Bursicon Functions within theDrosophilaCNS to Modulate Wing Expansion Behavior, Hormone Secretion, and Cell Death

Abstract

Hormones are often responsible for synchronizing somatic physiological changes with changes in behavior. Ecdysis (i.e., the shedding of the exoskeleton) in insects has served as a useful model for elucidating the molecular and cellular mechanisms of this synchronization, and has provided numerous insights into the hormonal coordination of body and behavior. An example in which the mechanisms have remained enigmatic is the neurohormone bursicon, which, after the final molt, coordinates the plasticization and tanning of the initially folded wings with behaviors that drive wing expansion. The somatic effects of the hormone are governed by bursicon that is released into the blood from neurons in the abdominal ganglion (the B AG ), which die after wing expansion. How bursicon induces the behavioral programs required for wing expansion, however, has remained unknown. Here we show by targeted suppression of excitability that a pair of bursicon-immunoreactive neurons distinct from the B AG and located within the subesophageal ganglion in Drosophila (the B SEG ) is involved in controlling wing expansion behaviors. Unlike the B AG , the B SEG arborize widely in the nervous system, including within the abdominal neuromeres, suggesting that, in addition to governing behavior, they also may modulate the B AG. Indeed, we show that animals lacking bursicon receptor function have deficits both in the humoral release of bursicon and in posteclosion apoptosis of the B AG . Our results reveal novel neuromodulatory functions for bursicon and support the hypothesis that the B SEG are essential for orchestrating both the behavioral and somatic processes underlying wing expansion.

Targeted inactivation of the rickets receptor in muscle compromisesDrosophilaviability

“…Bursicon is first released from the subesphogeal ganglion, followed by secretion from the abdominal ganglion into the hemolymph. The Drosophila circulatory system then disperses bursicon throughout the organism (Peabody et al, 2008;Peabody et al, 2009). While most studies have focused on the location of bursicon release, much less research has addressed the importance of tissue-selective rk activation .…”

“…We subsequently used a series of Gal4 driver lines to target our tethered ligand to selected tissues and thus define the critical cell type(s) that requires rk and underlies the lethality/wing expansion phenotypes (Table 1). Although many studies have focused on the spatial and temporal release of bursicon (Lahr et al, 2012;Peabody et al, 2008;Peabody et al, 2009), the localization of the bursicon receptors that are essential for survival has remained elusive. Our study strongly supports that a peripheral rk, localized in muscle, plays an important role in Drosophila development.…”

Eclosion gates progression of the adult ecdysis sequence ofDrosophila

“…The w 1118 ;+;+ line was from the Bloomington Stock Center (Indiana University, Bloomington, IN, USA). The following lines used in this study have been described previously: w;Burs-Gal4;+ (Peabody et al, 2008) (Peabody et al, 2009).…”

“…The hormone responsible for both wing plasticization and for wing expansion behaviors is bursicon, which is expressed in a small set of neuroendocrine cells in the abdominal ganglion (B AG ) and a single pair of cells in the subesophageal ganglion (B SEG ) (Peabody et al, 2008). The B SEG secrete bursicon into the central nervous system and principally mediate the behavioral effects of the hormone, while the B AG secrete bursicon into the hemolymph to mediate its somatic effects (Luan et al, 2012).…”

A Novel Approach for Directing Transgene Expression in Drosophila: T2A-Gal4 In-Frame Fusion

“…We further confirmed the fidelity of the rk pan -Gal4 expression pattern by examining the expression of a UAS-EGFP reporter. EGFP was readily detected in tissues known to have RK activity, such as the epidermis and the unfolded wings of newly emerged flies (Davis et al 2007) (Figure 3D), as well as in diverse cells of the central nervous system (Peabody et al 2008) (Figure 3E). The observed tissue distribution of EGFP also closely matched the distribution of rk mRNA reported at FlyAtlas (Chintapalli et al 2007), with all tissues having high message levels and showing robust EGFP signals, except the adult fat body (Table 1).…”