Cell and Tissue Research

, Volume 339, Issue 2, pp 321–336

Detailed analysis of leucokinin-expressing neurons and their candidate functions in the Drosophila nervous system

  • María de Haro
  • Ismael Al-Ramahi
  • Jonathan Benito-Sipos
  • Begoña López-Arias
  • Belén Dorado
  • Jan A. Veenstra
  • Pilar Herrero
Regular Article

Abstract

The distribution of leucokinin (LK) neurons in the central nervous system (CNS) of Drosophila melanogaster was described by immunolabelling many years ago. However, no detailed underlying information of the input or output connections of their neurites was then available. Here, we provide a more accurate morphological description by employing a novel LK-specific GAL4 line that recapitulates LK expression. In order to analyse the possible afferent and efferent neural candidates of LK neurons, we used this lk-GAL4 line together with other CNS-Gal4 lines, combined with antisera against various neuropeptides or neurotransmitters. We found four kinds of LK neurons in the brain. (1) The lateral horn neurons connect the antennal glomerula to the mushroom bodies. (2) The suboesophageal neurons connect the gustatory receptors to the suboesophageal ganglia and ventral nerve cord. (3) The anterior neurons innervate the corpus cardiacum of the ring gland but LK expression is surprisingly not detectable from the third instar onwards in these neurons. (4) A set of abdominal ganglion neurons connect to the dorsal median tract in larvae and send their axons to a segmental muscle 8. Thus, the methods employed in our study can be used to identify individual neuropeptidergic neurons and thereby characterize functional cues or developmental transformations in their differentiation.

Keywords

Neuropeptidergic characterization Nervous system Leucokinin Drosophila melanogaster 

References

  1. Acebes A, Ferrús A (2001) Increasing the number of synapses modifies olfactory perception in Drosophila. J Neurosci 21:6264–6273PubMedGoogle Scholar
  2. Cantera R, Nässel DR (1992) Segmental peptidergic innervation of abdominal targets in larval and adult dipteran insects revealed with antiserum against leucokinin I. Cell Tissue Res 269:459–471CrossRefPubMedGoogle Scholar
  3. Chen Y, Veenstra JA, Davis NT, Hagedorn HH (1994) A comparative study of leucokinin-immunoreactive neurons in insects. Cell Tissue Res 276:69–83CrossRefPubMedGoogle Scholar
  4. Clark E, Jan LY, Jan YN (1997) Reciprocal localization of Nod and kinesin fusion proteins indicates microtubule polarity in the Drosophila oocyte, epithelium neuron and muscle. Development 124:461–470PubMedGoogle Scholar
  5. Connolly JB, Roberts IJ, Armstrong JD, Kaiser K, Forte M (1996) Associative learning disrupted by impaired Gs signalling in Drosophila mushroom bodies. Science 274:2104–2107CrossRefPubMedGoogle Scholar
  6. Fischler W, Kong P, Marella S, Scott K (2007) The detection of carbonation by the Drosophila gustatory system. Nature 448:1054–1058CrossRefPubMedGoogle Scholar
  7. Friggi-Grelin F, Coulom H, Meller M, Gómez D, Hirsh J, Birman S (2003) Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. J Neurobiol 54:618–627CrossRefPubMedGoogle Scholar
  8. Gendre N, Lüer K, Friche S, Grillenzoni N, Ramaekers A, Technau GM, Stocker RF (2004) Integration of complex larval chemosensory organs into the adult nervous system of Drosophila. Development 131:83–92CrossRefPubMedGoogle Scholar
  9. Herrero P, Magariños M, Torroja L, Canal I (2003) Neurosecretory identity conferred by the apterous gene: lateral horn leucokinin neurons in Drosophila. J Comp Neurol 457:123–132CrossRefPubMedGoogle Scholar
  10. Herrero P, Magariños M, Molina I, Benito J, Dorado B, Turiégano E, Canal I, Torroja L (2007) Squeeze involvement in the specification of Drosophila leucokinergic neurons: different regulatory mechanisms endow the same neuropeptide selection. Mech Dev 124:427–440CrossRefPubMedGoogle Scholar
  11. Johard HA, Enell LE, Gustafsson E, Trifilieff P, Veenstra JA, Nässel DR (2008) Intrinsic neurons of Drosophila mushroom bodies express short neuropeptide F: relations to extrinsic neurons expressing different neurotransmitters. J Comp Neurol 507:1479–1496CrossRefPubMedGoogle Scholar
  12. Keene AC, Waddell S (2007) Drosophila olfactory memory: single genes to complex neural circuits. Nat Rev 8:341–354Google Scholar
  13. Landgraf M, Sánchez-Soriano N, Technau GM, Urban J, Prokop A (2003) Charting the Drosophila neuropile: a strategy for the standardised characterisation of genetically amenable neurites. Dev Biol 260:207–225CrossRefPubMedGoogle Scholar
  14. Mahr A, Aberle H (2006) The expression pattern of the Drosophila vesicular glutamate transporter: a marker protein for motoneurons and glutamatergic centers in the brain. Gene Expr Patterns 6:299–309CrossRefPubMedGoogle Scholar
  15. Marella S, Fischler W, Kong P, Asgarian S, Rueckert E, Scott K (2006) Imaging taste responses in the fly brain reveals a functional map of taste category and behaviour. Neuron 49:285–295CrossRefPubMedGoogle Scholar
  16. Melcher C, Pankratz MJ (2005) Candidate gustatory interneurons modulating feeding behaviour in the Drosophila brain. PLoS Biol 3:e305CrossRefPubMedGoogle Scholar
  17. Nässel DR (2002) Neuropeptides in the nervous system of Drosophila and other insects: multiple roles of neuromodulators and neurohormones. Prog Neurobiol 68:1–84CrossRefPubMedGoogle Scholar
  18. Nässel DR, Homberg U (2006) Neuropeptides in interneurons of insect brain. Cell Tissue Res 326:1–24CrossRefPubMedGoogle Scholar
  19. O’Donnell MJ, Rheault MR, Davies SA, Rosay P, Harvey BJ, Maddrell HP, Kaiser K, Dow JAT (1998) Hormonally controlled chloride movement across Drosophila tubules is via ion channels in stellate cells. Am J Physiol 43:R1039–R1049Google Scholar
  20. Rubin GM, Sprading AC (1982) Genetic transformation of Drosophila melanogaster with transposable element vectors. Science 218:348–353CrossRefPubMedGoogle Scholar
  21. Santos JG, Vömel M, Struck R, Homberg U, Nässel DR, Wegener C (2007) Neuroarchitecture of peptidergic systems in the larval ventral ganglion of Drosophila melanogaster. PlosOne 2:e695Google Scholar
  22. Schroll C, Riemensperger T, Bucher D, Ehmer J, Voller T, Erbguth K, Gerber B, Hendel T, Nagel G, Buchner F, Fiala A (2006) Light-induced activation of distinct modulatory neurons trigger appetitive or aversive learning in Drosophila larvae. Curr Biol 16:1741–1747CrossRefPubMedGoogle Scholar
  23. Scott K, Brady R, Cravchik A, Morozov P, Rzhetsky A, Zuker C, Axel R (2001) A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104:661–673CrossRefPubMedGoogle Scholar
  24. Schwaerzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M (2003) Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23:10496–10502Google Scholar
  25. Siegmund T, Korge G (2001) Innervations of the ring gland of Drosophila melanogaster. J Comp Neurol 431:481–491CrossRefPubMedGoogle Scholar
  26. Sinakevitch I, Strausfeld J (2004) Chemical neuroanatomy of the fly’s movement detection pathway. J Comp Neurol 468:6–23CrossRefPubMedGoogle Scholar
  27. Stocker RF (1994) The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res 275:3–26CrossRefPubMedGoogle Scholar
  28. Stocker RF, Heimbeck G, Gendre N, Belle JS de (1997) Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. J Neurobiol 32:443–456CrossRefPubMedGoogle Scholar
  29. Strausfeld NJ (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New YorkGoogle Scholar
  30. Taghert PH, Veenstra JA (2003) Drosophila neuropeptide signalling. Adv Genet 49:1–65CrossRefPubMedGoogle Scholar
  31. Terhzaz S, O’Connell FC, Pollock VP, Kean L, Davies SA, Veenstra JA, Dow JAT (1999) Isolation and characterization of a leucokinin-like peptide of Drosophila melanogaster. J Exp Biol 202:3667–3676PubMedGoogle Scholar
  32. Thorne N, Chromey C, Bray S, Amrein H (2004) Taste perception and coding in Drosophila. Curr Biol 14:1065–1079CrossRefPubMedGoogle Scholar
  33. Veenstra JA (2008) Regulatory peptides in fruit fly midgut. Cell Tissue Res 334:499–516CrossRefPubMedGoogle Scholar
  34. Veenstra JA, Pattillo JM, Petzel DH (1997) A single cDNA encodes all three Aedes leucokinins, which stimulate both fluid secretion by the Malpighian tubules and hindgut contractions. J Biol Chem 272:10402–10407CrossRefPubMedGoogle Scholar
  35. Waddell S, Armstrong JD, Kitamoto T, Kaiser K, Quinn WG (2000) The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory. Cell 103:805–813CrossRefPubMedGoogle Scholar
  36. Wang Z, Singhvi A, Kong P, Scott K (2004) Taste representations in the Drosophila brain. Cell 117:981–991CrossRefPubMedGoogle Scholar
  37. Wong AM, Wang JW, Axel R (2002) Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109:229–241CrossRefPubMedGoogle Scholar
  38. Zhang K, Guo JZ, Peng Y, Xi W, Guo A (2007) Dopamine-mushroom body circuit regulates saliency-based decision-making in Drosophila. Science 316:1901–1904CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • María de Haro
    • 1
  • Ismael Al-Ramahi
    • 1
  • Jonathan Benito-Sipos
    • 2
    • 4
  • Begoña López-Arias
    • 2
  • Belén Dorado
    • 2
  • Jan A. Veenstra
    • 3
  • Pilar Herrero
    • 2
    • 4
    • 5
  1. 1.Department of Molecular and Human GeneticsBaylor College of MedicineHoustonUSA
  2. 2.Departamento de BiologíaUniversidad Autónoma de MadridMadridSpain
  3. 3.Université de BordeauxCNIC CNRS UMR 5228TalenceFrance
  4. 4.Departamento de Biología del DesarrolloCentro de Biología Molecular “Severo Ochoa”—Universidad Autónoma de MadridMadridSpain
  5. 5.Departamento de Biología, Facultad de CienciasUniversidad Autónoma de MadridMadridSpain

Personalised recommendations