Heat Shock–Mediated Thermoprotection of Larval Locomotion Compromised by Ubiquitous Overexpression of Hsp70 inDrosophila melanogaster

Abstract

. Heat shock-mediated thermoprotection of larval locomotion compromised by ubiquitous overexpression of Hsp70 in Drosophila melanogaster. J Neurophysiol 94: 3563-3572, 2005. First published August 10, 2005 doi:10.1152/jn.00723.2005. Maintaining the competence of locomotor circuitry under stressful conditions can benefit organisms by enabling locomotion to more tolerable microhabitats. We show that prior heat shock protects locomotion and the locomotor central pattern generator of larval Drosophila against subsequent hyperthermic stress. We combined molecular genetic, electrophysiological, and behavioral techniques to investigate heat shock-mediated thermoprotection. Prior heat shock increased the distance traveled by larvae during hyperthermia before failure. The frequency of the rhythm of peristaltic locomotor contractions and the velocity of locomotion were both less thermosensitive after heat shock and were less susceptible to failure at high temperatures. Rhythmic coordinated motor patterns, recorded intracellularly as excitatory junction potentials in body wall muscles of dissected preparations, were centrally generated because patterns could still be generated in the absence of sensory feedback (sensory function disrupted with shibire). Prior heat shock protected central circuit operation during hyperthermic stress by increasing the temperature at which it failed. Overexpression of Hsp70 after a heat shock using transgenic flies (traII) did not enhance thermoprotection, as expected, but had deleterious effects on parameters of behavior.

Presynaptic Ryanodine Receptor-Activated Calmodulin Kinase II Increases Vesicle Mobility and Potentiates Neuropeptide Release

“…Therefore, this signaling pathway has a minor role until it is recruited by tetanic activity. The activity requirement for recruitment of RyR-CaMKII-activated mobilization and PTP is well matched to the native activity found at the larval NMJ [i.e., rhythmic bursting (Klose et al, 2005)] and the activity patterns known to be optimal for neuropeptide release. Given past in vitro studies of DCV mobility (Burke et al, 1997;Han et al, 1999;Ng et al, 2002Ng et al, , 2003, the in vivo results presented here are consistent with the conclusion that physiological activity triggers RyR-activated CaMKII to increase DCV mobility, which in turn contributes to PTP of neuropeptide secretion.…”

Hyperthermic Preconditioning of Presynaptic Calcium Regulation inDrosophila

“…At stressfully high temperatures, electrical stimulation exacerbates the [Ca 2ϩ ] r increases, and both synaptic transmission and stimulus-evoked presynaptic Ca 2ϩ responses eventually fail. Both HS preconditioning and Hsp70 expression in motor neurons, which have been shown to thermoprotect synaptic transmission, motor pattern generation, and locomotor behavior Klose et al 2005;Xiao et al 2007), attenuated the detrimental increase in [Ca 2ϩ ] r and maintained stimulus-evoked Ca 2ϩ -responses. In thermotolerant ter-FIG.…”

“…The last feature is dramatically evident in Drosophila, where the heat shock response was first discovered (Ritossa 1962). Drosophila locomotor behavior, motor pattern generation, and synaptic transmission are disrupted by hyperthermic stress; the thermal sensitivity of each of these functions is plastic Klose et al 2005). Whether hyperthermia-induced failure of synaptic function is due to disruption of critical protein function, lack of energy, accumulation of reactive oxygen species, disruption in Ca 2ϩ regulation, or interactions involving of several of these factors is unclear.…”

Peripheral multidendritic sensory neurons are necessary for rhythmic locomotion behavior in Drosophila larvae

“…1a); faster crawling and increased activity might be a natural avoidance response to high temperatures (16,17). We isolated 130 Gal4 lines that give rise to different types of defects in larval locomotion (see Methods).…”