Prepatterning the Drosophila notum: The three genes of the iroquois complex play intrinsically distinct roles

Developmental Biology

Volumn 317, Issue 2, 2008, Pages 634-648

  Ikmi, Aissam ^a   Netter, Sophie ^b   Coen, Dario ^a  

^a CNRS   (France)

^b LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

Author keywords

Drosophila notum; iroquois complex; Prepattern; Redundancy; stripe

Indexed keywords

HOMEODOMAIN PROTEIN; PROTEIN ARAUCAN; PROTEIN CAUPOLICAN; PROTEIN IROQUOIS; PROTEIN MIRROR;

ARTICLE; CONTROLLED STUDY; DROSOPHILA; GENE EXPRESSION; GENE MAPPING; GENE SEQUENCE; GENETIC ANALYSIS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSE ORGAN;

DROSOPHILA IROQUOIS; DROSOPHILA NOTUM;

EID: 43049173741     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2007.12.034     Document Type: Article

References (62)

1. S. Aldaz G. Morata N. Azpiazu The Pax-homeobox gene eyegone is involved in the subdivision of the thorax of Drosophila Development 130 2003 4473 4482
2. H.J. Bellen R.W. Levis G. Liao Y. He J.W. Carlson G. Tsang M. Evans-Holm P.R. Hiesinger K.L. Schulze G.M. Rubin R.A. Hoskins A.C. Spradling The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes Genetics 167 2004 761 781
3. A. Bilioni G. Craig C. Hill H. McNeill Iroquois transcription factors recognize a unique motif to mediate transcriptional repression in vivo Proc. Natl. Acad. Sci. U. S. A. 102 2005 14671 14676
4. B.G. Bruneau Z.Z. Bao D. Fatkin J. Xavier-Neto D. Georgakopoulos C.T. Maguire C.I. Berul D.A. Kass M.L. Kuroski-de Bold A.J. de Bold D.A. Conner N. Rosenthal C.L. Cepko C.E. Seidman J.G. Seidman Cardiomyopathy in Irx4-deficient mice is preceded by abnormal ventricular gene expression Mol. Cell. Biol. 21 2001 1730 1736
5. T.R. Burglin Analysis of TALE superclass homeobox genes (MEIS, PBC, KNOX, Iroquois, TGIF) reveals a novel domain conserved between plants and animals Nucleic Acids Res. 25 1997 4173 4180
6. M. Calleja H. Herranz C. Estella J. Casal P. Lawrence P. Simpson G. Morata Generation of medial and lateral dorsal body domains by the pannier gene of Drosophila Development 127 2000 3971 3980
7. M. Calleja O. Renaud K. Usui D. Pistillo G. Morata P. Simpson How to pattern an epithelium: lessons from achaete–scute regulation on the notum of Drosophila Gene 292 2002 1 12
8. S. Campuzano L. Carramolino C.V. Cabrera M. Ruiz-Gomez R. Villares A. Boronat J. Modolell Molecular genetics of the achaete–scute gene complex of D. melanogaster Cell 40 1985 327 338
9. F. Cavodeassi J. Modolell S. Campuzano The Iroquois homeobox genes function as dorsal selectors in the Drosophila head Development 127 2000 1921 1929
10. F. Cavodeassi J. Modolell J.L. Gomez-Skarmeta The Iroquois family of genes: from body building to neural patterning Development 128 2001 2847 2855
11. C.W. Cheng R.L. Chow M. Lebel R. Sakuma H.O. Cheung V. Thanabalasingham X. Zhang B.G. Bruneau D.G. Birch C.C. Hui R.R. McInnes S.H. Cheng The Iroquois homeobox gene, Irx5, is required for retinal cone bipolar cell development Dev. Biol. 287 2005 48 60
12. Y. Cubadda P. Heitzler R.P. Ray M. Bourouis P. Ramain W. Gelbart P. Simpson M. Haenlin u-shaped encodes a zinc finger protein that regulates the proneural genes achaete and scute during the formation of bristles in Drosophila Genes Dev. 11 1997 3083 3095
13. P. Cubas J.F. de Celis S. Campuzano J. Modolell Proneural clusters of achaete–scute expression and the generation of sensory organs in the Drosophila imaginal wing disc Genes Dev. 5 1991 996 1008
14. C. Dambly-Chaudiere L. Leyns The determination of sense organs in Drosophila: a search for interacting genes Int. J. Dev. Biol. 36 1992 85 91
15. J. de Navascues J. Modolell tailup, a LIM-HD gene, and Iro-C cooperate in Drosophila dorsal mesothorax specification Development 134 2007 1779 1788
16. R. Diez del Corral P. Aroca G.m.-S. JL F. Cavodeassi J. Modolell The Iroquois homeodomain proteins are required to specify body wall identity in Drosophila Genes Dev. 13 1999 1754 1761
17. J.B. Duffy GAL4 system in Drosophila: a fly geneticist's Swiss army knife Genesis 34 2002 1 15
18. C.G. Feijoo M. Manzanares E. de la Calle-Mustienes J.L. Gomez-Skarmeta M.L. Allende The Irx gene family in zebrafish: genomic structure, evolution and initial characterization of irx5b Dev. Genes Evol. 214 2004 277 284
19. J.J. Fernandes S.E. Celniker 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
20. A. Force M. Lynch F.B. Pickett A. Amores Y.L. Yan J. Postlethwait Preservation of duplicate genes by complementary, degenerative mutations Genetics 151 1999 1531 1545
21. M.J. Garcia-Garcia P. Ramain P. Simpson J. Modolell Different contributions of pannier and wingless to the patterning of the dorsal mesothorax of Drosophila Development 126 1999 3523 3532
22. A. Ghazi L. Paul K. VijayRaghavan Prepattern genes and signaling molecules regulate stripe expression to specify Drosophila flight muscle attachment sites Mech. Dev. 120 2003 519 528
23. J.L. Gomez-Skarmeta J. Modolell Iroquois genes: genomic organization and function in vertebrate neural development Curr. Opin. Genet. Dev. 12 2002 403 408
24. J.L. Gomez-Skarmeta I. Rodriguez C. Martinez J. Culi D. Ferres-Marco D. Beamonte J. Modolell Cis -regulation of achaete and scute: shared enhancer-like elements drive their coexpression in proneural clusters of the imaginal discs Genes Dev. 9 1995 1869 1882
25. J.L. Gomez-Skarmeta R. Diez del Corral E. de la Calle-Mustienes D. Ferre-Marco J. Modolell Araucan and caupolican, two members of the novel iroquois complex, encode homeoproteins that control proneural and vein-forming genes Cell 85 1996 95 105
26. J.L. Gomez-Skarmeta S. Campuzano J. Modolell Half a century of neural prepatterning: the story of a few bristles and many genes Nat. Rev., Neurosci. 4 2003 587 598
27. X. Gu Evolution of duplicate genes versus genetic robustness against null mutations Trends Genet. 19 2003 354 356
28. M. Haenlin Y. Cubadda F. Blondeau P. Heitzler Y. Lutz P. Simpson P. Ramain Transcriptional activity of pannier is regulated negatively by heterodimerization of the GATA DNA-binding domain with a cofactor encoded by the u-shaped gene of Drosophila Genes Dev. 11 1997 3096 3108
29. F. Huang C. Dambly-Chaudiere A. Ghysen The emergence of sense organs in the wing disc of Drosophila Development 111 1991 1087 1095
30. K.C. Jordan N.J. Clegg J.A. Blasi A.M. Morimoto J. Sen D. Stein H. McNeill W.M. Deng M. Tworoger H. Ruohola-Baker The homeobox gene mirror links EGF signalling to embryonic dorso-ventral axis formation through notch activation Nat. Genet. 24 2000 429 433
31. B.T. Kehl K.O. Cho K.W. Choi mirror, a Drosophila homeobox gene in the Iroquois complex, is required for sensory organ and alula formation Development 125 1998 1217 1227
32. K.M. Kozopas R. Nusse Direct flight muscles in Drosophila develop from cells with characteristics of founders and depend on DWnt-2 for their correct patterning Dev. Biol. 243 2002 312 325
33. D.C. Krakauer M.A. Nowak Evolutionary preservation of redundant duplicated genes Semin. Cell Dev. Biol. 10 1999 555 559
34. M. Lebel P. Agarwal C.W. Cheng M.G. Kabir T.Y. Chan V. Thanabalasingham X. Zhang D.R. Cohen M. Husain S.H. Cheng B.G. Bruneau C.C. Hui The Iroquois homeobox gene Irx2 is not essential for normal development of the heart and midbrain–hindbrain boundary in mice Mol. Cell. Biol. 23 2003 8216 8225
35. A. Letizia R. Barrio S. Campuzano Antagonistic and cooperative actions of the EGFR and Dpp pathways on the iroquois genes regulate Drosophila mesothorax specification and patterning Development 134 2007 1337 1346
36. L. Leyns J.L. Gomez-Skarmeta C. Dambly-Chaudiere iroquois : a prepattern gene that controls the formation of bristles on the thorax of Drosophila Mech. Dev. 59 1996 63 72
37. K.J. Livak T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(− Delta Delta C(T)) method Methods 25 2001 402 408
38. M. Lynch J.S. Conery The evolutionary fate and consequences of duplicate genes Science 290 2000 1151 1155
39. R.S. Mann G. Morata The developmental and molecular biology of genes that subdivide the body of Drosophila Annu. Rev. Cell Dev. Biol. 16 2000 243 271
40. S. Marcellini J.M. Gibert P. Simpson achaete, but not scute, is dispensable for the peripheral nervous system of Drosophila Dev. Biol. 285 2005 545 553
41. S.E. McGuire Z. Mao R.L. Davis Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila Sci. STKE 2004 2004, pl6
42. H. McNeill C.H. Yang M. Brodsky J. Ungos M.A. Simon mirror encodes a novel PBX-class homeoprotein that functions in the definition of the dorsal–ventral border in the Drosophila eye Genes Dev. 11 1997 1073 1082
43. H. Nabel-Rosen N. Dorevitch A. Reuveny T. Volk The balance between two isoforms of the Drosophila RNA-binding protein how controls tendon cell differentiation Mol. Cell 4 1999 573 584
44. S. Netter M.O. Fauvarque R. Diez del Corral J.M. Dura D. Coen White+ transgene insertions presenting a dorsal/ventral pattern define a single cluster of homeobox genes that is silenced by the polycomb-group proteins in Drosophila melanogaster Genetics 149 1998 257 275
45. S.P. Otto P. Yong The evolution of gene duplicates Adv. Genet. 46 2002 451 483
46. S. Perovic H.C. Schroder S. Sudek V.A. Grebenjuk R. Batel M. Stifanic I.M. Muller W.E. Muller Expression of one sponge Iroquois homeobox gene in primmorphs from Suberites domuncula during canal formation Evol. Dev. 5 2003 240 250
47. R.G. Phillips J.R. Whittle wingless expression mediates determination of peripheral nervous system elements in late stages of Drosophila wing disc development Development 118 1993 427 438
48. F. Pichaud F. Casares homothorax and iroquois-C genes are required for the establishment of territories within the developing eye disc Mech. Dev. 96 2000 15 25
49. P. Ramain R. Khechumian K. Khechumian N. Arbogast C. Ackermann P. Heitzler Interactions between chip and the achaete/scute-daughterless heterodimers are required for pannier-driven proneural patterning Mol. Cell 6 2000 781 790
50. S. Romani S. Campuzano E.R. Macagno J. Modolell Expression of achaete and scute genes in Drosophila imaginal discs and their function in sensory organ development Genes Dev. 3 1989 997 1007
51. M. Ruiz-Gomez J. Modolell Deletion analysis of the achaete–scute locus of Drosophila melanogaster Genes Dev. 1 1987 1238 1246
52. M. Sato T. Kojima T. Michiue K. Saigo Bar homeobox genes are latitudinal prepattern genes in the developing Drosophila notum whose expression is regulated by the concerted functions of decapentaplegic and wingless Development 126 1999 1457 1466
53. P. Simpson Lateral inhibition and the development of the sensory bristles of the adult peripheral nervous system of Drosophila Development 109 1990 509 519
54. P. Simpson A prepattern for sensory organs, Drosophila development Curr. Biol. 6 1996 948 950
55. A. Singh M. Kango-Singh K.W. Choi Y.H. Sun Dorso-ventral asymmetric functions of teashirt in Drosophila eye development depend on spatial cues provided by early DV patterning genes Mech. Dev. 121 2004 365 370
56. J.B. Skeath S.B. Carroll Regulation of achaete–scute gene expression and sensory organ pattern formation in the Drosophila wing Genes Dev. 5 1991 984 995
57. Y.H. Sun C.J. Tsai M.M. Green J.L. Chao C.T. Yu T.J. Jaw J.Y. Yeh V.N. Bolshakov White as a reporter gene to detect transcriptional silencers specifying position-specific gene expression during Drosophila melanogaster eye development Genetics 141 1995 1075 1086
58. S.T. Thibault M.A. Singer W.Y. Miyazaki B. Milash N.A. Dompe C.M. Singh R. Buchholz M. Demsky R. Fawcett H.L. Francis-Lang L. Ryner L.M. Cheung A. Chong C. Erickson W.W. Fisher K. Greer S.R. Hartouni E. Howie L. Jakkula D. Joo K. Killpack A. Laufer J. Mazzotta R.D. Smith L.M. Stevens C. Stuber L.R. Tan R. Ventura A. Woo I. Zakrajsek L. Zhao F. Chen C. Swimmer C. Kopczynski G. Duyk M.L. Winberg J. Margolis A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac Nat. Genet. 36 2004 283 287
59. K. Usui D. Pistillo P. Simpson Mutual exclusion of sensory bristles and tendons on the notum of dipteran flies Curr. Biol. 14 2004 1047 1055
60. E. Villa-Cuesta J. Modolell Mutual repression between msh and Iro-C is an essential component of the boundary between body wall and wing in Drosophila Development 132 2005 4087 4096
61. R. Villares C.V. Cabrera The achaete–scute gene complex of D. melanogaster: conserved domains in a subset of genes required for neurogenesis and their homology to myc Cell 50 1987 415 424
62. D. Zhao S. Woolner M. Bownes The Mirror transcription factor links signalling pathways in Drosophila oogenesis Dev. Genes Evol. 210 2000 449 457