Engrailed expression in subsets of adult Drosophila sensory neurons: An enhancer-trap study

Invertebrate Neuroscience

Volumn 8, Issue 3, 2008, Pages 133-146

  Blagburn, Jonathan M ^a  

^a UNIVERSITY OF PUERTO RICO MEDICAL SCIENCES CAMPUS   (Puerto Rico)

Author keywords

Drosophila melanogaster; Homeodomain; Sense organs; Transcription factor

Indexed keywords

GREEN FLUORESCENT PROTEIN; HOMEODOMAIN PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GAL4;

ANTENNA; ARTICLE; CONTROLLED STUDY; DROSOPHILA; NERVE FIBER; NONHUMAN; OLFACTORY NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSE ORGAN; SENSORY NERVE CELL;

AMINO ACIDS; ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GANGLIA, INVERTEBRATE; GREEN FLUORESCENT PROTEINS; HOMEODOMAIN PROTEINS; MALE; SENSORY RECEPTOR CELLS; TRANSCRIPTION FACTORS;

EID: 50249103245     PISSN: 13542516     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10158-008-0074-6     Document Type: Article

References (71)

1. SL Baader MW Vogel S Sanlioglu X Zhang J Oberdick 1999 Selective disruption of "late onset" sagittal banding patterns by ectopic expression of Engrailed-2 in cerebellar Purkinje cells J Neurosci 19 5370 5379
2. SP Bainbridge M Bownes 1981 Staging the metamorphosis of Drosophila melanogaster J Embryol Exp Morphol 66 57 80
3. KM Bhat P Schedl 1997 Requirement for engrailed and invected genes reveals novel regulatory interactions between engrailed/invected, patched, gooseberry and wingless during Drosophila neurogenesis Development 124 1675 1688
4. JM Blagburn CR Gibbon JP Bacon 1995 Expression of engrailed in an array of identified sensory neurons: comparison with position, axonal arborization, and synaptic connectivity J Neurobiol 28 493 505 10.1002/neu.480280409
5. R Brewster K Hardiman M Deo S Khan R Bodmer 2001 The selector gene cut represses a neural cell fate that is specified independently of the Achaete-Scute-Complex and atonal Mech Dev 105 57 68 10.1016/S0925-4773(01)00375- 6
6. SJ Certel PJ Clyne JR Carlson WA Johnson 2000 Regulation of central neuron synaptic targeting by the Drosophila POU protein, Acj6 Development 127 2395 2405
7. BG Condron NH Patel K Zinn 1994 Engrailed controls glial/neuronal cell fate decisions at the midline of the central nervous system Neuron 13 541 554 10.1016/0896-6273(94)90024-8
8. A Couto M Alenius BJ Dickson 2005 Molecular, anatomical, and functional organization of the Drosophila olfactory system Curr Biol 15 1535 1547 10.1016/j.cub.2005.07.034
9. DF Eberl RW Hardy MJ Kernan 2000 Genetically similar transduction mechanisms for touch and hearing in Drosophila J Neurosci 20 5981 5988
10. K Endo T Aoki Y Yoda K Kimura C Hama 2007 Notch signal organizes the Drosophila olfactory circuitry by diversifying the sensory neuronal lineages Nat Neurosci 10 153 160 10.1038/nn1832
11. GC Friedman DD O'Leary 1996 Retroviral misexpression of engrailed genes in the chick optic tectum perturbs the topographic targeting of retinal axons J Neurosci 16 5498 5509
12. JM Gibert 2002 The evolution of engrailed genes after duplication and speciation events Dev Genes Evol 212 307 318 10.1007/s00427-002-0243-2
13. MC Gopfert D Robert 2002 The mechanical basis of Drosophila audition J Exp Biol 205 1199 1208
14. SE Goulding P zur Lage AP Jarman 2000 amos, a proneural gene for Drosophila olfactory sense organs that is regulated by lozenge Neuron 25 69 78 10.1016/S0896-6273(00)80872-7
15. BP Gupta GV Flores U Banerjee V Rodrigues 1998 Patterning an epidermal field: Drosophila lozenge, a member of the AML-1/Runt family of transcription factors, specifies olfactory sense organ type in a dose-dependent manner Dev Biol 203 400 411 10.1006/dbio.1998.9064
16. C Hama Z Ali TB Kornberg 1990 Region-specific recombination and expression are directed by portions of the Drosophila engrailed promoter Genes Dev 4 1079 1093 10.1101/gad.4.7.1079
17. M Hanks W Wurst L Anson-Cartwright AB Auerbach AL Joyner 1995 Rescue of the En-1 mutant phenotype by replacement of En-1 with En-2 Science 269 679 682 10.1126/science.7624797
18. M Hiroi F Marion-Poll T Tanimura 2002 Differentiated response to sugars among labellar chemosensilla in Drosophila Zoolog Sci 19 1009 1018 10.2108/zsj.19.1009
19. M Hiroi N Meunier F Marion-Poll T Tanimura 2004 Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila J Neurobiol 61 333 342 10.1002/neu.20063
20. N Itasaki H Nakamura 1996 A role for gradient en expression in positional specification on the optic tectum Neuron 16 55 62 10.1016/S0896-6273(00)80023-9
21. D Jhaveri A Sen GV Reddy V Rodrigues 2000 Sense organ identity in the Drosophila antenna is specified by the expression of the proneural gene atonal Mech Dev 99 101 111 10.1016/S0925-4773(00)00487-1
22. W Joly B Mugat F Maschat 2007 Engrailed controls the organization of the ventral nerve cord through frazzled regulation Dev Biol 301 542 554 10.1016/j.ydbio.2006.10.019
23. A Kamikouchi T Shimada K Ito 2006 Comprehensive classification of the auditory sensory projections in the brain of the fruit fly Drosophila melanogaster J Comp Neurol 499 317 356 10.1002/cne.21075
24. T Komiyama JR Carlson L Luo 2004 Olfactory receptor neuron axon targeting: intrinsic transcriptional control and hierarchical interactions Nat Neurosci 7 819 825 10.1038/nn1284
25. T Kornberg 1981 Engrailed: a gene controlling compartment and segment formation in Drosophila Proc Natl Acad Sci USA 78 1095 1099 10.1073/pnas.78.2. 1095
26. B Kuemerle F Gulden N Cherosky E Williams K Herrup 2007 The mouse Engrailed genes: a window into autism Behav Brain Res 176 121 132 10.1016/j.bbr.2006.09.009
27. PP Laissue C Reiter PR Hiesinger S Halter KF Fischbach RF Stocker 1999 Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster J Comp Neurol 405 543 552 10.1002/(SICI)1096-9861(19990322)405:4<543::AID- CNE7>3.0.CO;2-A
28. PA Lawrence G Struhl 1982 Further studies of the engrailed phenotype in Drosophila EMBO J 1 827 833
29. T Lee L Luo 1999 Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis Neuron 22 451 461 10.1016/S0896-6273(00)80701-1
30. MH Lee PM Salvaterra 2002 Abnormal chemosensory jump 6 is a positive transcriptional regulator of the cholinergic gene locus in Drosophila olfactory neurons J Neurosci 22 5291 5299
31. X Li X Zhao Y Fang X Jiang T Duong C Fan 1998 Generation of destabilized green fluorescent protein as a transcription reporter J Biol Chem 273 34970 34975 10.1074/jbc.273.52.34970
32. MC Lienhard RF Stocker 1991 The development of the sensory neuron pattern in the antennal disc of wild-type and mutant (lz3, ssa) Drosophila melanogaster Development 112 1063 1075
33. C Logan A Wizenmann U Drescher B Monschau F Bonhoeffer A Lumsden 1996 Rostral optic tectum acquires caudal characteristics following ectopic engrailed expression Curr Biol 6 1006 1014 10.1016/S0960-9822(02)00645-0
34. MJ Lundell Q Chu-LaGraff CQ Doe J Hirsh 1996 The engrailed and huckebein genes are essential for development of serotonin neurons in the Drosophila CNS Mol Cell Neurosci 7 46 61 10.1006/mcne.1996.0004
35. B Marie JM Blagburn 2003 Differential roles of Engrailed paralogs in determining sensory axon guidance and synaptic target recognition J Neurosci 23 7854 7862
36. B Marie JP Bacon JM Blagburn 2000 Double-stranded RNA interference shows that Engrailed controls the synaptic specificity of identified sensory neurons Curr Biol 10 289 292 10.1016/S0960-9822(00)00361-4
37. B Marie L Cruz-Orengo JM Blagburn 2002 Persistent engrailed expression is required to determine sensory axon trajectory, branching, and target choice J Neurosci 22 832 841
38. DJ Merritt RK Murphey 1992 Projections of leg proprioceptors within the CNS of the fly Phormia in relation to the generalized insect ganglion J Comp Neurol 322 16 34 10.1002/cne.903220103
39. G Morata PA Lawrence 1975 Control of compartment development by the engrailed gene in Drosophila Nature 255 614 617 10.1038/255614a0
40. RK Murphey D Possidente G Pollack DJ Merritt 1989 Modality-specific axonal projections in the CNS of the flies Phormia and Drosophila J Comp Neurol 290 185 200 10.1002/cne.902900203
41. RK Murphey DR Possidente P Vandervorst A Ghysen 1989 Compartments and the topography of leg afferent projections in Drosophila J Neurosci 9 3209 3217
42. NH Patel TB Kornberg CS Goodman 1989 Expression of engrailed during segmentation in grasshopper and crayfish Development 107 201 212
43. NH Patel E Martin-Blanco KG Coleman SJ Poole MC Ellis TB Kornberg 1989 Expression of engrailed proteins in arthropods, annelids, and chordates Cell 58 955 968 10.1016/0092-8674(89)90947-1
44. AD Peel MJ Telford M Akam 2006 The evolution of hexapod engrailed-family genes: evidence for conservation and concerted evolution Proc Biol Sci 273 1733 1742 10.1098/rspb.2006.3497
45. LA Raftery M Sanicola RK Blackman WM Gelbart 1991 The relationship of decapentaplegic and engrailed expression in Drosophila imaginal disks: do these genes mark the anterior-posterior compartment boundary? Development 113 27 33
46. A Ray WG van Naters T Shiraiwa JR Carlson 2007 Mechanisms of odor receptor gene choice in Drosophila Neuron 53 353 369 10.1016/j.neuron.2006.12. 010
47. GV Reddy B Gupta K Ray V Rodrigues 1997 Development of the Drosophila olfactory sense organs utilizes cell-cell interactions as well as lineage Development 124 703 712
48. B Rogina SL Helfand 1997 Spatial and temporal pattern of expression of the wingless and engrailed genes in the adult antenna is regulated by age-dependent mechanisms Mech Dev 63 89 97 10.1016/S0925-4773(97)00033-6
49. H Saueressig J Burrill M Goulding 1999 Engrailed-1 and netrin-1 regulate axon pathfinding by association interneurons that project to motor neurons Development 126 4201 4212
50. O Sayeed S Benzer 1996 Behavioral genetics of thermosensation and hygrosensation in Drosophila Proc Natl Acad Sci USA 93 6079 6084 10.1073/pnas.93.12.6079
51. P Sgado L Alberi D Gherbassi SL Galasso GM Ramakers KN Alavian 2006 Slow progressive degeneration of nigral dopaminergic neurons in postnatal Engrailed mutant mice Proc Natl Acad Sci USA 103 15242 15247 10.1073/pnas.0602116103
52. SR Shanbhag K Singh RN Singh 1995 Fine structure and primary sensory projections of sensilla located in the sacculus of the antenna of Drosophila melanogaster Cell Tissue Res 282 237 249 10.1007/BF00319115
53. D Shepherd SA Smith 1996 Central projections of persistent larval sensory neurons prefigure adult sensory pathways in the CNS of Drosophila Development 122 2375 2384
54. Y Shigetani JI Funahashi H Nakamura 1997 En-2 regulates the expression of the ligands for Eph type tyrosine kinases in chick embryonic tectum Neurosci Res 27 211 217 10.1016/S0168-0102(96)01151-0
55. MV Siegler XX Jia 1999 Engrailed negatively regulates the expression of cell adhesion molecules connectin and neuroglian in embryonic Drosophila nervous system Neuron 22 265 276 10.1016/S0896-6273(00)81088-0
56. MV Siegler RR Pankhaniya XX Jia 2001 Pattern of expression of Engrailed in relation to gamma-aminobutyric acid immunoreactivity in the central nervous system of the adult grasshopper J Comp Neurol 440 85 96 10.1002/cne.1371
57. HH Simon H Saueressig W Wurst MD Goulding DD O'Leary 2001 Fate of midbrain dopaminergic neurons controlled by the engrailed genes J Neurosci 21 3126 3134
58. SA Smith D Shepherd 1996 Central afferent projections of proprioceptive sensory neurons in Drosophila revealed with the enhancer-trap technique J Comp Neurol 364 311 323 10.1002/(SICI)1096-9861(19960108)364:2<311::AID-CNE9>3. 0.CO;2-8
59. PJ Solano B Mugat D Martin F Girard JM Huibant C Ferraz 2003 Genome-wide identification of in vivo Drosophila Engrailed-binding DNA fragments and related target genes Development 130 1243 1254 10.1242/dev.00348
60. RF Stocker 1994 The organization of the chemosensory system in Drosophila melanogaster: a review Cell Tissue Res 275 3 26 10.1007/BF00305372
61. JR Trimarchi RK Murphey 1997 The shaking-B2 mutation disrupts electrical synapses in a flight circuit in adult Drosophila J Neurosci 17 4700 4710
62. LB Vosshall RF Stocker 2007 Molecular architecture of smell and taste in Drosophila Annu Rev Neurosci 30 505 533 10.1146/annurev.neuro.30.051606.094306
63. DA Wagh TM Rasse E Asan A Hofbauer I Schwenkert H Durrbeck 2006 Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila Neuron 49 833 844 10.1016/j.neuron.2006.02.008
64. Z Wang A Singhvi P Kong K Scott 2004 Taste representations in the Drosophila brain Cell 117 981 991 10.1016/j.cell.2004.06.011
65. PJ Webster TE Mansour 1992 Conserved classes of homeodomains in Schistosoma mansoni, an early bilateral metazoan Mech Dev 38 25 32 10.1016/0925-4773(92)90035-I
66. P Wenner MJ O'Donovan MP Matise 2000 Topographical and physiological characterization of interneurons that express Engrailed-1 in the embryonic chick spinal cord J Neurophysiol 84 2651 2657
67. DW Williams D Shepherd 1999 Persistent larval sensory neurons in adult Drosophila melanogaster J Neurobiol 39 275 286 10.1002/(SICI)1097-4695(199905) 39:2<275::AID-NEU11>3.0.CO;2-0
68. DW Williams M Tyrer D Shepherd 2000 Tau and tau reporters disrupt central projections of sensory neurons in Drosophila J Comp Neurol 428 630 640 10.1002/1096-9861(20001225)428:4<630::AID-CNE4>3.0.CO;2-X
69. W Wurst AB Auerbach AL Joyner 1994 Multiple developmental defects in Engrailed-1 mutant mice: an early mid-hindbrain deletion and patterning defects in forelimbs and sternum Development 120 2065 2075
70. K Yasunaga K Saigo T Kojima 2006 Fate map of the distal portion of Drosophila proboscis as inferred from the expression and mutations of basic patterning genes Mech Dev 123 893 906 10.1016/j.mod.2006.08.008
71. KB Yoffe AS Manoukian EL Wilder AH Brand N Perrimon 1995 Evidence for engrailed-independent wingless autoregulation in Drosophila Dev Biol 170 636 650 10.1006/dbio.1995.1243