The syncytial visceral and somatic musculature develops independently of β3-Tubulin during Drosophila embryogenesis, while maternally supplied β1-Tubulin is stable until the early steps of myoblast fusion

European Journal of Cell Biology

Volumn 91, Issue 3, 2012, Pages 192-203

  Rudolf, Anja ^a   Buttgereit, Detlev ^a   Rexer, Karl Heinz ^a   Renkawitz Pohl, Renate ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

1 Tubulin; 2 Tubulin; 3 Tubulin; Drosophila myogenesis; Microtubules; Myoblast fusion; Swiprosin; Visceral muscles

Indexed keywords

BETA 1 TUBULIN; BETA TUBULIN; BETA3 TUBULIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CULTURE; CELL FUSION; DROSOPHILA; EMBRYO DEVELOPMENT; GENE DELETION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INSECT GENETICS; LOSS OF FUNCTION MUTATION; MESODERM; MICROTUBULE; MUSCLE DEVELOPMENT; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCANNING ELECTRON MICROSCOPE; SOMATIC CELL; TRANSGENIC ORGANISM; VISCERA; WESTERN BLOTTING;

ANIMALS; CALCIUM-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; MICROTUBULES; MORPHOGENESIS; MUTANT PROTEINS; MYOBLASTS; SARCOMERES; TUBULIN;

VERTEBRATA;

EID: 84857121635     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2011.11.002     Document Type: Article

References (86)

1. Armknecht S., Boutros M., Kiger A., Nybakken K., Mathey-Prevot B., Perrimon N. High-throughput RNA interference screens in Drosophila tissue culture cells. Methods Enzymol. 2005, 392:55-73.
2. Azpiazu N., Frasch M. Tinman and bagpipe: two homeo box genes that determine cell fates in the dorsal mesoderm of Drosophila. Genes Dev. 1993, 7:1325-1340.
3. Bialojan S., Falkenburg D., Renkawitz-Pohl R. Characterization and developmental expression of beta tubulin genes in Drosophila melanogaster. EMBO J. 1984, 3:2543-2548.
4. Bienz M. Homeotic genes and positional signalling in the Drosophila viscera. Trends Genet. 1994, 10:22-26.
5. Bischof J., Maeda R.K., Hediger M., Karch F., Basler K. An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:3312-3317.
6. Bischoff R., Holtzer H. The effect of mitotic inhibitors on myogenesis in vitro. J. Cell Biol. 1968, 36:111-127.
7. Bodmer R., Jan L.Y., Jan Y.N. A new homeobox-containing gene, msh-2, is transiently expressed early during mesoderm formation of Drosophila. Development 1990, 110:661-669.
8. Bugnard E., Zaal K.J., Ralston E. Reorganization of microtubule nucleation during muscle differentiation. Cell Motil. Cytoskeleton 2005, 60:1-13.
9. Buszczak M., Paterno S., Lighthouse D., Bachman J., Planck J., Owen S., Skora A.D., Nystul T.G., Ohlstein B., Allen A., Wilhelm J.E., Murphy T.D., Levis R.W., Matunis E., Srivali N., Hoskins R.A., Spradling A.C. The carnegie protein trap library: a versatile tool for Drosophila developmental studies. Genetics 2007, 175:1505-1531.
10. Buttgereit D., Leiss D., Michiels F., Renkawitz-Pohl R. During Drosophila embryogenesis the beta 1 tubulin gene is specifically expressed in the nervous system and the apodemes. Mech. Dev. 1991, 33:107-118.
11. Buttgereit D., Paululat A., Renkawitz-Pohl R. Muscle development and attachment to the epidermis is accompanied by expression of beta 3 and beta 1 tubulin isotypes, respectively. Int. J. Dev. Biol. 1996, 40:189-196.
12. Cornfine S., Himmel M., Kopp P., El Azzouzi K., Wiesner C., Krüger M., Rudel T., Linder S. The kinesin KIF9 and reggie/flotillin proteins regulate matrix degradation by macrophage podosomes. Mol. Biol. Cell 2011, 22:202-215.
13. Currie D.A., Bate M. The development of adult abdominal muscles in Drosophila: myoblasts express twist and are associated with nerves. Development 1991, 113:91-102.
14. Damm C., Wolk A., Buttgereit D., Löher K., Wagner E., Lilly B., Olson E., Hasenpusch-Theil K., Renkawitz-Pohl R. Independent regulatory elements in the upstream region of the Drosophila beta 3 tubulin gene (beta Tub60D) guide expression in the dorsal vessel and the somatic muscles. Dev. Biol. 1998, 199:138-149.
15. Destaing O., Saltel F., Gilquin B., Chabadel A., Khochbin S., Ory S., Jurdic P. A novel Rho-mDia2-HDAC6 pathway controls podosome patterning through microtubule acetylation in osteoclasts. J. Cell Sci. 2005, 118:2901-2911.
16. Dettman R.W., Turner F.R., Hoyle H.D., Raff E.C. Embryonic expression of the divergent Drosophila beta3-tubulin isoform is required for larval behavior. Genetics 2001, 158:253-263.
17. Dettman R.W., Turner F.R., Raff E.C. Genetic analysis of the Drosophila beta3-tubulin gene demonstrates that the microtubule cytoskeleton in the cells of the visceral mesoderm is required for morphogenesis of the midgut endoderm. Dev. Biol. 1996, 177:117-135.
18. Doberstein S.K., Fetter R.D., Mehta A.Y., Goodman C.S. Genetic analysis of myoblast fusion: blown fuse is required for progression beyond the prefusion complex. J. Cell Biol. 1997, 136:1249-1261.
19. Dobi K.C., Metzger T., Baylies M.K. Characterization of early steps in muscle morphogenesis in a Drosophila primary culture system. Fly (Austin) 2011, 5:68-75.
20. Evans I.R., Wood W. Understanding in vivo blood cell migration - Drosophila hemocytes lead the way. Fly (Austin) 2011, 5:110-114.
21. Fuller M.T., Caulton J.H., Hutchens J.A., Kaufman T.C., Raff E.C. Genetic analysis of microtubule structure: a beta-tubulin mutation causes the formation of aberrant microtubules in vivo and in vitro. J. Cell Biol. 1987, 104:385-394.
22. Gasch A., Hinz U., Renkawitz-Pohl R. Intron and upstream sequences regulate expression of the Drosophila beta 3-tubulin gene in the visceral and somatic musculature, respectively. Proc. Natl. Acad. Sci. U. S. A. 1989, 86:3215-3218.
23. Georgias C., Wasser M., Hinz U. A basic-helix-loop-helix protein expressed in precursors of Drosophila longitudinal visceral muscles. Mech. Dev. 1997, 69:115-124.
24. Guerin C.M., Kramer S.G. RacGAP50C directs perinuclear gamma-tubulin localization to organize the uniform microtubule array required for Drosophila myotube extension. Development 2009, 136:1411-1421.
25. Haralalka S., Shelton C., Cartwright H.N., Katzfey E., Janzen E., Abmayr S.M. Asymmetric Mbc, active Rac1 and F-actin foci in the fusion-competent myoblasts during myoblast fusion in Drosophila. Development 2011, 138:1551-1562.
26. Hinz U., Wolk A., Renkawitz-Pohl R. Ultrabithorax is a regulator of beta 3 tubulin expression in the Drosophila visceral mesoderm. Development 1992, 116:543-554.
27. Hornbruch-Freitag C., Griemert B., Buttgereit D., Renkawitz-Pohl R. Drosophila Swiprosin-1/EFHD2 accumulates at the prefusion complex stage during Drosophila myoblast fusion. J. Cell Sci. 2011, 124:3266-3278.
28. Hoyle H.D., Raff E.C. Two Drosophila beta tubulin isoforms are not functionally equivalent. J. Cell Biol. 1990, 111:1009-1026.
29. Hoyle H.D., Turner F.R., Raff E.C. A transient specialization of the microtubule cytoskeleton is required for differentiation of the Drosophila visual system. Dev. Biol. 2000, 221:375-389.
30. Häcker U., Kaufmann E., Hartmann C., Jürgens G., Knöchel W., Jäckle H. The Drosophila fork head domain protein crocodile is required for the establishment of head structures. EMBO J. 1995, 14:5306-5317.
31. Immerglück K., Lawrence P.A., Bienz M. Induction across germ layers in Drosophila mediated by a genetic cascade. Cell 1990, 62:261-268.
32. Jattani R., Patel U., Kerman B., Myat M.M. Deficiency screen identifies a novel role for beta 2 tubulin in salivary gland and myoblast migration in the Drosophila embryo. Dev. Dyn. 2009, 238:853-863.
33. Kaltschmidt B., Glätzer K.H., Michiels F., Leiss D., Renkawitz-Pohl R. During Drosophila spermatogenesis beta 1, beta 2 and beta 3 tubulin isotypes are cell-type specifically expressed but have the potential to coassemble into the axoneme of transgenic flies. Eur. J. Cell Biol. 1991, 54:110-120.
34. Karr T.L. Intracellular sperm/egg interactions in Drosophila: a three-dimensional structural analysis of a paternal product in the developing egg. Mech. Dev. 1991, 34:101-111.
35. Kesper D., Stute C., Buttgereit D., Kreisköther N., Vishnu S., Fischbach K., Renkawitz-Pohl R. Myoblast fusion in Drosophila melanogaster is mediated through a fusion-restricted myogenic-adhesive structure (FuRMAS). Dev. Dyn. 2007, 236:404-415.
36. Kim S., Shilagardi K., Zhang S., Hong S.N., Sens K.L., Bo J., Gonzalez G.A., Chen E.H. A critical function for the actin cytoskeleton in targeted exocytosis of prefusion vesicles during myoblast fusion. Dev. Cell 2007, 12:571-586.
37. Kimble M., Dettman R.W., Raff E.C. The beta 3-tubulin gene of Drosophila melanogaster is essential for viability and fertility. Genetics 1990, 126:991-1005.
38. Kimble M., Incardona J.P., Raff E.C. A variant beta-tubulin isoform of Drosophila melanogaster (beta 3) is expressed primarily in tissues of mesodermal origin in embryos and pupae, and is utilized in populations of transient microtubules. Dev. Biol. 1989, 131:415-429.
39. Klapper R., Heuser S., Strasser T., Janning W. A new approach reveals syncytia within the visceral musculature of Drosophila melanogaster. Development 2001, 128:2517-2524.
40. Klapper R., Stute C., Schomaker O., Strasser T., Janning W., Renkawitz-Pohl R., Holz A. The formation of syncytia within the visceral musculature of the Drosophila midgut is dependent on duf, sns and mbc. Mech. Dev. 2002, 110:85-96.
41. Kopp P., Lammers R., Aepfelbacher M., Woehlke G., Rudel T., Machuy N., Steffen W., Linder S. The kinesin KIF1C and microtubule plus ends regulate podosome dynamics in macrophages. Mol. Biol. Cell 2006, 17:2811-2823.
42. Kremser T., Gajewski K., Schulz R., Renkawitz-Pohl R. Tinman regulates the transcription of the beta3 tubulin gene (betaTub60D) in the dorsal vessel of Drosophila. Dev. Biol. 1999, 216:327-339.
43. Kremser T., Hasenpusch-Theil K., Wagner E., Buttgereit D., Renkawitz-Pohl R. Expression of the beta3 tubulin gene (beta Tub60D) in the visceral mesoderm of Drosophila is dependent on a complex enhancer that binds Tinman and UBX. Mol. Gen. Genet. 1999, 262:643-658.
44. Kusch T., Reuter R. Functions for Drosophila brachyenteron and forkhead in mesoderm specification and cell signalling. Development 1999, 126:3991-4003.
45. Leiss D., Hinz U., Gasch A., Mertz R., Renkawitz-Pohl R. Beta 3 tubulin expression characterizes the differentiating mesodermal germ layer during Drosophila embryogenesis. Development 1988, 104:525-531.
46. Leiss, D., 1989. Distinkte stadien-und gewebespezifische Verteilung der β-Tubuline von Drosophila melanogaster. Dissertation. Johann Wolfgang Goethe-Universität Frankfurt.
47. Lilly B., Galewsky S., Firulli A.B., Schulz R.A., Olson E.N. D-MEF2: a MADS box transcription factor expressed in differentiating mesoderm and muscle cell lineages during Drosophila embryogenesis. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:5662-5666.
48. Linder S. The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol. 2007, 17:107-117.
49. Linder S., Hüfner K., Wintergerst U., Aepfelbacher M. Microtubule-dependent formation of podosomal adhesion structures in primary human macrophages. J. Cell Sci. 2000, 113(Pt. 23):4165-4176.
50. Massarwa R., Carmon S., Shilo B.Z., Schejter E.D. WIP/WASp-based actin-polymerization machinery is essential for myoblast fusion in Drosophila. Dev. Cell 2007, 12:557-569.
51. Michiels F., Falkenburg D., Müller A.M., Hinz U., Otto U., Bellmann R., Glätzer K.H., Brand R., Bialojan S., Renkawitz-Pohl R. Testis-specific beta 2 tubulins are identical in Drosophila melanogaster and D. hydei but differ from the ubiquitous beta 1 tubulin. Chromosoma 1987, 95:387-395.
52. Mukherjee P., Gildor B., Shilo B.Z., VijayRaghavan K., Schejter E.D. The actin nucleator WASp is required for myoblast fusion during adult Drosophila myogenesis. Development 2011, 138:2347-2357.
53. Ng D.C., Gebski B.L., Grounds M.D., Bogoyevitch M.A. Myoseverin disrupts sarcomeric organization in myocytes: an effect independent of microtubule assembly inhibition. Cell Motil. Cytoskeleton 2008, 65:40-58.
54. Nguyen H.T., Bodmer R., Abmayr S.M., McDermott J.C., Spoerel N.A. D-mef2: a Drosophila mesoderm-specific MADS box-containing gene with a biphasic expression profile during embryogenesis. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:7520-7524.
55. Nogales E., Wolf S.G., Downing K.H. Structure of the alpha beta tubulin dimer by electron crystallography. Nature 1998, 391:199-203.
56. Nose A., Isshiki T., Takeichi M. Regional specification of muscle progenitors in Drosophila: the role of the msh homeobox gene. Development 1998, 125:215-223.
57. Önel S.F., Renkawitz-Pohl R. FuRMAS: triggering myoblast fusion in Drosophila. Dev. Dyn. 2009, 238:1513-1525.
58. Parrish J.Z., Kim M.D., Jan L.Y., Jan Y.N. Genome-wide analyses identify transcription factors required for proper morphogenesis of Drosophila sensory neuron dendrites. Genes Dev. 2006, 20:820-835.
59. Patel N.H., Snow P.M., Goodman C.S. Characterization and cloning of fasciclin III: a glycoprotein expressed on a subset of neurons and axon pathways in Drosophila. Cell 1987, 48:975-988.
60. Pizon V., Gerbal F., Diaz C.C., Karsenti E. Microtubule-dependent transport and organization of sarcomeric myosin during skeletal muscle differentiation. EMBO J. 2005, 24:3781-3792.
61. Pizon V., Iakovenko A., Van Der Ven P.F., Kelly R., Fatu C., Fürst D.O., Karsenti E., Gautel M. Transient association of titin and myosin with microtubules in nascent myofibrils directed by the MURF2 RING-finger protein. J. Cell Sci. 2002, 115:4469-4482.
62. Raff E.C., Fuller M.T., Kaufman T.C., Kemphues K.J., Rudolph J.E., Raff R.A. Regulation of tubulin gene expression during embryogenesis in Drosophila melanogaster. Cell 1982, 28:33-40.
63. Rathke C., Barckmann B., Burkhard S., Jayaramaiah-Raja S., Roote J., Renkawitz-Pohl R. Distinct functions of Mst77F and protamines in nuclear shaping and chromatin condensation during Drosophila spermiogenesis. Eur. J. Cell Biol. 2010, 89:326-338.
64. Reedy M.C., Beall C. Ultrastructure of developing flight muscle in Drosophila. I. Assembly of myofibrils. Dev. Biol. 1993, 160:443-465.
65. Reedy M.C., Beall C. Ultrastructure of developing flight muscle in Drosophila. II. Formation of the myotendon junction. Dev. Biol. 1993, 160:466-479.
66. Reuter R. The gene serpent has homeotic properties and specifies endoderm versus ectoderm within the Drosophila gut. Development 1994, 120:1123-1135.
67. Reuter R., Grunewald B., Leptin M. A role for the mesoderm in endodermal migration and morphogenesis in Drosophila. Development 1993, 119:1135-1145.
68. Reuter R., Scott M.P. Expression and function of the homoeotic genes Antennapedia and Sex combs reduced in the embryonic midgut of Drosophila. Development 1990, 109:289-303.
69. Richardson B.E., Beckett K., Nowak S.J., Baylies M.K. SCAR/WAVE and Arp2/3 are crucial for cytoskeletal remodeling at the site of myoblast fusion. Development 2007, 134:4357-4367.
70. Rudolph J.E., Kimble M., Hoyle H.D., Subler M.A., Raff E.C. Three Drosophila beta-tubulin sequences: a developmentally regulated isoform (beta 3), the testis-specific isoform (beta 2), and an assembly-defective mutation of the testis-specific isoform (B2t8) reveal both an ancient divergence in metazoan isotypes and structural constraints for beta-tubulin function. Mol. Cell. Biol. 1987, 7:2231-2242.
71. San Martin B., Bate M. Hindgut visceral mesoderm requires an ectodermal template for normal development in Drosophila. Development 2001, 128:233-242.
72. Schröter R.H., Buttgereit D., Beck L., Holz A., Renkawitz-Pohl R. Blown fuse regulates stretching and outgrowth but not myoblast fusion of the circular visceral muscles in Drosophila. Differentiation 2006, 74:608-621.
73. Schäfer G., Weber S., Holz A., Bogdan S., Schumacher S., Müller A., Renkawitz-Pohl R., Onel S. The Wiskott-Aldrich syndrome protein (WASP) is essential for myoblast fusion in Drosophila. Dev. Biol. 2007, 304:664-674.
74. Sherwood N.T., Sun Q., Xue M., Zhang B., Zinn K. Drosophila spastin regulates synaptic microtubule networks and is required for normal motor function. PLoS Biol. 2004, 2:e429.
75. Stramer B., Moreira S., Millard T., Evans I., Huang C.Y., Sabet O., Milner M., Dunn G., Martin P., Wood W. Clasp-mediated microtubule bundling regulates persistent motility and contact repulsion in Drosophila macrophages in vivo. J. Cell Biol. 2010, 189:681-689.
76. Stute C., Schimmelpfeng K., Renkawitz-Pohl R., Palmer R., Holz A. Myoblast determination in the somatic and visceral mesoderm depends on Notch signalling as well as on milliways(mili(Alk)) as receptor for Jeb signalling. Development 2004, 131:743-754.
77. Tassin A.M., Paintrand M., Berger E.G., Bornens M. The Golgi apparatus remains associated with microtubule organizing centers during myogenesis. J. Cell Biol. 1985, 101:630-638.
78. Tautz D., Pfeifle C. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 1989, 98:81-85.
79. Tepass U., Hartenstein V. Epithelium formation in the Drosophila midgut depends on the interaction of endoderm and mesoderm. Development 1994, 120:579-590.
80. Terman J.R., Kolodkin A.L. Nervy links protein kinase a to plexin-mediated semaphorin repulsion. Science 2004, 303:1204-1207.
81. Toyama Y., Forry-Schaudies S., Hoffman B., Holtzer H. Effects of taxol and Colcemid on myofibrillogenesis. Proc. Natl. Acad. Sci. U. S. A. 1982, 79:6556-6560.
82. Warren R.H. Microtubular organization in elongating myogenic cells. J. Cell Biol. 1974, 63:550-566.
83. Wolfstetter G., Shirinian M., Stute C., Grabbe C., Hummel T., Baumgartner S., Palmer R.H., Holz A. Fusion of circular and longitudinal muscles in Drosophila is independent of the endoderm but further visceral muscle differentiation requires a close contact between mesoderm and endoderm. Mech. Dev. 2009, 126:721-736.
84. Zaffran S., Frasch M. The beta 3 tubulin gene is a direct target of bagpipe and biniou in the visceral mesoderm of Drosophila. Mech. Dev. 2002, 114:85-93.
85. Zaffran S., Küchler A., Lee H.H., Frasch M. biniou (FoxF), a central component in a regulatory network controlling visceral mesoderm development and midgut morphogenesis in Drosophila. Genes Dev. 2001, 15:2900-2915.
86. Zhang T., Zaal K.J., Sheridan J., Mehta A., Gundersen G.G., Ralston E. Microtubule plus-end binding protein EB1 is necessary for muscle cell differentiation, elongation and fusion. J. Cell Sci. 2009, 122:1401-1409.