Diversification of Muscle Types in Drosophila. Upstream and Downstream of Identity Genes

Current Topics in Developmental Biology

Volumn 98, Issue , 2012, Pages 277-301

  de Joussineau, Cyrille ^a   Bataillé, Laetitia ^a,b   Jagla, Teresa ^a   Jagla, Krzysztof ^a  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

Author keywords

Cell fate specification; Development; Diversification; Drosophila embryo; Identity factors; Mesoderm; Somatic muscle

Indexed keywords

EID: 84856457356     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-386499-4.00011-2     Document Type: Chapter

References (116)

1. Artero R., Furlong E.E., Beckett K., Scott M.P., Baylies M. Notch and Ras signaling pathway effector genes expressed in fusion competent and founder cells during Drosophila myogenesis. Development 2003, 130:6257-6272.
2. Azpiazu N., Lawrence P.A., Vincent J.P., Frasch M. Segmentation and specification of the Drosophila mesoderm. Genes Dev. 1996, 10:3183-3194.
3. Baker R., Schubiger G. Ectoderm induces muscle-specific gene expression in Drosophila embryos. Development 1995, 121:1387-1398.
4. Bataillé L., Delon I., Da Ponte J.P., Brown N.H., Jagla K. Downstream of identity genes: Muscle-type-specific regulation of the fusion process. Dev. Cell 2010, 19:317-328.
5. Bate M., Broadie K. Wiring by fly: The neuromuscular system of the Drosophila embryo. Neuron 1995, 15:513-525.
6. Bate M., Rushton E., Currie D.A. Cells with persistent twist expression are the embryonic precursors of adult muscles in Drosophila. Development 1991, 113:79-89.
7. Baylies M.K., Bate M. Twist: A myogenic switch in Drosophila. Science 1996, 272:1481-1484.
8. Baylies M.K., Martinez Arias A., Bate M. Wingless is required for the formation of a subset of muscle founder cells during Drosophila embryogenesis. Development 1995, 121:3829-3837.
9. Baylies M.K., Bate M., Ruiz Gomez M. Myogenesis: A view from Drosophila. Cell 1998, 93:921-927.
10. Beckett K., Baylies M.K. The development of the Drosophila larval body wall muscles. Int. Rev. Neurobiol. 2006, 75:55-70.
11. Beckett K., Baylies M.K. 3D analysis of founder cell and fusion competent myoblast arrangements outlines a new model of myoblast fusion. Dev. Biol. 2007, 309:113-125.
12. Borkowski O.M., Brown N.H., Bate M. Anterior-posterior subdivision and the diversification of the mesoderm in Drosophila. Development 1995, 121:4183-4193.
13. Bour B.A., Chakravarti M., West J.M., Abmayr S.M. Drosophila SNS, a member of the immunoglobulin superfamily that is essential for myoblast fusion. Genes Dev. 2000, 14:1498-1511.
14. Bourgouin C., Lundgren S.E., Thomas J.B. Apterous is a Drosophila LIM domain gene required for the development of a subset of embryonic muscles. Neuron 1992, 9:549-561.
15. Brennan K., Baylies M., Arias A.M. Repression by Notch is required before Wingless signalling during muscle progenitor cell development in Drosophila. Curr. Biol. 1999, 9:707-710.
16. Buff E., Carmena A., Gisselbrecht S., Jimenez F., Michelson A.M. Signalling by the Drosophila epidermal growth factor receptor is required for the specification and diversification of embryonic muscle progenitors. Development 1998, 125:2075-2086.
17. Callahan C.A., Bonkovsky J.L., Scully A.L., Thomas J.B. Derailed is required for muscle attachment site selection in Drosophila. Development 1996, 122:2761-2767.
18. Capovilla M., Kambris Z., Botas J. Direct regulation of the muscle-identity gene apterous by a Hox protein in the somatic mesoderm. Development 2001, 128:1221-1230.
19. Carmena A., Bate M., Jimenez F. Lethal of scute, a proneural gene, participates in the specification of muscle progenitors during Drosophila embryogenesis. Genes Dev. 1995, 9:2373-2383.
20. Carmena A., Gisselbrecht S., Harrison J., Jimenez F., Michelson A.M. Combinatorial signaling codes for the progressive determination of cell fates in the Drosophila embryonic mesoderm. Genes Dev. 1998, 12:3910-3922.
21. Carmena A., Buff E., Halfon M.S., Gisselbrecht S., Jimenez F., Baylies M.K., Michelson A.M. Reciprocal regulatory interactions between the Notch and Ras signaling pathways in the Drosophila embryonic mesoderm. Dev. Biol. 2002, 244:226-242.
22. Chanana B., Steigemann P., Jackle H., Vorbruggen G. Reception of Slit requires only the chondroitin-sulphate-modified extracellular domain of Syndecan at the target cell surface. Proc. Natl. Acad. Sci. USA 2009, 106:11984-11988.
23. Chiba A., Hing H., Cash S., Keshishian H. Growth cone choices of Drosophila motoneurons in response to muscle fiber mismatch. J. Neurosci. 1993, 13:714-732.
24. Chiba A., Snow P., Keshishian H., Hotta Y. Fasciclin III as a synaptic target recognition molecule in Drosophila. Nature 1995, 374:166-168.
25. Ciglar L., Furlong E.E. Conservation and divergence in developmental networks: A view from Drosophila myogenesis. Curr. Opin. Cell Biol. 2009, 21:754-760.
26. Cox V.T., Baylies M.K. Specification of individual Slouch muscle progenitors in Drosophila requires sequential Wingless signaling. Development 2005, 132:713-724.
27. Cox V.T., Beckett K., Baylies M.K. Delivery of wingless to the ventral mesoderm by the developing central nervous system ensures proper patterning of individual slouch-positive muscle progenitors. Dev. Biol. 2005, 287:403-415.
28. Crozatier M., Vincent A. Requirement for the Drosophila COE transcription factor Collier in formation of an embryonic muscle: Transcriptional response to Notch signalling. Development 1999, 126:1495-1504.
29. Deal R.B., Henikoff S. The INTACT method for cell type-specific gene expression and chromatin profiling in Arabidopsis thaliana. Nat. Protoc. 2011, 6:56-68.
30. Deng H., Bell J.B., Simmonds A.J. Vestigial is required during late-stage muscle differentiation in Drosophila melanogaster embryos. Mol. Biol. Cell 2010, 21:3304-3316.
31. Dohrmann C., Azpiazu N., Frasch M. A new Drosophila homeo box gene is expressed in mesodermal precursor cells of distinct muscles during embryogenesis. Genes Dev. 1990, 4:2098-2111.
32. Duan H., Skeath J.B., Nguyen H.T. Drosophila Lame duck, a novel member of the Gli superfamily, acts as a key regulator of myogenesis by controlling fusion-competent myoblast development. Development 2001, 128:4489-4500.
33. Duan H., Zhang C., Chen J., Sink H., Frei E., Noll M. A key role of Pox meso in somatic myogenesis of Drosophila. Development 2007, 134:3985-3997.
34. Elgar S.J., Han J., Taylor M.V. mef2 activity levels differentially affect gene expression during Drosophila muscle development. Proc. Natl. Acad. Sci. USA 2008, 105:918-923.
35. Enriquez J., Boukhatmi H., Dubois L., Philippakis A.A., Bulyk M.L., Michelson A.M., Crozatier M., Vincent A. Multi-step control of muscle diversity by Hox proteins in the Drosophila embryo. Development 2010, 137:457-466.
36. Estrada B., Choe S.E., Gisselbrecht S.S., Michaud S., Raj L., Busser B.W., Halfon M.S., Church G.M., Michelson A.M. An integrated strategy for analyzing the unique developmental programs of different myoblast subtypes. PLoS Genet. 2006, 2:e16.
37. Estrada B., Gisselbrecht S.S., Michelson A.M. The transmembrane protein Perdido interacts with Grip and integrins to mediate myotube projection and attachment in the Drosophila embryo. Development 2007, 134:4469-4478.
38. Figeac N., Jagla T., Aradhya R., Da Ponte J.P., Jagla K. Drosophila adult muscle precursors form a network of interconnected cells and are specified by the rhomboid-triggered EGF pathway. Development 2010, 137:1965-1973.
39. Frasch M. Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo. Nature 1995, 374:464-467.
40. Frasch M. Controls in patterning and diversification of somatic muscles during Drosophila embryogenesis. Curr. Opin. Genet. Dev. 1999, 9:522-529.
41. Furlong E.E. Molecular biology: A fly in the face of genomics. Nature 2011, 471:458-459.
42. Gilsohn E., Volk T. Slowdown promotes muscle integrity by modulating integrin-mediated adhesion at the myotendinous junction. Development 2010, 137:785-794.
43. Gryzik T., Muller H.A. FGF8-like1 and FGF8-like2 encode putative ligands of the FGF receptor Htl and are required for mesoderm migration in the Drosophila gastrula. Curr. Biol. 2004, 14:659-667.
44. Guerin C.M., Kramer S.G. Cytoskeletal remodeling during myotube assembly and guidance: Coordinating the actin and microtubule networks. Commun. Integr. Biol. 2009, 2:452-457.
45. Halpern M.E., Chiba A., Johansen J., Keshishian H. Growth cone behavior underlying the development of stereotypic synaptic connections in Drosophila embryos. J. Neurosci. 1991, 11:3227-3238.
46. Heiman M., Schaefer A., Gong S., Peterson J.D., Day M., Ramsey K.E., Suarez-Farinas M., Schwarz C., Stephan D.A., Surmeier D.J., Greengard P., Heintz N. A translational profiling approach for the molecular characterization of CNS cell types. Cell 2008, 135:738-748.
47. Hooper J.E. Homeotic gene function in the muscles of Drosophila larvae. EMBO J. 1986, 5:2321-2329.
48. Inaki M., Shinza-Kameda M., Ismat A., Frasch M., Nose A. Drosophila Tey represses transcription of the repulsive cue Toll and generates neuromuscular target specificity. Development 2010, 137:2139-2146.
49. Jagla T., Bellard F., Lutz Y., Dretzen G., Bellard M., Jagla K. Ladybird determines cell fate decisions during diversification of Drosophila somatic muscles. Development 1998, 125:3699-3708.
50. Jagla T., Bellard F., Vonesch J.L., Bellard M., Dastugue B., Jagla K. Plasticity within the lateral somatic mesoderm of Drosophila embryos. Int. J. Dev. Biol. 1999, 43:571-573.
51. Jagla K., Bellard M., Frasch M. A cluster of Drosophila homeobox genes involved in mesoderm differentiation programs. Bioessays 2001, 23:125-133.
52. Jagla T., Bidet Y., Da Ponte J.P., Dastugue B., Jagla K. Cross-repressive interactions of identity genes are essential for proper specification of cardiac and muscular fates in Drosophila. Development 2002, 129:1037-1047.
53. Junion G., Jagla T., Duplant S., Tapin R., Da Ponte J.P., Jagla K. Mapping Dmef2-binding regulatory modules by using a ChIP-enriched in silico targets approach. Proc. Natl. Acad. Sci. USA 2005, 102:18479-18484.
54. Junion G., Bataille L., Jagla T., Da Ponte J.P., Tapin R., Jagla K. Genome-wide view of cell fate specification: Ladybird acts at multiple levels during diversification of muscle and heart precursors. Genes Dev. 2007, 21:3163-3180.
55. Kadam S., McMahon A., Tzou P., Stathopoulos A. FGF ligands in Drosophila have distinct activities required to support cell migration and differentiation. Development 2009, 136:739-747.
56. Keller C.A., Grill M.A., Abmayr S.M. A role for nautilus in the differentiation of muscle precursors. Dev. Biol. 1998, 202:157-171.
57. Kesper D.A., Stute C., Buttgereit D., Kreiskother N., Vishnu S., Fischbach K.F., Renkawitz-Pohl R. Myoblast fusion in Drosophila melanogaster is mediated through a fusion-restricted myogenic-adhesive structure (FuRMAS). Dev. Dyn. 2007, 236:404-415.
58. Klingseisen A., Clark I.B., Gryzik T., Muller H.A. Differential and overlapping functions of two closely related Drosophila FGF8-like growth factors in mesoderm development. Development 2009, 136:2393-2402.
59. Knirr S., Azpiazu N., Frasch M. The role of the NK-homeobox gene slouch (S59) in somatic muscle patterning. Development 1999, 126:4525-4535.
60. Kohsaka H., Nose A. Target recognition at the tips of postsynaptic filopodia: Accumulation and function of Capricious. Development 2009, 136:1127-1135.
61. Kolodziej P.A., Timpe L.C., Mitchell K.J., Fried S.R., Goodman C.S., Jan L.Y., Jan Y.N. Frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell 1996, 87:197-204.
62. Kramer S.G., Kidd T., Simpson J.H., Goodman C.S. Switching repulsion to attraction: Changing responses to slit during transition in mesoderm migration. Science 2001, 292:737-740.
63. Kraut R., Campos-Ortega J.A. Inscuteable, a neural precursor gene of Drosophila, encodes a candidate for a cytoskeleton adaptor protein. Dev. Biol. 1996, 174:65-81.
64. Landgraf M., Thor S. Development of Drosophila motoneurons: Specification and morphology. Semin. Cell Dev. Biol. 2006, 17:3-11.
65. Landgraf M., Baylies M., Bate M. Muscle founder cells regulate defasciculation and targeting of motor axons in the Drosophila embryo. Curr. Biol. 1999, 9:589-592.
66. Lawrence P.A., Bodmer R., Vincent J.P. Segmental patterning of heart precursors in Drosophila. Development 1995, 121:4303-4308.
67. Leptin M. Twist and snail as positive and negative regulators during Drosophila mesoderm development. Genes Dev. 1991, 5:1568-1576.
68. Levine M. Paused RNA polymerase II as a developmental checkpoint. Cell 2011, 145:502-511.
69. Lopez A.J., Hogness D.S. Immunochemical dissection of the Ultrabithorax homeoprotein family in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 1991, 88:9924-9928.
70. Lord P.C., Lin M.H., Hales K.H., Storti R.V. Normal expression and the effects of ectopic expression of the Drosophila muscle segment homeobox (msh) gene suggest a role in differentiation and patterning of embryonic muscles. Dev. Biol. 1995, 171:627-640.
71. Maggert K., Levine M., Frasch M. The somatic-visceral subdivision of the embryonic mesoderm is initiated by dorsal gradient thresholds in Drosophila. Development 1995, 121:2107-2116.
72. Maqbool T., Jagla K. Genetic control of muscle development: Learning from Drosophila. J. Muscle Res. Cell Motil. 2007, 28:397-407.
73. McGinnis W., Krumlauf R. Homeobox genes and axial patterning. Cell 1992, 68:283-302.
74. Michelson A.M. Muscle pattern diversification in Drosophila is determined by the autonomous function of homeotic genes in the embryonic mesoderm. Development 1994, 120:755-768.
75. Michelson A.M., Gisselbrecht S., Zhou Y., Baek K.H., Buff E.M. Dual functions of the heartless fibroblast growth factor receptor in development of the Drosophila embryonic mesoderm. Dev. Genet. 1998, 22:212-229.
76. Miller M.R., Robinson K.J., Cleary M.D., Doe C.Q. TU-tagging: Cell type-specific RNA isolation from intact complex tissues. Nat. Methods 2009, 6:439-441.
77. Muller D., Jagla T., Bodart L.M., Jahrling N., Dodt H.U., Jagla K., Frasch M. Regulation and functions of the lms homeobox gene during development of embryonic lateral transverse muscles and direct flight muscles in Drosophila. PLoS One 2010, 5:e14323.
78. Nose A., Van Vactor D., Auld V., Goodman C.S. Development of neuromuscular specificity in Drosophila. Cold Spring Harb. Symp. Quant. Biol. 1992, 57:441-449.
79. Nose A., Takeichi M., Goodman C.S. Ectopic expression of connectin reveals a repulsive function during growth cone guidance and synapse formation. Neuron 1994, 13:525-539.
80. 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.
81. 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.
82. Philippakis A.A., Busser B.W., Gisselbrecht S.S., He F.S., Estrada B., Michelson A.M., Bulyk M.L. Expression-guided in silico evaluation of candidate cis regulatory codes for Drosophila muscle founder cells. PLoS Comput. Biol. 2006, 2:e53.
83. Ranganayakulu G., Schulz R.A., Olson E.N. Wingless signaling induces nautilus expression in the ventral mesoderm of the Drosophila embryo. Dev. Biol. 1996, 176:143-148.
84. Reed H.C., Hoare T., Thomsen S., Weaver T.A., White R.A., Akam M., Alonso C.R. Alternative splicing modulates Ubx protein function in Drosophila melanogaster. Genetics 2010, 184:745-758.
85. Riechmann V., Irion U., Wilson R., Grosskortenhaus R., Leptin M. Control of cell fates and segmentation in the Drosophila mesoderm. Development 1997, 124:2915-2922.
86. Ritzenthaler S., Chiba A. Multiple personalities: Synaptic target cells as introverts and extroverts. Dev. Growth Differ. 2001, 43:503-508.
87. Ritzenthaler S., Suzuki E., Chiba A. Postsynaptic filopodia in muscle cells interact with innervating motoneuron axons. Nat. Neurosci. 2000, 3:1012-1017.
88. Ruiz Gomez M., Bate M. Segregation of myogenic lineages in Drosophila requires numb. Development 1997, 124:4857-4866.
89. Ruiz-Gomez M., Romani S., Hartmann C., Jackle H., Bate M. Specific muscle identities are regulated by Kruppel during Drosophila embryogenesis. Development 1997, 124:3407-3414.
90. Ruiz-Gomez M., Coutts N., Price A., Taylor M.V., Bate M. Drosophila dumbfounded: A myoblast attractant essential for fusion. Cell 2000, 102:189-198.
91. Sandmann T., Jakobsen J.S., Furlong E.E. ChIP-on-chip protocol for genome-wide analysis of transcription factor binding in Drosophila melanogaster embryos. Nat. Protoc. 2006, 1:2839-2855.
92. Sandmann T., Girardot C., Brehme M., Tongprasit W., Stolc V., Furlong E.E. A core transcriptional network for early mesoderm development in Drosophila melanogaster. Genes Dev. 2007, 21:436-449.
93. Schejter E.D., Baylies M.K. Born to run: Creating the muscle fiber. Curr. Opin. Cell Biol. 2010, 22:566-574.
94. Schnorrer F., Dickson B.J. Muscle building: Mechanisms of myotube guidance and attachment site selection. Dev. Cell 2004, 7:9-20.
95. Schnorrer F., Kalchhauser I., Dickson B.J. The transmembrane protein Kon-tiki couples to Dgrip to mediate myotube targeting in Drosophila. Dev. Cell 2007, 12:751-766.
96. Schnorrer F., Schonbauer C., Langer C.C., Dietzl G., Novatchkova M., Schernhuber K., Fellner M., Azaryan A., Radolf M., Stark A., Keleman K., Dickson B.J. Systematic genetic analysis of muscle morphogenesis and function in Drosophila. Nature 2011, 464:287-291.
97. Schulz R.A., Gajewski K. Ventral neuroblasts and the heartless FGF receptor are required for muscle founder cell specification in Drosophila. Oncogene 1999, 18:6818-6823.
98. Schweitzer R., Zelzer E., Volk T. Connecting muscles to tendons: Tendons and musculoskeletal development in flies and vertebrates. Development 2010, 137:2807-2817.
99. Shilo B.Z., Schejter E.D., Segal D., Ginsberg D.S., Glazer L. The Drosophila epidermal growth factor receptor homolog: Structure, evolution, and possible functions. Symp. Fundam. Cancer Res. 1986, 39:87-97.
100. Shishido E., Higashijima S., Emori Y., Saigo K. Two FGF-receptor homologues of Drosophila: One is expressed in mesodermal primordium in early embryos. Development 1993, 117:751-761.
101. Shishido E., Ono N., Kojima T., Saigo K. Requirements of DFR1/Heartless, a mesoderm-specific Drosophila FGF-receptor, for the formation of heart, visceral and somatic muscles, and ensheathing of longitudinal axon tracts in CNS. Development 1997, 124:2119-2128.
102. Sparrow J.C., Schock F. The initial steps of myofibril assembly: Integrins pave the way. Nat. Rev. Mol. Cell Biol. 2009, 10:293-298.
103. Staehling-Hampton K., Hoffmann F.M., Baylies M.K., Rushton E., Bate M. dpp induces mesodermal gene expression in Drosophila. Nature 1994, 372:783-786.
104. Stathopoulos A., Tam B., Ronshaugen M., Frasch M., Levine M. pyramus and thisbe: FGF genes that pattern the mesoderm of Drosophila embryos. Genes Dev. 2004, 18:687-699.
105. Strunkelnberg M., Bonengel B., Moda L.M., Hertenstein A., de Couet H.G., Ramos R.G., Fischbach K.F. rst and its paralogue kirre act redundantly during embryonic muscle development in Drosophila. Development 2001, 128:4229-4239.
106. Subramanian A., Wayburn B., Bunch T., Volk T. Thrombospondin-mediated adhesion is essential for the formation of the myotendinous junction in Drosophila. Development 2007, 134:1269-1278.
107. Tixier V., Bataille L., Jagla K. Diversification of muscle types: Recent insights from Drosophila. Exp. Cell Res. 2010, 316:3019-3027.
108. van der Geer P., Hunter T., Lindberg R.A. Receptor protein-tyrosine kinases and their signal transduction pathways. Annu. Rev. Cell Biol. 1994, 10:251-337.
109. Volk T. A new member of the spectrin superfamily may participate in the formation of embryonic muscle attachments in Drosophila. Development 1992, 116:721-730.
110. Volk T. Singling out Drosophila tendon cells: A dialogue between two distinct cell types. Trends Genet. 1999, 15:448-453.
111. Vorbruggen G., Constien R., Zilian O., Wimmer E.A., Dowe G., Taubert H., Noll M., Jackle H. Embryonic expression and characterization of a Ptx1 homolog in Drosophila. Mech. Dev. 1997, 68:139-147.
112. Wayburn B., Volk T. LRT, a tendon-specific leucine-rich repeat protein, promotes muscle-tendon targeting through its interaction with Robo. Development 2009, 136:3607-3615.
113. Winberg M.L., Mitchell K.J., Goodman C.S. Genetic analysis of the mechanisms controlling target selection: Complementary and combinatorial functions of netrins, semaphorins, and IgCAMs. Cell 1998, 93:581-591.
114. Yarnitzky T., Min L., Volk T. The Drosophila neuregulin homolog Vein mediates inductive interactions between myotubes and their epidermal attachment cells. Genes Dev. 1997, 11:2691-2700.
115. Yarnitzky T., Min L., Volk T. An interplay between two EGF-receptor ligands, Vein and Spitz, is required for the formation of a subset of muscle precursors in Drosophila. Mech. Dev. 1998, 79:73-82.
116. Ypsilanti A.R., Zagar Y., Chedotal A. Moving away from the midline: New developments for Slit and Robo. Development 2010, 137:1939-1952.