Drosophila araucan and caupolican integrate intrinsic and signalling inputs for the acquisition by muscle progenitors of the lateral transverse fate

PLoS Genetics

Volumn 7, Issue 7, 2011, Pages

  Carrasco Rando, Marta ^a   Tutor, Antonio S ^a   Prieto Sánchez, Silvia ^a   González Pérez, Esther ^a   Barrios, Natalia ^a   Letizia, Annalisa ^b   Martín, Paloma ^a   Campuzano, Sonsoles ^a   Ruiz Gómez, Mar ^a  

^a CSIC   (Spain)

^b INSTITUT DE BIOLOGIA MOLECULAR DE BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ARAUCAN; BETA GALACTOSIDASE; CAUPOLICAN; FIREFLY LUCIFERASE; HOMEODOMAIN PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; RAS PROTEIN; UNCLASSIFIED DRUG; ARAUCAN PROTEIN, DROSOPHILA; CAUP PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; NUCLEAR PROTEIN; SLOU PROTEIN, DROSOPHILA; TRANSCRIPTION FACTOR; VESTIGIAL PROTEIN, DROSOPHILA;

ARAUCAN GENE; ARTICLE; CAUPOLICAN GENE; CELL FATE; CONTROLLED STUDY; DROSOPHILA; ECTODERM; EMBRYO; EMBRYO PATTERN FORMATION; ENZYME ACTIVITY; GENE; GENE EXPRESSION; GENE REPRESSION; GENETIC IDENTIFICATION; HOMEOBOX; IN SITU HYBRIDIZATION; IN VITRO STUDY; IN VIVO STUDY; INSECT CELL; INTRACELLULAR SIGNALING; LATERAL TRANSVERSE MUSCLE; MESODERM; MUSCLE; MUSCLE DEVELOPMENT; NONHUMAN; PHENOTYPE; PROMOTER REGION; REGULATORY SEQUENCE; SLOUCH GENE; STEM CELL; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; TRANSGENIC ORGANISM; VESTIGIAL GENE; WILD TYPE; ANIMAL; ANIMAL EMBRYO; CELL LINE; CONFOCAL MICROSCOPY; CYTOLOGY; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PRENATAL DEVELOPMENT; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; CELL LINE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MICROSCOPY, CONFOCAL; MITOGEN-ACTIVATED PROTEIN KINASES; MUSCLE DEVELOPMENT; MUSCLES; NUCLEAR PROTEINS; RAS PROTEINS; SEQUENCE HOMOLOGY, NUCLEIC ACID; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 79960962033     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002186     Document Type: Article

References (65)

1. Bate M, (1993) The mesoderm and its derivatives; In: Martinez-Arias MBaA, editors. Cold Spring Harbor, New York CHS Laboratory Press pp. 1013-1090.
2. Baylies MK, Bate M, Ruiz Gomez M, (1998) Myogenesis: a view from Drosophila. Cell 93: 921-927.
3. Carmena A, Bate M, Jimenez F, (1995) Lethal of scute, a proneural gene, participates in the specification of muscle progenitors during Drosophila embryogenesis. Genes Dev 9: 2373-2383.
4. Carmena A, Gisselbrecht S, Harrison J, Jimenez F, Michelson AM, (1998) Combinatorial signaling codes for the progressive determination of cell fates in the Drosophila embryonic mesoderm. Genes Dev 12: 3910-3922.
5. Carmena A, Murugasu-Oei B, Menon D, Jimenez F, Chia W, (1998) Inscuteable and numb mediate asymmetric muscle progenitor cell divisions during Drosophila myogenesis. Genes Dev 12: 304-315.
6. Ruiz-Gómez M, Bate M, (1997) Segregation of myogenic lineages in Drosophila requires numb. Development 124: 4857-4866.
7. Duan H, Skeath JB, Nguyen HT, (2001) Drosophila Lame duck, a novel member of the Gli superfamily, acts as a key regulator of myogenesis by controlling fusion-competent myoblast development. Development 128: 4489-4500.
8. Furlong EE, Andersen EC, Null B, White KP, Scott MP, (2001) Patterns of gene expression during Drosophila mesoderm development. Science 293: 1629-1633.
9. Ruiz-Gómez M, Coutts N, Suster ML, Landgraf M, Bate M, (2002) myoblasts incompetent encodes a zinc finger transcription factor required to specify fusion-competent myoblasts in Drosophila. Development 129: 133-141.
10. Baylies MK, Michelson AM, (2001) Invertebrate myogenesis: looking back to the future of muscle development. Curr Opin Genet Dev 11: 431-439.
11. Tixier V, Bataille L, Jagla K, (2010) Diversification of muscle types: recent insights from Drosophila. Exp Cell Res 316: 3019-3027.
12. Rushton E, Drysdale R, Abmayr SM, Michelson AM, Bate M, (1995) Mutations in a novel gene, myoblast city, provide evidence in support of the founder cell hypothesis for Drosophila muscle development. Development 121: 1979-1988.
13. Bourgouin C, Lundgren SE, Thomas JB, (1992) Apterous is a Drosophila LIM domain gene required for the development of a subset of embryonic muscles. Neuron 9: 549-561.
14. Duan H, Zhang C, Chen J, Sink H, Frei E, et al. (2007) A key role of Pox meso in somatic myogenesis of Drosophila. Development 134: 3985-3997.
15. Jagla T, Bellard F, Lutz Y, Dretzen G, Bellard M, et al. (1998) ladybird determines cell fate decisions during diversification of Drosophila somatic muscles. Development 125: 3699-3708.
16. Crozatier M, Vincent A, (1999) Requirement for the Drosophila COE transcription factor Collier in formation of an embryonic muscle: transcriptional response to notch signalling. Development 126: 1495-1504.
17. Knirr S, Azpiazu N, Frasch M, (1999) The role of the NK-homeobox gene slouch (S59) in somatic muscle patterning. Development 126: 4525-4535.
18. Ruiz-Gómez M, Romani S, Hartmann C, Jackle H, Bate M, (1997) Specific muscle identities are regulated by Kruppel during Drosophila embryogenesis. Development 124: 3407-3414.
19. Bate M, Rushton E, Frasch M, (1993) A dual requirement for neurogenic genes in Drosophila myogenesis. Dev Suppl pp. 149-161.
20. Nose A, Mahajan VB, Goodman CS, (1992) Connectin: a homophilic cell adhesion molecule expressed on a subset of muscles and the motoneurons that innervate them in Drosophila. Cell 70: 553-567.
21. Gomez-Skarmeta JL, Modolell J, (2002) Iroquois genes: genomic organization and function in vertebrate neural development. Curr Opin Genet Dev 12: 403-408.
22. Cavodeassi F, Modolell J, Campuzano S, (2000) The Iroquois homeobox genes function as dorsal selectors in the Drosophila head. Development 127: 1921-1929.
23. Diez del Corral R, Aroca P, JL Gm-S, Cavodeassi F, Modolell J, (1999) The Iroquois homeodomain proteins are required to specify body wall identity in Drosophila. Genes Dev 13: 1754-1761.
24. Feijoo CG, Manzanares M, de la Calle-Mustienes E, Gomez-Skarmeta JL, Allende ML, (2004) The Irx gene family in zebrafish: genomic structure, evolution and initial characterization of irx5b. Dev Genes Evol 214: 277-284.
25. Cavodeassi F, Diez Del Corral R, Campuzano S, Dominguez M, (1999) Compartments and organising boundaries in the Drosophila eye: the role of the homeodomain Iroquois proteins. Development 126: 4933-4942.
26. Glavic A, Gomez-Skarmeta JL, Mayor R, (2002) The homeoprotein Xiro1 is required for midbrain-hindbrain boundary formation. Development 129: 1609-1621.
27. Gomez-Skarmeta J, de La Calle-Mustienes E, Modolell J, (2001) The Wnt-activated Xiro1 gene encodes a repressor that is essential for neural development and downregulates Bmp4. Development 128: 551-560.
28. Gomez-Skarmeta JL, Diez del Corral R, de la Calle-Mustienes E, Ferre-Marco D, Modolell J, (1996) Araucan and caupolican, two members of the novel iroquois complex, encode homeoproteins that control proneural and vein-forming genes. Cell 85: 95-105.
29. Leyns L, Gomez-Skarmeta JL, Dambly-Chaudiere C, (1996) iroquois: a prepattern gene that controls the formation of bristles on the thorax of Drosophila. Mech Dev 59: 63-72.
30. Rodriguez-Seguel E, Alarcon P, Gomez-Skarmeta JL, (2009) The Xenopus Irx genes are essential for neural patterning and define the border between prethalamus and thalamus through mutual antagonism with the anterior repressors Fezf and Arx. Dev Biol 329: 258-268.
31. Michelson AM, Abmayr SM, Bate M, Arias AM, Maniatis T, (1990) Expression of a MyoD family member prefigures muscle pattern in Drosophila embryos. Genes Dev 4: 2086-2097.
32. Nose A, Isshiki T, Takeichi M, (1998) Regional specification of muscle progenitors in Drosophila: the role of the msh homeobox gene. Development 125: 215-223.
33. Dubois L, Enriquez J, Daburon V, Crozet F, Lebreton G, et al. (2007) Collier transcription in a single Drosophila muscle lineage: the combinatorial control of muscle identity. Development 134: 4347-4355.
34. Knirr S, Frasch M, (2001) Molecular integration of inductive and mesoderm-intrinsic inputs governs even-skipped enhancer activity in a subset of pericardial and dorsal muscle progenitors. Dev Biol 238: 13-26.
35. Philippakis AA, Busser BW, Gisselbrecht SS, He FS, Estrada B, et al. (2006) Expression-guided in silico evaluation of candidate cis regulatory codes for Drosophila muscle founder cells. PLoS Comput Biol 2: e53 doi:10.1371/journal.pcbi.0020053.
36. Hartmann C, Landgraf M, Bate M, Jackle H, (1997) Kruppel target gene knockout participates in the proper innervation of a specific set of Drosophila larval muscles. Embo J 16: 5299-5309.
37. Junion G, Bataille L, Jagla T, Da Ponte JP, Tapin R, et al. (2007) Genome-wide view of cell fate specification: ladybird acts at multiple levels during diversification of muscle and heart precursors. Genes Dev 21: 3163-3180.
38. Bataille L, Delon I, Da Ponte JP, Brown NH, Jagla K, (2010) Downstream of identity genes: muscle-type-specific regulation of the fusion process. Dev Cell 19: 317-328.
39. Calleja M, Herranz H, Estella C, Casal J, Lawrence P, et al. (2000) Generation of medial and lateral dorsal body domains by the pannier gene of Drosophila. Development 127: 3971-3980.
40. Letizia A, Barrio R, Campuzano S, (2007) Antagonistic and cooperative actions of the EGFR and Dpp pathways on the iroquois genes regulate Drosophila mesothorax specification and patterning. Development 134: 1337-1346.
41. McNeill H, Yang CH, Brodsky M, Ungos J, Simon MA, (1997) mirror encodes a novel PBX-class homeoprotein that functions in the definition of the dorsal-ventral border in the Drosophila eye. Genes Dev 11: 1073-1082.
42. González-Pérez E, (2009) Función y regulación de las homeoproteínas del complejo génico Iroquois en los discos imaginales de ala y ojo-antena de Drosophila melanogaster Madrid Autónoma de Madrid.
43. Muller D, Jagla T, Bodart LM, Jahrling N, Dodt HU, et al. (2010) Regulation and functions of the lms homeobox gene during development of embryonic lateral transverse muscles and direct flight muscles in Drosophila. PLoS ONE 5: e14323 doi:10.1371/journal.pone.0014323.
44. Herranz H, (2001) Estudio de la función del gen pannier en el desarrollo embrionario de Drosophila melanogaster Madrid Autónoma de Madrid.
45. Ruiz-Gómez M, Coutts N, Price A, Taylor MV, Bate M, (2000) Drosophila dumbfounded: a myoblast attractant essential for fusion. Cell 102: 189-198.
46. Kim SJ, Park T, Lee KK, (1999) Identification of a novel cis-acting positive element responsible for the cell-specific expression of the NK-1 homeobox gene. Biochem Biophys Res Commun 257: 538-544.
47. Bilioni A, Craig G, Hill C, McNeill H, (2005) Iroquois transcription factors recognize a unique motif to mediate transcriptional repression in vivo. Proc Natl Acad Sci U S A 102: 14671-14676.
48. Matsumoto K, Nishihara S, Kamimura M, Shiraishi T, Otoguro T, et al. (2004) The prepattern transcription factor Irx2, a target of the FGF8/MAP kinase cascade, is involved in cerebellum formation. Nat Neurosci 7: 605-612.
49. Lee T, Feig L, Montell DJ, (1996) Two distinct roles for Ras in a developmentally regulated cell migration. Development 122: 409-418.
50. Deng H, Bell JB, Simmonds AJ, (2010) Vestigial is required during late-stage muscle differentiation in Drosophila melanogaster embryos. Mol Biol Cell 21: 3304-3316.
51. Buff E, Carmena A, Gisselbrecht S, Jimenez F, Michelson AM, (1998) Signalling by the Drosophila epidermal growth factor receptor is required for the specification and diversification of embryonic muscle progenitors. Development 125: 2075-2086.
52. Cavodeassi F, Modolell J, Gomez-Skarmeta JL, (2001) The Iroquois family of genes: from body building to neural patterning. Development 128: 2847-2855.
53. Baumgardt M, Miguel-Aliaga I, Karlsson D, Ekman H, Thor S, (2007) Specification of neuronal identities by feedforward combinatorial coding. PLoS Biol 5: e37 doi:10.1371/journal.pbio.0050037.
54. de Celis JF, Barrio R, Kafatos FC, (1996) A gene complex acting downstream of dpp in Drosophila wing morphogenesis. Nature 381: 421-424.
55. Ranganayakulu G, Elliott DA, Harvey RP, Olson EN, (1998) Divergent roles for NK-2 class homeobox genes in cardiogenesis in flies and mice. Development 125: 3037-3048.
56. Calleja M, Moreno E, Pelaz S, Morata G, (1996) Visualization of gene expression in living adult Drosophila. Science 274: 252-255.
57. Brand AH, Perrimon N, (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
58. Martin BS, Ruiz-Gomez M, Landgraf M, Bate M, (2001) A distinct set of founders and fusion-competent myoblasts make visceral muscles in the Drosophila embryo. Development 128: 3331-3338.
59. Kosman D, Small S, Reinitz J, (1998) Rapid preparation of a panel of polyclonal antibodies to Drosophila segmentation proteins. Dev Genes Evol 208: 290-294.
60. Goubeaud A, Knirr S, Renkawitz-Pohl R, Paululat A, (1996) The Drosophila gene alien is expressed in the muscle attachment sites during embryogenesis and encodes a protein highly conserved between plants, Drosophila and vertebrates. Mech Dev 57: 59-68.
61. Meadows LA, Gell D, Broadie K, Gould AP, White RA, (1994) The cell adhesion molecule, connectin, and the development of the Drosophila neuromuscular system. J Cell Sci 107 (Pt 1): 321-328.
62. Williams JA, Bell JB, Carroll SB, (1991) Control of Drosophila wing and haltere development by the nuclear vestigial gene product. Genes Dev 5: 2481-2495.
63. Kiehart DP, Feghali R, (1986) Cytoplasmic myosin from Drosophila melanogaster. J Cell Biol 103: 1517-1525.
64. Gilchrist DA, Nechaev S, Lee C, Ghosh SK, Collins JB, et al. (2008) NELF-mediated stalling of Pol II can enhance gene expression by blocking promoter-proximal nucleosome assembly. Genes Dev 22: 1921-1933.
65. Wharton KA Jr, Crews ST, (1993) CNS midline enhancers of the Drosophila slit and Toll genes. Mech Dev 40: 141-154.