Skip to main content
Log in

Morphology and metamorphosis of the peptidergic Va neurons and the median nerve system of the fruit fly, Drosophila melanogaster

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Metamorphosis is a fundamental developmental process and has been intensively studied for various neuron types of Drosophila melanogaster. However, detailed accounts of the fate of identified peptidergic neurons are rare. We have performed a detailed study of the larval morphology and pupal remodelling of identified peptidergic neurons, the CAPA-expressing Va neurons of D. melanogaster. In the larva, Va neurons innervate abdominal median and transverse nerves that are typically associated with perisympathetic organs (PSOs), major neurohaemal release sites in insects. Since median and transverse nerves are lacking in the adult, Va neurites have to undergo substantial remodelling during metamorphosis. We have examined the hitherto uncharacterised gross morphology of the thoracic PSOs and the abdominal median and transverse nerves by scanning electron microscopy and found that the complete reduction of these structures during metamorphosis starts around pupal stage P7 and is completed at P9. Concomitantly, neurite pruning of the Va neurons begins at P6 and is preceded by the high expression of the ecdysone receptor (EcR) subtype B1 in late L3 larvae and the first pupal stages. New neuritic outgrowth mainly occurs from P7-P9 and coincides with the expression of EcR-A, indicating that the remodelling of the Va neurons is under ecdysteroid control. Immunogold-labelling has located the CAPA peptides to large translucent vesicles, which are released from the transverse nerves, as suggested by fusion profiles. Hence, the transverse nerves may serve a neurohaemal function in D. melanogaster.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Allan DW, St. Pierre SE, Miguel-Aliaga I, Thor S (2003) Specification of neuropeptide cell identity by the integration of retrograde BMP signaling and a combinatorial transcription factor code. Cell 113:73–86

    Article  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 

  • Baudry-Partiaoglou N (1983) Ultrastructure of perisympathetic organs in insects. In: Gupta AP (ed) Neurohemal organs in arthropods. Thomas, Springfield, Ill., pp 513–551

    Google Scholar 

  • Brady J, Maddrell SHP (1967) Neurohaemal organs in the medial nervous system of insects. Z Zellforsch 76:389–404

    Article  CAS  PubMed  Google Scholar 

  • Cabrero P, Radford JC, Broderick KE, Costes L, Veenstra JA, Spana EP, Davies SA, Dow JAT (2002) The Dh gene of Drosophila melanogaster encodes a diuretic peptide that acts through cyclic AMP. J Exp Biol 205:3799–3807

    PubMed  CAS  Google Scholar 

  • Cannata MA, Morris JF (1973) Changes in the appearance of hypothalamo-neurohypophysial neurosecretory granules associated with their maturation. J Endocrinol 56:91–98

    Google Scholar 

  • Cheng Y, Endo K, Wu K, Rodan AR, Heberlein U, Davis RL (2001) Drosophila fasciclinII is required for the formation of odor memories and for normal sensitivity to alcohol. Cell 105:757–768

    Article  PubMed  CAS  Google Scholar 

  • Chiang C, Patel NH, Young KE, Beachy PA (1994) The novel homeodomain gene buttonless specifies differentiation and axonal guidance functions of Drosophila dorsal median cells. Development 120:3581–3593

    PubMed  CAS  Google Scholar 

  • Choi MY, Rafaeli A, Jurenka RA (2001) Pyrokinin/PBAN-like peptides in the central nervous system of Drosophila melanogaster. Cell Tissue Res 306:459–465

    Article  PubMed  CAS  Google Scholar 

  • Dai JD, Gilbert LI (1991) Metamorphosis of the corpus allatum and degeneration of the prothoracic glands during the larval-pupal-adult transformation of Drosophila melanogaster: a cytophysiological analysis of the ring gland. Dev Biol 144:309–326

    Article  PubMed  CAS  Google Scholar 

  • Dellmann HD, Sikora-Vanmeter KC (1982) Reversible fine structural changes in the supraoptic nucleus of the rat following intraventricular administration of colchicine. Brain Res Bull 8:171–182

    Article  PubMed  CAS  Google Scholar 

  • Douglas WW, Nagasawa J, Schulz R (1970) Electron microscopic studies on the mechanism of secretion of posterior pituitary hormones and significance of microvesicles (“synaptic vesicles”): evidence of secretion by exocytosis and formation of microvesicles as a byproduct of this process. Mem Soc Endocrinol 19:353–377

    Google Scholar 

  • Eckert M, Predel R, Gundel M (1999) Periviscerokinin-like immunoreactivity in the nervous system of the American cockroach. Cell Tissue Res 295:159–170

    Article  PubMed  CAS  Google Scholar 

  • Eckert M, Herbert Z, Pollák E, Molnár L, Predel R (2002) Identical cellular distribution of all abundant neuropeptides in the major abdominal neurohemal system of an insect (Periplaneta americana). J Comp Neurol 452:264–275

    Article  PubMed  CAS  Google Scholar 

  • Ewer J (2005) Behavioral actions of neuropeptides in invertebrates: insights from Drosophila. Horm Behav 48:418–429

    Article  PubMed  CAS  Google Scholar 

  • Finlayson LH, Osborne MP (1968) Peripheral neurosecretory cells in the stick insect (Carausius morosus) and the blowfly larva (Phormia terra-novae). J Insect Physiol 14:1793–1801

    Article  PubMed  CAS  Google Scholar 

  • Gorczyca MG, Phillis RW, Budnik V (1994) The role of tinman, a mesodermal cell fate gene, in axon pathfinding during the development of the transverse nerve in Drosophila. Development 120:2143–2152

    PubMed  CAS  Google Scholar 

  • Grenningloh G, Rehm EJ, Goodman CS (1991) Genetic analysis of growth cone guidance in Drosophila: fasciclin II functions as a neuronal recognition molecule. Cell 67:45–57

    Article  PubMed  CAS  Google Scholar 

  • Grillot JP (1983) Morphology and evolution of perisympathetic organs in insects. In: Gupta AP (ed) Neurohemal organs of arthropods. Thomas, Springfield, Ill., pp 481–512

    Google Scholar 

  • Johnson EC, Shafer OT, Trigg JS, Park J, Schooley DA, Dow JA, Taghert PH (2005) A novel diuretic hormone receptor in Drosophila: evidence for conservation of CGRP signaling. J Exp Biol 208:1239–1246

    Article  PubMed  CAS  Google Scholar 

  • Kean L, Cazenave W, Costes L, Broderick KE, Graham S, Pollock VP, Davies SA, Veenstra JA, Dow JAT (2002) Two nitridergic peptides are encoded by the gene capability in Drosophila melanogaster. Am J Physiol 282:R1297–R1307

    CAS  Google Scholar 

  • Landgraf M, Sánchez-Soriano N, Technau GM, Urban J, Prokop A (2003) Charting the Drosophila neuropile: a strategy for the standardised characterisation of the genetically amenable neurites. Dev Biol 260:207–225

    Article  PubMed  CAS  Google Scholar 

  • Lin D, Fetter RD, Kopczynski C, Grenningloh G, Goodman CS (1994) Genetic analysis of fasciclin II in Drosophila: defasciculation, refasciculation, and altered fasciculation. Neuron 13:1055–1069

    Article  PubMed  CAS  Google Scholar 

  • Miksys S, Lange AB, Orchard I, Wong V (1997) Localization and neurohemal release of FMRFamide-related peptides in the stick insect Carausius morosus. Peptides 18:27–40

    Article  PubMed  CAS  Google Scholar 

  • Morris JF, Dyball REJ (1974) A quantitative study of the ultrastructural changes in the hypothalamo-neurohypophysial system during and after experimentally induced hypersecretion. Cell Tissue Res 149:525–535

    Article  PubMed  CAS  Google Scholar 

  • Morris JF, Nordmann JJ (1982) Membrane retrieval by vacuoles after exocytosis in the neural lobe of Brattleboro rats. Neuroscience 7:1631–1639

    Article  PubMed  CAS  Google Scholar 

  • Nässel DR, Elekes K (1985) Serotonergic terminals in the neural sheath of the blowfly nervous system: electron microscopical immunocytochemistry and 5,7-dihydroxytryptamine labeling. Neuroscience 15:293–307

    Article  PubMed  Google Scholar 

  • Nässel DR, Ohlsson LG, Cantera R (1988) Metamorphosis of identified neurons innervating thoracic neurohemal organs in the blowfly: transformation of cholecystokininlike immunoreactive neurons. J Comp Neurol 267:343–356

    Article  PubMed  Google Scholar 

  • Nässel DR, Bayraktaroglu E, Dircksen H (1994) Neuropeptides in neurosecretory and efferent neural systems of insect thoracic and abdominal ganglia. Zool Sci 11:15–31

    Google Scholar 

  • O’Brien MA, Taghert PH (1998) A peritracheal neuropeptide system in insects: release of myomodulin-like peptides at ecdysis. J Exp Biol 201:193–209

    PubMed  CAS  Google Scholar 

  • Osborne MP (1964) The structure of the unpaired ventral nerves in the blowfly larva. Q J Microsc Sci 105:325–329

    Google Scholar 

  • Pollák E, Eckert M, Molnár L, Predel R (2005) Differential sorting and packaging of capa-gene related products in an insect. J Comp Neurol 481:84–95

    Article  PubMed  Google Scholar 

  • Pollock VP, McGettigan J, Cabrero P, Maudlin IM, Dow JAT, Davies SA (2004) Conservation of Capa peptide-induced nitric oxide signalling in Diptera. J Exp Biol 207:4135–4145

    Article  PubMed  CAS  Google Scholar 

  • Pow DV, Morris JF (1991) Membrane routing during exocytosis in neuroendocrine neurones and endocrine cells: use of colloidal gold particles and immunocytochemical discrimination of membrane compartments. Cell Tissue Res 264:299–316

    Article  PubMed  CAS  Google Scholar 

  • Predel R, Russell WK, Tichy SE, Russell DH, Nachman RJ (2003a) Mass spectrometric analysis of putative Capa-gene products in Musca domestica and Neobellieria bullata. Peptides 24:1487–1491

    Article  PubMed  CAS  Google Scholar 

  • Predel R, Herbert Z, Eckert M (2003b) Neuropeptides in perisympathetic organs of Manduca sexta: specific composition and changes during development. Peptides 24:1457–1464

    Article  PubMed  CAS  Google Scholar 

  • Predel R, Wegener C, Russell WK, Tichy SE, Russell DH, Nachman RJ (2004) Peptidomics of CNS-associated neurohemal systems of adult Drosophila melanogaster: a mass spectrometric survey of peptides from individual flies. J Comp Neurol 474:379–392

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Soriano N, Prokop A (2005) The influence of pioneer neurons on a growing motor nerve in Drosophila requires the neural cell adhesion molecule homolog fasciclin II. J Neurosci 25:78–87

    Article  PubMed  CAS  Google Scholar 

  • Schooneveld H (1974) Ultrastructure of the neurosecretory system of the Colorado potato beetle, Leptinotarsa decemlineata (Say). Cell Tissue Res 154:275–288

    Article  PubMed  CAS  Google Scholar 

  • Schubiger M, Wade AA, Carney GE, Truman JW, Bender M (1998) Drosophila EcR-B ecdysone receptor isoforms are required for larval molting and for neuron remodeling during metamorphosis. Development 125:2053–2062

    PubMed  CAS  Google Scholar 

  • Schubiger M, Tomita S, Sung C, Robinow S, Truman JW (2003) Isoform specific control of gene activity in vivo by the Drosophila ecdysone receptor. Mech Dev 120:909–918

    Article  PubMed  CAS  Google Scholar 

  • Sivasubramanian P (1991) FMRFamide-like immunoreactivity in the ventral ganglion of the fly Sarcophaga bullata: metamorphic changes. Comp Biochem Physiol [C] 99:507–512

    Article  CAS  Google Scholar 

  • Smith U, Smith DS (1966) Observations on the secretory processes in the corpus cardiacum of the stick insect, Carausius morosus. J Cell Sci 1:59–66

    PubMed  CAS  Google Scholar 

  • Taghert PH (1999) FMRFamide neuropeptides and neuropeptide-associated enzymes in Drosophila. Microsc Res Tech 45:80–95

    Article  PubMed  CAS  Google Scholar 

  • Talbot WS, Swyryd EA, Hogness DS (1993) Drosophila tissues with different metamorphic responses to ecdysone express different ecdysone receptor isoforms. Cell 73:1323–1337

    Article  PubMed  CAS  Google Scholar 

  • 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 202:3667–3676

    PubMed  CAS  Google Scholar 

  • Tissot M, Stocker RF (2000) Metamorphosis in Drosophila and other insects: the fate of neurons throughout the stages. Progr Neurobiol 62:89–111

    Article  CAS  Google Scholar 

  • Truman JW (1990) Metamorphosis of the central nervous system of Drosophila. J Neurobiol 21:1072–1084

    Article  PubMed  CAS  Google Scholar 

  • Truman JW, Talbot WS, Fahrbach SE, Hogness DS (1994) Ecdysone receptor expression in the CNS correlates with stage-specific responses to ecdysteroids during Drosophila and Manduca development. Development 120:219–234

    PubMed  CAS  Google Scholar 

  • Vallés AN, White K (1988) Serotonin-containing neurons in Drosophila melanogaster: development and distribution. J Comp Neurol 268:414–428

    Article  PubMed  Google Scholar 

  • Wegener C, Linde D, Eckert M (2001) Periviscerokinins in cockroaches: release, localization, and taxon-specific action on the hyperneural muscle. Gen Comp Endocrinol 121:1–12

    Article  PubMed  CAS  Google Scholar 

  • Wegener C, Herbert Z, Eckert M, Predel R (2002) The periviscerokinin (PVK) peptide family in insects: evidence for the inclusion of CAP2b as a PVK family member. Peptides 23:605–611

    Article  PubMed  CAS  Google Scholar 

  • Wegener C, Reinl T, Jänsch L, Predel R (2006) Direct mass spectrometric peptide profiling and fragmentation of larval peptide hormone release sites in Drosophila melanogaster reveals tagma-specific peptide expression and differential processing. J Neurochem 96:1362–1374

    Article  PubMed  CAS  Google Scholar 

  • Williams DW, Truman JW (2005) Remodeling dendrites during insect metamorphosis. J Neurobiol 64:24–33

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We express our thanks to Stefan Thor, Stéphane Noselli, Paul Taghert and the Bloomington Stock Center for the kind gift of flies, to Manfred Eckert and the DSHB for the kind gift of antibodies, to Petra Touzani for excellent technical help with the preparations for SEM, to Reinhard Predel, Heinrich Dircksen and Joachim Schachtner for useful suggestions, to Ruth Hyland and Renate Renkawitz-Pohl for providing fly housing, to Ian Orchard for hints regarding the older literature, to Wolf Huetteroth for expert advise with Amira, to Matthias Vömel for contributing to the layout of the Fas2 scheme, and to Uwe Homberg for general support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christian Wegener.

Additional information

This work was supported by the German Science Foundation (Deutsche Forschungsgemeinschaft, DFG), grant We 2652/2-1.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Santos, J.G., Pollák, E., Rexer, KH. et al. Morphology and metamorphosis of the peptidergic Va neurons and the median nerve system of the fruit fly, Drosophila melanogaster . Cell Tissue Res 326, 187–199 (2006). https://doi.org/10.1007/s00441-006-0211-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-006-0211-7

Keywords

Navigation