Mechanical tension and spontaneous muscle twitching precede the formation of cross-striated muscle in vivo

Development (Cambridge)

Volumn 144, Issue 7, 2017, Pages 1261-1272

  Weitkunat, Manuela ^a   Brasse, Martina ^b   Bausch, Andreas R ^b   Schnorrer, Frank ^a,c  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

Drosophila; Muscle; Myofibrillogenesis; Sarcomere; Self organization; Tension

Indexed keywords

ACTIN; CALCIUM; CALCIUM ION; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN HEAVY CHAIN;

ABDOMINAL WALL MUSCULATURE; ADULT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; FILOPODIUM; IMAGING; LASER; MORPHOGENESIS; MUSCLE CONTRACTILITY; MUSCLE DEVELOPMENT; MUSCLE FIBER CONTRACTION; MUSCLE FIBRIL; MUSCLE STRENGTH; MUSCLE TWITCH; MYOTUBE; NONHUMAN; OPTOGENETICS; SARCOMERE; SKELETAL MUSCLE; SKELETAL MUSCLE CELL; TENSION; ABDOMEN; ANIMAL; BIOLOGICAL MODEL; DROSOPHILA MELANOGASTER; MECHANICAL STRESS; METABOLISM; MUSCLE CONTRACTION; PHYSIOLOGY;

ABDOMEN; ANIMALS; DROSOPHILA MELANOGASTER; LASERS; MODELS, BIOLOGICAL; MORPHOGENESIS; MUSCLE CONTRACTION; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; MYOFIBRILS; OPTOGENETICS; SARCOMERES; STRESS, MECHANICAL;

EID: 85016420844     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.140723     Document Type: Article

References (67)

1. Akerboom, J., Chen, T.-W., Wardill, T. J., Tian, L., Marvin, J. S., Mutlu, S., Calderón, N. C., Esposti, F., Borghuis, B. G., Sun, X. R. et al. (2012). Optimization of a GCaMP calcium indicator for neural activity imaging. J. Neurosci. 32, 13819-13840.
2. Barone, V., Bertocchini, F., Bottinelli, R., Protasi, F., Allen, P. D., Franzini Armstrong, C., Reggiani, C. and Sorrentino, V. (1998). Contractile impairment and structural alterations of skeletal muscles from knockout mice lacking type 1 and type 3 ryanodine receptors. FEBS Lett. 422, 160-164
3. Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G. and Deisseroth, K. (2005). Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8, 1263-1268
4. Brown, N. H., Gregory, S. L. and Martin-Bermudo, M. D. (2000). Integrins as mediators of morphogenesis in Drosophila. Dev. Biol. 223, 1-16
5. Bullard, B., Burkart, C., Labeit, S. and Leonard, K. (2005). The function of elastic proteins in the oscillatory contraction of insect flight muscle. J. Muscle Res. Cell Motil. 26, 479-485
6. Burkholder, T. J. and Lieber, R. L. (2001). Sarcomere length operating range of vertebrate muscles during movement. J. Exp. Biol. 204, 1529-1536
7. Chen, T.-W., Wardill, T. J., Sun, Y., Pulver, S. R., Renninger, S. L., Baohan, A., Schreiter, E. R., Kerr, R. A., Orger, M. B., Jayaraman, V. et al. (2013). Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300
8. Clark, K. A., McElhinny, A. S., Beckerle, M. C. and Gregorio, C. C. (2002). Striated muscle cytoarchitecture: an intricateweb of form and function. Annu. Rev. Dev.l Biol. 18, 637-706
9. Clarke, N. F. (2008). Skeletal muscle disease due to mutations in tropomyosin, troponin and cofilin. Adv. Exp. Med. Biol. 642, 40-54
10. Clyne, P. J., Brotman, J. S., Sweeney, S. T. and Davis, G. (2003). Green fluorescent protein tagging Drosophila proteins at their native genomic loci with small P elements. Genetics 165, 1433-1441
11. Colombelli, J., Besser, A., Kress, H., Reynaud, E. G., Girard, P., Caussinus, E., Haselmann, U., Small, J. V., Schwarz, U. and Stelzer, E. H. K. (2009). Mechanosensing in actin stress fibers revealed by a close correlation between force and protein localization. J. Cell Sci. 122, 1665-1679
12. Currie, D. A. and Bate, M. (1991). The development of adult abdominal muscles in Drosophila: myoblasts express twist and are associated with nerves. Development 113, 91-102.
13. De Deyne, P. G. (2000). Formation of sarcomeres in developing myotubes: role of mechanical stretch and contractile activation. Am. J. Physiol. Cell Physiol. 279, C1801-C1811
14. Dutta, D., Bloor, J. W., Ruiz-Gomez, M., VijayRaghavan, K. and Kiehart, D. P. (2002). Real-time imaging of morphogenetic movements in Drosophila using Gal4-UAS-driven expression of GFP fused to the actin-binding domain of moesin. Genesis 34, 146-151
15. Dutta, D., Anant, S., Ruiz-Gomez, M., Bate, M. and VijayRaghavan, K. (2004). Founder myoblasts and fibre number during adult myogenesis in Drosophila. Development 131, 3761-3772
16. Ebrahim, S., Fujita, T., Millis, B. A., Kozin, E., Ma, X., Kawamoto, S., Baird, M. A., Davidson, M., Yonemura, S., Hisa, Y. et al. (2013). NMII forms a contractile transcellular sarcomeric network to regulate apical cell junctions and tissue geometry. Curr. Biol. 23, 731-736
17. Ehler, E. and Gautel, M. (2008). The sarcomere and sarcomerogenesis. Adv. Exp. Med. Biol. 642, 1-14
18. Ehler, E., Rothen, B. M., Hämmerle, S. P., Komiyama, M. and Perriard, J. C. (1999). Myofibrillogenesis in the developing chicken heart: assembly of Z-disk, Mline and the thick filaments. J. Cell Sci. 112, 1529-1539
19. Fenno, L., Yizhar, O. and Deisseroth, K. (2011). The development and application of optogenetics. Annu. Rev. Neurosci. 34, 389-412
20. Ferrari, M. B., Ribbeck, K., Hagler, D. J. and Spitzer, N. C. (1998). A calcium signaling cascade essential for myosin thick filament assembly in Xenopus myocytes. J. Cell Biol. 141, 1349-1356
21. Friedrich, B. M., Fischer-Friedrich, E., Gov, N. S. and Safran, S. A. (2012). Sarcomeric pattern formation by actin cluster coalescence. PLoS Comput. Biol. 8, e1002544
22. Fujita, H., Nedachi, T. and Kanzaki, M. (2007). Accelerated de novo sarcomere assembly by electric pulse stimulation in C2C12 myotubes. Exp. Cell Res. 313, 1853-1865
23. Fürst, D. O., Osborn, M., Nave, R. and Weber, K. (1988). The organization of titin filaments in the half-sarcomere revealed by monoclonal antibodies in immunoelectron microscopy: a map of ten nonrepetitive epitopes starting at the Z line extends close to the M line. J. Cell Biol. 106, 1563-1572
24. Gautel, M. (2011). The sarcomeric cytoskeleton: who picks up the strain? Curr. Opin. Cell Biol. 23, 39-46
25. Gautel, M. and Djinovic-Carugo, K. (2016). The sarcomeric cytoskeleton: from molecules to motion. J. Exp. Biol. 219, 135-145
26. Gokhin, D. S. and Fowler, V. M. (2013). A two-segment model for thin filament architecture in skeletal muscle. Nat. Rev. Mol. Cell Biol. 14, 113-119
27. Harris, B. N., Li, H., Terry, M. and Ferrari, M. B. (2005). Calcium transients regulate titin organization during myofibrillogenesis. Cell Motil. Cytoskeleton 60, 129-139
28. Hatan, M., Shinder, V., Israeli, D., Schnorrer, F. and Volk, T. (2011). The Drosophila blood brain barrier is maintained by GPCR-dependent dynamic actin structures. J. Cell Biol. 192, 307-319
29. Hill, J. and Olson, E. (2012). Muscle: fundamental biology and mechanisms of disease (ed. J. A. Hill, and E. N. Olson). London, UK: Academic Press.
30. Holtzer, H., Hijikata, T., Lin, Z. X., Zhang, Z. Q., Holtzer, S., Protasi, F., Franzini-Armstrong, C. and Sweeney, H. L. (1997). Independent assembly of 1.6 microns long bipolar MHC filaments and I-Z-I bodies. Cell Struct. Funct. 22, 83-93
31. Huxley, H. and Hanson, J. (1954). Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature 173, 973-976
32. Huxley, A. F. and Niedergerke, R. (1954). Structural changes in muscle during contraction; interference microscopy of living muscle fibres. Nature 173, 971-973
33. Josephson, R. (2006). Comparative physiology of insect flight muscle. In Nature’s Versatile Engine: Insect Flight Muscle Inside and Out (ed. J. Vigoreaux), pp. 35-43 Georgetown, TX: Landes Bioscience.
34. Kagawa, M., Sato, N. and Obinata, T. (2006). Effects of BTS (N-benzyl-p-toluene sulphonamide), an inhibitor for myosin-actin interaction, on myofibrillogenesis in skeletal muscle cells in culture. Zool. Sci. 23, 969-975
35. Kidokoro, Y. and Saito, M. (1988). Early cross-striation formation in twitching Xenopus myocytes in culture. Proc. Natl. Acad. Sci. USA 85, 1978-1982
36. Krzemien, J., Fabre, C. C. G., Casal, J. and Lawrence, P. A. (2012). The muscle pattern of the Drosophila abdomen depends on a subdivision of the anterior compartment of each segment. Development 139, 75-83
37. Lemke, S. B. and Schnorrer, F. (2016). Mechanical forces during muscle development. Mech. Dev. doi:10.1016/j.mod.2016.11.003
38. Leptin, M., Bogaert, T., Lehmann, R. and Wilcox, M. (1989). The function of PS integrins during Drosophila embryogenesis. Cell 56, 401-408
39. Llewellyn, M., Barretto, R., Delp, S. L. and Schnitzer, M. (2008). Minimally invasive high-speed imaging of sarcomere contractile dynamics in mice and humans. Nature 454, 784-788
40. Marino, T. A., Kuseryk, L. and Lauva, I. K. (1987). Role of contraction in the structure and growth of neonatal rat cardiocytes. Am. J. Physiol. 253, H1391-H1399
41. Mayer, M., Depken, M., Bois, J. S., Jülicher, F. and Grill, S. W. (2010). Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows. Nature 467, 617-621
42. Millard, T. H. and Martin, P. (2008). Dynamic analysis of filopodial interactions during the zippering phase of Drosophila dorsal closure. Development 135, 621-626
43. Ohtsuki, I. and Morimoto, S. (2008). Troponin: Regulatory function and disorders. Biochem. Biophys. Res. Commun. 369, 62-73
44. Orfanos, Z. and Sparrow, J. C. (2013). Myosin isoform switching during assembly of the Drosophila flight muscle thick filament lattice. J. Cell Sci. 126, 139-148
45. Pellegrin, S. and Mellor, H. (2007). Actin stress fibres. J. Cell Sci. 120, 3491-3499
46. Perriard, J.-C., Hirschy, A. and Ehler, E. (2003). Dilated cardiomyopathy: a disease of the intercalated disc? Trends Cardiovasc. Med. 13, 30-38
47. Pulver, S. R., Pashkovski, S. L., Hornstein, N. J., Garrity, P. A. and Griffith, L. C. (2009). Temporal dynamics of neuronal activation by Channelrhodopsin-2 and TRPA1 determine behavioral output in Drosophila larvae. J. Neurophysiol. 101, 3075-3088
48. Ranganayakulu, G., Schulz, R. A. and Olson, E. N. (1996). Wingless signaling induces nautilus expression in the ventral mesoderm of the Drosophila embryo. Dev. Biol. 176, 143-148
49. Rhee, D., Sanger, J. M. and Sanger, J.W. (1994). The premyofibril: evidence for its role in myofibrillogenesis. Cell Motil. Cytoskeleton 28, 1-24
50. Rui, Y., Bai, J. and Perrimon, N. (2010). Sarcomere formation occurs by the assembly of multiple latent protein complexes. PLoS Genet. 6, e1001208
51. Sanger, J.W., Wang, J., Fan, Y., White, J. and Sanger, J. M. (2010). Assembly and dynamics of myofibrils. J. Biomed. Biotechnol. 2010, 858606
52. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B. et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682.
53. Schönbauer, C., Distler, J., Jährling, N., Radolf, M., Dodt, H.-U., Frasch, M. and Schnorrer, F. (2011). Spalt mediates an evolutionarily conserved switch to fibrillar muscle fate in insects. Nature 479, 406-409
54. Schwander, M., Leu, M., Stumm, M., Dorchies, O. M., Ruegg, U. T., Schittny, J. and Müller, U. (2003). Beta1 integrins regulate myoblast fusion and sarcomere assembly. Dev. Cell 4, 673-685
55. Sparrow, J. C. and Schöck, F. (2009). The initial steps of myofibril assembly: integrins pave the way. Nat. Rev. Mol. Cell Biol. 10, 293-298
56. Tajsharghi, H. and Oldfors, A. (2013). Myosinopathies: pathology and mechanisms. Acta Neuropathol. 125, 3-18
57. Takeshima, H., Iino, M., Takekura, H., Nishi, M., Kuno, J., Minowa, O., Takano, H. and Noda, T. (1994). Excitation-contraction uncoupling and muscular degeneration in mice lacking functional skeletal muscle ryanodine-receptor gene. Nature 369, 556-559
58. Treiman, M., Caspersen, C. and Christensen, S. B. (1998). A tool coming of age: thapsigargin as an inhibitor of sarco-endoplasmic reticulum Ca(2+)-ATPases. Trends Pharmacol. Sci. 19, 131-135
59. Tskhovrebova, L. and Trinick, J. (2003). Titin: properties and family relationships. Nat. Rev. Mol. Cell Biol. 4, 679-689
60. Tskhovrebova, L. and Trinick, J. (2012). Molecular rulers? Curr. Biol. 22, R317-R318
61. Tskhovrebova, L., Bennett, P., Gautel, M. and Trinick, J. (2015). Titin ruler hypothesis not refuted. Proc. Natl Acad. Sci. USA 112, E1172
62. Udd, B. (2008). Third filament diseases. Adv. Exp. Med. Biol. 642, 99-115
63. Wang, J., Shaner, N., Mittal, B., Zhou, Q., Chen, J., Sanger, J. M. and Sanger, J. W. (2005). Dynamics of Z-band based proteins in developing skeletal muscle cells. Cell Motil. Cytoskeleton 61, 34-48
64. Weitkunat, M. and Schnorrer, F. (2014). A guide to study Drosophila muscle biology. Methods 68, 2-14
65. Weitkunat, M., Kaya-Çopur, A., Grill, S.W. and Schnorrer, F. (2014). Tension and force-resistant attachment are essential for myofibrillogenesis in Drosophila flight muscle. Curr. Biol. 24, 705-716
66. Whiting, A., Wardale, J. and Trinick, J. (1989). Does titin regulate the length of muscle thick filaments? J. Mol. Biol. 205, 263-268
67. Yoshinaga, N., Joanny, J.-F., Prost, J. and Marcq, P. (2010). Polarity Patterns of Stress Fibers. Phys. Rev. Lett. 105, 238103.