Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Invertebrate Neuroscience

Abstract

Engrailed (En) has an important role in neuronal development in vertebrates and invertebrates. In adult Drosophila, although En expression persists throughout adulthood, a detailed description of its expression in sensory neurons has not been made. In this study, en-GAL4 was used to drive UAS-CD8::GFP expression and the projections of sensory neurons were examined with confocal microscopy. En protein expression was confirmed using immunocytochemistry. In the antenna, En is present in subsets of Johnston’s organ neurons and of olfactory neurons. En-driven GFP is expressed in axons projecting to 18 identified olfactory glomeruli, originating from basiconic, trichoid and coeloconic sensilla. In most cases both neurons of a sensillum express En. En expression overlaps with that of Acj6, another transcription factor. En-driven GFP is also expressed in a subset of maxillary palp olfactory neurons and in all mechanosensory and gustatory sensilla in the posterior compartment of the labial palps. In the legs and halteres, en-driven GFP is expressed in only a subset of the sensory neurons of different modalities that arise in the posterior compartment. Finally, en-driven GFP is expressed in a single multidendritic sensory neuron in each abdominal segment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Baader SL, Vogel MW, Sanlioglu S, Zhang X, Oberdick J (1999) Selective disruption of “late onset” sagittal banding patterns by ectopic expression of Engrailed-2 in cerebellar Purkinje cells. J Neurosci 19:5370–5379

    PubMed  CAS  Google Scholar 

  • Bainbridge SP, Bownes M (1981) Staging the metamorphosis of Drosophila melanogaster. J Embryol Exp Morphol 66:57–80

    PubMed  CAS  Google Scholar 

  • Bhat KM, Schedl P (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

    PubMed  CAS  Google Scholar 

  • Blagburn JM, Gibbon CR, Bacon JP (1995) Expression of engrailed in an array of identified sensory neurons: comparison with position, axonal arborization, and synaptic connectivity. J Neurobiol 28:493–505. doi:10.1002/neu.480280409

    Article  PubMed  CAS  Google Scholar 

  • Brewster R, Hardiman K, Deo M, Khan S, Bodmer R (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. doi:10.1016/S0925-4773(01)00375-6

    Article  PubMed  CAS  Google Scholar 

  • Certel SJ, Clyne PJ, Carlson JR, Johnson WA (2000) Regulation of central neuron synaptic targeting by the Drosophila POU protein, Acj6. Development 127:2395–2405

    PubMed  CAS  Google Scholar 

  • Condron BG, Patel NH, Zinn K (1994) Engrailed controls glial/neuronal cell fate decisions at the midline of the central nervous system. Neuron 13:541–554. doi:10.1016/0896-6273(94)90024-8

    Article  PubMed  CAS  Google Scholar 

  • Couto A, Alenius M, Dickson BJ (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15:1535–1547. doi:10.1016/j.cub.2005.07.034

    Article  PubMed  CAS  Google Scholar 

  • Eberl DF, Hardy RW, Kernan MJ (2000) Genetically similar transduction mechanisms for touch and hearing in Drosophila. J Neurosci 20:5981–5988

    PubMed  CAS  Google Scholar 

  • Endo K, Aoki T, Yoda Y, Kimura K, Hama C (2007) Notch signal organizes the Drosophila olfactory circuitry by diversifying the sensory neuronal lineages. Nat Neurosci 10:153–160. doi:10.1038/nn1832

    Article  PubMed  CAS  Google Scholar 

  • Friedman GC, O’Leary DD (1996) Retroviral misexpression of engrailed genes in the chick optic tectum perturbs the topographic targeting of retinal axons. J Neurosci 16:5498–5509

    PubMed  CAS  Google Scholar 

  • Gibert JM (2002) The evolution of engrailed genes after duplication and speciation events. Dev Genes Evol 212:307–318. doi:10.1007/s00427-002-0243-2

    Article  PubMed  CAS  Google Scholar 

  • Gopfert MC, Robert D (2002) The mechanical basis of Drosophila audition. J Exp Biol 205:1199–1208

    PubMed  Google Scholar 

  • Goulding SE, zur Lage P, Jarman AP (2000) amos, a proneural gene for Drosophila olfactory sense organs that is regulated by lozenge. Neuron 25:69–78. doi:10.1016/S0896-6273(00)80872-7

    Article  PubMed  CAS  Google Scholar 

  • Gupta BP, Flores GV, Banerjee U, Rodrigues V (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. doi:10.1006/dbio.1998.9064

    Article  PubMed  CAS  Google Scholar 

  • Hama C, Ali Z, Kornberg TB (1990) Region-specific recombination and expression are directed by portions of the Drosophila engrailed promoter. Genes Dev 4:1079–1093. doi:10.1101/gad.4.7.1079

    Article  PubMed  CAS  Google Scholar 

  • Hanks M, Wurst W, Anson-Cartwright L, Auerbach AB, Joyner AL (1995) Rescue of the En-1 mutant phenotype by replacement of En-1 with En-2. Science 269:679–682. doi:10.1126/science.7624797

    Article  PubMed  CAS  Google Scholar 

  • Hiroi M, Marion-Poll F, Tanimura T (2002) Differentiated response to sugars among labellar chemosensilla in Drosophila. Zoolog Sci 19:1009–1018. doi:10.2108/zsj.19.1009

    Article  PubMed  Google Scholar 

  • Hiroi M, Meunier N, Marion-Poll F, Tanimura T (2004) Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila. J Neurobiol 61:333–342. doi:10.1002/neu.20063

    Article  PubMed  Google Scholar 

  • Itasaki N, Nakamura H (1996) A role for gradient en expression in positional specification on the optic tectum. Neuron 16:55–62. doi:10.1016/S0896-6273(00)80023-9

    Article  PubMed  CAS  Google Scholar 

  • Jhaveri D, Sen A, Reddy GV, Rodrigues V (2000) Sense organ identity in the Drosophila antenna is specified by the expression of the proneural gene atonal. Mech Dev 99:101–111. doi:10.1016/S0925-4773(00)00487-1

    Article  PubMed  CAS  Google Scholar 

  • Joly W, Mugat B, Maschat F (2007) Engrailed controls the organization of the ventral nerve cord through frazzled regulation. Dev Biol 301:542–554. doi:10.1016/j.ydbio.2006.10.019

    Article  PubMed  CAS  Google Scholar 

  • Kamikouchi A, Shimada T, Ito K (2006) Comprehensive classification of the auditory sensory projections in the brain of the fruit fly Drosophila melanogaster. J Comp Neurol 499:317–356. doi:10.1002/cne.21075

    Article  PubMed  Google Scholar 

  • Komiyama T, Carlson JR, Luo L (2004) Olfactory receptor neuron axon targeting: intrinsic transcriptional control and hierarchical interactions. Nat Neurosci 7:819–825. doi:10.1038/nn1284

    Article  PubMed  CAS  Google Scholar 

  • Kornberg T (1981) Engrailed: a gene controlling compartment and segment formation in Drosophila. Proc Natl Acad Sci USA 78:1095–1099. doi:10.1073/pnas.78.2.1095

    Article  PubMed  CAS  Google Scholar 

  • Kuemerle B, Gulden F, Cherosky N, Williams E, Herrup K (2007) The mouse Engrailed genes: a window into autism. Behav Brain Res 176:121–132. doi:10.1016/j.bbr.2006.09.009

    Article  PubMed  CAS  Google Scholar 

  • Laissue PP, Reiter C, Hiesinger PR, Halter S, Fischbach KF, Stocker RF (1999) Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J Comp Neurol 405:543–552. doi:10.1002/(SICI)1096-9861(19990322)405:4<543::AID-CNE7>3.0.CO;2-A

    Article  PubMed  CAS  Google Scholar 

  • Lawrence PA, Struhl G (1982) Further studies of the engrailed phenotype in Drosophila. EMBO J 1:827–833

    PubMed  CAS  Google Scholar 

  • Lee T, Luo L (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:451–461. doi:10.1016/S0896-6273(00)80701-1

    Article  PubMed  CAS  Google Scholar 

  • Lee MH, Salvaterra PM (2002) Abnormal chemosensory jump 6 is a positive transcriptional regulator of the cholinergic gene locus in Drosophila olfactory neurons. J Neurosci 22:5291–5299

    PubMed  CAS  Google Scholar 

  • Li X, Zhao X, Fang Y, Jiang X, Duong T, Fan C et al (1998) Generation of destabilized green fluorescent protein as a transcription reporter. J Biol Chem 273:34970–34975. doi:10.1074/jbc.273.52.34970

    Article  PubMed  CAS  Google Scholar 

  • Lienhard MC, Stocker RF (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

    PubMed  CAS  Google Scholar 

  • Logan C, Wizenmann A, Drescher U, Monschau B, Bonhoeffer F, Lumsden A (1996) Rostral optic tectum acquires caudal characteristics following ectopic engrailed expression. Curr Biol 6:1006–1014. doi:10.1016/S0960-9822(02)00645-0

    Article  PubMed  CAS  Google Scholar 

  • Lundell MJ, Chu-LaGraff Q, Doe CQ, Hirsh J (1996) The engrailed and huckebein genes are essential for development of serotonin neurons in the Drosophila CNS. Mol Cell Neurosci 7:46–61. doi:10.1006/mcne.1996.0004

    Article  PubMed  CAS  Google Scholar 

  • Marie B, Blagburn JM (2003) Differential roles of Engrailed paralogs in determining sensory axon guidance and synaptic target recognition. J Neurosci 23:7854–7862

    PubMed  CAS  Google Scholar 

  • Marie B, Bacon JP, Blagburn JM (2000) Double-stranded RNA interference shows that Engrailed controls the synaptic specificity of identified sensory neurons. Curr Biol 10:289–292. doi:10.1016/S0960-9822(00)00361-4

    Article  PubMed  CAS  Google Scholar 

  • Marie B, Cruz-Orengo L, Blagburn JM (2002) Persistent engrailed expression is required to determine sensory axon trajectory, branching, and target choice. J Neurosci 22:832–841

    PubMed  CAS  Google Scholar 

  • Merritt DJ, Murphey RK (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. doi:10.1002/cne.903220103

    Article  PubMed  CAS  Google Scholar 

  • Morata G, Lawrence PA (1975) Control of compartment development by the engrailed gene in Drosophila. Nature 255:614–617. doi:10.1038/255614a0

    Article  PubMed  CAS  Google Scholar 

  • Murphey RK, Possidente D, Pollack G, Merritt DJ (1989a) Modality-specific axonal projections in the CNS of the flies Phormia and Drosophila. J Comp Neurol 290:185–200. doi:10.1002/cne.902900203

    Article  PubMed  CAS  Google Scholar 

  • Murphey RK, Possidente DR, Vandervorst P, Ghysen A (1989b) Compartments and the topography of leg afferent projections in Drosophila. J Neurosci 9:3209–3217

    PubMed  CAS  Google Scholar 

  • Patel NH, Kornberg TB, Goodman CS (1989a) Expression of engrailed during segmentation in grasshopper and crayfish. Development 107:201–212

    PubMed  CAS  Google Scholar 

  • Patel NH, Martin-Blanco E, Coleman KG, Poole SJ, Ellis MC, Kornberg TB et al (1989b) Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58:955–968. doi:10.1016/0092-8674(89)90947-1

    Article  PubMed  CAS  Google Scholar 

  • Peel AD, Telford MJ, Akam M (2006) The evolution of hexapod engrailed-family genes: evidence for conservation and concerted evolution. Proc Biol Sci 273:1733–1742. doi:10.1098/rspb.2006.3497

    Article  PubMed  CAS  Google Scholar 

  • Raftery LA, Sanicola M, Blackman RK, Gelbart WM (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

    PubMed  CAS  Google Scholar 

  • Ray A, van Naters WG, Shiraiwa T, Carlson JR (2007) Mechanisms of odor receptor gene choice in Drosophila. Neuron 53:353–369. doi:10.1016/j.neuron.2006.12.010

    Article  PubMed  CAS  Google Scholar 

  • Reddy GV, Gupta B, Ray K, Rodrigues V (1997) Development of the Drosophila olfactory sense organs utilizes cell-cell interactions as well as lineage. Development 124:703–712

    PubMed  CAS  Google Scholar 

  • Rogina B, Helfand SL (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. doi:10.1016/S0925-4773(97)00033-6

    Article  PubMed  CAS  Google Scholar 

  • Saueressig H, Burrill J, Goulding M (1999) Engrailed-1 and netrin-1 regulate axon pathfinding by association interneurons that project to motor neurons. Development 126:4201–4212

    PubMed  CAS  Google Scholar 

  • Sayeed O, Benzer S (1996) Behavioral genetics of thermosensation and hygrosensation in Drosophila. Proc Natl Acad Sci USA 93:6079–6084. doi:10.1073/pnas.93.12.6079

    Article  PubMed  CAS  Google Scholar 

  • Sgado P, Alberi L, Gherbassi D, Galasso SL, Ramakers GM, Alavian KN et al (2006) Slow progressive degeneration of nigral dopaminergic neurons in postnatal Engrailed mutant mice. Proc Natl Acad Sci USA 103:15242–15247. doi:10.1073/pnas.0602116103

    Article  PubMed  CAS  Google Scholar 

  • Shanbhag SR, Singh K, Singh RN (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. doi:10.1007/BF00319115

    Article  PubMed  CAS  Google Scholar 

  • Shepherd D, Smith SA (1996) Central projections of persistent larval sensory neurons prefigure adult sensory pathways in the CNS of Drosophila. Development 122:2375–2384

    PubMed  CAS  Google Scholar 

  • Shigetani Y, Funahashi JI, Nakamura H (1997) En-2 regulates the expression of the ligands for Eph type tyrosine kinases in chick embryonic tectum. Neurosci Res 27:211–217. doi:10.1016/S0168-0102(96)01151-0

    Article  PubMed  CAS  Google Scholar 

  • Siegler MV, Jia XX (1999) Engrailed negatively regulates the expression of cell adhesion molecules connectin and neuroglian in embryonic Drosophila nervous system. Neuron 22:265–276. doi:10.1016/S0896-6273(00)81088-0

    Article  PubMed  CAS  Google Scholar 

  • Siegler MV, Pankhaniya RR, Jia XX (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. doi:10.1002/cne.1371

    Article  PubMed  CAS  Google Scholar 

  • Simon HH, Saueressig H, Wurst W, Goulding MD, O’Leary DD (2001) Fate of midbrain dopaminergic neurons controlled by the engrailed genes. J Neurosci 21:3126–3134

    PubMed  CAS  Google Scholar 

  • Smith SA, Shepherd D (1996) Central afferent projections of proprioceptive sensory neurons in Drosophila revealed with the enhancer-trap technique. J Comp Neurol 364:311–323. doi:10.1002/(SICI)1096-9861(19960108)364:2<311::AID-CNE9>3.0.CO;2-8

    Article  PubMed  CAS  Google Scholar 

  • Solano PJ, Mugat B, Martin D, Girard F, Huibant JM, Ferraz C et al (2003) Genome-wide identification of in vivo Drosophila Engrailed-binding DNA fragments and related target genes. Development 130:1243–1254. doi:10.1242/dev.00348

    Article  PubMed  CAS  Google Scholar 

  • Stocker RF (1994) The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res 275:3–26. doi:10.1007/BF00305372

    Article  PubMed  CAS  Google Scholar 

  • Trimarchi JR, Murphey RK (1997) The shaking-B2 mutation disrupts electrical synapses in a flight circuit in adult Drosophila. J Neurosci 17:4700–4710

    PubMed  CAS  Google Scholar 

  • Vosshall LB, Stocker RF (2007) Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci 30:505–533. doi:10.1146/annurev.neuro.30.051606.094306

    Article  PubMed  CAS  Google Scholar 

  • Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, Durrbeck H et al (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. doi:10.1016/j.neuron.2006.02.008

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Singhvi A, Kong P, Scott K (2004) Taste representations in the Drosophila brain. Cell 117:981–991. doi:10.1016/j.cell.2004.06.011

    Article  PubMed  CAS  Google Scholar 

  • Webster PJ, Mansour TE (1992) Conserved classes of homeodomains in Schistosoma mansoni, an early bilateral metazoan. Mech Dev 38:25–32. doi:10.1016/0925-4773(92)90035-I

    Article  PubMed  CAS  Google Scholar 

  • Wenner P, O’Donovan MJ, Matise MP (2000) Topographical and physiological characterization of interneurons that express Engrailed-1 in the embryonic chick spinal cord. J Neurophysiol 84:2651–2657

    PubMed  CAS  Google Scholar 

  • Williams DW, Shepherd D (1999) Persistent larval sensory neurons in adult Drosophila melanogaster. J Neurobiol 39:275–286. doi:10.1002/(SICI)1097-4695(199905)39:2<275::AID-NEU11>3.0.CO;2-0

    Article  PubMed  CAS  Google Scholar 

  • Williams DW, Tyrer M, Shepherd D (2000) Tau and tau reporters disrupt central projections of sensory neurons in Drosophila. J Comp Neurol 428:630–640. doi:10.1002/1096-9861(20001225)428:4<630::AID-CNE4>3.0.CO;2-X

    Article  PubMed  CAS  Google Scholar 

  • Wurst W, Auerbach AB, Joyner AL (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

    PubMed  CAS  Google Scholar 

  • Yasunaga K, Saigo K, Kojima T (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. doi:10.1016/j.mod.2006.08.008

    Article  PubMed  CAS  Google Scholar 

  • Yoffe KB, Manoukian AS, Wilder EL, Brand AH, Perrimon N (1995) Evidence for engrailed-independent wingless autoregulation in Drosophila. Dev Biol 170:636–650. doi:10.1006/dbio.1995.1243

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

JMB was supported by NIH GM S06 008224, with partial infrastructure support from NIH RCMI RR03051. The monoclonal antibodies developed by Dr. Corey Goodman, Dr. E. Buchner and Dr. W. A. Johnson were obtained from the Developmental Studies Hybridoma Bank developed under the auspices of the NICHD and maintained by The University of Iowa, Department of Biological Sciences, Iowa City, IA 52242. Thanks go to Dr. Bruno Marie for comments on the manuscript.

Author information

Authors and Affiliations

  1. Institute of Neurobiology and Department of Physiology, University of Puerto Rico Medical Sciences Campus, Puerto Rico, USA

    Jonathan M. Blagburn

Authors
  1. Jonathan M. Blagburn
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jonathan M. Blagburn.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Blagburn, J.M. Engrailed expression in subsets of adult Drosophila sensory neurons: an enhancer-trap study. Invert Neurosci 8, 133–146 (2008). https://doi.org/10.1007/s10158-008-0074-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10158-008-0074-6

Keywords

Search

Navigation