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

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.

A Drosophila Gain-of-Function Screen for Candidate Genes Involved in Steroid-Dependent Neuroendocrine Cell Remodeling

“…In Drosophila neuroendocrine cells as well as in other neuronal cell types, loss of the EcR-B isoforms leads to pruning defects. In contrast, EcR-A is thought to regulate the outgrowth of the adult-specific neurites Truman 1996;Schubiger et al 1998;Lee et al 2000;Brown et al 2006;Santos et al 2006).…”

Biology of the CAPA peptides in insects

“…In the larva, these so-called Va neurons send axons dorsally that project into the respective median and proximal transverse nerves that show swellings indicative for a PSO. During metamorphosis, the median/transverse nerves become completely reduced and the Va neurons show a distinct neurite pruning [31]. Subsequent neuritic outgrowth in later pupal stages leads to a network of CAPA peptide-containing fibers just below the dorsal ganglionic sheath.…”

“…2, 3), which may reflect a reduction process in this insect with a conservation of the most important part of this peptidergic system, the neuroendocrine cells in the VNC. In the fruit fly, CAPA peptides are expressed in a single pair of ventral median neurons in each of the first three abdominal neuromeres of the fused VNC [4,31]. In the larva, these so-called Va neurons send axons dorsally that project into the respective median and proximal transverse nerves that show swellings indicative for a PSO.…”

Isoform-Specific Regulation of a Steroid Hormone Nuclear Receptor by an E3 Ubiquitin Ligase inDrosophila melanogaster

“…In Drosophila, the steroid hormone 20-hydroxyecdysone (20E) triggers the transcriptional changes required for gonad development, larval molting, and the onset and completion of metamorphosis (Sliter and Gilbert 1992;Henrich et al 1993;Carney and Bender 2000;Riddiford et al 2000; Beckstead et al 2005). Differentiation of imaginal structures and neuronal remodeling, two major features of metamorphosis, have been used as cellular systems to analyze the functional role of proteins that elicit morphogenetic changes at this phase of the life cycle (Schubiger et al 2005;Brown et al 2006;Santos et al 2006). 20E regulates gene expression by binding to its nuclear receptor, EcR (King-Jones and Thummel 2005).…”