. Biol. 176 1996 166 184
33. M.C. Reedy, and C. Beall Ultrastructure of developing flight muscle in Drosophila. I. Assembly of myofibrils Dev. Biol. 160 1993 443 465
34. M.C. Reedy, and C. Beall Ultrastructure of developing flight muscle in Drosophila. II. Formation of the myotendon junction Dev. Biol. 160 1993 466 479
35. P.G. De Deyne Formation of sarcomeres in developing myotubes: role of mechanical stretch and contractile activation Am. J. Physiol. Cell Physiol. 279 2000 C1801 C1811
36. A.J. Engler, M.A. Griffin, S. Sen, C.G. Bönnemann, H.L. Sweeney, and D.E. Discher Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments J. Cell Biol. 166 2004 877 887
37. M. Kagawa, N. Sato, and T. Obinata Effects of BTS (N-benzyl-p-toluene sulphonamide), an inhibitor for myosin-actin interaction, on myofibrillogenesis in skeletal muscle cells in culture Zoolog. Sci. 23 2006 969 975
38. F. Schnorrer, C. Schönbauer, C.C.H. Langer, G. Dietzl, M. Novatchkova, K. Schernhuber, M. Fellner, A. Azaryan, M. Radolf, and A. Stark et al. Systematic genetic analysis of muscle morphogenesis and function in Drosophila Nature 464 2010 287 291
39. W. Bottenberg, N. Sanchez-Soriano, J. Alves-Silva, I. Hahn, M. Mende, and A. Prokop Context-specific requirements of functional domains of the Spectraplakin Short stop in vivo Mech. Dev. 126 2009 489 502
40. A. Subramanian, A. Prokop, M. Yamamoto, K. Sugimura, T. Uemura, J. Betschinger, J.A. Knoblich, and T. Volk Shortstop recruits EB1/APC1 and promotes microtubule assembly at the muscle-tendon junction Curr. Biol. 13 2003 1086 1095
41. N.H. Brown, S.L. Gregory, W.L. Rickoll, L.I. Fessler, M. Prout, R.A.H. White, and J.W. Fristrom Talin is essential for integrin function in Drosophila Dev. Cell 3 2002 569 579
42. C. Grabbe, C.G. Zervas, T. Hunter, N.H. Brown, and R.H. Palmer Focal adhesion kinase is not required for integrin function or viability in Drosophila Development 131 2004 5795 5805
43. A. Katzemich, N. Kreisköther, A. Alexandrovich, C. Elliott, F. Schöck, K. Leonard, J. Sparrow, and B. Bullard The function of the M-line protein obscurin in controlling the symmetry of the sarcomere in the flight muscle of Drosophila J. Cell Sci. 125 2012 3367 3379
44. J.D. Saide, S. Chin-Bow, J. Hogan-Sheldon, L. Busquets-Turner, J.O. Vigoreaux, K. Valgeirsdottir, and M.L. Pardue Characterization of components of Z-bands in the fibrillar flight muscle of Drosophila melanogaster J. Cell Biol. 109 1989 2157 2167
45. C. Burkart, F. Qiu, S. Brendel, V. Benes, P. Hååg, S. Labeit, K. Leonard, and B. Bullard Modular proteins from the Drosophila sallimus (sls) gene and their expression in muscles with different extensibility J. Mol. Biol. 367 2007 953 969
46. R.M. Cripps, J.A. Suggs, and S.I. Bernstein Assembly of thick filaments and myofibrils occurs in the absence of the myosin head EMBO J. 18 1999 1793 1804
47. M.D. Martin-Bermudo, and N.H. Brown The localized assembly of extracellular matrix integrin ligands requires cell-cell contact J. Cell Sci. 113 2000 3715 3723
48. B. Wehrle-Haller Structure and function of focal adhesions Curr. Opin. Cell Biol. 24 2012 116 124
49. M. Pines, R. Das, S.J. Ellis, A. Morin, S. Czerniecki, L. Yuan, M. Klose, D. Coombs, and G. Tanentzapf Mechanical force regulates integrin turnover in Drosophila in vivo Nat. Cell Biol. 14 2012 935 943
50. M. Moser, K.R. Legate, R. Zent, and R. Fässler The tail of integrins, talin, and kindlins Science 324 2009 895 899
51. D.P. Kiehart, C.G. Galbraith, K.A. Edwards, W.L. Rickoll, and R.A. Montague Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila J. Cell Biol. 149 2000 471 490
52. J. Solon, A. Kaya-Copur, J. Colombelli, and D. Brunner Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure Cell 137 2009 1331 1342
53. K.P. Landsberg, R. Farhadifar, J. Ranft, D. Umetsu, T.J. Widmann, T. Bittig, A. Said, F. Jülicher, and C. Dahmann Increased cell bond tension governs cell sorting at the Drosophila anteroposterior compartment boundary Curr. Biol. 19 2009 1950 1955
54. T.A. Marino, L. Kuseryk, and I.K. Lauva Role of contraction in the structure and growth of neonatal rat cardiocytes Am. J. Physiol. 253 1987 H1391 H1399